time variation in phytoplankton assemblages in a ...time variation in phytoplankton assemblages in a...

Pacific Science (1998), vol. 52, no. 1: 79-97© 1998 by University of Hawai'i Press. All rights reserved

Time Variation in Phytoplankton Assemblages in a Subtropical Lagoon Systemafter the 1982-1983 "EI Nmo" Event (1984 to 1986)1

ISMAEL GARATE-LIZARRAGA2 AND DAVID A. SIQUEIROS BELTRONES3

ABSTRACT: An analysis of seasonal and geographical distribution andabundance of the total and separate fractions of phytoplankton (nanno- andmicrophytoplankton) in the Magdalena-Almejas lagoon system was done afterthe 1982-1983 "El Niiio" event. In spite of its being in a subtropical region,the annual variation of phytoplankton abundance in the area was similar tothe annual cycle of production of coastal lagoons in temperate regions. Therewere two peaks of phytoplankton abundance, in spring and in autumn. Theupwelling and tidal currents enriching the waters of Bahia Magdalena wereresponsible for the high concentrations of phytoplankton in the bay. Microphytoplankton was the most important fraction throughout the study period.Nannophytoplankton was somewhat abundant. Using principal componentanalysis, seasonal variation and frequency were the two factors determining thestructure of species assemblages. Lowest values of diversity and dominancewere related to circulation patterns and to the phytoplankton blooms thatoccurred throughout the year in Bahia Magdalena-Almejas. High values ofdiversity and low dominance were estimated at those areas under the influenceof oceanic waters. The 1982-1983 El Nifio caused a drastic drop in phytoplankton abundance during 1984. The recuperation process was slow, startingin 1985 and completed by 1986. Recorded increases in phytoplankton abundance surpassed all previous records. "El Niiio" caused changes in the structureof the microphytoplankton assemblages. Species richness and specific diversitydiminished because of the occurrence of few species.

SEVERAL STUDIES ON THE periodic variationof primary productivity and phytoplanktonabundance have been done on coastal ecosystems in temperate regions subject to amarked seasonality (Margalef 1958, Boney1975, Raymont 1980) and in tropical regions

1 Financial support to carry out this research was provided by the Direccion de Estudios de Posgrado e lnvestigaci6n (Proyectos: DEPI 900318 and DEPI 966584).I.G.L. is a Comisi6n de Operaci6n y Fomento de Actividades Academicas-IPN fellow. Manuscript accepted 4November 1996.

2 Laboratorio de Fitoplancton, Departamento dePlancton y Ecologia Marina, Centro lnterdisciplinariode Ciencias Marinas, A.P. 592, La paz, B.C.S., Mexico23000.

3 Departamento de Biologia Marina, UniversidadAut6noma de Baja California Sur, A.P. 19-B, La Paz,B.C.S., Mexico 23081. '

where species successions are much less pronounced (Guillard and Kilham 1977).

In areas between those two biogeographical regions, such as the southern part of theBaja California peninsula (Dawson 1960),time variations in the structure of marinecommunities are subject to a complex interaction of oceanographic conditions. Thesedetermine a zone with transitional characteristics where tropical and subtropical phytoplanktonic species have been reported(Hernandez Becerril 1989).

These conditions also determine the distribution limits of macroalgae and mangrovespecies in the Bahia Magdalena-Almejaslagoon system (Dawson 1961, Blasco1984a,b, Garcia de la Rosa 1990, RiosmenaRodriguez and Siqueiros Beltrones 1995).There, differential occurrence of well-definedpopulations and morphotypes of macroalgal

79

80

taxa have been observed (Garza Sanchez1994, Riosmena Rodriguez and SiqueirosBeltrones 1996).

The Bahia Magdalena-Almejas system isan area of great biological and fisheries significance. It is the main area for sardine catchin the southern Baja California peninsula.There have been few hydrographic studies inthe lagoon system (Alvarez-Borrego et al.1975, Acosta-Ruiz and Lara Lara 1978,Guerrero-Godinez et al. 1988). However, in1980, the Center for Scientific Marine Research (CICIMAR) in La Paz, Mexico, begancontinuing studies on plankton dynamics(Funes Rodriguez 1985, Cota-Meza et al.1992, Palomares-Garcia and Gomez-Gutierrez 1996) and on the distribution andabundance of ichthyoplankton (Anonymous1984, 1985, Saldierna Martinez et al. 1987).

Very few studies are available concerning phytoplankton species distribution andabundance in the area. Microphytoplanktonstructure and abundance (including nannophytoplankton) were determined for anannual cycle (1980-1981) by Nienhuis andGuerrero (1985). Later, they also reportedon the distribution of the dominant species,diversity (H') values, and abundance of thetwo phytoplankton fractions (Nienhuis andGuerrero 1986). Sampling was carried outbefore and during the 1982-1983 "El Nino"event.

That "El Nino" caused numerous changesin marine populations. A decrease in phytoplankton production along the coasts ofChile and Peru was reported by Cowles et al.(1977), Barber et al. (1983), Guillen et al.(1985), and Avaria and Munoz (1987).Torres Moye and Alvarez Borrego (1985)and Martinez Lopez (1993) reported similarresults for the western coast of the Baja California peninsula. Lara Lara et al. (1984) observed an enrichment in the production andplankton biomass in the Gulf of California.For Bahia Magdalena-Almejas, this eventwas recorded from the summer of 1982 untilthe end of 1984 (Salclierna Martinez et al.1987).

