research article planktonic rotifers in a subtropical shallow...

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Hindawi Publishing Corporation e Scientific World Journal Volume 2013, Article ID 702942, 14 pages http://dx.doi.org/10.1155/2013/702942 Research Article Planktonic Rotifers in a Subtropical Shallow Lake: Succession, Relationship to Environmental Factors, and Use as Bioindicators Gaohua Ji, 1,2 Xianyun Wang, 3 and Liqing Wang 1 1 College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China 2 College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China 3 Shanghai National Engineering Research Center of Urban Water Resources Co., Ltd., Shanghai 200082, China Correspondence should be addressed to Gaohua Ji; [email protected] Received 17 April 2013; Accepted 13 May 2013 Academic Editors: B. B. Castro and S. Nautiyal Copyright © 2013 Gaohua Ji et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Changes in the density and species composition of planktonic rotifers as well as their relationship to several environmental variables were studied at Dadian Lake, a shallow subtropical lake, which was completely dredged and reconstructed. Samples were taken monthly (2006–2009) at five stations. e total rotifer abundance exponentially declined and reached a relatively stable stage in 2009. Polyarthra dolichoptera and Trichocerca pusilla dominated the rotifer community in most seasons. TN, TP, and COD Mn went down at the beginning of the monitoring period, rebounded in the second winter, and then decreased and reached a stable state in 2009. CCA showed that the most significant variations were caused by fluctuations in temperature, COD Mn , SRP, and NO 2 -N. e rotifer community experienced a two-stage succession and the difference of species between the stages was exhibited during warm seasons. GAMs indicated that the selected factors were responsible for 64.8% of the total rotifer abundance variance and 16.564.3% of the variances of individual species abundance. Most of the environmental parameters had effects on rotifer abundance that could only be described by complicated curves, characterised by unimodality and bimodality instead of linearity. Our study highlighted the temperature influence on rotifer species composition and total abundance in subtropical lakes. 1. Introduction In aquatic ecosystems, among the earliest responses to stress are changes in the species composition of small, rapidly reproducing species with wide dispersal powers [1]. Zoo- plankton is composed of organisms with high environmental sensitivity, which can be used as bioindicators of environ- mental changes [2]. Rotifers are small animals and react faster to changes in water conditions than other zoological groups of freshwater zooplankton due to their short development cycle ( strategists). ey are considered to be the most sensitive group to physical and chemical environmental changes [3]. Many studies have focused on rotifer response to abiotic factors, and some have tried to establish one-to-one causal relationships between rotifer composition and trophic con- ditions [411]. Most of these studies have either explored relationships between rotifers and environmental factors based on linear models or studied the distribution of species using redundancy analysis (RDA) [12, 13]. However, (gen- eralised) linear models are not the most adequate models for rotifer abundance-environmental factor processes. Castro et al. studies rotifer community structure in three shallow lakes using correspondence analysis (CCA), which assumes a unimodal response model to environmental gradients [4]. e use of CCA in community ordination deserves more attention. e generalised additive model (GAM) is an extension of the generalised linear model [14]. e advantage of the GAM lies in its adaptability for nonnormally distributing variables. As a flexible and effective technique for dealing with nonlinear relationships between the response and the set of explanatory variables, it is less restrictive in its assumptions concerning the underlying distribution of data. e model

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Page 1: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

Hindawi Publishing CorporationThe Scientific World JournalVolume 2013 Article ID 702942 14 pageshttpdxdoiorg1011552013702942

Research ArticlePlanktonic Rotifers in a Subtropical Shallow LakeSuccession Relationship to Environmental Factors andUse as Bioindicators

Gaohua Ji12 Xianyun Wang3 and Liqing Wang1

1 College of Fisheries and Life Science Shanghai Ocean University Shanghai 201306 China2 College of Environmental Science and Engineering Tongji University Shanghai 200092 China3 Shanghai National Engineering Research Center of Urban Water Resources Co Ltd Shanghai 200082 China

Correspondence should be addressed to Gaohua Ji ghjishoueducn

Received 17 April 2013 Accepted 13 May 2013

Academic Editors B B Castro and S Nautiyal

Copyright copy 2013 Gaohua Ji et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Changes in the density and species composition of planktonic rotifers as well as their relationship to several environmental variableswere studied at Dadian Lake a shallow subtropical lake which was completely dredged and reconstructed Samples were takenmonthly (2006ndash2009) at five stations The total rotifer abundance exponentially declined and reached a relatively stable stage in2009 Polyarthra dolichoptera and Trichocerca pusilla dominated the rotifer community in most seasons TN TP and CODMn wentdown at the beginning of the monitoring period rebounded in the second winter and then decreased and reached a stable state in2009 CCA showed that the most significant variations were caused by fluctuations in temperature CODMn SRP and NO2-NTherotifer community experienced a two-stage succession and the difference of species between the stages was exhibited during warmseasons GAMs indicated that the selected factors were responsible for 648 of the total rotifer abundance variance and 165sim643of the variances of individual species abundance Most of the environmental parameters had effects on rotifer abundance that couldonly be described by complicated curves characterised by unimodality and bimodality instead of linearity Our study highlightedthe temperature influence on rotifer species composition and total abundance in subtropical lakes

1 Introduction

In aquatic ecosystems among the earliest responses to stressare changes in the species composition of small rapidlyreproducing species with wide dispersal powers [1] Zoo-plankton is composed of organisms with high environmentalsensitivity which can be used as bioindicators of environ-mental changes [2] Rotifers are small animals and react fasterto changes in water conditions than other zoological groupsof freshwater zooplankton due to their short developmentcycle (119903 strategists) They are considered to be the mostsensitive group to physical and chemical environmentalchanges [3]

Many studies have focused on rotifer response to abioticfactors and some have tried to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions [4ndash11] Most of these studies have either explored

relationships between rotifers and environmental factorsbased on linear models or studied the distribution of speciesusing redundancy analysis (RDA) [12 13] However (gen-eralised) linear models are not the most adequate modelsfor rotifer abundance-environmental factor processes Castroet al studies rotifer community structure in three shallowlakes using correspondence analysis (CCA) which assumesa unimodal response model to environmental gradients [4]The use of CCA in community ordination deserves moreattention

The generalised additive model (GAM) is an extensionof the generalised linear model [14] The advantage of theGAM lies in its adaptability for nonnormally distributingvariables As a flexible and effective technique for dealingwithnonlinear relationships between the response and the set ofexplanatory variables it is less restrictive in its assumptionsconcerning the underlying distribution of data The model

2 The Scientific World Journal

0 200

Taihu Lake

East China Sea

East China Sea

Yangtze River

CHINA

Villa

Hotel

Dadian Lake

S4

S1

S2

S3

S5

N

S

W E

Villa

Shanghai

400

(m)

31∘07998400N

31∘0799840015998400998400

N31∘0799840030998400998400

N

120∘02

99840045

998400998400E 120∘03

998400E 120∘03

99840015

998400998400E

Yangtze River

Figure 1 Location of Dadian Lake China and the sampling stations

assumes that the dependent variable is dependent on theunivariate smooth terms of the independent variables ratherthan the independent variables themselves [15] The basicGAMmodel used for this study follows this formula

119892 (119884 | 119883

1 119883

2 119883

119901)

= 120572 + 119891

1(119883

1) + 119891

2(119883

2) + sdot sdot sdot + 119891

119901(119883

119901)

(1)

where 119892(sdot) is a link function and 119891119894(119883

119894) 119894 = 1 2 119901

are nonparametric smooth functions (smoothing spline) forindependent variable 119883

119894 The function 119891

119894is estimated in a

flexible manner and does not have to be nonlinear for allindependent variables in the GAM The model is a usefulscientific tool applied in many scientific fields [15ndash18]

In this study the physicochemical and biological charac-teristics of a shallow sediment-dredged lake were investigatedover a period of four years GAMs as well as other statisticalanalyses were conducted to (a) test the hypotheses thatit would take a long time for the rotifer community toreach a relatively stable state after sediment dredging inthe lake and that rotifer diversity indices could reflect thetrophic states and (b) investigate the way that environmental

factors affected the rotifer abundance (including the total andindividual species abundance) and species compositions

2 Materials and Methods

21 Study Area Dadian Lake (31∘071015840N 120∘031015840E) is locatedin the lower reaches of the Yangtze River (Figure 1) in ChinaIt is a small subtropical shallow and freshwater lake withan area of 50 ha The average and maximum depths are30m and 40m respectively The lake surface is 256mabove sea level The hydraulic residence time of the lakeis more than 05 years There are hotels restaurants andvillas nearby and there are typically yachts on the lakeThe lake was previously used for aquaculture thus before2005 cyanobacterial blooms occurred frequently during thesummer due to nutrient enrichment from fish aquaculture

The lake was drained completely insolated and dredgedfrom July 2005 to May 2006 Dredged silt from the lakewas heaped to construct islands in the southern lake Thelakeshore was also reconstructed and consolidated Afterthe comprehensive improvement the lake was refilled withwater from the northwest river essentially making it a newlyconstructed lake Meanwhile submerged macrophytes were

The Scientific World Journal 3

planted in the lake from May to July 2006 The macrophyteswere limited to the littoral zone during our study which com-prised an area of ca 15 of the lake The lake was protectedand less affected by anthropogenic activities thereafter

22 Sampling Samples were taken monthly from July 2006to Dec 2009 at five stations (Figure 1) Depth-integratedsamples were obtained from mixed water collected from thebottom to the surface at an interval of 05m using a modified5-l sampler for water and zooplankton analysis Chemicalparameters including total nitrogen (TN) nitrite nitrogen(NO2-N) nitrate nitrogen (NO

3-N) total phosphorus (TP)

soluble reactive phosphorus (SRP) and chlorophyll a (chla)were measured for each sample using standard methods[19] Ammonium-nitrogen (NH

4-N) and the potassium

permanganate index (CODMn) were determined using thenesslerisation and potassium permanganate index methodsrespectively [20] Temperature (Tem) was determined usinga mercury thermometer

For qualitative analyses rotifer samples were collected byvertical hauls using a 50 120583m mesh net with a reducing coneSpecies were identified according to [21 22] For quantitativeanalyses the sedimentation method was used to concentrate1 litre of a depth-integrated sample Counting was performedunder a microscope in a 1mL Sedgwick-Rafter chamber [23]

Crustacean samples were collected by vertical haulsfor qualitative analyses and by filtering 20 litres of depth-integrated water through a 50120583m mesh net for quantitativeanalyses [13] The entire sample was counted under a micro-scope Juvenile (nauplii and copepodite) copepods were alsocounted but only the copepodite and adult were included inthe total copepod density Crustaceans were recorded fromJuly 2006 to Oct 2007 and from Jan 2009 to Dec 2009

23 Data Analysis The Shannon-Wiener index (1198671015840) Pieloursquosevenness index (119869) and Margalef rsquos index (119863Mg) were cal-culated using the formulas 1198671015840 = minus119875

119894Σ log2119875

119894 119869 = 1198671015840

log2119878 and 119863Mg = (119878 minus 1) ln119873 where 119875119894 is the proportion

of individuals belonging to the 119894th species 119878 is the number ofspecies in the sample and119873 is the density of all species in thesample [12 24]

Notched box plots were used to detect the differencesbetween the seasonal rotifer densities If the notches fortwo medians do not overlap in the display the medians areapproximately significantly different at about a 95 confi-dence level [25]The notched box plots were provided byOri-gin 85 (OriginLab Corporation Northampton MA USA)

CCA was used to reduce the data dimensionality andidentify themain variables affecting rotifer community struc-ture We opted for a unimodal model of ordination insteadof a linear one because the GAMs showed the nonlineareffects of environmental factors on rotifers Even thoughthe preliminary DCA (detrended correspondence analysis)showed a short gradient length on the biological data (SD =196) we were still able to use CCA [26] To reduce theinfluence of spatial variability the species and environmen-tal data were averaged for each sampling occasion Thisresulted in 35 samples with 26 main species (comprising

gt5 in more than three samples before averaging) Forthis analysis we used the rotifer species and the values ofabiotic variables and chlorophyll a (log-transformed data)The statistical significance of the first and all the ordinationaxes was tested using a Monte Carlo permutation test (4999unrestricted permutations) CCA and DCA were conductedusing CANOCO for windows 45 (Biometris-Plant ResearchInternational Wageningen The Netherlands)

GAM was used to assess the effects of the environ-mental factors on rotifer densities A preliminary step-wiseGAM was performed to determine the best-fitting modelThe response variable in the model was the log (119909 + 1)-transformed rotifer density (total or individual species pre-sented in more than 18 samples) and the explanatory vari-ables were abiotic factors and chla GAM analysis and plotswere performed using S-PLUS 80 (Insightful CorporationSeattle WA USA) Considering that crustacean (copepodand cladoceran) records were not complete and that theypresented themselves in extremely low densities in coldseasons they were not included in GAM analysis Pearsonpartial correlation analysis was performed between rotifercladoceran and copepod using the PROC CORR procedureof SAS 91 (SAS Institute Incorporated Cary NC USA)

