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Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia) Anissa Souissi a , Sami Souissi a, , Mohamed Néjib Daly Yahia b a Université des Sciences et Technologie de Lille-Lille 1; Laboratoire d'Océanologie et de Géosciences, UMR CNRS 8187 LOG, Station Marine de Wimereux, 28 avenue Foch, F-62930 Wimereux, France b Laboratoire de Bio-surveillance de l'Environnement, Groupe de Recherche en Planctonologie et en Hydrologie, Faculté des sciences de Bizerte, Zarzouna, Bizerte 7021, Tunisia Received 11 June 2007; received in revised form 6 December 2007; accepted 11 December 2007 Abstract Abundance and reproductive traits (spawning female, egg production, egg hatching success) and naupliar survival of the dominant calanoid copepod Centropages kroyeri were investigated in relation to biotic (chlorophyll a, phytoplankton and microplankton) and abiotic (temperature and salinity) parameters at a monitoring station located in Bizerte Channel, northern Tunisia. The monitoring was carried out between July 2004 and December 2004, according to two temporal sampling strategies. First, during July, the supposed maximum abundance period of C. kroyeri, daily sampling was conducted. Thereafter, sampling was carried out weekly until the end of the sampling period. The temporal variability of the environmental factors in relation to the reproductive traits of C. kroyeri revealed, first, that temperature is important in controlling the reproduction and dynamics of this species, and second, that the quantity and quality of food available in the field also strongly influence its reproduction. On several sampling dates, the output of certain reproductive traits such as hatching success after 24 h was very weak. It is possible that C. kroyeri produced resting eggs during the study period. Nerveless, the analysis of the phytoplankton during these periods showed that low reproductive activity may have been caused by low phytoplankton quantity and/or by the dominant presence of certain diatom species that are supposed to have an inhibitory effect on the reproductive traits of C. kroyeri, especially on egg hatching success. Among the considered external parameters, temperature and food quality and availability seem to be the most important factors for the reproduction and dynamics of C. kroyeri. Under these biotic and abiotic field conditions, this copepod seems able to modulate the abundance of its population while controlling its reproduction. © 2007 Elsevier B.V. All rights reserved. Keywords: Abundance; Bizerte Channel; Centropages kroyeri; Phytoplankton; Reproductive traits; Temperature 1. Introduction Calanoid copepods are the dominant secondary producers of pelagic ecosystems, and play a considerable role in the transfer of energy and organic matter from primary producers to higher trophic levels (Mauchline, 1998 and references therein). The reproduction of pelagic copepods constitutes an appreciable physiological indication of the water quality (Paffenhöfer and Knowles, 1978). The survey of reproductive traits of copepods is therefore necessary to investigate recruitment variability in the natural habitat (Edmondson, 1962) and to understand the routes of energy transfer in the pelagic food web (Lee et al., 2003). Copepods are constantly confronted with variations of abiotic and biotic factors which can affect their growth, their reproduction or the progress of their life cycle. Many studies have shown that water temperature and quantity and quality of the food available to copepods represent the main factors affecting reproduction (Abou Debs and Nival, 1983; Ban, 1994; Halsband-Lenk et al., Journal of Experimental Marine Biology and Ecology 355 (2008) 125 136 www.elsevier.com/locate/jembe Corresponding author. Tel.: +33 321 992 908; fax: +33 321 992 901. E-mail address: [email protected] (S. Souissi). 0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2007.12.011

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Page 1: Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

and Ecology 355 (2008) 125–136www.elsevier.com/locate/jembe

Journal of Experimental Marine Biology

Temporal variability of abundance and reproductive traits ofCentropages kroyeri (Calanoida; Copepoda) in Bizerte

Channel (SW Mediterranean Sea, Tunisia)

Anissa Souissi a, Sami Souissi a,⁎, Mohamed Néjib Daly Yahia b

a Université des Sciences et Technologie de Lille-Lille 1; Laboratoire d'Océanologie et de Géosciences, UMR CNRS 8187 LOG,Station Marine de Wimereux, 28 avenue Foch, F-62930 Wimereux, France

b Laboratoire de Bio-surveillance de l'Environnement, Groupe de Recherche en Planctonologie et en Hydrologie, Faculté des sciences de Bizerte,Zarzouna, Bizerte 7021, Tunisia

Received 11 June 2007; received in revised form 6 December 2007; accepted 11 December 2007

Abstract

Abundance and reproductive traits (spawning female, egg production, egg hatching success) and naupliar survival of the dominant calanoidcopepod Centropages kroyeri were investigated in relation to biotic (chlorophyll a, phytoplankton and microplankton) and abiotic (temperatureand salinity) parameters at a monitoring station located in Bizerte Channel, northern Tunisia. The monitoring was carried out between July 2004and December 2004, according to two temporal sampling strategies. First, during July, the supposed maximum abundance period of C. kroyeri,daily sampling was conducted. Thereafter, sampling was carried out weekly until the end of the sampling period.