The purpose of this paper is to describethe spatial and seasonal variation of the totalphytoplankton abundance (cells 1-1), abundance by size fractions (nanno- and micro-

PACIFIC SCIENCE, Volume 52, January 1998

phytoplankton), and the structure of microphytoplankton assemblages in BahiaMagdalena-Almejas through two and a halfannual cycles (June 1984-0ctober 1986). Wealso aimed to assess these changes duringthe last phase and immediate period of relaxation of the 1982-1983 "El Nino" warming event.

Study Area

The Magdalena-Almejas lagoon system ison the west coast of Baja California Sur, between 240 15' and 250 20' N and III 0 30' and1120 15' W (Figure 1). The lagoon system hasbeen divided into three hydrologic zones: (a)northern (zona de canales), composed mainlyof estuaries and channels with an averagedepth of 3.5 m, an area of 137 km2, and surrounded by small but abundant mangrovetrees, Laguncularia racemosa and Rhizophoramangle; (b) central (Bahia Magdalena), connected to the Pacific Ocean by a mouth 40 mdeep; (c) southeastern (Bahia Almejas), connected to the ocean by a narrow (0.2 km),shallow (5-7 m) channel (Alvarez Borrego etal. 1975). In the last two zones, Avicenniagerminans is also present, and there are consolidated mangrove forests (Blasco 1984a, b).

MATERIALS AND METHODS

Field Sampling

Twenty-eight stations in the MagdalenaAlmejas lagoon system (Figure 1) were sampled monthly from June 1984 to December1984 and seasonally from January 1985 toOctober 1986. A total of 187 surface samples(500 to 1000 ml) was collected using oceanographic bottles. To support the taxonomicdeterminations of species, surface net hauls(223 samples) were made at each stationusing a phytoplankton net with 54-11m mesh.All samples were preserved in buffered 5%formalin. Surface water temperatures wererecorded using a Kahlsico thermometer.These values were coupled with temperaturemeasurements taken since 1982 by staff of theDepartment of Plankton and Marine Ecology of CICIMAR.

Phytoplankton after El Nifio-GWTE-LIZARRAGA AND SIQUEIROS BELTRONES 81

110°

MEXICO

112°

PACIFIC

OCEAN

BAHIA ALMEJAS

24°

26°

BAHIA MAGDALENA

CANAL DE SANTO DOMINGO

CANAL DE LA

RE HUSA ---''''---'il-

ISLA

MARGARITA

40'

10'

30'

20'

_-----,r--..."..,.......,.,....--,r------,....-r---~ 28°

FIGURE 1. Location of Magdalena-Almejas lagoon system, Mexico, and sampling stations.

Sample Analysis

Phytoplankton bottle samples were sedimented in 5-ml settling chambers and observed using phase-contrast inverted microscopy (Hasle 1978). The total phytoplanktonand nanno- (organisms <20 pm) and mi-

crophytoplankton (organisms >20 pm)abundances (cells I-I) were estimated simultaneously with species composition determinations. Phytoplankton collected by nethauls was analyzed using a phase-contrastmicroscope (Zeiss STDI6). Quantificationswere made using a sample size of 250 or-

82

ganisms, adapted after Margalef and Vives(1972) and Nienhuis and Guerrero (1985).

Taxonomic determinations were madeconsulting the works of Hustedt (1930, 1959),Schiller (1937), Cupp (1943), Graham andBronikovsky (1944), Soumia (1967), Ferguson Wood (1968), Saunders and Glenn(1969), Steidinger and Williams (1970), LiceaDuran (1974), Taylor (1976), Pesantes (1978),Soumia et al. (1979), Humm and Wicks(1980), Navarro (198la,b, 1982), Murray andSchrader (1983), and Sundstrom (1986).

To define the structure of the phytoplankton assemblages for each sampling station, species richness (8), diversity (H'), anddominance (D) indices were computed (peet1974, Brower and Zar 1979). Abundancedata from December 1982 to June 1984were used to estimate the annual cycle andanomalies of the phytoplankton. The annualvariability was examined by plotting monthlymean values, where mean values were calculated as follows:

MMV= 'LXi/N

where MMV = monthly mean value, Xi =value of the variable in the ith month for allyears, and N = mumber of months used inthe analysis. Phytoplankton anomalies werecalculated by:

where Aij = anomaly of the ith month in thejth year, Xij = value of the variable in the ithmonth of the jth year; and Yi = mean valueof the ith month.

Based on the frequency of species occurrence, a principal component analysis wasdone to explore annual variations in themicrophytoplankton assemblages and to detect changes in the species composition. An Rmatrix was computed using only one transect. This transect included seven samplingstations (I, J, K2, L2, M2, Nl, and 0) inthe middle of Bahia Magdalena. These stations were the only ones sampled regularly(Figure 1).

Following Matta and Marshall (1984),


only those species represented in at least 10%of the samples were used because rare speciesincrease variability without adding any important information. However, during ouranalysis, rare species were grouped into clusters of taxonomic affinities, species of thesame genus, or by life forms: thycoplanktonicspecies, neritic and oceanic forms, etc. Suchspecies were included in the analysis becauseof their numerical importance and possibleecological significance.

RESULTS

Sea surface water temperatures from 1982to 1986 showed clear seasonal changesduring our sampling period. Low valuesoccurred in winter-spring, and high valuesin summer-autumn (Figure 2). However,during our sampling, the lowest averagevalues for water temperatures were recordedin April 1984 (20.2°C), February 1985(18.4°C), and April 1985 (19.3°C). The highest values were in September 1984 (28.2°C).In August 1985 (26°C) and October 1986(23.6°C), values were significantly lower. Thetemperature increased during 1982-1984 inthe lagoon system because of the influence ofthe 1982-1983 "El Nino" and began to recede during the relaxation period, at the startof our sampling period.