3 Results

31 Abiotic Parameters All of the abiotic parameters fluctu-ated strongly during the study period (Figure 2) The highestwater temperature was 32∘C and the lowest was 36∘C TNand TP were similar in the seasonal dynamics (119877 = 055119875 lt 00001) They decreased shortly after lake refilling andincreased in the next year with the highest value occurringduring the 2nd winter (TN 406mg Lminus1 TP 025mg Lminus1on average) In the 3rd and 4th years there was a decliningtrend from spring to winter The lowest TN values were 060(2nd winter) and 074mg Lminus1 (4th winter) and the lowest TPvalue was 0043mg Lminus1 (4th winter) CODMn also reboundedduring the 2nd winter and it declined overall without anydistinctive pattern

The monthly average and maximum and minimum val-ues for NH

4-N NO

2-N NO

3-N and SRP were 058 (0018ndash

218) 0049 (00023ndash0206) 028 (0012ndash0892) and 0021(00035-0083)mg Lminus1 respectively NH

4-N and SRP peaked

in the 2nd winter and NO2-N peaked in the 3rd and 4th

winters

32 Rotifers A total of 91 rotifer species belonging to 18families and 29 generawere recorded during the study periodincluding 26 abundant species (comprising gt5 in morethan three samples) (Table 1) The total species numbers ofBrachionus Keratella and Trichocerca accounted for nearlyhalf of the abundant species Species richness was relativelylow in winter

The rotifer community varied with the season Polyarthradolichoptera was classified as superdominant (seasonal rel-ative abundance gt30) while Tr pusilla was eudominant(gt10) in most seasons (Figure 3)They accounted for 463of the total rotifer abundance on average Tr pusilla and Bcalyciflorus were superdominant in the 3rd summer and in

4 The Scientific World Journal

Jul Jan Jul Jan Jul Jan Jul0

5

10

15

20

25

30

35

4th year3rd year2nd year1st year

Tem

(∘C)

(a)

25

75

50

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

1

2

3

4

5

6

4th year3rd year2nd year1st year

Lowest

Highest

Mean

TN (m

g Lminus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

01

02

03

04

05

4th year3rd year2nd year1st year

TP (m

g Lminus1)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

5

10

15

20

4th year3rd year2nd year1st year

COD

Mn

(mg L

minus1)

(d)

Figure 2 Seasonal dynamics of Tem TN TP and CODMn in Dadian Lake from 2006 to 2009 Outliers (gt1198763+15Δ119876 or lt1198761minus15Δ119876 Δ119876 =1198763 minus 1198761) are not shown in the plots Sp spring (from Mar to May) Su summer (from June to Aug) Au autumn (from Sep to Nov) Wiwinter (from Dem to Feb) No data were recorded in the 2nd autumn except for Tem

the 4th winter respectively B forficula Cephalodella inquilaK valga K ticinensis Lecane elachis and Tr Longiseta wereeudominant in the seasons of the 1st and 2nd years andAsplanchna priodonta Hexarthra mira K quadrata Kcochlearis and Dicranophorus forcipatus were eudominant inthe seasons of the 3rd and 4th years Anuraeopsis fissa waseudominant in autumn except for autumn of the 4th yearIt is noticeable that An fissa B forficula and L elachis wereeudominant but P dolichoptera was not eudominant in the2nd summer

The total rotifer density exhibited a clear decrease from2006 to 2009 The equation describing this is ln (rotiferdensity) = 839 minus 0171 t (119877 = 08789 119875 lt 0001) (Figure 4)The density was very high and fluctuated greatly in the 1st and2nd years but decreased in the 3rd and 4th years and becamemore stable The rotifer densities in each season of the 4thyear were lower than those in the 1st or 2nd year (120572 = 005)The highest density occurred in spring or summer and thelowest occurred in winter within one year

33 Biotic Parameters Chlorophyll a showed a similar pat-tern to TN and TP that is it decreased in the 1st year thenincreased and decreased again during the 3rd and 4th yearsHowever Pearson correlation analysis revealed that there wasno significant relationship between chla and TN or TP Thehighest seasonal chla was 453mgmminus3 (1st summer) and thelowest was 45mgmminus3 (4th winter)

Cladoceran and copepod densities were found to be ext-remely low except in the summer and autumn during thestudy period The main cladoceran species were Diaphan-osoma dubium and Bosmina spp (B longirostris and B core-goni) both in 2006-2007 and 2009 while Bosminopsis deitersiand Moina spp (M micrura Moina brachiata) appearedin large numbers in 2009 The copepods mainly consistedof Cyclopoida (Thermocyclops spp) which is a carnivorousspecies both in 2006-2007 and 2009 Cladoceran peaked inthe 4th summer (39 ind Lminus1) while the highest copepod den-sity occurred shortly after the lake was refilled (1st summer88 ind Lminus1) Cladoceran density was negatively correlated

The Scientific World Journal 5

Table 1 Abundant species in Dadian Lake from 2006 to 2009 (inabundance order)

Rotifer species AbbreviationsPolyarthra dolichoptera Idelson 1925 P dolicTrichocerca pusilla (Jennings 1903) Tr pusiAnuraeopsis fissa Gosse 1851 An fssaKeratella valga (Ehrenberg 1834) K valgaBrachionus angularis Gosse 1851 B angulAsplanchna priodonta Gosse 1850 As prioK ticinensis (Callerio 1921) K ticinB calyciflorus Pallas 1766 B calycFilinia longiseta (Ehrenberg 1834) F longiK cochlearis (Gosse 1851) K cochlB forficulaWierzejski 1891 B forfiCephalodella inquilinaMyers 1924 Ce inquK quadrata (Muller 1786) K quadrAscomorpha saltans Bartsch 1870 Asc saltB diversicornis (Daday 1883) B diverHexarthra mira (Hudson 1871) H miraLecane elachis (Harring amp Myers 1926) L elachT longiseta (Schrank 1802) Tr longEpiphanes senta (Muller 1773) E sentaB budapestinensis Daday 1885 B budapConochilus hippocrepis (Schrank 1803) Co hippF passa (Muller 1786) F passaF terminalis (Plate 1886) F termiL cornuta (Muller 1786) L cornuPompholyx complanata Gosse 1851 Po compT inermis (Linder 1904) Tr iner

with the rotifer population (119877 = minus0223 119875 = 00083 119899 =140) while copepod density was positively associated with it(119877 = 0235 119875 = 00053 119899 = 140)

34 Statistical Analysis The first two ordination axesexplained 241 of the variance of the species data in CCA(Figure 5) Forward selection and associated Monte Carlopermutation tests of the significance of the environmentalvariables (Table 2) indicated that Tem NO

2-N SRP CODMn

and NO3-N accounted for most of the variation in species

distribution when considered by themselves (120582-1) After theaddition of Tem to the ordination only NO

2-N accounted for

any significant amount of the remaining variation (119875 lt 005)(120582-A) The ten variables in Table 2 explained 559 of thetotal variance in the species data Tem chla and CODMnwere negatively associated with axis 1 but NO

3-N and TN

were positively associated with axis 1 NO2-N TP and Tem

were positively associated with axis 2 and CODMn wasnegatively associated with axis 2

The CCA revealed four main groups of species Someof the abundant species for example Tr inermis B for-ficula and Ce inquilina preferred high Tem and CODMn(Figure 5(a) bottom-left quadrant) and they mostly pre-sented themselves in warm seasons during the first two years

Su Au Wi Sp Su Au Sp Su Au Wi Sp Su Au Wi0

20

40

60

80

100

Relat

ive a

bund

ance

()

OthersAsp priodontaK ticinensisK valga

B calyciflorusAn fissaTr pusillaP dolichoptera

4th year3rd year2nd year1st year

Figure 3 Seasonal variations of the relative abundance of the mostrepresentative rotifer species (average relative abundancegt3) from2006 to 2009 in Dadian Lake (no data recorded during the 2ndwinter)

Table 2 Results of forward selection andMonte Carlo permutationtests from CCA of rotifer species Environmental variables are listedby the order of their inclusion in the model (120582-A)

Factors 120582-1 120582-A 119875(120582-1) 119875(120582-A)Tem 0145 0145 00002 00002

NO2-N 0104 0107 00006 00002

SRP 0057 0047 0068 0075

CODMn 0075 0046 0008 0084

NO3-N 0108 0045 00006 0089

TP 0043 0038 029 020

Chla 0053 003 0112 046

NP 0041 0037 036 023

NH4-N 0034 0029 055 047

TN 0062 0035 005 028

(Figure 5(b) bottom-left quadrant)Hmira E senta andCohippocrepis preferred high NO

2-N and low CODMn and were

abundant in warm seasons of the last two years K quadrataF passa and B calyciflorus populations grew in cold seasonAs priodonta and other species preferred warm temperatureand occurred in every year of the study

The CCA also showed that the rotifer community expe-rienced a two-stage succession (Figure 5(b)) The differencebetween the stages was exhibited duringwarm seasons In thefirst stage the rotifer community wasmainly composed of Pocomplanata Ce inquilina and other species In the secondstage H mira Co hippocrepis E senta and other speciesdominated the communityThere were also some species thatoccurred throughout the study period such as P dolichopteraand K valga In the cold seasons the species in the rotifercommunity were similar in different stages

The best general additive models (GAMs) determinedusing a stepwise procedure are shown in Table 3 The envi-ronmental factors selected by the procedure differed greatly

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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ClimatologyJournal of

Page 2: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

2 The Scientific World Journal

0 200

Taihu Lake

East China Sea

East China Sea

Yangtze River

CHINA

Villa

Hotel

Dadian Lake

S4

S1

S2

S3

S5

N

S

W E

Villa

Shanghai

400

(m)

31∘07998400N

31∘0799840015998400998400

N31∘0799840030998400998400

N

120∘02

99840045

998400998400E 120∘03

998400E 120∘03

99840015

998400998400E

Yangtze River

Figure 1 Location of Dadian Lake China and the sampling stations

assumes that the dependent variable is dependent on theunivariate smooth terms of the independent variables ratherthan the independent variables themselves [15] The basicGAMmodel used for this study follows this formula

119892 (119884 | 119883

1 119883

2 119883

119901)

= 120572 + 119891

1(119883

1) + 119891

2(119883

2) + sdot sdot sdot + 119891

119901(119883

119901)

(1)

where 119892(sdot) is a link function and 119891119894(119883

119894) 119894 = 1 2 119901

are nonparametric smooth functions (smoothing spline) forindependent variable 119883

119894 The function 119891

119894is estimated in a

flexible manner and does not have to be nonlinear for allindependent variables in the GAM The model is a usefulscientific tool applied in many scientific fields [15ndash18]

In this study the physicochemical and biological charac-teristics of a shallow sediment-dredged lake were investigatedover a period of four years GAMs as well as other statisticalanalyses were conducted to (a) test the hypotheses thatit would take a long time for the rotifer community toreach a relatively stable state after sediment dredging inthe lake and that rotifer diversity indices could reflect thetrophic states and (b) investigate the way that environmental

factors affected the rotifer abundance (including the total andindividual species abundance) and species compositions

2 Materials and Methods

21 Study Area Dadian Lake (31∘071015840N 120∘031015840E) is locatedin the lower reaches of the Yangtze River (Figure 1) in ChinaIt is a small subtropical shallow and freshwater lake withan area of 50 ha The average and maximum depths are30m and 40m respectively The lake surface is 256mabove sea level The hydraulic residence time of the lakeis more than 05 years There are hotels restaurants andvillas nearby and there are typically yachts on the lakeThe lake was previously used for aquaculture thus before2005 cyanobacterial blooms occurred frequently during thesummer due to nutrient enrichment from fish aquaculture

The lake was drained completely insolated and dredgedfrom July 2005 to May 2006 Dredged silt from the lakewas heaped to construct islands in the southern lake Thelakeshore was also reconstructed and consolidated Afterthe comprehensive improvement the lake was refilled withwater from the northwest river essentially making it a newlyconstructed lake Meanwhile submerged macrophytes were

The Scientific World Journal 3

planted in the lake from May to July 2006 The macrophyteswere limited to the littoral zone during our study which com-prised an area of ca 15 of the lake The lake was protectedand less affected by anthropogenic activities thereafter

22 Sampling Samples were taken monthly from July 2006to Dec 2009 at five stations (Figure 1) Depth-integratedsamples were obtained from mixed water collected from thebottom to the surface at an interval of 05m using a modified5-l sampler for water and zooplankton analysis Chemicalparameters including total nitrogen (TN) nitrite nitrogen(NO2-N) nitrate nitrogen (NO