The temporal variability of the environmental factors in relation to the reproductive traits of C. kroyeri revealed, first, that temperature isimportant in controlling the reproduction and dynamics of this species, and second, that the quantity and quality of food available in the field alsostrongly influence its reproduction. On several sampling dates, the output of certain reproductive traits such as hatching success after 24 h wasvery weak. It is possible that C. kroyeri produced resting eggs during the study period. Nerveless, the analysis of the phytoplankton during theseperiods showed that low reproductive activity may have been caused by low phytoplankton quantity and/or by the dominant presence of certaindiatom species that are supposed to have an inhibitory effect on the reproductive traits of C. kroyeri, especially on egg hatching success.

Among the considered external parameters, temperature and food quality and availability seem to be the most important factors for thereproduction and dynamics of C. kroyeri. Under these biotic and abiotic field conditions, this copepod seems able to modulate the abundance of itspopulation while controlling its reproduction.© 2007 Elsevier B.V. All rights reserved.

Keywords: Abundance; Bizerte Channel; Centropages kroyeri; Phytoplankton; Reproductive traits; Temperature

1. Introduction

Calanoid copepods are the dominant secondary producers ofpelagic ecosystems, and play a considerable role in the transferof energy and organic matter from primary producers to highertrophic levels (Mauchline, 1998 and references therein).

The reproduction of pelagic copepods constitutes anappreciable physiological indication of the water quality

⁎ Corresponding author. Tel.: +33 321 992 908; fax: +33 321 992 901.E-mail address: [email protected] (S. Souissi).

0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.jembe.2007.12.011

(Paffenhöfer and Knowles, 1978). The survey of reproductivetraits of copepods is therefore necessary to investigaterecruitment variability in the natural habitat (Edmondson,1962) and to understand the routes of energy transfer in thepelagic food web (Lee et al., 2003). Copepods are constantlyconfronted with variations of abiotic and biotic factors whichcan affect their growth, their reproduction or the progress oftheir life cycle. Many studies have shown that watertemperature and quantity and quality of the food available tocopepods represent the main factors affecting reproduction(Abou Debs and Nival, 1983; Ban, 1994; Halsband-Lenk et al.,

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126 A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

2001; Devreker et al., 2005). It has been shown that temperatureis a key parameter which can affect the reproduction ofcopepods by regulating their metabolic rate (Hirche et al.,1997). Therefore, the values of reproductive traits of copepodsmay be indicative of food and thermal conditions where theylive (Halsband-Lenk et al., 2001; Ianora et al., 2007). Theimpact of food quality, especially when it is composed ofdiatoms, on the reproductive traits of copepods has lately beenthe topic of several studies (e.g., Kleppel and Burkhart, 1995;Lacoste et al., 2001; Ianora et al., 2003). Miralto et al. (1999)showed that some diatom species can inhibit the reproductiveoutput of copepods by the production of certain chemicalcompounds that limit their egg production and hatching success.

In the Mediterranean, most investigations have been carriedout off the northern coasts, and studies of copepod ecology offthe southern coasts are few. In the southwestern Mediterranean,the northern coasts of Tunisia represent an interesting hydro-logical zone forming the connection between the western andeastern basins of the Mediterranean (Souissi et al., 2000). Thisarea is affected by the Atlantic Current, whereas the offshore andcoastal areas are more affected by local processes (loading, etc.).

Centropages kroyeri Giesbrecht, 1892 is a dominant speciesoff the southwestern Mediterranean coast, where it replaces itscongener C. typicus (Daly Yahia et al., 2004), which dominatesoff the northern coast of the western Mediterranean basin(Souissi et al., 2001; Molinero et al., 2005). Conversely to theabundant studies on C. typicus, little is known of the ecologyand population dynamics of other Centropages species,particularly for some of them that need careful morphologicalanalysis to distinguish between them such as C. ponticus,C. hamatus and C. kroyeri (Soler et al., 1988). Little attentionhas been given to the reproductive biology of C. kroyeri. Exceptfor a single paper concerning the ultrastructure of C. kroyerireproductive morphology (Corni et al., 2000), the egg pro-duction and, more generally, the dynamics of this key species

Fig. 1. Location of the sampling sit

off the south coasts of the western Mediterranean are littleknown.