The estimated annual phytoplanktonstanding crops exhibited two peaks of abundance (Figure 3): a spring peak, with anaverage of 277,000 cells 1-1, and an autumnpeak, with an average of 330,000 cells 1-1.

The lowest abundances were during the summer and winter. In general, of the three areasthat constitute this lagoon system, lowestabundance was in the Santo Domingo channel, particularly during 1984. The richestarea was in Bahia Magdalena, particularlyin the April 1985 and October 1986 samples(Figure 4).

The microphytoplankton fraction was themajor contributor to phytoplankton abundance (Figure 5). The highest mean valuesof this fraction were closely related to hightotal phytoplankton abundances. Nannophytoplankton was abundant only in the

Phytoplankton after El Nifio-GARATE-LIZARRAGA AND SIQUEIROS BELTRONES 83

700000"1""'---------""""="'-----------------""T"30

18

26 Uo.....

................ 24 ~

=-c................. 22 Q;:

Q.

EQ)

................. 20 ~

M 5M 5MM 5

.............................................................. \\.............\ ;

\ /.. / .\.... I

I

M 5

300000

100000 .

200000 .

400000 .

o Phytoplankton abundance- Temperature

600000 . 28

500000

Q)

U

MJNMJNM NM NMJN

f--1982 1983 1984 1985 1986---;

FIGURE 2. Variation of mean temperature and phytoplankton abundance values, 1982 to 1986.

MONTHS

350000

300000

250000

L200000

~....Q)

150000U

100000

50000

0J F M A M J J A 5 o N o

FiGURE 3. Average annual phytoplankton abundance variations in the Magdalena-Almejas lagoon system from1982 to 1986.

August and September 1984 samples, coinciding with the highest temperatures.

A total of 270 taxa in 87 genera was recorded. Diatoms and dinoflagellates were byfar the most diverse and abundant groupsin number of taxa determined, with 171 and84 representatives, respectively. Other groups

recorded were silicoflagellates (five species),cyanobacteria (five), and euglenophytes (one)(Garate-Lizarraga 1992). The most diverseand abundant groups within the microphytoplankton assemblages were diatoms.The genera with most species represented wereChaetoceros (27), Rhizosolenia (15), and Co-

84 PACIFIC SCIENCE, Volume 52, January 1998

Q)uc:o"0c:~

.0«c:o-~c:oa.o->..ca..

oof-

700000

c=J ZONA DE CANALES600000

~ BAHIA MAGDALENA

_ BAHIA ALMEJAS500000

, 400000

Q) 3000000

200000

100000

0J JA SON DA J N J F A J 0

I 1984 11----1985--11 I 986 I

FIGURE 4. Variation of mean phytoplankton abundance values for the three different areas of the Magdalena-A1mejas lagoon system, 1984 to 1986.

-r--------------------------:::----,r-30

26 Q)

28 .......oo.....,

20

24 ::Q)Q.

E22 Q)~

JFNA

- TEMPERATURE

D NANNOPHYTOPLANKTON

_ MICROPHYTOPLANKTON

NJ 5

t----- 1984 ------1"-1985 ---tI-l---1986---l

450000

400000

350000

300000

~250000-Q) 200000

0

150000

100000

50000

0

FIGURE 5. Variation of mean of temperature and fractionated phytoplankton abundance values (nanno- andmicrophytoplankton) in the Magdalena-Almejas lagoon system from 1984 to 1986.

scinodiscus (9). Table I shows the most abundant microphytoplankton species found in thisstudy.

Among the species that can be consideredcharacteristic of the warm seasons, P. a/ata,e. asterompha/us, P. calcar avis, Rh. robusta,Ch. coarctatus, S. pa/meriana, H. membra-

naceus, Rh. hyalina, and e. perforatus werethe most frequent taxa. In the cold seasons,Rh. imbricata, G. flaccida, Ch. compressus, e.pe/agica, A. g/acialis, Th. frauenfe/dii, andTh. nitzschioides were dominant. Ch. curvisetus and E. zodiacus were present during bothseasons. From the warm season group, an

Phytoplankton after El Nifio-GARATE-LIZARRAGA AND SIQUEIROS BELTRONES

TABLE 1

MICROPHYTOPLANKTON IN THE MAGDALENA-ALMEJAS LAGOON SYSTEM, 1984-1986(SETS OF DOMINANT SPECIES BY SAMPLING PERIOD ARE SHOWN)

85

DATE

June 1984July 1984*Aug. 1984*Sept. 1984

Nov. 1984Dec. 1984Jan. 1985Apr. 1985July 1985Nov. 1985Jan. 1986Feb. 1986Apr. 1986June 1986Oct. 1986

DOMINANT SPECIES

Coscinodiscus radiatus, C. asteromphalus, Ceratium fusus, Chaetoceros curvisetus, Noctiluca scintillansProboscia alata, Ch. curvisetusP. alata, Pseudosolenia calcar avis, C. fususP. alata, Stephanopyxis palmeriana, C. asteromphalus, Chaetoceros compressus, Oscillatoria

erythraeum, Rhizosolenia robusta, C. asteromphalusP. alata, Ditylum brightwellii, P. calcar avis, Rh. imbricataP. alata, P. calcar avis, Bacteriastrum hyalinum var. princeps, Nitzschia pungensGuinardiaflaccida, Chaetoceros affinis, Paralia sulcataEucampia zodiacus, G. flaccida, Cerataulina pelagicaP. alata, Ch. curvisetus, P. calcar avisG. flaccida, P. alata, P. calcar avis, Odontella auritaP. calcar avis, G. flaccida, Rhizosolenia stolterfothiiCh. curvisetus, Rhizosolenia imbricata, 0. erythraeum, Hemiaulus sinensisCh. curvisetus, C. pelagica, E. zodiacus, Chaetoceros californiensisHaslea warwikae, Thalassiosira rotula, P. sulcata, E. zodiacus, Rhizosolenia hyalinaP. alata, Rh. imbricata, G. flaccida