3-N) total phosphorus (TP)

soluble reactive phosphorus (SRP) and chlorophyll a (chla)were measured for each sample using standard methods[19] Ammonium-nitrogen (NH

4-N) and the potassium

permanganate index (CODMn) were determined using thenesslerisation and potassium permanganate index methodsrespectively [20] Temperature (Tem) was determined usinga mercury thermometer

For qualitative analyses rotifer samples were collected byvertical hauls using a 50 120583m mesh net with a reducing coneSpecies were identified according to [21 22] For quantitativeanalyses the sedimentation method was used to concentrate1 litre of a depth-integrated sample Counting was performedunder a microscope in a 1mL Sedgwick-Rafter chamber [23]

Crustacean samples were collected by vertical haulsfor qualitative analyses and by filtering 20 litres of depth-integrated water through a 50120583m mesh net for quantitativeanalyses [13] The entire sample was counted under a micro-scope Juvenile (nauplii and copepodite) copepods were alsocounted but only the copepodite and adult were included inthe total copepod density Crustaceans were recorded fromJuly 2006 to Oct 2007 and from Jan 2009 to Dec 2009

23 Data Analysis The Shannon-Wiener index (1198671015840) Pieloursquosevenness index (119869) and Margalef rsquos index (119863Mg) were cal-culated using the formulas 1198671015840 = minus119875

119894Σ log2119875

119894 119869 = 1198671015840

log2119878 and 119863Mg = (119878 minus 1) ln119873 where 119875119894 is the proportion

of individuals belonging to the 119894th species 119878 is the number ofspecies in the sample and119873 is the density of all species in thesample [12 24]

Notched box plots were used to detect the differencesbetween the seasonal rotifer densities If the notches fortwo medians do not overlap in the display the medians areapproximately significantly different at about a 95 confi-dence level [25]The notched box plots were provided byOri-gin 85 (OriginLab Corporation Northampton MA USA)

CCA was used to reduce the data dimensionality andidentify themain variables affecting rotifer community struc-ture We opted for a unimodal model of ordination insteadof a linear one because the GAMs showed the nonlineareffects of environmental factors on rotifers Even thoughthe preliminary DCA (detrended correspondence analysis)showed a short gradient length on the biological data (SD =196) we were still able to use CCA [26] To reduce theinfluence of spatial variability the species and environmen-tal data were averaged for each sampling occasion Thisresulted in 35 samples with 26 main species (comprising

gt5 in more than three samples before averaging) Forthis analysis we used the rotifer species and the values ofabiotic variables and chlorophyll a (log-transformed data)The statistical significance of the first and all the ordinationaxes was tested using a Monte Carlo permutation test (4999unrestricted permutations) CCA and DCA were conductedusing CANOCO for windows 45 (Biometris-Plant ResearchInternational Wageningen The Netherlands)

GAM was used to assess the effects of the environ-mental factors on rotifer densities A preliminary step-wiseGAM was performed to determine the best-fitting modelThe response variable in the model was the log (119909 + 1)-transformed rotifer density (total or individual species pre-sented in more than 18 samples) and the explanatory vari-ables were abiotic factors and chla GAM analysis and plotswere performed using S-PLUS 80 (Insightful CorporationSeattle WA USA) Considering that crustacean (copepodand cladoceran) records were not complete and that theypresented themselves in extremely low densities in coldseasons they were not included in GAM analysis Pearsonpartial correlation analysis was performed between rotifercladoceran and copepod using the PROC CORR procedureof SAS 91 (SAS Institute Incorporated Cary NC USA)

3 Results

31 Abiotic Parameters All of the abiotic parameters fluctu-ated strongly during the study period (Figure 2) The highestwater temperature was 32∘C and the lowest was 36∘C TNand TP were similar in the seasonal dynamics (119877 = 055119875 lt 00001) They decreased shortly after lake refilling andincreased in the next year with the highest value occurringduring the 2nd winter (TN 406mg Lminus1 TP 025mg Lminus1on average) In the 3rd and 4th years there was a decliningtrend from spring to winter The lowest TN values were 060(2nd winter) and 074mg Lminus1 (4th winter) and the lowest TPvalue was 0043mg Lminus1 (4th winter) CODMn also reboundedduring the 2nd winter and it declined overall without anydistinctive pattern

The monthly average and maximum and minimum val-ues for NH

4-N NO

2-N NO

3-N and SRP were 058 (0018ndash

218) 0049 (00023ndash0206) 028 (0012ndash0892) and 0021(00035-0083)mg Lminus1 respectively NH

4-N and SRP peaked

in the 2nd winter and NO2-N peaked in the 3rd and 4th

winters

32 Rotifers A total of 91 rotifer species belonging to 18families and 29 generawere recorded during the study periodincluding 26 abundant species (comprising gt5 in morethan three samples) (Table 1) The total species numbers ofBrachionus Keratella and Trichocerca accounted for nearlyhalf of the abundant species Species richness was relativelylow in winter

The rotifer community varied with the season Polyarthradolichoptera was classified as superdominant (seasonal rel-ative abundance gt30) while Tr pusilla was eudominant(gt10) in most seasons (Figure 3)They accounted for 463of the total rotifer abundance on average Tr pusilla and Bcalyciflorus were superdominant in the 3rd summer and in

4 The Scientific World Journal

Jul Jan Jul Jan Jul Jan Jul0

5

10

15

20

25

30

35

4th year3rd year2nd year1st year

Tem

(∘C)

(a)

25

75

50

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

1

2

3

4

5

6

4th year3rd year2nd year1st year

Lowest

Highest

Mean

TN (m

g Lminus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

01

02

03

04

05

4th year3rd year2nd year1st year

TP (m

g Lminus1)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

5

10

15

20

4th year3rd year2nd year1st year

COD

Mn

(mg L

minus1)

(d)

Figure 2 Seasonal dynamics of Tem TN TP and CODMn in Dadian Lake from 2006 to 2009 Outliers (gt1198763+15Δ119876 or lt1198761minus15Δ119876 Δ119876 =1198763 minus 1198761) are not shown in the plots Sp spring (from Mar to May) Su summer (from June to Aug) Au autumn (from Sep to Nov) Wiwinter (from Dem to Feb) No data were recorded in the 2nd autumn except for Tem

the 4th winter respectively B forficula Cephalodella inquilaK valga K ticinensis Lecane elachis and Tr Longiseta wereeudominant in the seasons of the 1st and 2nd years andAsplanchna priodonta Hexarthra mira K quadrata Kcochlearis and Dicranophorus forcipatus were eudominant inthe seasons of the 3rd and 4th years Anuraeopsis fissa waseudominant in autumn except for autumn of the 4th yearIt is noticeable that An fissa B forficula and L elachis wereeudominant but P dolichoptera was not eudominant in the2nd summer

The total rotifer density exhibited a clear decrease from2006 to 2009 The equation describing this is ln (rotiferdensity) = 839 minus 0171 t (119877 = 08789 119875 lt 0001) (Figure 4)The density was very high and fluctuated greatly in the 1st and2nd years but decreased in the 3rd and 4th years and becamemore stable The rotifer densities in each season of the 4thyear were lower than those in the 1st or 2nd year (120572 = 005)The highest density occurred in spring or summer and thelowest occurred in winter within one year

33 Biotic Parameters Chlorophyll a showed a similar pat-tern to TN and TP that is it decreased in the 1st year thenincreased and decreased again during the 3rd and 4th yearsHowever Pearson correlation analysis revealed that there wasno significant relationship between chla and TN or TP Thehighest seasonal chla was 453mgmminus3 (1st summer) and thelowest was 45mgmminus3 (4th winter)

Cladoceran and copepod densities were found to be ext-remely low except in the summer and autumn during thestudy period The main cladoceran species were Diaphan-osoma dubium and Bosmina spp (B longirostris and B core-goni) both in 2006-2007 and 2009 while Bosminopsis deitersiand Moina spp (M micrura Moina brachiata) appearedin large numbers in 2009 The copepods mainly consistedof Cyclopoida (Thermocyclops spp) which is a carnivorousspecies both in 2006-2007 and 2009 Cladoceran peaked inthe 4th summer (39 ind Lminus1) while the highest copepod den-sity occurred shortly after the lake was refilled (1st summer88 ind Lminus1) Cladoceran density was negatively correlated

The Scientific World Journal 5

Table 1 Abundant species in Dadian Lake from 2006 to 2009 (inabundance order)

Rotifer species AbbreviationsPolyarthra dolichoptera Idelson 1925 P dolicTrichocerca pusilla (Jennings 1903) Tr pusiAnuraeopsis fissa Gosse 1851 An fssaKeratella valga (Ehrenberg 1834) K valgaBrachionus angularis Gosse 1851 B angulAsplanchna priodonta Gosse 1850 As prioK ticinensis (Callerio 1921) K ticinB calyciflorus Pallas 1766 B calycFilinia longiseta (Ehrenberg 1834) F longiK cochlearis (Gosse 1851) K cochlB forficulaWierzejski 1891 B forfiCephalodella inquilinaMyers 1924 Ce inquK quadrata (Muller 1786) K quadrAscomorpha saltans Bartsch 1870 Asc saltB diversicornis (Daday 1883) B diverHexarthra mira (Hudson 1871) H miraLecane elachis (Harring amp Myers 1926) L elachT longiseta (Schrank 1802) Tr longEpiphanes senta (Muller 1773) E sentaB budapestinensis Daday 1885 B budapConochilus hippocrepis (Schrank 1803) Co hippF passa (Muller 1786) F passaF terminalis (Plate 1886) F termiL cornuta (Muller 1786) L cornuPompholyx complanata Gosse 1851 Po compT inermis (Linder 1904) Tr iner

with the rotifer population (119877 = minus0223 119875 = 00083 119899 =140) while copepod density was positively associated with it(119877 = 0235 119875 = 00053 119899 = 140)

34 Statistical Analysis The first two ordination axesexplained 241 of the variance of the species data in CCA(Figure 5) Forward selection and associated Monte Carlopermutation tests of the significance of the environmentalvariables (Table 2) indicated that Tem NO

2-N SRP CODMn

and NO3-N accounted for most of the variation in species

distribution when considered by themselves (120582-1) After theaddition of Tem to the ordination only NO

2-N accounted for

any significant amount of the remaining variation (119875 lt 005)(120582-A) The ten variables in Table 2 explained 559 of thetotal variance in the species data Tem chla and CODMnwere negatively associated with axis 1 but NO

3-N and TN

were positively associated with axis 1 NO2-N TP and Tem

were positively associated with axis 2 and CODMn wasnegatively associated with axis 2

The CCA revealed four main groups of species Someof the abundant species for example Tr inermis B for-ficula and Ce inquilina preferred high Tem and CODMn(Figure 5(a) bottom-left quadrant) and they mostly pre-sented themselves in warm seasons during the first two years

Su Au Wi Sp Su Au Sp Su Au Wi Sp Su Au Wi0

20

40

60

80

100

Relat

ive a

bund

ance

()

OthersAsp priodontaK ticinensisK valga

B calyciflorusAn fissaTr pusillaP dolichoptera

4th year3rd year2nd year1st year

Figure 3 Seasonal variations of the relative abundance of the mostrepresentative rotifer species (average relative abundancegt3) from2006 to 2009 in Dadian Lake (no data recorded during the 2ndwinter)

Table 2 Results of forward selection andMonte Carlo permutationtests from CCA of rotifer species Environmental variables are listedby the order of their inclusion in the model (120582-A)

Factors 120582-1 120582-A 119875(120582-1) 119875(120582-A)Tem 0145 0145 00002 00002

NO2-N 0104 0107 00006 00002

SRP 0057 0047 0068 0075

CODMn 0075 0046 0008 0084

NO3-N 0108 0045 00006 0089

TP 0043 0038 029 020

Chla 0053 003 0112 046

NP 0041 0037 036 023

NH4-N 0034 0029 055 047

TN 0062 0035 005 028

(Figure 5(b) bottom-left quadrant)Hmira E senta andCohippocrepis preferred high NO

2-N and low CODMn and were

abundant in warm seasons of the last two years K quadrataF passa and B calyciflorus populations grew in cold seasonAs priodonta and other species preferred warm temperatureand occurred in every year of the study

The CCA also showed that the rotifer community expe-rienced a two-stage succession (Figure 5(b)) The differencebetween the stages was exhibited duringwarm seasons In thefirst stage the rotifer community wasmainly composed of Pocomplanata Ce inquilina and other species In the secondstage H mira Co hippocrepis E senta and other speciesdominated the communityThere were also some species thatoccurred throughout the study period such as P dolichopteraand K valga In the cold seasons the species in the rotifercommunity were similar in different stages