In this study, our goal was to characterize the temporalvariability of the reproductive traits of C. kroyeri in relation toenvironmental factors, and to investigate the dynamics of thiscalanoid copepod during the summer and autumn of the year2004.

2. Materials and methods

Plankton was collected in a coastal sampling site ‘Point C’(37°16'1"N; 9°52'50"E) located in Bizerte Channel near theSea (Fig. 1). This channel is a transition area between BizerteBay, which opens directly to the Mediterranean Sea, and BizerteLagoon, which is under the influence of terrestrial input (Fig. 1).The tidal regime is dominated by a semi-diurnal cycle andcharacterized by low amplitude that rarely reached 15 cm duringspring tide (Harzallah, 2002). Although the low tidal activity inthis region the highest current velocities were recorded in themiddle of the channel and can reach 1 m/s (Harzallah, 2002).

No initial hypothesis of the pertinent temporal scale wasconsidered, because the reproduction of C. kroyeri had not beenstudied at this transition site. Consequently, daily sampling wascarried out during 30 days in the beginning of the study (July, 5–August, 3, 2004), corresponding to the seasonal peak ofabundance of this species observed in a neighbouring area, theBay of Tunis (Daly Yahia et al., 2004). Thereafter, samplingcontinued weekly until the end of the study period. For eachsampling date, two horizontal hauls were taken at the surfacelayer, with a 200 µm-mesh Hansen net to collect zooplanktonsamples. One sample was preserved in 2% buffered formalde-hyde-seawater for later enumeration and identification ofcopepods. The other, live sample was brought to the laboratorywithin 15 min after collection, and adult females of C. kroyeriwere immediately sorted individually for experiments. According

e ‘point C’ in Bizerte Channel.

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127A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

to the small size ofC. kroyeri, our sampling net only captured latedevelopmental stages which are mainly composed by adults andsometimes late copepodids C5. Then males and females ofC. kroyeri were identified and counted according to their charac-teristic morphological criteria (Rose, 1933; Soler et al., 1988;Corni et al., 2000).

Temperature (°C), salinity (‰) and chlorophyll a (Chl a)content (µg/l) were also measured from surface-water samplestaken with a 2-l Ruttner bottle. Water temperature was measuredusing a Testomicro thermometer. For the salinitymeasurements, aWTW LF 196 salinometer with a microprocessor and automaticcompensation was used. Chl a concentration was determined byspectrophotometric analysis after filtration of 1 l of water througha GF/C Whatman filter. Daily air temperature and precipitationwere obtained from the Meteorological Monitoring Station atBizerte, which is close to our sampling site.

Fig. 2. Temporal variation in water and air temperature (A), salinity and precipitatiothrough December 2004 in Bizerte Channel.

Microplankton samples were collected using a 2-l Ruttnerbottle at the surface layer and fixed with 2% bufferedformaldehyde. In order to determine quantity and quality of thediet available for copepods, microplankton cells were countedusing an inverted microscope following Throndsen (1995), andthe different groups were identified.

At certain dates, when the egg hatching success rate was verylow or nil, the species composition of diatoms was checkedagain in order to test at least the hypothesis of inhibition due tocertain diatom species. Because the incubation period of eggswas 24 h, it was not possible to test the hypothesis of existenceof resting eggs.

In the laboratory, 30 females of C. kroyeri randomly sortedfrom the sample (at certain dates, when females were rare, asmall number (b15) were used) were incubated individually inbeakers equipped with 200 µm mesh chambers filled with 35 ml

n (B) and chlorophyll a concentration (C) at the surface layer, from July 2004

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128 A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

of filtered seawater (GF/C Whatman, 0.45 µm porosity). Theinner chamber was used for separating eggs and females, andthus prevented cannibalism. The beakers were incubated atambient temperature with the natural day-light photoperiod.After 24 h, females were removed and preserved in 2% bufferedformaldehyde-seawater for later measurement of the prosomelength, using a video image digitizing system connected to aLeica binocular microscope. Then, the egg production wasestimated by counting eggs in each beaker. Egg productionduring the first 24 h of incubation reflects the feeding history ofthe females in the field (Laabir et al., 1995; Hirche et al., 1997;Devreker et al., 2005).