• From Martinez Lopez (1987).

association was observed between Rh. cleveiivar. communis, Rh. acuminata, H. sinensis, H.membranaceus, Ch. compressus, and the cyanobacteria Richelia intercellularis, which occurred as an endophyte, particularly during1984. Another association was seen betweenthe protozoan Vorticella oceanica and the diatoms Ch. coarctatus and C. asteromphalus.The last species is recorded for the first timein the Mexican Pacific. These types of associations are common in tropical areas. Theirincreased frequency during 1984 may well bein response to the warming of the westernwaters of the peninsula caused by El Nifio.

Although most dinoflagellate taxa werepresent throughout the study period, only N.scintillans, C. furca, C. fusus, P. steinii, Diplopsalis sp., D. caudata, C. dens, and G. sanguineum showed a preference for the warmseasons. From this group, a great number oftemperate-tropical species were present: Amphisolenia bidentata, C. macroceros var. gal!icum, C. carriense, C. declinatum, C. euarcatum, C. falcatum, C. gibberum var. dispar, C.hexacanthum, C. massiliense, C. pentagonumvar. robustum, C. ranipes, and C. vultur.These all are considered rare within theMagdalena-Almejas system.

The lowest mean values of diversity (H' =0.50) and species richness (8 = 6) were foundin October 1986 (Figure 6). This was causedby a bloom of P. alata throughout the lagoonsystem. In consequence, the highest value ofdominance was recorded (D = 0.86) in thatmonth. The highest diversity (H' = 3.47) andthe lowest value of dominance (D = 0.017)were in June 1986. The highest species richness was in February. This indicates that amore uniform distribution of organisms fromdifferent species occurred in June 1986.

Monthly Variation of Temperature andPhytoplanktonic Abundance from 1982 to1986

The mean values of phytoplankton abundance varied from a minimum of 21,600cells 1-1 in May 1984 to a maximum 610,000cells I-I in October 1986. Three peaks ofabundance are shown in Figure 2. The firstwas in November 1982, the second in April1985, and the third in October 1986. Thesecond and third peaks coincide with theblooms of spring and autumn characteristicof temperate coastal lagoons. In the 19831984 annual cycle, the average values of


5 40

430 If)

If)

wz

I 3 ---- I----......... U----, ..... 0::-", 20,, If)2 w

S uw10 a..

If)

r1)0

L -----0 0J S N 0 J A J N J F A J 0

~1984 1985 1986 I

FIGURE 6. Variation of mean values of diversity (H'), dominance (D), and species richness (8) from June 1984 toOctober 1986.

abundance were lower, exhibiting only aspring peak of low magnitude.

A drastic drop in phytoplankton abundance was seen, with values below 100,000cells 1-1, from December 1982 until the endof 1984. The reduction in phytoplanktonabundance corresponds with the increase ofsurface water temperature caused by the "ElNino" event, which replaced the nutrient-richcoastal waters off Baja California Sur withwarm oligotrophic waters. Phytoplanktonconcentrations increased during 1985 and1986 with abundances similar to those recorded in 1982, except for the bloom observedin autumn 1986, which was the highest peakrecorded.

By comparing annual cycles (Figure 7a), athermal anomaly of +4°C can be noted during 1983-1984. The warming confirms theinfluence of the "El Nino" event along thecoast of the Mexican Pacific, particularly inthe Magdalena-Almejas lagoon system, andsupports our explanation of phytoplanktonabundance variations.

An inverse correspondence can be observedfor thermal anomalies and phytoplanktonabundance anomalies. These were detected atthe beginning of 1983 (Figure 7b). Negativeanomalies were recorded during 1983 and

1984, which coincided with marked positivethermal anomalies. Since 1985, positiveanomalies of phytoplankton abundance havebeen observed. Although these are lower,they indicate the recuperation of phytoplankton abundance in the lagoon system.

When comparing values from 1984 and1985, a drastic drop in the surface watertemperature is evident for the second year.Negative anomalies were recorded for thefirst half of the year and positive anomaliesfor the rest of the year. In addition to therelaxation phase of the El Nino warming,the "normal" temperature variations in theMagdalena-Almejas lagoon system are seen(Figure 7). Correspondingly, negative thermalanomalies during 1986 (-2.65°C) indicatecooling of the Magdalena-Almejas waters,similar to those recorded during 1981 and1982 before the onset of the El Nino event.During 1986, the average values of abundance were the highest, yielding positiveanomalies of phytoplankton abundance.

Principal Component Analysis

Only the first two components derivedshowed any relation with variations in themicrophytoplankton assemblages. The com-

I EL NINO

l4 I I a

- 3u~

(f)2w

-.J<{

~0

~rz

~ ~<{

~D--.J 0 [<{

0 ~~ ~ I ~~a::wI -II-

wu -2<{LLa::::>(f)

-3

-481 82 83

2 b(f)

W

-.J<{

~oz<{

zoI:IeZ<{--.J0...oI>I0...