The best general additive models (GAMs) determinedusing a stepwise procedure are shown in Table 3 The envi-ronmental factors selected by the procedure differed greatly

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 3: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 3

planted in the lake from May to July 2006 The macrophyteswere limited to the littoral zone during our study which com-prised an area of ca 15 of the lake The lake was protectedand less affected by anthropogenic activities thereafter

22 Sampling Samples were taken monthly from July 2006to Dec 2009 at five stations (Figure 1) Depth-integratedsamples were obtained from mixed water collected from thebottom to the surface at an interval of 05m using a modified5-l sampler for water and zooplankton analysis Chemicalparameters including total nitrogen (TN) nitrite nitrogen(NO2-N) nitrate nitrogen (NO

3-N) total phosphorus (TP)

soluble reactive phosphorus (SRP) and chlorophyll a (chla)were measured for each sample using standard methods[19] Ammonium-nitrogen (NH

4-N) and the potassium

permanganate index (CODMn) were determined using thenesslerisation and potassium permanganate index methodsrespectively [20] Temperature (Tem) was determined usinga mercury thermometer

For qualitative analyses rotifer samples were collected byvertical hauls using a 50 120583m mesh net with a reducing coneSpecies were identified according to [21 22] For quantitativeanalyses the sedimentation method was used to concentrate1 litre of a depth-integrated sample Counting was performedunder a microscope in a 1mL Sedgwick-Rafter chamber [23]

Crustacean samples were collected by vertical haulsfor qualitative analyses and by filtering 20 litres of depth-integrated water through a 50120583m mesh net for quantitativeanalyses [13] The entire sample was counted under a micro-scope Juvenile (nauplii and copepodite) copepods were alsocounted but only the copepodite and adult were included inthe total copepod density Crustaceans were recorded fromJuly 2006 to Oct 2007 and from Jan 2009 to Dec 2009

23 Data Analysis The Shannon-Wiener index (1198671015840) Pieloursquosevenness index (119869) and Margalef rsquos index (119863Mg) were cal-culated using the formulas 1198671015840 = minus119875

119894Σ log2119875

119894 119869 = 1198671015840

log2119878 and 119863Mg = (119878 minus 1) ln119873 where 119875119894 is the proportion

of individuals belonging to the 119894th species 119878 is the number ofspecies in the sample and119873 is the density of all species in thesample [12 24]

Notched box plots were used to detect the differencesbetween the seasonal rotifer densities If the notches fortwo medians do not overlap in the display the medians areapproximately significantly different at about a 95 confi-dence level [25]The notched box plots were provided byOri-gin 85 (OriginLab Corporation Northampton MA USA)

CCA was used to reduce the data dimensionality andidentify themain variables affecting rotifer community struc-ture We opted for a unimodal model of ordination insteadof a linear one because the GAMs showed the nonlineareffects of environmental factors on rotifers Even thoughthe preliminary DCA (detrended correspondence analysis)showed a short gradient length on the biological data (SD =196) we were still able to use CCA [26] To reduce theinfluence of spatial variability the species and environmen-tal data were averaged for each sampling occasion Thisresulted in 35 samples with 26 main species (comprising

gt5 in more than three samples before averaging) Forthis analysis we used the rotifer species and the values ofabiotic variables and chlorophyll a (log-transformed data)The statistical significance of the first and all the ordinationaxes was tested using a Monte Carlo permutation test (4999unrestricted permutations) CCA and DCA were conductedusing CANOCO for windows 45 (Biometris-Plant ResearchInternational Wageningen The Netherlands)

GAM was used to assess the effects of the environ-mental factors on rotifer densities A preliminary step-wiseGAM was performed to determine the best-fitting modelThe response variable in the model was the log (119909 + 1)-transformed rotifer density (total or individual species pre-sented in more than 18 samples) and the explanatory vari-ables were abiotic factors and chla GAM analysis and plotswere performed using S-PLUS 80 (Insightful CorporationSeattle WA USA) Considering that crustacean (copepodand cladoceran) records were not complete and that theypresented themselves in extremely low densities in coldseasons they were not included in GAM analysis Pearsonpartial correlation analysis was performed between rotifercladoceran and copepod using the PROC CORR procedureof SAS 91 (SAS Institute Incorporated Cary NC USA)

3 Results

31 Abiotic Parameters All of the abiotic parameters fluctu-ated strongly during the study period (Figure 2) The highestwater temperature was 32∘C and the lowest was 36∘C TNand TP were similar in the seasonal dynamics (119877 = 055119875 lt 00001) They decreased shortly after lake refilling andincreased in the next year with the highest value occurringduring the 2nd winter (TN 406mg Lminus1 TP 025mg Lminus1on average) In the 3rd and 4th years there was a decliningtrend from spring to winter The lowest TN values were 060(2nd winter) and 074mg Lminus1 (4th winter) and the lowest TPvalue was 0043mg Lminus1 (4th winter) CODMn also reboundedduring the 2nd winter and it declined overall without anydistinctive pattern

The monthly average and maximum and minimum val-ues for NH

4-N NO

2-N NO

3-N and SRP were 058 (0018ndash

218) 0049 (00023ndash0206) 028 (0012ndash0892) and 0021(00035-0083)mg Lminus1 respectively NH

4-N and SRP peaked

in the 2nd winter and NO2-N peaked in the 3rd and 4th

winters

32 Rotifers A total of 91 rotifer species belonging to 18families and 29 generawere recorded during the study periodincluding 26 abundant species (comprising gt5 in morethan three samples) (Table 1) The total species numbers ofBrachionus Keratella and Trichocerca accounted for nearlyhalf of the abundant species Species richness was relativelylow in winter

The rotifer community varied with the season Polyarthradolichoptera was classified as superdominant (seasonal rel-ative abundance gt30) while Tr pusilla was eudominant(gt10) in most seasons (Figure 3)They accounted for 463of the total rotifer abundance on average Tr pusilla and Bcalyciflorus were superdominant in the 3rd summer and in

4 The Scientific World Journal

Jul Jan Jul Jan Jul Jan Jul0

5

10

15

20

25

30

35

4th year3rd year2nd year1st year

Tem

(∘C)

(a)

25

75

50

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

1

2

3

4

5

6

4th year3rd year2nd year1st year

Lowest

Highest

Mean

TN (m

g Lminus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

01

02

03

04

05

4th year3rd year2nd year1st year

TP (m

g Lminus1)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

5

10

15

20

4th year3rd year2nd year1st year

COD

Mn

(mg L

minus1)

(d)

Figure 2 Seasonal dynamics of Tem TN TP and CODMn in Dadian Lake from 2006 to 2009 Outliers (gt1198763+15Δ119876 or lt1198761minus15Δ119876 Δ119876 =1198763 minus 1198761) are not shown in the plots Sp spring (from Mar to May) Su summer (from June to Aug) Au autumn (from Sep to Nov) Wiwinter (from Dem to Feb) No data were recorded in the 2nd autumn except for Tem

the 4th winter respectively B forficula Cephalodella inquilaK valga K ticinensis Lecane elachis and Tr Longiseta wereeudominant in the seasons of the 1st and 2nd years andAsplanchna priodonta Hexarthra mira K quadrata Kcochlearis and Dicranophorus forcipatus were eudominant inthe seasons of the 3rd and 4th years Anuraeopsis fissa waseudominant in autumn except for autumn of the 4th yearIt is noticeable that An fissa B forficula and L elachis wereeudominant but P dolichoptera was not eudominant in the2nd summer

The total rotifer density exhibited a clear decrease from2006 to 2009 The equation describing this is ln (rotiferdensity) = 839 minus 0171 t (119877 = 08789 119875 lt 0001) (Figure 4)The density was very high and fluctuated greatly in the 1st and2nd years but decreased in the 3rd and 4th years and becamemore stable The rotifer densities in each season of the 4thyear were lower than those in the 1st or 2nd year (120572 = 005)The highest density occurred in spring or summer and thelowest occurred in winter within one year

33 Biotic Parameters Chlorophyll a showed a similar pat-tern to TN and TP that is it decreased in the 1st year thenincreased and decreased again during the 3rd and 4th yearsHowever Pearson correlation analysis revealed that there wasno significant relationship between chla and TN or TP Thehighest seasonal chla was 453mgmminus3 (1st summer) and thelowest was 45mgmminus3 (4th winter)

Cladoceran and copepod densities were found to be ext-remely low except in the summer and autumn during thestudy period The main cladoceran species were Diaphan-osoma dubium and Bosmina spp (B longirostris and B core-goni) both in 2006-2007 and 2009 while Bosminopsis deitersiand Moina spp (M micrura Moina brachiata) appearedin large numbers in 2009 The copepods mainly consistedof Cyclopoida (Thermocyclops spp) which is a carnivorousspecies both in 2006-2007 and 2009 Cladoceran peaked inthe 4th summer (39 ind Lminus1) while the highest copepod den-sity occurred shortly after the lake was refilled (1st summer88 ind Lminus1) Cladoceran density was negatively correlated

The Scientific World Journal 5

Table 1 Abundant species in Dadian Lake from 2006 to 2009 (inabundance order)

Rotifer species AbbreviationsPolyarthra dolichoptera Idelson 1925 P dolicTrichocerca pusilla (Jennings 1903) Tr pusiAnuraeopsis fissa Gosse 1851 An fssaKeratella valga (Ehrenberg 1834) K valgaBrachionus angularis Gosse 1851 B angulAsplanchna priodonta Gosse 1850 As prioK ticinensis (Callerio 1921) K ticinB calyciflorus Pallas 1766 B calycFilinia longiseta (Ehrenberg 1834) F longiK cochlearis (Gosse 1851) K cochlB forficulaWierzejski 1891 B forfiCephalodella inquilinaMyers 1924 Ce inquK quadrata (Muller 1786) K quadrAscomorpha saltans Bartsch 1870 Asc saltB diversicornis (Daday 1883) B diverHexarthra mira (Hudson 1871) H miraLecane elachis (Harring amp Myers 1926) L elachT longiseta (Schrank 1802) Tr longEpiphanes senta (Muller 1773) E sentaB budapestinensis Daday 1885 B budapConochilus hippocrepis (Schrank 1803) Co hippF passa (Muller 1786) F passaF terminalis (Plate 1886) F termiL cornuta (Muller 1786) L cornuPompholyx complanata Gosse 1851 Po compT inermis (Linder 1904) Tr iner

with the rotifer population (119877 = minus0223 119875 = 00083 119899 =140) while copepod density was positively associated with it(119877 = 0235 119875 = 00053 119899 = 140)

34 Statistical Analysis The first two ordination axesexplained 241 of the variance of the species data in CCA(Figure 5) Forward selection and associated Monte Carlopermutation tests of the significance of the environmentalvariables (Table 2) indicated that Tem NO

2-N SRP CODMn

and NO3-N accounted for most of the variation in species

distribution when considered by themselves (120582-1) After theaddition of Tem to the ordination only NO

2-N accounted for

any significant amount of the remaining variation (119875 lt 005)(120582-A) The ten variables in Table 2 explained 559 of thetotal variance in the species data Tem chla and CODMnwere negatively associated with axis 1 but NO

3-N and TN

were positively associated with axis 1 NO2-N TP and Tem

were positively associated with axis 2 and CODMn wasnegatively associated with axis 2

The CCA revealed four main groups of species Someof the abundant species for example Tr inermis B for-ficula and Ce inquilina preferred high Tem and CODMn(Figure 5(a) bottom-left quadrant) and they mostly pre-sented themselves in warm seasons during the first two years

Su Au Wi Sp Su Au Sp Su Au Wi Sp Su Au Wi0

20

40

60

80

100

Relat

ive a

bund

ance

()

OthersAsp priodontaK ticinensisK valga

B calyciflorusAn fissaTr pusillaP dolichoptera

4th year3rd year2nd year1st year

Figure 3 Seasonal variations of the relative abundance of the mostrepresentative rotifer species (average relative abundancegt3) from2006 to 2009 in Dadian Lake (no data recorded during the 2ndwinter)

Table 2 Results of forward selection andMonte Carlo permutationtests from CCA of rotifer species Environmental variables are listedby the order of their inclusion in the model (120582-A)

Factors 120582-1 120582-A 119875(120582-1) 119875(120582-A)Tem 0145 0145 00002 00002

NO2-N 0104 0107 00006 00002

SRP 0057 0047 0068 0075

CODMn 0075 0046 0008 0084

NO3-N 0108 0045 00006 0089

TP 0043 0038 029 020

Chla 0053 003 0112 046

NP 0041 0037 036 023

NH4-N 0034 0029 055 047

TN 0062 0035 005 028

(Figure 5(b) bottom-left quadrant)Hmira E senta andCohippocrepis preferred high NO