All of the newly spawned eggs found in the beakers werecombined in a small recipient in filtered sea water at roomtemperature, to facilitate observation of egg hatching after 24 h,allowing the estimation of hatching success. Finally, in order tostudy maternal effects on the new born nauplii, these later aregrouped in a new container filled with freshly filtered seawaterusing a GF/C Whatman, 0.45 µm porosity. Then the survival ofthe nauplii under starvation is a measure of quality of reservestransferred by mothers (Devreker et al., 2004) was determinedfor each cohort 24 h and 48 h after their emergence from allhatched eggs.

All measured parameters were correlated with reproductivetraits of C. kroyeri using the Pearson correlation test. To avoidmisinterpretation of results, only highly significant correlationlevels were considered in this analysis.

In order to quantify the temporal variability of all measuredparameters at the daily scale during July 2004 and also at theweekly scale for the period August–December 2004, thecoefficient of variation (CV (%)=100×SD / Mean) was used.

Finally the study period was separated into two seasons:summer (July–September) and autumn (October–December).Because the total number of females observed during summerwas much higher than those observed during autumn, the use ofstandard statistical tests to compare both seasons can be biased.Consequently we calculated the probability density functions offemales' prosome length and females' egg production rate(EPR) for each season. Then the observed cumulative distri-butions were fitted with a normal cumulative density functionby using Curve Fitting Toolbox of Matlab software ver. 7.01(Mathworkc, Inc.). The mean (µ) and standard deviation (σ)

Fig. 3. Temporal variation in the abundance of the population of Centropages kroyeri

were estimated for each distribution with 95% confidencebounds. This procedure permits to compare the effect of seasonon the whole distribution of each considered parameter.

3. Results

3.1. Temperature, salinity and chlorophyll a concentration

During the study period, temperature decreased from 27.5 °Cto 15.1 °C with a mean of 23.3 °C (Fig. 2A). Temperaturevariability is mainly driven by season; consequently thecoefficient of variation at the daily scale (CVd) during July2004 was low (0.86%) compared to the variability measured atthe weekly scale between August and December 2004(CVw=18.52%).

The salinity of the surface water in the Bizerte Channeloscillated between a minimum of 36.3 and a maximum of 38.1(Fig. 2B). The highest salinities were recorded from August toOctober, and coincided with high temperatures. Salinitydecreased to 36.8 during November, after an increase inprecipitation (Fig. 2B).

Chlorophyll a concentration was characterized by similarfluctuations at daily and weekly scales (CVd=76.94% andCVw=76.57%), showing a minimum of 0.32 µg/l, a maximumof 18.6 µg/l and a mean of 3.5 µg/l. The highest concentrationswere recorded during July, with a daily mean of 4.52 µg/l and amaximum of 18.6 µg/l, which may reflect phytoplanktonproliferation. The weekly mean during the rest of the studyperiod was only 2.10 µg/l (Fig. 2C).

3.2. Temporal variation of C. kroyeri population dynamics

During the study period, the population of C. kroyeri showeda fluctuating density that was higher at the weekly scale(CVw=134.3%) than at the daily scale (CVd=91.05%).Abundance varied between a minimum of 1.3 ind/m3 inNovember and a maximum of 773.5 ind/m3 in July (Fig. 3).This species seems to have a preference for warm water: onaverage its abundance was 238 ind/m3 during summer, whereasthe autumnal abundance was only 18.0 ind/m3.

Females of C. kroyeri were always more abundant thanmales. The mean ratio of males/females was 0.24. Males were

at the surface layer from July 2004 through December 2004 in Bizerte Channel.

Page 5: Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

Fig. 4. Temporal variation in the sex ratio (male/female) of C. kroyeri in Bizerte Channel from July 2004 through December 2004.

129A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

entirely absent during the last week of October, throughoutNovember, and in the first half of December 2004 (Fig. 4).

The prosome length of females fluctuated between aminimumof 525 µm in July and a maximum of 855 µm towards the end ofOctober (Fig. 5). The mean value calculated for the entire studyperiod was 614 µm, with a summer mean of 579 µm and anautumnal mean of 717 µm; thus the prosome length seemed to beinfluenced by the temperature. In fact, this parameter wasnegatively correlated with temperature (r=−0.664; pb0.01).

3.3. Reproductive traits

The percentage of spawning females was highly variable,particularly at the weekly scale after July, with a CVw of 73.11%(CVd=38.31%). Indeed, in one week this percentage fluctuatedfrom 87.5% (October 4) to 15.4% (October 11), beforeincreasing again to 65.2% one week later. This variability wasalso observed at the daily scale, for example on July 14, wherethe percentage was 76.6% and decreased to 12.5% one day later(Fig. 6A).