1.5

0.5

J A J 0 J A J 0 J A J 0 J A J 0 J A J 0

1--1982----i 1--1983 ---j 1--1984-11--1985---1 f--1986---1

FIGURE 7. Variation of (a) thermal anomalies (from Saldierna Martinez et al. 1987) and (b) anomalies of phytoplankton abundance, 1980 to 1986.


TABLE 2

AMOUNT (%) OF VARIANCE EXPLAINED BY THE FIRST (SEASONAL) AND SECOND (ABUNDANCE) PRINCIPAL COMPONENTS

FOR THE MICROPHYTOPLANKTON ASSEMBLAGES SAMPLED AT MAGDALENA-ALMEJAS LAGOON SYSTEM, 1984-1986

1984 1985 1986

COMPONENT VARIANCE ACCUMULATED VARIANCE ACCUMULATED VARIANCE ACCUMULATED

First component 14.31 14.31 13.82 13.82 16.68 16.68Second component 12.60 26.91 11.80 25.62 15.57 32.25

ponents were defined as follows: the first isthe seasonal component, which reflects temporal variation of species throughout theyear; the second component represents theabundance or frequency of occurrence ofthe species.

Although the amount of variance explained by the two components was low(Table 2), they were used for further analysisbecause an acceptable grouping of specieswas observed. The graphic representation ofthe components and their association withthe microphytoplankton assemblages shows,for the 3 yr of the study, that much variationoccurred from one season to another in termsof species abundance, biogeographic affinities, and substrate preferences.

The 1984 cycle (Figure 8) shows fourclusters of species and their association withthe principal components. Only the springcluster had a positive correlation with thefirst component. The summer, autumn, andwinter clusters were inversely related to thefirst component, which means the groupedspecies occurred in at least two seasons.

The most abundant species in the springcluster were A. sp/endens, A. lineo/ata, 0.aurita, P. sulcata, T. favus, and the subgroupdesignated as thycoplanktonic (pennate) diatoms, indicating sediment resuspension processes. Temperate species accounted for 48%of the total. The most abundant species (related to the second component) were Rh.fragilissjmjJ. and C centralis. The only warmwater species was th. peruvlanus. The summer group was characterized by a largernumber of dinoflagellate species from warmwaters (e.g., C. fusus, N. scintillans, and P.steinii). Such tropical influence also definedthe affinity of the diatom species. Their

abundances relate the group to the secondcomponent.

The autumn cluster was inversely correlated with both components. Four subgroupscould be defined by species affinities: ubiquitous (P. alata); miscellaneous (thycoplanktonic diatoms and dinoflagellates); temperateand tropical species (N. pungens var. atlantica and C. lineatus; P. calcar avis and C.deflexum); and warm oceanic species (Rh.hyalina and C. massiliense). The lack ofassociation with seasonal or abundance patterns shows the marked transitional characteristics of Magdalena-Almejas during thattime of year. A mixture of species fromdifferent habitats and biogeographical affinities composed the winter group. The speciespresent most frequently were G. flaccida, H.sinensis, and R. stolterfothii. The last, awarm-water representative, shows a remaining tropical influence.

Figure 9 represents the 1985 cycle. Thespring and summer clusters showed a positivecorrelation with both components and weredefined mainly by ubiquitous species fromcoastal lagoons. Only in spring were twowarm-water dinoflagellates represented. Thehigh frequency of temperate species (A. glacialis, 0. aurita, and C. fusus) is explainedby the lower temperatures recorded that yearversus 1984. The autumn group was inverselycorrelated with the first component. Thisshows that no exclusive autumn species werepresent; all occurred in more than one season.The group also ll.ad a partial positive association with the second component (high abundances), especially those species from thesouthern part of the central transect in BahiaMagdalena. Species showing a negative association with this component were mainly neri-

Phytoplankton after El Niiio-GARATE-LIZARRAGA AND SIQUEIROS BELTRONES 89

0.28

0.29

.15

12°045

°Il

0 0.145

FIRST COMPONENT-0.29

0.18

WINTER

AUTUMN

-0.22

-0.32

~ 0.08 SPRINGz 49WZ ,ra 21_0a.. SUMMER~ ji4013 3_ 30 -0.02c..> I 52e~ -0 - -4Z .180c..>w(f) -0.12

• DIATOMS °DINOFLAGELLATES YSILICOFLAGELLATES VCYANOPHYTA

FIGURE 8. Graphic representation of microphytoplankton species using the first two principal components, for1984. I, Actinoptychus splendens; 2, Amphora lineolata; 3, Bacteriastrum delicatulum; 4, B. elongatum; 5, Cerataulinapelagica; 6, Ceratium deflexum; 7, C. furca; 8, C. fusus; 9, C. lineatus; 10, C. macroceros; II, C. massiliense; 12, C.trichoceros; 13, Chaetoceros compressus; 14, Ch. curvisetus; 15, Ch. didymus; 16, Ch. lorenzianus; 17, Ch. messanensis;18, Ch. peruvianus; 19, Climacodium frauenfeldianum; 20, Coscinodiscus asteromphalus; 21, C. centralis; 22, C. perforatus; 23, C. radiatus; 24, Dictyocha messanensis; 25, Dinophysis caudata; 26, D. hastata; 27, Ditylum brightwellii;28, Eucampia zodicus; 29, Guinardiaflaccida; 30, Hemiaulus hauckii; 31, H. sinensis; 32, Leptocylindrus danicus; 33,Nitzschia delicatissima; 34, N. pungens var. atlantica; 35, Noctiluca scintillans; 36, Odontella aurita; 37, Oscillatoriaerythraeae; 38, Paralia sulcata; 39, Protoperidinium assymetricum; 40, Phyrophacus steinii; 41, Pleurosigmaformosum;42, Proboscia alata; 43, Protoperidinium sp.; 44, Pseudosolenia calcar avis; 45, Rhizosolenia hyalina; 46, Rh. berognii;47, Rh. cleveii vaL communis; 48, Rh. delicatula; 49, Rh. fragilissima; 50, Rh. imbricata; 51, Rh. robusta; 52, Rh. setigera; 53, Rh. stolterothii; 54, Stephanopyxis tUTTis; 55, Thalassionema frauenfeldii; 56, Thalassiosira eccentricus; 57,Triceratium favus; 58, "tycoplanktonic diatoms;" 59, "neritic diatoms;" 60, "oceanic diatoms;" 61, "Ceratiumspp.;" 62, "Protoperidinium spp.;" 63, "dinoflagellates;" 64, "Chaetoceros spp."