2-N and low CODMn and were

abundant in warm seasons of the last two years K quadrataF passa and B calyciflorus populations grew in cold seasonAs priodonta and other species preferred warm temperatureand occurred in every year of the study

The CCA also showed that the rotifer community expe-rienced a two-stage succession (Figure 5(b)) The differencebetween the stages was exhibited duringwarm seasons In thefirst stage the rotifer community wasmainly composed of Pocomplanata Ce inquilina and other species In the secondstage H mira Co hippocrepis E senta and other speciesdominated the communityThere were also some species thatoccurred throughout the study period such as P dolichopteraand K valga In the cold seasons the species in the rotifercommunity were similar in different stages

The best general additive models (GAMs) determinedusing a stepwise procedure are shown in Table 3 The envi-ronmental factors selected by the procedure differed greatly

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 4: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

4 The Scientific World Journal

Jul Jan Jul Jan Jul Jan Jul0

5

10

15

20

25

30

35

4th year3rd year2nd year1st year

Tem

(∘C)

(a)

25

75

50

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

1

2

3

4

5

6

4th year3rd year2nd year1st year

Lowest

Highest

Mean

TN (m

g Lminus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

01

02

03

04

05

4th year3rd year2nd year1st year

TP (m

g Lminus1)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

5

10

15

20

4th year3rd year2nd year1st year

COD

Mn

(mg L

minus1)

(d)

Figure 2 Seasonal dynamics of Tem TN TP and CODMn in Dadian Lake from 2006 to 2009 Outliers (gt1198763+15Δ119876 or lt1198761minus15Δ119876 Δ119876 =1198763 minus 1198761) are not shown in the plots Sp spring (from Mar to May) Su summer (from June to Aug) Au autumn (from Sep to Nov) Wiwinter (from Dem to Feb) No data were recorded in the 2nd autumn except for Tem

the 4th winter respectively B forficula Cephalodella inquilaK valga K ticinensis Lecane elachis and Tr Longiseta wereeudominant in the seasons of the 1st and 2nd years andAsplanchna priodonta Hexarthra mira K quadrata Kcochlearis and Dicranophorus forcipatus were eudominant inthe seasons of the 3rd and 4th years Anuraeopsis fissa waseudominant in autumn except for autumn of the 4th yearIt is noticeable that An fissa B forficula and L elachis wereeudominant but P dolichoptera was not eudominant in the2nd summer

The total rotifer density exhibited a clear decrease from2006 to 2009 The equation describing this is ln (rotiferdensity) = 839 minus 0171 t (119877 = 08789 119875 lt 0001) (Figure 4)The density was very high and fluctuated greatly in the 1st and2nd years but decreased in the 3rd and 4th years and becamemore stable The rotifer densities in each season of the 4thyear were lower than those in the 1st or 2nd year (120572 = 005)The highest density occurred in spring or summer and thelowest occurred in winter within one year

33 Biotic Parameters Chlorophyll a showed a similar pat-tern to TN and TP that is it decreased in the 1st year thenincreased and decreased again during the 3rd and 4th yearsHowever Pearson correlation analysis revealed that there wasno significant relationship between chla and TN or TP Thehighest seasonal chla was 453mgmminus3 (1st summer) and thelowest was 45mgmminus3 (4th winter)

Cladoceran and copepod densities were found to be ext-remely low except in the summer and autumn during thestudy period The main cladoceran species were Diaphan-osoma dubium and Bosmina spp (B longirostris and B core-goni) both in 2006-2007 and 2009 while Bosminopsis deitersiand Moina spp (M micrura Moina brachiata) appearedin large numbers in 2009 The copepods mainly consistedof Cyclopoida (Thermocyclops spp) which is a carnivorousspecies both in 2006-2007 and 2009 Cladoceran peaked inthe 4th summer (39 ind Lminus1) while the highest copepod den-sity occurred shortly after the lake was refilled (1st summer88 ind Lminus1) Cladoceran density was negatively correlated

The Scientific World Journal 5

Table 1 Abundant species in Dadian Lake from 2006 to 2009 (inabundance order)

Rotifer species AbbreviationsPolyarthra dolichoptera Idelson 1925 P dolicTrichocerca pusilla (Jennings 1903) Tr pusiAnuraeopsis fissa Gosse 1851 An fssaKeratella valga (Ehrenberg 1834) K valgaBrachionus angularis Gosse 1851 B angulAsplanchna priodonta Gosse 1850 As prioK ticinensis (Callerio 1921) K ticinB calyciflorus Pallas 1766 B calycFilinia longiseta (Ehrenberg 1834) F longiK cochlearis (Gosse 1851) K cochlB forficulaWierzejski 1891 B forfiCephalodella inquilinaMyers 1924 Ce inquK quadrata (Muller 1786) K quadrAscomorpha saltans Bartsch 1870 Asc saltB diversicornis (Daday 1883) B diverHexarthra mira (Hudson 1871) H miraLecane elachis (Harring amp Myers 1926) L elachT longiseta (Schrank 1802) Tr longEpiphanes senta (Muller 1773) E sentaB budapestinensis Daday 1885 B budapConochilus hippocrepis (Schrank 1803) Co hippF passa (Muller 1786) F passaF terminalis (Plate 1886) F termiL cornuta (Muller 1786) L cornuPompholyx complanata Gosse 1851 Po compT inermis (Linder 1904) Tr iner

with the rotifer population (119877 = minus0223 119875 = 00083 119899 =140) while copepod density was positively associated with it(119877 = 0235 119875 = 00053 119899 = 140)

34 Statistical Analysis The first two ordination axesexplained 241 of the variance of the species data in CCA(Figure 5) Forward selection and associated Monte Carlopermutation tests of the significance of the environmentalvariables (Table 2) indicated that Tem NO

2-N SRP CODMn

and NO3-N accounted for most of the variation in species

distribution when considered by themselves (120582-1) After theaddition of Tem to the ordination only NO

2-N accounted for

any significant amount of the remaining variation (119875 lt 005)(120582-A) The ten variables in Table 2 explained 559 of thetotal variance in the species data Tem chla and CODMnwere negatively associated with axis 1 but NO

3-N and TN

were positively associated with axis 1 NO2-N TP and Tem

were positively associated with axis 2 and CODMn wasnegatively associated with axis 2

The CCA revealed four main groups of species Someof the abundant species for example Tr inermis B for-ficula and Ce inquilina preferred high Tem and CODMn(Figure 5(a) bottom-left quadrant) and they mostly pre-sented themselves in warm seasons during the first two years

Su Au Wi Sp Su Au Sp Su Au Wi Sp Su Au Wi0

20

40

60

80

100

Relat

ive a

bund

ance

()

OthersAsp priodontaK ticinensisK valga

B calyciflorusAn fissaTr pusillaP dolichoptera

4th year3rd year2nd year1st year

Figure 3 Seasonal variations of the relative abundance of the mostrepresentative rotifer species (average relative abundancegt3) from2006 to 2009 in Dadian Lake (no data recorded during the 2ndwinter)

Table 2 Results of forward selection andMonte Carlo permutationtests from CCA of rotifer species Environmental variables are listedby the order of their inclusion in the model (120582-A)

Factors 120582-1 120582-A 119875(120582-1) 119875(120582-A)Tem 0145 0145 00002 00002

NO2-N 0104 0107 00006 00002

SRP 0057 0047 0068 0075

CODMn 0075 0046 0008 0084

NO3-N 0108 0045 00006 0089

TP 0043 0038 029 020

Chla 0053 003 0112 046

NP 0041 0037 036 023

NH4-N 0034 0029 055 047

TN 0062 0035 005 028

(Figure 5(b) bottom-left quadrant)Hmira E senta andCohippocrepis preferred high NO

2-N and low CODMn and were

abundant in warm seasons of the last two years K quadrataF passa and B calyciflorus populations grew in cold seasonAs priodonta and other species preferred warm temperatureand occurred in every year of the study

The CCA also showed that the rotifer community expe-rienced a two-stage succession (Figure 5(b)) The differencebetween the stages was exhibited duringwarm seasons In thefirst stage the rotifer community wasmainly composed of Pocomplanata Ce inquilina and other species In the secondstage H mira Co hippocrepis E senta and other speciesdominated the communityThere were also some species thatoccurred throughout the study period such as P dolichopteraand K valga In the cold seasons the species in the rotifercommunity were similar in different stages

The best general additive models (GAMs) determinedusing a stepwise procedure are shown in Table 3 The envi-ronmental factors selected by the procedure differed greatly

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 5: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 5

Table 1 Abundant species in Dadian Lake from 2006 to 2009 (inabundance order)

Rotifer species AbbreviationsPolyarthra dolichoptera Idelson 1925 P dolicTrichocerca pusilla (Jennings 1903) Tr pusiAnuraeopsis fissa Gosse 1851 An fssaKeratella valga (Ehrenberg 1834) K valgaBrachionus angularis Gosse 1851 B angulAsplanchna priodonta Gosse 1850 As prioK ticinensis (Callerio 1921) K ticinB calyciflorus Pallas 1766 B calycFilinia longiseta (Ehrenberg 1834) F longiK cochlearis (Gosse 1851) K cochlB forficulaWierzejski 1891 B forfiCephalodella inquilinaMyers 1924 Ce inquK quadrata (Muller 1786) K quadrAscomorpha saltans Bartsch 1870 Asc saltB diversicornis (Daday 1883) B diverHexarthra mira (Hudson 1871) H miraLecane elachis (Harring amp Myers 1926) L elachT longiseta (Schrank 1802) Tr longEpiphanes senta (Muller 1773) E sentaB budapestinensis Daday 1885 B budapConochilus hippocrepis (Schrank 1803) Co hippF passa (Muller 1786) F passaF terminalis (Plate 1886) F termiL cornuta (Muller 1786) L cornuPompholyx complanata Gosse 1851 Po compT inermis (Linder 1904) Tr iner

with the rotifer population (119877 = minus0223 119875 = 00083 119899 =140) while copepod density was positively associated with it(119877 = 0235 119875 = 00053 119899 = 140)

34 Statistical Analysis The first two ordination axesexplained 241 of the variance of the species data in CCA(Figure 5) Forward selection and associated Monte Carlopermutation tests of the significance of the environmentalvariables (Table 2) indicated that Tem NO

2-N SRP CODMn

and NO3-N accounted for most of the variation in species

distribution when considered by themselves (120582-1) After theaddition of Tem to the ordination only NO

2-N accounted for

any significant amount of the remaining variation (119875 lt 005)(120582-A) The ten variables in Table 2 explained 559 of thetotal variance in the species data Tem chla and CODMnwere negatively associated with axis 1 but NO

3-N and TN

were positively associated with axis 1 NO2-N TP and Tem

were positively associated with axis 2 and CODMn wasnegatively associated with axis 2

The CCA revealed four main groups of species Someof the abundant species for example Tr inermis B for-ficula and Ce inquilina preferred high Tem and CODMn(Figure 5(a) bottom-left quadrant) and they mostly pre-sented themselves in warm seasons during the first two years

Su Au Wi Sp Su Au Sp Su Au Wi Sp Su Au Wi0

20

40

60

80

100

Relat

ive a

bund

ance

()

OthersAsp priodontaK ticinensisK valga

B calyciflorusAn fissaTr pusillaP dolichoptera

4th year3rd year2nd year1st year

Figure 3 Seasonal variations of the relative abundance of the mostrepresentative rotifer species (average relative abundancegt3) from2006 to 2009 in Dadian Lake (no data recorded during the 2ndwinter)

Table 2 Results of forward selection andMonte Carlo permutationtests from CCA of rotifer species Environmental variables are listedby the order of their inclusion in the model (120582-A)

Factors 120582-1 120582-A 119875(120582-1) 119875(120582-A)Tem 0145 0145 00002 00002

NO2-N 0104 0107 00006 00002

SRP 0057 0047 0068 0075

CODMn 0075 0046 0008 0084

NO3-N 0108 0045 00006 0089

TP 0043 0038 029 020

Chla 0053 003 0112 046

NP 0041 0037 036 023

NH4-N 0034 0029 055 047

TN 0062 0035 005 028

(Figure 5(b) bottom-left quadrant)Hmira E senta andCohippocrepis preferred high NO

2-N and low CODMn and were

abundant in warm seasons of the last two years K quadrataF passa and B calyciflorus populations grew in cold seasonAs priodonta and other species preferred warm temperatureand occurred in every year of the study

The CCA also showed that the rotifer community expe-rienced a two-stage succession (Figure 5(b)) The differencebetween the stages was exhibited duringwarm seasons In thefirst stage the rotifer community wasmainly composed of Pocomplanata Ce inquilina and other species In the secondstage H mira Co hippocrepis E senta and other speciesdominated the communityThere were also some species thatoccurred throughout the study period such as P dolichopteraand K valga In the cold seasons the species in the rotifercommunity were similar in different stages