During the study period, the percentage of spawning femalesshowed a mean of 43.5%, with maxima of 83.3% and 87.5%during July and October, respectively.

Fig. 5. Temporal variation in the prosome length of C. kroyeri f

From the beginning of the sampling period until October 19,the percentage of spawning females fluctuated between 12.5%and 87.5%. After this date, the percentage progressively de-creased, to 3.3% and then reached 0 (November 21, December 5and 26 respectively). Thereafter, it rose to a new peak of 50% inmid-December. This period of percentage decrease and eventualabsence of spawning females corresponds to the same period ofabsence of males in our samples (Fig. 4.); whereas the maximumvalue observed inDecember coincides with the increase in the sexratio. The percentage of spawning females was positivelycorrelated with the sex ratio (rp=0.35, pb0.02). The temporalevolution of the egg production rate showed a strong weeklyvariability: CVw was 82.4% whereas CVd was only 26.7%.

Fig. 6B showed that during summer, egg production rate variedbetween 3.2 and 13.1 eggs f −1 d−1 whereas in autumn all themaxima were recorded with 20.3 and 34.5 eggs f −1 d−1 inOctober (4/10 and 31/10, respectively) and 25.66 and 24 eggsf −1 d−1 in December (12/12 and 19/12). The low rates of eggproduction observed in this period seem to be a direct con-sequence of the decrease and zeroing of the sex ratio (Fig. 4) andthe percentage of spawning females.

The hatching success rate of C. kroyeri fluctuated during thestudy period, more so during the second period of study

emales. Vertical bars correspond to one standard deviation.

Page 6: Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

Fig. 6. Temporal variation in reproductive features of C. kroyeri in Bizerte Channel. (A) Percentage of spawning females; (B) egg production after 24 h, vertical barsrepresent one standard deviation; (C) hatching success.

130 A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

(CVd=99.96%; CVw=181.37%). The overall success rate wasvery low, with a mean of 10.9% and a maximum of 52%.Summer seemed to be favorable to hatching success, indeed allthe maxima were recorded in summer, more precisely duringJuly (Fig. 6C).

The hatching success rate showed two critical periods of sharpdecrease and zero. The first period was observed during summer,between August 2 and September 13. The second period occurredin autumn, betweenNovember 7 andDecember 12. The autumnalperiod with no hatching success coincides with the zero valueobserved for the previous reproductive traits. These criticalperiods may be the result of inhibitory factors (i.e., deleteriouseffects of diatoms) as well as the absence of either males orspawning females.Moreover, the percentage of spawning femalesseems to be a good indicator of the quality of reproduction,because it was correlated with both egg production rate andhatching success (Table 1).

The high number of observed females during the study periodallowed performing accurate statistical analyses. Among a total of1221 females observed individually 569 were spawning females.Fig. 7B shows a clear shift towards the right of the EPRdistribution during autumn compared to summer. Particularly thedifference between summer and autumn distributions increasetowards the high percentiles. The same pattern was observed forthe distributions of female's prosome length (Fig. 7A). Largerfemales of C. kroyeri were observed during autumn when theaverage temperature was 19.24 °C (SD=3.12 °C) whereas theaverage temperature during summerwas 24.78 °C (SD=1.48 °C).

The rate of naupliar survival showed high variability at bothtemporal scales (after 24 h: CVd=209.46%, CVw=182.38%and after 48 h: CVd=304.15%, CVw=307.16%). Survivalremained extremely low during the entire study period, with amean of 11.85% 24 h after hatching and 2.43% after 48 h. Thehighest survivorship was recorded on December 19, when after

Page 7: Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

Fig. 7. Cumulative probabilities of the female's prosome length distributions (A)and egg production rate distributions (B) for summer (July–September) andautumn (October–December). The observed distributions (filled circles:summer; open diamonds: autumn) were fitted by a cumulative normalprobability (continuous black line: summer; continuous grey line: autumn).The initial number of individual females (n); the fitted parameters (µ and σ) andthe determination coefficient (R2) are shown in figure legend.

131A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

24 h, 100% of the total number of hatched nauplii survived, and62.5% after 48 h. Most of the time, there was no survivorship,especially in summer, when no nauplii survival was recorded inalmost the entire period from July to mid-September (Fig. 8).