tic forms (G. flaccida and Ch. debilis) or thycoplanktonic (A. sp/endens and N. cancel/ata),indicating a mixing process in the system.

Figure 10 shows four clusters of speciesfor 1986, all located in different quadrants.

The autumn cluster had a positive correlationwith the two principal components. The seasonal component was related to P. a/atamassive blooms that, because of its abundance, showed a positive relation with the


027

0.162 27.

0 44 SPRING

SUMMER

t-.,26 0Z 0" •

LLJ 0.054 46 ·72Z v 16. .59 .3 40 • .29

550 ::4a. 37~ 61.~ 13 .150 47U 33· ·35 ·10 .70Z 39. 0 500 -0.054 .41ULLJ 25.(f)

AUTUMN .67

.49

-0.162 0 12

tJ43 22.42

.20• .66

.1660 WINTER140 • .66

-0.27 .51

-0.05 0.05 0.15 0.25

FIRST COMPONENT

• DIATOMS o DINOFLAGELLATES • SILICOFLAGELLATES VCYANOPH'

FIGURE 9. Graphic representation of microphytopIankton species using the first two principal components, for1985. I, Actinoptychus splendens; 2, Amphora marina; 3, Amphora sp., 4, Asterionellopsis glacialis; 5, Bacterwstrumcomosum; 6, Bacteriastrum delicatulum; 7, Cerataulina pelagica; 8, Ceratium azoricum; 9, Ceratium dens; 10, C. furca;II, C. fusus; 12, C. horridum; 13, C. lineatus; 14, C. trichoceros; 15, Chaetoceros affinis; 16, Ch. brevis; 17, Ch. coarctatus; 18, Ch. compressus; 19, Ch. curvisetus; 20, Ch. didymus; 21, Ch. lorenzianus; 22, Ch. messanensis; 23, Ch. peruvianus; 24, Ch. debilis; 25, Climacodiumfrauenfeldianum; 26, Coscinodiscus asteromphalus; 27, C. perforatus; 28, Cylindrotheca closterium; 29, Detonula pumila; 30, Dictyocha messanensis; 31, Dinophysis forthii; 32, Distephanuspulchra; 33, Ditylum brightwellii; 34, Eucampia zodiacus; 35, Guinardiaflaccida; 36, Hemiaulus hauckii; 37, H. membranaceus; 38, Lauderia annulatta; 39, Leptocylindrus danicus; 40, Lithodesmium undulatus; 41, Navicula cancellata;42, Navicula distans; 43, Nitzschia pungens var. atlantica; 44, Noctiluca scintillans; 45, Odontella alternans; 46, O.aurita; 47, 0. mobiliensis; 48, Oscillatoria erythraeae; 49, Paralia sulcata; 50, Phyrophacus steinii; 51, Planktoniellasol; 52, Pleurosigma spp.; 53, Proboscia alata; 54, Protoperidinium claudicans; 55, P. conicum; 56, P. pellucidum; 57,P. pyrum; 58, Pseudosolenia calcar avis; 59, Rhizosolenia hyalina; 60, Rh. bergonii; 61, Rh. cleveii var. communis; 62,Rh. imbricata; 63, Rh. setigera;64, Rh. stolterfothii; 65, Stephanopyxis palmeriana; 66, Streptotheca tamensis; 67, Thalassionema-frauenfeldii:-68,_ Th. _nit.z~r;,hjQi.des,·M.,_I}JflJassiosira rotula; 70, Thalassisira sp.; 71, Thalassiothrix hetera-morpha var. mediterranea; 72, Triceratium favus. -- -- -- - -- -- - - - -- - -

second component. The winter group showedan inverse correlation with both components.It was defined mainly by ubiquitous diatomstypical of coastal environments (Ch. affinis,

Ch. curvisetus, H hauckii, and Rh. imbricata) and by the temperate dinoflagellate C.lineatus.

The spring group had an inverse correla-

Phytoplankton after EI Niiio-GARATE-LIZARRAGA AND SIQUEIROS BELTRONES 91

0.26AUTUMN

SPRING

0.156

I-.23Z

ILl0.052Z

41.0 0 8 .40ll. 59

0~ ';;0100 .33 0'CJ 350 ~ e54 0 13 .19Z0 -0.052

28.CJ 50ILl • .27(f)

62.