The best general additive models (GAMs) determinedusing a stepwise procedure are shown in Table 3 The envi-ronmental factors selected by the procedure differed greatly

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 6: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

6 The Scientific World Journal

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

2000

4000

6000

8000

75

LCI

Mean50

UCI

25

Highest

LowestRotie

r (in

dmiddotLminus

1)

(a)

25

75

50

Lowest

Highest

Mean

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

10

20

30

40

50

Clad

ocer

an (i

ndmiddotL

minus1)

(b)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi

0

20

40

60

80

100

120

4th year3rd year2nd year1st year

Chlo

roph

yll-a

(mg m

minus3)

(c)

Su Au Wi Sp Su Au Wi Sp Su Au Wi Sp Su Au Wi0

50

100

150

200

4th year3rd year2nd year1st year

Cope

poda

(ind

middotLminus1)

(d)

Figure 4 Seasonal variations of the total rotifer density and biotic parameters (chlorophyll a cladoceran and copepoda) LCI UCI lowerand upper bound of 95 confidence interval of median respectively (If the notches of two box plots do not overlap we can assume that thetwo median values differ at a 95 confidence level) No data were recorded for rotifers in the 2nd winter or for crustaceans in the 3rd year

Axis 1 1

Axis 2

1

P dolic

Tr pusil

An fissK valga

B angul

As prio

K ticin

B calycF longi

K cochlB forfic

Ce inquK quadr

As salt

B diver

H mira

L elach

Tr long

E senta

B budap

Co hipp

F passaF termi

L ornuPo comp

Tr inerChla

TNSRP

TPTem

NPNH4

NO2

NO3

CODMn

minus1

minus1

(a)

Chla

TNSRP

TPTem

NP

607

608609

610

611612

701702703

704 705706

707

708

803804805

806

808

809

810

811

812

901

902

903904

905

906

907

908

909

910

911912

NH3

NO2

NO3

CODMn

Axis 1 1

Axis 2

1

minus1minus1

(b)

Figure 5 CCA ordination plots Species abbreviations are presented in Table 1 (a) Species and environmental variables (b) Samples andenvironmental variables Numbers represented sample times for example 907 means Jul 2009 The eigenvalues for the first two axes are 018and 0126 The Monte Carlo permutation test was significant on the first axis (119865 = 3965 119875 = 0002) and on all axes (119865 = 1885 119875 = 0002)

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 7: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 7

Table 3 GAMs generated by the forward and backward stepwise selection procedure

Response variables Explanatory variables selected by stepwise procedure Explained variance ()Total s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)lowast 648

An fissa s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(CODMn) + s(Tem) 576

Asc Saltans s(NH4-N) + s(TN) + s(Tem) 202

Asp priodonta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 343

B angularis s(NO2-N) + s(NO3-N) + s(SRP) + s(Tem) 307

B budapestinensis s(NH4-N) + s(NO3-N) + s(TP) 357

B calyciflorus s(NH4-N) + s(NO3-N) + s(Tem) 205

B diversicornis s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 344

B forficula s(chla) + s(NO2-N) + s(NO3-N) + s(CODMn) + s(Tem) 643

Ce inquilina s(chla) + s(NH4-N) + s(NO2-N) + s(NO3-N) + s(Tem) 486

E senta s(NH4-N) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 411

F longiseta s(CODMn) + s(Tem) 364

F terminalis s(NO3-N) + s(TN) + s(TP) + s(CODMn) + s(Tem) 340

H mira s(NO2-N) + s(SRP) + s(CODMn) + s(Tem) 643

K cochlearis s(NO3-N) + s(Tem) 171

K quadrata s(chla) + s(NH4-N) + s(NO3-N) + s(Tem) 369

K ticinensis s(NO3-N) + s(SRP) + s(TP) + s(CODMn) + s(Tem) 534

K valga s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(Tem) 447

L elachis s(chla) + s(TN) + s(CODMn) + s(Tem) 345

P dolichoptera s(CODMn) + s(Tem) 211

Po complanata s(chla) + s(NO2-N) + s(CODMn) + s(Tem) 332

Tr longiseta s(chla) + s(TN) + s(CODMn) 165

Tr pusilla s(chla) + s(NO3-N) + s(TN) + s(Tem) 611

lowastThe GAM formula is ln(densities + 1) sim s(chla) + s(NO2-N) + s(NO3-N) + s(TN) + s(SRP) + s(CODMn) + s(Tem)

with respect to different species and can explain 165sim648of the response variance Environmental parameters includedin the GAM for total rotifer density explained approximately648 of the variations in the total rotifer density NO

2-N

TN SRP and Tem were significant while chla NO3-N and

CODMn were not significant at a 5 level The effects of theselected environmental parameters on rotifer densities areshown in Figure 6

Total rotifer density increased with the increase in tem-perature reaching its maximum at approximately 23∘C butdecreased slightly when the temperature exceeded 25∘CEighteen species out of the 22 frequent species (present in gt18samples) were significantly affected by temperatureThere arefour main types of rotifer responses to temperature One typepreferred high temperature (25ndash30∘C) including B forficulaCe inquilina and H mira The second type consisting ofmost of the abundant species that is An fissa E senta FterminalisK valga L elachis P dolichoptera Po complanataand T pusilla peaked at a temperature of 20ndash25∘CThereforethe total rotifer density was largest at 23∘C The third typepeaked at approximately 15∘C and this type includes Aspriodonta K cochlearis and K ticinensis The fourth typepreferred a low temperature (K quadrata and B calyciflorus)Interestingly B angularis had two peaks at approximately 12and 25∘C

Chla was only significant in the GAMs of three species(Ce inquilina K quadrata and T longiseta) The total rotiferdensity showed an overall increase with increasing chla but

decreased during 30ndash50mgmminus3 although not significantThe confidence intervals broadened when chla was greaterthan 40mgmminus3 because few samples had high numbers ofchla Six species responded significantly to CODMn andtheir fitting cures greatly varied H mira decreased with theincrease of CODMn

Only three GAMs identified TP as an explanatory vari-able and seven GAMs identified TN as an explanatoryvariable B budapestinensis and F terminalis had a similarcurve fit for TP with a peak before 02mg Lminus1 but the curvefor K ticinensis was at a minimum there E senta increasedwith increased TN but the others did not exhibit a trend

Inorganic ions also had some effects on rotifer abundanceE senta increased with NH

4-N when it was lower than

1mg Lminus1 The fitting-curve confidence interval broadenedwhen NH

4-N was greater than 15mg Lminus1 because there were

a few data in that range Most of the curves for NO2-N and

NO3-N were wavy but E senta showed a clear trend with

increasing NO2-N There was a negative effect of SRP on the

total density and the densities of the three species in the rangefrom 002 to 006mg Lminus1

35 Rotifer Community as Bioindicators All of the diversityindices variedmonthly but they exhibited little annual fluctu-ation (Figure 7)1198671015840 119869 and species richness (119877) were stronglypositively correlated with Tem119863Mg was positively associatedwith chla and TP 1198671015840 and 119877 were positively associated with

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

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Environmental Chemistry

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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ClimatologyJournal of

Page 8: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

8 The Scientific World Journal

5 10 15 20 25 30

0

1s(

Tem

)

Total

P dolic

0

2

s(Te

m)

4

Tr pusi

0

2

4

6

s(Te

m)

An fiss

5 10 15 20 25 30

B angul

K valga

0

2

4

s(Te

m)

As prio

K ticin

B calyc

K cochl

B forfi

01234

s(Te

m)

Asc salt

L elach

Ce inqu

K quadr

E senta

Po comp

0

1

2

3

4

s(Te

m)

H miraF termi

0 1 2 3

As prio

B calyc

0 1 2 3 4

Asc salt

K quadr

E sentaB budap

0 01 02 03 04 05

s(TP

)

B budap F termi K ticin

F = 392 P = 001 F = 1139 P = 0000001 F = 1114 P = 00000012 F = 535 P = 00015

F = 449 P = 00047 F = 314 P = 0027 F = 142 P lt 00000001 F = 668 P = 000029

F = 431 P = 00059F = 631 P = 000047 F = 14 P lt 00000001F = 304 P = 0031

F = 524 P = 00018F = 1184 P = 00000005 F = 951 P = 00000085F = 305 P = 003

F = 864 P = 000002 F = 18 P lt 00000001F = 75 P = 00001 F = 358 P = 0015

F = 337 P = 002F = 325 P = 0024 F = 131 P = 00000001F = 371 P = 0013

F = 686 P = 000022 F = 136 P lt 00000001 F = 436 P = 000056 F = 599 P = 00007

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

5 10 15 20 25 30 5 10 15 20 25 30

0 1 2 3 4

0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0 01 02 03 04 05 0 01 02 03 04 05

minus3

minus2minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

6

s(Te

m)

minus2

0

2

4

minus2

minus2

minus4

minus6

0

2

minus2

minus4

minus6

0

2

4

6

s(Te

m)

minus2

minus2

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

0

2

4

s(Te

m)

minus2

minus1

minus1

0

1

2

3

4

s(Te

m)

minus1

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

0

2

4

s(Te

m)

minus2

minus4

minus2

minus1

s(N

H4-N

)

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

s(N

H4-N

)

0

2

4

minus2

s(N

H4-N

)

0

2

4

minus2

minus2

minus4

minus6

s(N

H4-N

)

0

2

4

6

s(TP

)

0

2

4

6

s(TP

)

0

2

4

68

NH4-N (mg Lminus1)

NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1) NH4-N (mg Lminus1)

NH4-N (mg Lminus1)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C) Tem (∘C) Tem (∘C)

Tem (∘C)

TP (mg Lminus1) TP (mg Lminus1) TP (mg Lminus1)

(a)

Figure 6 Continued

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 9: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 9

0 1 2 3 4 5

1 2 3 4 51 2 3 4 51 2 3 4 51 2 3 4 5

1 2 3 4 5 1 2 3 4 5

s(TN

)

Total

s(TN

)

An fiss

s(TN

)

Asc salt

L elach Tr long

s(TN

)

E senta

0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20

Total An fiss

K ticin

B forfi

01234

H mira

F termi

Po comp

0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120

0

1

2s(

Chla

)

Total

0

2

4

6

s(Ch

la)

Tr long

0

1234

s(Ch

la)

K quadr

0

2

4

6

s(Ch

la)

Ce inqu

0 01 02 03 04 0 01 02 03 04

Total An fiss

B angul

K valga

As prio B diver B forfi

Ce inqu E senta

01234

H mira

F termi

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

0 01 02 03 04 0 01 02 03 04 0 01 02 03 04 0 01 02 03 04

Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3) Chla (mg mminus3)

CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

CODMn (mg Lminus1) CODMn (mg Lminus1) CODMn (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

TN (mg Lminus1) TN (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

NO2-N (mg Lminus1) NO2-N (mg Lminus1) NO2-N (mg Lminus1)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(CO

DM

n)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

s(N

O2-N

)

minus4minus2 minus2

minus1

0

1

2

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

01234

minus1

0

1

2

minus1

minus2

minus2

minus2

0

2

4

6

minus4

minus2

0

2

4

6

minus4

minus2

s(TN

)

0

2

4

minus2

0

2

4

minus4

02

4

6

minus2

minus4

0

2

4

minus2

s(N

O2-N

)

minus4

minus6

024

minus2

s(N

O2-N

)

minus4

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(N

O2-N

)

0

2

4

minus2

s(TN

)

0

2

4

6

minus2

minus2

s(TN

)

0

2

4

6

minus2

0

2

4

6

minus2

s(N

O2-N

)

0

2

4

6

minus2

minus4

s(CO

DM

n)

0

2

4

6

minus2

s(CO

DM

n)

0

2

4

minus2

0

2

4

minus4

minus2

minus1

minus2

minus1

F = 11 P = 035 F = 283 P = 004F = 385 P = 0011F = 269 P = 0049

F = 18 P = 015 F = 323 P = 0024 F = 939 P = 000001 F = 309 P = 0029

F = 506 P = 00023F = 421 P = 00069F = 827 P = 0000039 F = 279 P = 0043

F = 501 P = 00025 F = 358 P = 0015 F = 865 P = 0000025 F = 333 P = 0021

F = 877 P = 0000021 F = 283 P = 004 F = 68 P = 000026 F = 422 P = 00068

F = 756 P = 0000096F = 341 P = 0019 F = 455 P = 0004 F = 915 P = 0000014

F = 298 P = 0034F = 461 P = 00041 F = 396 P = 00095 F = 78 P = 0000071

(b)

Figure 6 Continued

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 10: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