3.4. Quality and quantity of food

During the study period, the microplankton community inBizerte Channel was composed of 96% phytoplankton and 4%ciliates. Phytoplankton was represented mainly by 41% diatoms,26% dinoflagellates, 26% chlorophytes and 7% cryptophytes(Fig. 9). Ciliates comprised 90% of non-tintinnids and only10% of tintinnids. Microplankton showed a mean density of16 · 104 cells/l with a minimum of 9 · 104 cells/l and a maximumof 60.2 · 104 cells/l. All microplankton maxima were observedduring summer. Of these microplankton cells, diatoms showed amean density of 5.5 · 104 cells/l, fluctuating between a minimumof 0.3 · 104 cell/l and a maximum of 19 · 104 cells/l.

Diatoms were composed mainly by the genera Thalassio-sira, Chaetoceros, Pseudo-nitzschia, Nitzschia, Rhizosoleniaand Leptocylindrus. For the summer period, Thalassiosira andChaetoceros were the characteristic genera, representing46.9% and 16.7% of total diatoms. During autumn, the diatom

assemblage was dominated by Rhizosolenia, Pseudo-nitzschia,Chaetoceros and Leptocylindrus, representing 32.4%, 22%,17.7% and 17.6%, respectively.

Dinoflagellates showed a mean density of 3 · 104 cells/lreaching a maximum of 10 · 104 cells/l in July (Fig. 9B). Thisphytoplankton class was represented mainly by the generaGymnodinium, Prorocentrum and Hermesinium. During sum-mer, dinoflagellates were represented by Gymnodinium (60%),Prorocentrum (31%) and Hermesinium (6%). In autumn, theproportion of Gymnodinium increased to 70%, whereas Pror-ocentrum decreased to 27% and Hermesinium was absent.

Other phytoplankton classes were also observed in the BizerteChannel, such as Chlorophytes and Cryptophytes. These twoclasses had a preference for the summer period, since theirmaximum concentrationswere observed in Julywith 21 · 104 cell/lfor Chlorophytes and 13 · 104 cell/l for Cryptophytes (Fig. 9B).

3.5. Effects of temperature, salinity and food conditions onreproductive traits

Reproductive traits of C. kroyeri are under the influence andcontrol of all surrounding factors, including abiotic and bioticparameters. Temperature and salinity seem to be important abioticparameters for the reproduction ofC. kroyeri. Temperature showeda significant positive correlation with the percentage of spawningfemales (rp=0.49; pb0.01) and a negative one (rp=−0.36;pb0.01) with the nauplii survival rate after 48 h of egg hatching.The same pattern was observed for salinity, but the correlationswere weaker than those for temperature. Female prosome lengthappeared to influence the reproductive traits: it was negativelycorrelated with the percentage of spawning females (rp=−0.451;pb0.01) and the hatching success rate (rp=−0.340; pb0.02), andpositively correlated with the egg production rate (rp=0.418;pb0.01) (Table 1).

The survey of the links between food conditions (micro-plankton components in the field) and the reproductive traits ofC. kroyeri revealed the existence of a positive correlationbetween the quantity of microplankton in the field andchlorophytes, with the percentage of spawning females andthe hatching success rate. The presence of ciliates in themicroplankton samples seemed to enhance reproduction ofC. kroyeri by increasing the percentage of spawning females.But it is difficult to confirm this hypothesis, because ciliates didnot dominate during the study period, and the significance levelsof correlations are low. Finally, correlations between hatchingsuccess rate and the concentrations of cryptophytes and diatomswere low.

4. Discussion

We have shown that reproductive features of C. kroyeri inBizerte Channel varied seasonally. C. kroyeri seems to be oneof the most important calanoid species in this ecosystem, whichis much warmer than the northern European coasts. This speciesis much smaller and seems to be more thermophilic than itscongener C. typicus, which is better studied off the northernMediterranean coasts. As far as we know, the present study is