-0.156

.51

·12

58. .!56WINTER 0 61

-0.26 SUMMER

-0.29 -0.174 -0.058 0.29

FIRST COMPONENT• DIATOMS o DINOFLAGELLATES ~ SILICOFLAGELLATES

FIGURE 10. Graphic representation of microphytoplankton species using the first two principal components, for1986. 1, Actinoptychus splendens; 2, A. vulgaris; 3, Asterionellopsis glacialis; 4, Cerataulina pelagica; 5, Ceratiumdens; 6, C. falcatum; 7, C. furca; 8, C. fusus; 9, C. lineatus; 10, C. trichoceros; 11, Chaetoceros affinis; 12, Ch. brevis;13, Ch. compressus; 14, Ch. costatus; 15, Ch. curvisetus; 16, Ch. danicus; 17, Ch. didymus; 18, Ch. lorenzianus; 19, Ch.criophilum; 20, Coscinodiscus perforatus; 21, C. radiatus; 22, Cylindrotheca ciosterium; 23, Detonula pumila; 24, Dictyocha messanensis; 25, Dissodinium lunula; 26, Distephanus pulchra; 27, Ditylum brightwelli; 28, Eucampia zodiacus;29, Guinardiaflaccida; 30, Gymnodinium sanguineum; 31, Haslea warwikae; 32, Hemiaulus hauckii; 33, H. sinensis; 34,Leptocylindrus danicus; 35, L. mediterraneus; 36, Nitzschia pacifica; 37, N. pesudodelicatissima; 38, N. pungens var.atlantica; 39, Odontella mobiliensis; 40, Paralia sulcata; 41, Pleurosigmaformosum; 42, Proboscia alata; 43, Prorocentrum micans; 44, Protoperidinium ciaudicans; 45, P. conicum; 46, P. pellucidum; 47, Rhizosolenia hyalina; 48, Rh. fragilissima; 49, Rh. imbricata; 50, Rh. setigera; 51, Rh. stolterfothii; 52, Stephanopyxis palmeriana; 53, Thalassionemafrauenfeldii; 54, Th. nitzschioides; 55, Thalassiosira rotula; 56, "tycoplanktonic diatoms;" 57, "neritic diatoms;" 58,"oceanic diatoms;" 59, "Ceratium spp.;" 60, Protoperidinium spp.;" 61, "subgroup of dinoflagellates;" 62, "Chaetoceros spp."

tion with the first component and a positiveone with the second component. It wasdefined mostly by ubiquitous species fromneritic systems, plus three warm-water species: Rh. hyalina, C. Jalcatum, and P. pelluci-

dum. The summer cluster showed a positivecorrelation with the first component and anegative one with the second. It consisted of amiscellaneous array of diatoms from differentenvironments and biogeographical affinities.

92

Ubiquitous diatoms from coastal lagoonswere somewhat dominant.

DISCUSSION

The seasonal cycle of phytoplanktonstanding stocks observed in the MagdalenaAlmejas lagoon system exhibited the classical patterns described elsewhere for coastallagoons of temperate regions (Robinson1970). The temperature pattern was the sameas reported by Saldierna-Martlnez et al.(1987) from 1981 to 1983, with the warm(summer-autumn) and cold (winter-spring)periods being similar in both studies. Correspondingly, two annual peaks of phytoplankton abundance were recorded, one inspring and another in autumn.

Upwelling events are common off BahiaMagdalena-Almejas. Alvarez-Borrego et al.(1975) determined upwelling conditions during March, June, July, August, and Octoberwest of the bay. Upwellings are more intenseduring March and June (Bakun and Nelson1977), which explains the more prominentspring peak in April observed in our study.The resulting nutrient enrichment of the surface waters may have supported the phytoplankton abundances that coincided with thelow temperatures recorded for the westernside of the bay and were detected in ourstudy.

Earlier, Nienhuis and Guerrero (1985,1986) suggested that the higher phytoplankton biomass in Bahia Magdalena wascaused by upwellings. Guerrero-Godinez etal. (1988) determined that high primary production inside the bay depended on tidalcurrents transporting the rich upwelled waterinto the bay. This agrees with our high estimates of phytoplankton abundances forthe mouth of the bay. Tidal currents alsoresuspend bottom sediments, explaining thehigh concentrations of thycoplanktonic dia-

. t.oms in our_ samQles.~IgL the J!!gher ovt:.rallbiomass.

The observed dominance of microphytoplankton over the nanno fraction throughoutthe period of the study agrees with earlier estimates (Nienhuis and Guerrero 1986). High


phytoplankton production in coastal watersis frequently related to the larger fraction(Varela and Costas 1987). Such correspondence was noted in Magdalena-Almejas, butin some periods high production was due tohigh concentrations of nannophytoplankton.

Grazing by zooplankton can cause amarked decrease in phytoplankton abundance during summer (Dawes 1991). Inagreement with Saldierna-Martinez et al.(1987), in our study zooplankton biomass increased after the phytoplankton spring peak,reaching its peak in July 1982. The autumnblooms in October and November can be related to nutrient availability. Cushing (1975)indicated that these blooms coincide with thedecline in zooplankton biomass. Zooplankton grazing may also alter the fraction composition of phytoplankton.

Size fraction in phytoplankton may bequite important in energy transfer in theupper trophic levels (Varela and Costas1987). When microphytoplankton dominatesthe scene, the trophic chain is shorter; macrozooplankton is the sole intermediary. Thisis of utmost importance because microphytoplankton constitutes the major foodsource for several sardine species (Rojas deMendiola 1979, Kawasaki and Kumagai1984, Varela et al. 1988). In Bahia Magdalena, phytoplankton may be as much as 60%of the diet of Opisthonema libertate (RomeroIbarra and Esquivel Herrera 1989).