10 The Scientific World Journal

0 03 06 09 12 0 03 06 09 12

0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

0 03 06 09 12 0 03 06 09 12 0 03 06 09 12

Total An fiss

0 02 04 06 08 1 12

As prio

K ticin

B calyc Ce inqu

01234

K quadr

E senta

F termi

B budap

0 003 006 009 012 0 003 006 009 012

0

1

2

s(SR

P)

Total

0 004 008 012 0 004 008 012

0

2

4

s(SR

P)

B angul

0

2

s(SR

P)

B diver

01234

s(SR

P)

H mira

0 004 008 012

K ticin

Combined effect for each predictor 95 bayesian confidence limits

SRP (mg Lminus1)

SRP (mg Lminus1)

SRP (mg Lminus1) SRP (mg Lminus1) SRP (mg Lminus1)

NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1) NO3-N (mg Lminus1)

NO3-N (mg Lminus1) NO3-N (mg Lminus1)

minus4minus2

minus2

02

64

minus4

minus2

0

2

4

minus4

minus6

minus20

2

4

s(SR

P)

minus2

0

2

4

minus2

minus4

minus2minus1

minus2

minus1

0

1

2

minus2

minus1

minus2

minus1

s(N

O3-N

)

s(N

O3-N

)

0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus2

s(N

O3-N

)

s(N

O3-N

)0

2

4

minus4

minus2

0

2

4

minus4

minus2

s(N

O3-N

)0

2

4

minus4

minus2

s(N

O3-N

)s(

NO

3-N

)

F = 46 P = 00042 F = 432 P = 00059 F = 309 P = 0028 F = 365 P = 0014

F = 248 P = 0063 F = 463 P = 0004 F = 627 P = 000048F = 266 P = 005

F = 294 P = 0035 F = 295 P = 0035 F = 457 P = 00043F = 273 P = 0046

F = 455 P = 00044F = 435 P = 00057F = 368 P = 0014

(c)

Figure 6 Plots showing the effect of selected environmental parameters on rotifer densities For the total rotifer density all of the selectedparameters are shown For the individual species densities only the selected parameters with significance (119875 lt 005) are shown (119899 = 169)

Jul Jan Jul Jan Jul Jan Jul1

152

253

354

Shannon-Wiener index

Smoothed index

Shan

non-

Wie

ner i

ndex

0

02

04

06

08

1

Piel

oursquos

even

ness

inde

x

Pieloursquos evenness index

(a)

Jul Jan Jul Jan Jul Jan Jul

005

115

225

335

Number of rotifer taxaRotier density

4th year3rd year2nd year1st year

05101520253035

Num

ber o

f

0minus05

Margalef rsquos index

Mar

gale

frsquos in

dex

1k2k3k4k5k

taxa

Rotif

er d

ensit

y (in

dmiddotLminus

1)

(b)

Figure 7 Rotifer diversity indices in Dadian Lake Smoothed method FFT filter six points

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 11: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 11

Table 4 Correlations between the diversity indices including the Shannon-Wiener index (1198671015840) species richness (119877) evenness index (119869)Margalef rsquos index (119863Mg) total rotifer density (119873) and environmental factors

119867

1015840119869 119863Mg 119877 119873 Chla TN TP Tem

119867

1015840 1 0705 0768 0702 0316 0344 0165 0238 0435lt00001 lt00001 lt00001 0053 0037 0342 0168 0006

119869

0705 1 0138 0019 minus0204 0054 0082 0048 0079

lt00001 0410 0909 0219 0753 0638 0783 0636

119863Mg0768 0138 1 0957 0505 0365 0242 0380 0451lt00001 0410 lt00001 0001 0027 0161 0024 0005

119877

0702 0019 0957 1 0716 0442 0093 0256 0490lt00001 0909 lt00001 lt00001 0006 0594 0138 0002

chla There was a positive correlation between 119877 1198671015840 and119863Mg but only 119869 is related to1198671015840(Table 4) The average valuesof1198671015840 119869 and119863Mg were 195 068 and 256 respectively

There was a positive correlation between 119863Mg and 119873When temperature rose both 119877 and 119873 increased but 119877increased more than ln119873 so 119863Mg increased Both 119863Mg and119873 were positively correlated with Tem resulting in a positivecorrelation between119863Mg and119873

4 Discussion

Sediment dredging disrupted the ecological balance anddestroyed the benthos and aquatic vegetation [27 28] Dredg-ing likely took the zooplankton resting eggs away but thesediment was used to create islands in the southern areaof the lake These islands have become important banks forrotifer resting eggs We only have a few data regarding thezooplankton before dredgingThe average rotifer density was3573 ind Lminus1 in April 2005 However the intensive dredgingand construction rendered the lake analogous to a newlyconstructed one and we cared more about the succession ofrotifer community after the lake was refilledThe rotifer com-munity mainly originated from the river and from the restingegg banks The refilled water from the connected rivers waslow quality with a TN of 505mg Lminus1 and a TP of 034mg Lminus1both of which decreased shortly after refilling The absenceof a relationship between TN TP and Chl-a may be partlyexplained by themacrophytes Becausemacrophytes competewith phytoplankton nutrient and chlorophyll a will decreaseas the macrophyte population increases [29] Furthermorefish and other zooplankton can also constrain TP Chl-aratios Unfortunately we do have not any exact biomass forthem

There was a clear change in the rotifer community bothin density and species structure after refilling The rotiferdensity exponentially declined over the four years but TNandTP rebounded in the 2ndwinter and springTheywere allshown low values in the 4th year with smaller variationsThismay indicate that the ecosystem in the water column reacheda stable state This phenomenon has also been observed innewly constructed reservoirs [30] In addition to the densityvariations there were also changes in the dominant speciesof the rotifer community P dolichoptera and Tr pusilla were

widely found and dominated most subtropical lakes frommesotrophic to eutrophic [13 23 31] They also dominatedDadian Lake during most of the study period but otherdominant species changed for example there were more Anfissa in the first two years and moreH mira in the later yearsas mentioned above

The rotifer community variations were correlated withchanges in abiotic and biotic environmental factors Abioticfactors affected the rotifers directly or indirectly Temperatureand some toxic ions may have directly affected the rotifersand temperature accounted for a relatively high proportionof the variability in the rotifer community The total rotiferdensity reached its maximum at approximately 23∘C butindividual species differed in their temperature preferencesin this study

Rotifers generally have a very wide tolerance to tempera-ture but in separate lakes they are often strongly restrictedby and connected with temperature differences [32] Pdolichoptera peaked at approximately 20∘C and was a peren-nial superdominant in the present study but it was consideredto be a ldquowinter speciesrdquo by [24 33] However other studiesalso found that it could occur at higher temperatures in smalllakes and ponds [32] As priodonta and F terminalis wereconsidered to prefer temperatures below 10∘C [24] but theypeaked at 15 and 25∘C in our study and behaved similarlyin another study [32] B calyciflorus was found to preferlow temperatures in this study but not in others [32] Thereis some agreement among different studies for example Kquadrata preferred low temperatures and T pusilla peakedat high temperatures in our study as well as in other studies[24 31 34] The thermal preference discrepancy of the samespecies between different individual lakes may be attributedto the fact that temperature alone does not generally decidewhen and where a species occurs Other abiotic and bioticfactors also play a role [32]

Some abiotic factors are toxic to rotifers Chen et al [35]observed that a nitrite concentration of 10mg Lminus1 NO

2-N

markedly inhibited the growth ofB calyciflorus Although thetolerance of B calyciflorus to nitrite was high lower nitritelevels may have increased the production of microcystinFurthermore nitrite and microcystin could have acted in asynergisticmanner causing toxicity Schluter andGroeneweg[36] found that the reproduction of B rubens was unaffectedup to a concentration of 3mg Lminus1 of ammonia and in

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 12: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

12 The Scientific World Journal

the range of 3ndash5mg Lminus1 the reproduction rate decreased butnone died and there was a trend of declining populations formost species with NH

4-N gt 2mg Lminus1 in our study However

in our study the nitrite and NH4-N concentrations were

found to be below 05 and 4mg Lminus1 respectivelyThe effects ofnitrate and ammonia on some species in this study are morelikely to be indirect and further investigation is needed

Abiotic factors including NH4-N NO

3-N NO

2-N SRP

TN and TP can indirectly affect rotifers via trophic cas-cade The abundance of these materials has an influenceon the quantity and quality of plankton as well as bacteriaRotifers feed on bacteria protozoa including ciliates andheterotrophic flagellates and algae including pico- andnanophytoplankton Many planktonic rotifers are known asrelatively unselective microfiltrators feeding on particles inthe range of 05 to 20120583m and other grasping species feedpreferentially on larger organisms (esp ciliates) [37] Chlamay be representative of algal quantity and TP was found topositively correlate with chla When chla was included inCCA or GAMs TP could not explain the more significantvariations of the rotifer community TN may influence theplankton community The average TN TP of Dadian Lakewas 17 1 A total N P ratio below 29 1 may indicate thedominance of cyanobacteria in this lake [38] Limitation of Nmay favour nitrogen-fixing cyanobacteria But the dominatephytoplankton species in Dadian Lake were Phormidiumspp and Spirulina sp which cannot fix nitrogen Thus theincreased TN may favour the growth of those cyanobacteriawhich cannot be ingested by many rotifers [39] Moreoversome cyanobacteria species may release toxicants such asmicrocystin As a result the total rotifer density declinedwithincreasedTN in theGAMWhenTNwas greater than 3 therewas no limitation of nitrogen to other algae such as greenalgae and the total rotifer density increased The differencesin tolerance of rotifer species to TNmay reflect their adaptionto different algae

COD is an indicator of the organic matter in waterOrganic matter mainly consists of living and dead plantsand animal organisms [40] Algae bacteria protozoa anddebris can contribute to COD and they are considered foodfor rotifers Bacteria and protozoa may constitute 20ndash50 ofrotifer food [37]Therefore COD can explainmore variationsin rotifers than chla explained in the CCA and the GAM inour study

Biotic factors affect rotifers directly The edible algaedensity can determine rotifer abundance Generally there isa positive correlation between rotifer abundance and chla Inthis study a linear relationship between chla and total rotiferabundance was observed in the case of chla lt30mgmminus3However the rotifer abundance slightly declined with theincrease of chla when it was greater than 30 and smallerthan 60mgmminus3most likely because cyanobacteria especiallyMicrocystis dominated in this interval Each suspension-feeding rotifer in a community may have a different foodpreference hence the impact on the ecosystem will bedifferent according to its feeding habits [41] Polyarthraprefers food in a large size range (approximately 1ndash40120583m)[37] which enables it to dominate throughout the year

Cladocerans had a negative correlationwith rotifer densi-ties in this study Planktonic rotifers often are abundant whenonly small cladocerans occur but typically are rare when largecladocerans are present Cladocerans share available foodwith rotifersThemain species of cladocerans are filter feeders[4ndash11 42] They feed on nanoplankton and other small parti-cles but cladocerans often show dominance over rotifers dueto their large body sizes and other factors [43]The extremelylow density of cladocerans in this lake could be attributedto fish predation There were approximately 11000 kg of fishmainly composed of silver and bighead carp released to thelake after it was refilled Though the primary purpose offish release was to inhibit the potential Microcystis bloomby direct predation the fish also predated the large zoo-plankton population especially cladocerans because of theirnonselective filtering habitThe rotifers may benefit from thisfish behaviour The observed copepods mainly consisted ofCyclopoida which prey on rotifers [44 45] however therewas no significant relationship between them detected in ourstudy most likely due to the low prey pressure on rotifers

It has been often observed that the abundance of rotifers isproportional to the trophic status of a water body [23] Manyrotifer indices were established to evaluate the lake trophicstatus The average values of 1198671015840 119869 and 119863Mg indicate thatthe lake was somewhat mesotrophic However these indicesexhibited poor relationships to TP TN and chla Comparedto the nutrient concentration the relatively high index wasmost likely due to the instability of the lake ecosystem afterdredging According to the intermediate disturbance hypoth-esis disturbance should promote biodiversity Furthermorea diversity of aquatic environments such as islands andmacrophytes may provide more niches

More complex indices for rotifers including the sapro-bic index and 119876

119861119879[5] were established for saprobic and

trophic evaluation according to rotifer trophic preferenceSome studies have established a linear regression formuladescribing the relationship between trophic status and therotifer community index [11 46] These indices were reliablein the lakes they studied