Page 8: Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

Table1

Pearson

correlationcoefficients(r)betweenpaired

biological

andenvironm

entalfactorsmeasureddu

ring

thestud

yperiod

(Julythroug

hDecem

ber20

04)in

Bizerte

Chann

el

SF

EP

HS

NS1

NS2

SR

PL

TS

CHL

MD

DN

CH

CR

CL

SF

10.138

0.34

4⁎⁎

0.17

90.04

30.352⁎⁎

−0.45

2⁎⁎⁎

0.493⁎

⁎⁎0.116

0.235

0.312⁎

0.31

3⁎0.001

0.390⁎⁎⁎

0.082

0.27

8⁎

EP

1−0.03

10.48

0⁎⁎⁎

0.55

4⁎⁎⁎

0.165

0.41

8⁎⁎⁎

−0.081

0.284⁎

−0.045

−0.036

−0.00

3−0.065

−0.146

−0.098

−0.02

6HS

10.42

1⁎⁎⁎

0.05

60.018

−0.34

0⁎⁎

0.227

−0.304⁎

0.556⁎⁎⁎

0.255

0.14

30.221

0.639⁎⁎⁎

0.350⁎⁎

0.21

8NS1

10.71

9⁎⁎⁎

0.319⁎

0.12

5−0.180

0.066

0.012

0.029

0.05

6−0.060

0.178

0.096

0.04

0NS2

10.272

0.33

1⁎⁎

−0.364⁎

⁎⁎0.077

−0.080

−0.118

−0.118

0.013

−0.059

−0.076

−0.12

2SR

1−0.17

80.308

0.385⁎⁎⁎

−0.035

0.116

0.09

00.074

−0.152

−0.133

0.07

3

Significancelevels:⁎pb0.05;⁎⁎

pb0.02

;⁎⁎

⁎pb0.01.

SF,percentage

ofspaw

ning

females;E

P,eggproductio

nrate;H

S,h

atchingsuccessrate;N

S1,nauplii

survivalrate24

hafterhatching;N

S2,nauplii

survivalrate48

hafterhatching;S

R,sex

ratio

;PL,prosomelength;

T,temperature;S,

salin

ity;CHL,chlorophy

llaconcentration;

M,microplankton

(D+DN+CH+CR+CL);D,diatom

s;DN,dino

flagellates;CH,chlorophy

tes;CR,cryptophy

tes;CL,ciliates.

132 A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

the first one focusing on C. kroyeri reproduction and dynamics.In the context of climate change and particularly the conse-quences of future temperature increases for Mediterranean bio-geography and ecosystem reorganization, studies of southerncoasts are necessary. These ecosystems are characterized by thedominance of small copepods, which are important for pelagicecosystems (Turner, 2004) and may be incipient ecologicalsystems for future climate changes.

4.1. Percentage of spawning females

The percentage of spawning females was strongly correlatedwith temperature and with microplankton and phytoplanktonabundances (respectively rp=0.49; pb0.01; rp=0.36; pb0.01and rp=0.35; pb0.02). In fact, this percentage reached somemaxima not only when the temperature increased but also whenphytoplankton densities were high, as on August 10 when thetemperature showed a maximum of 27.5 °C and the percentageof spawning females increased to 60%. The situation onOctober 4 showed a coincidence between a high phytoplanktoncell density (18 · 104 cells/l) and the maximum percentage ofspawning females (87.5%). This percentage may have beenincreased by the combined effects of an increase in bothtemperature and phytoplankton quantity, which was the case forthe August 26 sampling showing 73.3% spawning females.

A negative correlation was also found between the percentageof spawning females and prosome length (rp=−0.452; pb0.01).This can be attributed to the influence of temperature on body size(rp=−0.664; pb0.01), which increases with decreasing tempera-ture (Devreker et al., 2005), thus affecting the reproductivepotential of the females (Halsband-Lenk et al., 2001).

According to these results, we confirm here that temperatureand quantity of food available are important parameters for thereproduction of C. kroyeri, as shown for other copepod species(Abou Debs and Nival, 1983; Ban, 1994; Ianora, 1998;Halsband-Lenk et al., 2001). Temperature directly affectsmetabolic activity, and also increases the copepod reproductionby accelerating the maturation of the oocytes (Ianora, 1998;Halsband-Lenk et al., 2002). The availability and the quantity offood are two determining factors that strongly affect ingestionand therefore reproductive output (Devreker et al., 2005).

The variability observed in the percentage of spawningfemales of C. kroyeri may be caused by turbulence and by thecontinual presence of currents that can have a negative effect onfemale spawning. Higher levels of turbulence can decrease eggproduction if maintained for long periods (Irigoien et al., 2000).

The summer period is characterized by temperatures andphytoplankton densities favorable for the increase of thepercentage of spawning females. During autumn, this percentagedecreased progressively following the gradual decrease oftemperature and the quantity of food. In addition to temperatureand food quantity, other factors may be the cause of the decline inpercentage of spawning females. The progressive decrease in thispercentage was followed by two dates of zero (at the end ofNovember and at the beginning of December), which coincidedwith the period of absence of males. We can also assign a highproportion of the decrease in the percentage of spawning females

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Fig. 8. Temporal variation in the survival rate of C. kroyeri nauplii, 24 h (black line) and 48 h (gray line) after hatching in the laboratory.