The species composition and relativeabundances within the assemblages did notshow constant changes or seasonal variations. Throughout the study, a few speciesdetermined the structure of the assemblages.This agrees with the reports by Nienhuisand Guerrero (1985,1986) for the 1980-1981period. About 22 phytoplankton species weredominant and may be regarded as responsible for the main phytoplankton dynamics inMagdalena-Almejas.

The hydrographic characteristics of Magdalena-Almejas, such as water temperaturevariation, are - determined· 6y -its-locationwithin a transitional zone. These, combinedwith the availability of nutrients throughperiodic upwelling events, determine the diacmic nature of the observed phytoplankton

Phytoplankton after El Nifio-GARATE-LIZARRAGA AND SIQUEIROS BELTRONES 93

species. Many important species (neritic orbenthic) in the lagoon system belong togenera that develop resting spores (Chaetoceros, Coscinodiscus, Paralia, and Odontella).This mechanism may be being used to overcome periods of unfavorable conditions.

The species responsible for most blooms inthe lagoon system was P. a/ata. It begins toproliferate when water temperature increases,becoming very abundant in the warm season,which in 1984 extended to December. According to our observations and previous reports for P. a/ata, it is a ubiquitous species,quite common along the coasts of California,Baja California, and the Gulf of California(Cupp 1943, Round 1967, Venrick 1971,Gonzalez-Lopez and Siqueiros Beltrones1990). It is adapted to proliferate in oligotrophic waters, but frequently thrives undernutrient pulses (Guillard and Kilham 1977).The transitional nature of the study areaposes an ideal environment for the behaviorof this highly opportunistic species.

The positive thermal anomalies caused bythe 1982-1983 "El Nino" lasted throughout 1984 in the California Current (Glynn1988) and were detected even into 1985inside the Magdalena-Almejas lagoon system, causing a drastic drop in phytoplanktonabundance from 1983 to December 1984.This caused a decrease in egg production forSardinops caeru/ae and an increase for Opisthonema libertate, a species of tropical affinity (Saldierna-Martinez et al. 1987), in spiteof the low estimated availability of food.

The phytoplankton recuperation processwas slow, developing in 1985 and completedby 1986. This constrasts with observationsfor the Peruvian coast, where recuperationoccurred by the end of the warming event(Barber et al. 1983). This could be becausethe warm water mass was displaced northward, where it remained, permitting normalupwelling off Peru. This did not happen alongthe west coast of southern Baja Californiawhere the upwelling was warm and poor inillllnents WielOer T984r" .~"

In both regions, the subsequent increasesin phytoplankton biomass surpassed allprevious records. During the influence ofEl Nino in 1982-1983, P. a/ata proliferated

more in the warmer months. In spite of theprevailing conditions, dinoflagellate specieswere never abundant, developing isolatedblooms of C. furca, C. fusus, and N. scintilfans, which did not displace the diatoms. Although the presence of several dinoflagellatespecies characteristic of oligotrophic warmwaters could indicate the influence of the ElNino event of 1982-1983, only C. declinatumand C. vu/tur have been closely associatedwith the event in the Gulf of Californiaand these are not considered good indicators (Gonzalez-Lopez 1994). They morelikely represent the Costa Rican Current orgulf water influence during normal oceaniccirculation.

During our study, species richness and diversity were much lower in 1984, similar tothe 1983-1984 estimates by Nienhuis andGuerrero (1986). This can be attributed tothe El Nino warming in Magdalena-Almejas.By 1985 and 1986, species richness and diversity had increased notably. Ocean circulation patterns, which determine the spatialdistribution of phytoplankton, are closelyrelated to diversity and dominance in theMagdalena-Almejas assemblages.

The low diversity and high dominancemeasurements were associated with monospecific blooms occurring all year long (P.a/ata). This is typical of coastal lagoons andis considered characteristic of immaturecommunities (Margalef 1977). The highestdiversity values corresponded to those areaswith great oceanic influence (e.g., the mouthof Bahia Magdalena). The mixing of differentwater masses causes an increase in diversity(Margalef 1977). In shallow systems, diversity rises because of mixing with benthicdiatom associations.

The species composition analysis usingprincipal components confirms the above.This analysis was a useful tool to permit theidentification of associations among the species and to describe their seasonal variation.According to seasonal and abundance compOiients~austersofspec[esoTdiverse habitatsand biogeographical affinities were defined.These reflected the transitional nature of thestudy area, showing the influence of the California Current and warm waters.

94

The discussion above describes the conditions during 1984. The following year thewaters were colder, and a typical behavior ofthe system was expected, except perhaps forthe thermal anomaly at the end. But thepositive association of the spring clusters remained, corresponding with the abundancepeak. The rest of the groups varied more orless erratically.

Finally, the reestablished colder conditions in 1986, similar to those in 1981-1982,precluded the proliferation of warm-waterspecies, although they did appear in summerwhen a mixture of species with different biogeographical affinities occurred. The influenceof benthic forms indicates the importance ofmixing processes in a system that dependson tidal periodicity, given the shallow depthof the system.

The particular hydrological conditionsof Magdalena-Almejas are the main factorsdetermining variations in the associationstructure of phytoplankton assemblages. Although the subtropical definition of the region ensures a constant supply of temperateand tropical species and favors the establishment of euritolerant and diacmic species, thetransitional nature of the study area somewhat clouded the effects of the 1982-1983 ElNino on the phytoplankton assemblages.

ACKNOWLEDGMENTS

We acknowledge Gerardo Verdugo Diazand Rafael Guerrero for providing data onphytoplankton abundance. We thank EllisGlazier for editorial help with English in themanuscript.

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time variation in phytoplankton assemblages in a ...time variation in phytoplankton assemblages in a...

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