However it is very hard to establish one-to-one causalrelationships between rotifer composition and trophic con-ditions The responses of rotifers to environmental factorswere found to be nonlinear sometimes unimodal or bimodalin our study Nutrient elements indirectly affect rotifers viathe food chain Moreover apart from trophic conditionsother abiotic factors [47] as well as food composition (espalgae species) vegetation cover [48] and predation [3] alsoplay important roles in determining the abundance andspecies composition of the rotifer community As a resultthe trophic preferences of individual rotifer species maydiffer by region Tr pusilla occurs in mesotrophic lakes andP dolichoptera is associated with a low trophic state [56 49] but they were observed to dominate regardless ofchanges in trophic status in our study and other studies[31] Nevertheless rotifers still have their value when assess-ing trophic conditions Some authors recommended usingrotifer abundance to obtain a rough estimate of lake trophicstatus 500ndash1000 ind Lminus1 mesotrophic or mesoeutrophic

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 13: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

The Scientific World Journal 13

1000ndash2500 ind Lminus1 eutrophic and 3000ndash4000 ind Lminus1 mod-erately eutrophic [9 31] Our results fit within those criteria

5 Conclusions

It would take a long time to completely restore the aquaticecosystem in a completely dredged lake because both thetotal rotifer abundance and abiotic parameters reached arelatively stable stage in the fourth year CCA showed thatchanges of rotifer species composition along with trophicstate are exhibited in warm seasons The GAMs indicatedthat most of the environmental parameters had complexeffects on the rotifer abundance as demonstrated by thecomplicated curves describing their relationships Althoughrotifer species distribution and total abundance can be usedto roughly assess trophic state it is very hard to establishone-to-one causal relationships between the rotifer com-munity and trophic conditions due to the unimodal effectsof nutrient elements on rotifers In addition temperaturehad a predominant influence on rotifers compared to thatof trophic conditions in subtropical lakes Rotifers used forbioindicators should be sampled in warm seasons

Acknowledgments

Our sincere thanks are deserved to many other members ofthe research group for field and laboratory assistance Wegreatly appreciate the valuable comments and suggestions byDr Hendrik Segers Financial support was provided both bythe Shanghai Water Authority (SWA) the Science and Tech-nology Commission of ShanghaiMunicipality (STCSM) andthe Shanghai Municipal Education Commission (SHMEC)

References

[1] D W Schindler ldquoDetecting ecosystem responses to anthro-pogenic stressrdquo Canadian Journal of Fisheries and AquaticSciences vol 44 no 1 pp 6ndash25 1987

[2] R Pinto-Coelho B Pinel-Alloul G Methot and K E HavensldquoCrustacean zooplankton in lakes and reservoirs of temperateand tropical regions variation with trophic statusrdquo CanadianJournal of Fisheries and Aquatic Sciences vol 62 no 2 pp 348ndash361 2005

[3] J E Gannon and R S Stemberger ldquoZooplankton (especiallycrustaceans and rotifers) as indicators of water qualityrdquo Trans-actions of the American Microscopical Society vol 97 pp 16ndash351978

[4] B B Castro S C Antunes R Pereira AM VM Soares and FGoncalves ldquoRotifer community structure in three shallow lakesseasonal fluctuations and explanatory factorsrdquo Hydrobiologiavol 543 no 1 pp 221ndash232 2005

[5] V Sladecek ldquoRotifers as indicators of water qualityrdquoHydrobiolo-gia vol 100 pp 169ndash201 1983

[6] I C Duggan J D Green and R J Shiel ldquoDistribution of rotiferassemblages in North Island New zealand lakes relationshipsto environmental and historical factorsrdquo Freshwater Biology vol47 no 2 pp 195ndash206 2002

[7] I Sellami A Hamza M A Mhamdi L Aleya A Bouain andH Ayadi ldquoAbundance and biomass of rotifers in relation to

the environmental factors in geothermal waters in SouthernTunisiardquo Journal of Thermal Biology vol 34 no 6 pp 267ndash2752009

[8] I Bielanska-Grajner ldquoThe influence of biotic and abiotic factorson psammic rotifers in artificial and natural lakesrdquo Hydrobiolo-gia vol 546 no 1 pp 431ndash440 2005

[9] L May andM OrsquoHare ldquoChanges in rotifer species compositionand abundance along a trophic gradient in Loch LomondScotland UKrdquoHydrobiologia vol 546 no 1 pp 397ndash404 2005

[10] H C Arora ldquoRotifera as indicators of trophic nature ofenvironmentsrdquoHydrobiologia vol 27 no 1-2 pp 146ndash159 1966

[11] I C Duggan J D Green and R J Shiel ldquoDistribution ofrotifers in North Island New Zealand and their potential useas bioindicators of lake trophic staterdquo Hydrobiologia vol 446-447 pp 155ndash164 2001

[12] J Arora andN KMehra ldquoSeasonal dynamics of rotifers in rela-tion to physical and chemical conditions of the river Yamuna(Delhi) Indiardquo Hydrobiologia vol 491 pp 101ndash109 2003

[13] S Zhang Q Zhou D Xu J Lin S Cheng and Z Wu ldquoEffectsof sediment dredging on water quality and zooplankton com-munity structure in a shallow of eutrophic lakerdquo Journal ofEnvironmental Sciences vol 22 no 2 pp 218ndash224 2010

[14] T J Hastie and R J Tibshirani Generalized Additive ModelsChapman and Hall London UK 1990

[15] MTao P Xie J Chen et al ldquoUse of a generalized additivemodelto investigate key abiotic factors affecting microcystin cellularquotas in heavy bloom areas of lake Taihurdquo PLoS ONE vol 7no 2 article e32020 2012

[16] P Bertaccini V Dukic and R Ignaccolo ldquoModeling the short-term effect of traffic and meteorology on air pollution in turinwith generalized additivemodelsrdquoAdvances inMeteorology vol2012 Article ID 609328 16 pages 2012

[17] A Benedetti M Abrahamowicz K Leffondr M S Goldbergand R Tamblyn ldquoUsing generalized additive models to detectand estimate threshold associationsrdquo International Journal ofBiostatistics vol 5 no 1 article 26 2009

[18] R Morton and B L Henderson ldquoEstimation of nonlineartrends in water quality an improved approach using general-ized additive modelsrdquo Water Resources Research vol 44 no 7Article IDW07420 2008

[19] APHA Standard Methods for the Examination of Water andWastewater American Public Health Association WashingtonDC USA 20th edition 1998

[20] State EPA of ChinaMonitoring and Analysis Methods for Waterand Wastewater China Environmental Sscience Press BeijingChina 4th edition 2002

[21] W Koste and M Voigt Rotatoria Die Radertiere MitteleuropasUberordnung Monogononta Ein Bestimmungswerk GebruderBorntraeger Berlin Germany 1978

[22] H Segers ldquoAnnotated checklist of the rotifers (PhylumRotifera) with notes on nomenclature taxonomy and distribu-tionrdquo Zootaxa no 1564 pp 1ndash104 2007

[23] Z Shao P Xie and Y Zhuge ldquoLong-term changes of planktonicrotifers in a subtropical Chinese lake dominated by filter-feeding fishesrdquo Freshwater Biology vol 46 no 7 pp 973ndash9862001

[24] G A Galkovskaya D VMolotkov and I FMityanina ldquoSpeciesdiversity and spatial structure of pelagic zooplankton in a lakeof glacial origin during summer stratificationrdquo Hydrobiologiavol 568 no 1 pp 31ndash40 2006

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 14: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

14 The Scientific World Journal

[25] R McGill J W Tukey and W A Larsen ldquoVariations of boxplotsrdquoThe American Statistician vol 32 pp 12ndash16 1978

[26] J Leps and P S Smilauer Multivariate Analysis of EcologicalData Using Canoco Cambridge University Press CambridgeUK 2003

[27] A Brookes ldquoRecovery and adjustment of aquatic vegetationwithin channelization works in England and Walesrdquo Journal ofEnvironmental Management vol 24 no 4 pp 365ndash382 1987

[28] M A Lewis D E Weber R S Stanley and J C MooreldquoDredging impact on an urbanized Florida bayou effects onbenthos and algal-periphytonrdquo Environmental Pollution vol115 no 2 pp 161ndash171 2001

[29] D E Canfield Jr J V Shireman D E Colle W T Haller CE Watkins II and M J Maceina ldquoPrediction of chlorophyll aconcentrations in Florida lakes importance of aquatic macro-phytesrdquo Canadian Journal of Fisheries and Aquatic Sciences vol41 no 3 pp 497ndash501 1984

[30] T Ioriya S Inoue M Haga and N Yogo ldquoChange of chemicaland biological water environment at a newly constructedreservoirrdquoWater Science and Technology vol 37 no 2 pp 187ndash194 1998

[31] X Wen Y Xi F Qian G Zhang and X Xiang ldquoComparativeanalysis of rotifer community structure in five subtropicalshallow lakes in East China role of physical and chemicalconditionsrdquo Hydrobiologia vol 661 no 1 pp 303ndash316 2011

[32] B Berzins and B Pejler ldquoRotifer occurrence in relation totemperaturerdquo Hydrobiologia vol 175 no 3 pp 223ndash231 1989

[33] B Carlin ldquoDie planktonrotatorien des motalastrom Zur tax-onomie und kologie der planktonrotatorienrdquo MeddelandenLunds Universitets Limnologiska Institution vol 5 p 256 1943

[34] L May ldquoRotifer occurrence in relation to water temperature inLoch Leven ScotlandrdquoHydrobiologia vol 104 no 1 pp 311ndash3151983

[35] W Chen H Liu Q Zhang and S Dai ldquoEffects of nitrite andtoxic Microcystis aeruginosa PCC7806 on the growth of fresh-water rotifer Brachionus calyciflorusrdquo Bulletin of EnvironmentalContamination and Toxicology vol 86 no 3 pp 263ndash267 2011

[36] M Schluter and J Groeneweg ldquoThe inhibition by ammoniaof population growth of the rotifer Brachionus rubens incontinuous culturerdquo Aquaculture vol 46 no 3 pp 215ndash2201985

[37] HArndt ldquoRotifers as predators on components of themicrobialweb (bacteria heterotrophic flagellates ciliates)mdasha reviewrdquoHydrobiologia vol 255-256 no 1 pp 231ndash246 1993

[38] V H Smith ldquoLow nitrogen to phosphorus ratios favor domi-nance by blue green algae in lake phytoplanktonrdquo Science vol221 no 4611 pp 669ndash671 1983

[39] M C S Soares M Lurling and V L M Huszar ldquoResponsesof the rotifer brachionus calyciflorus to two tropical toxic cya-nobacteria (cylindrospermopsis raciborskii and microcystisaeruginosa) in pure and mixed diets with green algaerdquo Journalof Plankton Research vol 32 no 7 pp 999ndash1008 2010

[40] S Radwan ldquoThe influence of some abiotic factors on theoccurrence of rotifers of Łeogonekzna andWlmiddle dotodawaLake Districtrdquo Hydrobiologia vol 112 no 2 pp 117ndash124 1984

[41] AHerzig ldquoThe analysis of planktonic rotifer populations a pleafor long-term investigationsrdquo Hydrobiologia vol 147 no 1 pp163ndash180 1987

[42] J J Gilbert ldquoRotifer ecology and embryological inductionrdquoScience vol 151 no 3715 pp 1234ndash1237 1966

[43] H J MacIsaac and J J Gilbert ldquoCompetition between rotifersand cladocerans of different body sizesrdquo Oecologia vol 81 no3 pp 295ndash301 1989

[44] C E Williamson and N M Butler ldquoPredation on rotifers bythe suspension-feeding calanoid copepod Diaptomus pallidusrdquoLimnology amp Oceanography vol 31 no 2 pp 393ndash402 1986

[45] J M Conde-Porcuna and S Declerck ldquoRegulation of rotiferspecies by invertebrate predators in a hypertrophic lake selec-tive predation on egg-bearing females and induction of mor-phological defencesrdquo Journal of Plankton Research vol 20 no4 pp 605ndash618 1998

[46] J Ejsmont-Karabin ldquoThe usefulness of zooplankton as lakeecosystem indicators rotifer trophic sate indexrdquo Polish Journalof Ecology vol 60 pp 339ndash350 2012

[47] I Bielanska-Grajner and A GŁadysz ldquoPlanktonic rotifers inmining lakes in the Silesian Upland relationship to environ-mental parametersrdquo Limnologica vol 40 no 1 pp 67ndash72 2010

[48] R M Viayeh and M Spoljar ldquoStructure of rotifer assemblagesin shallow waterbodies of semi-arid northwest Iran differing insalinity and vegetation coverrdquoHydrobiologia vol 686 no 1 pp73ndash89 2012

[49] A Maemets ldquoRotifers as indicators of lake types in EstoniardquoHydrobiologia vol 104 no 1 pp 357ndash361 1983

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 15: Research Article Planktonic Rotifers in a Subtropical Shallow …downloads.hindawi.com/journals/tswj/2013/702942.pdf · 2019. 7. 31. · et al. studies rotifer community structure

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of