133A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

to the reduction or to the absence of fertile females, seeing that thispercentage was enhanced by the presence of males at the end ofDecember. Recently, Kiørboe (2007) showed that the growth ofthe population of the small copepod Oithona davisae is severelylimited by fertilization rate and by a shortage of males.

4.2. Egg production rate

The mean value of egg production (9.1 eggs per female perday) was higher in autumn, with a mean of 12.2 eggs f −1 d−1

against a mean of 8.0 eggs f −1 d−1 in summer. This ratefollowed inversely, on one hand the percentage of spawning

Fig. 9. Temporal variation in the densities of ciliates (A) and diatoms, dinoflagellatesDecember 2004.

females was higher in summer with 49.5% against 25.8% inautumn, and on the other hand the C. kroyeri population wasmore abundant in summer. We may hypothesize that thefemales of C. kroyeri undergo the density-dependence effect,consisting of the production of fewer eggs when the populationdensity is high in summer, and the production of large clutcheswhen its population density decreases.

According to the strong positive correlation found withfemale body size (rp=0.418; pb0.01), egg production rateseemed to be influenced by the size of females. With the bias oftemperature on the seasonal temporal scale, egg production iscontrolled by body size; in fact, females are large in the cold

, chlorophytes and cryptophytes (B) in Bizerte Channel from July 2004 through

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134 A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

season and consequently can produce larger clutches than insummer (Halsband-Lenk et al., 2001, 2002).

As in the case of the percentage of spawning females, eggproduction showed a progressive decrease to zero during theperiod that coincided with the absence of males. We can ascribethis phenomenon to two reasons: either to the logical con-sequence of the absence of spawning or fertile females, or to theabsence of re-mating because some copepod species require re-insemination to maintain their production.

Aswe previously showed, the percentage of spawning femalesofC. kroyeriwas affected by the quantity of food available, whichwas mainly composed of diatoms; therefore they constituted adominant part of the females' diet. However, the presence ofciliates in the diet can apparently increase the percentage ofspawning females, but in view of the quantity of diatoms, we candeduce that the presence of ciliates in the food of C. kroyerifemales is negligible.

The effect of quality and quantity of the food ingested by thefemales will affect their reproductive traits, especially at the levelof egg production and hatching success rates (Lacoste et al., 2001;Calbet et al., 2002). Several studies have demonstrated the directrelationship between egg production and ingestion rates ofcopepods (Sanders et al., 1996; Bonnet and Carlotti, 2001; Damand Lopes, 2003). Recently, other studies have also shown thatfluctuations in the hatching success rate can be explained by thequality of food available, particularly when it is composed ofcertain diatom species that can alter the embryogenesis and reducehatching success rate and egg viability (Laabir et al., 1995; Banet al., 1997; Miralto et al., 1999; Ianora et al., 2004). Classically,diatomswere considered to be a good source of food for copepods,encouraging their production (Turner, 1984; Mann, 1993).

4.3. The hatching success rate

The hatching success rate was low during the entire studyperiod, with a mean value of 10.9%. On average only 3.2% ofeggs hatched during autumn whereas during summer the meanhatching success was 13.6%. The decrease in water temperatureduring autumn necessarily affected some reproductive pro-cesses and embryo development. Consequently, the hatchingsuccess rate might be directly or indirectly affected bytemperature although the absence of statistical evidence(Table 1). C. kroyeri mean density decreased drastically froman average value of 237.7 ind/m3 during summer to 18 ind/m3

during autumn. Even if our experimental protocol was notdesigned to study egg diapause, the very low hatching successduring the study period and particularly during autumn may bedue to egg diapause production. Recently Wu et al. (2007)studied the seasonal reproductive biology of Centropagestenuiremis in a coastal area and found that the production ofsubitaneous EPR decreased during summer and autumn whenthe species switches to produce diapause eggs. Other species ofthe genus Centropages are known to produce resting eggs(Marcus and Lutz, 1998). The seasonal patterns of egg pro-duction in temperate freshwater calanoid copepods alreadyshowed a switching from subitaneous to diapausing eggs duringsummer and autumn (Ban and Minoda, 1991; Lohner et al.,

1990). It is thus probable that C. kroyeri produced diapausingeggs during the study period. Even if Centropages typicus ismuch more studied than C. kroyeri, there is no evidence thatC. typicus produces diapause eggs (Ianora et al., 2007). Conse-quently careful studies are still needed in the future to de-monstrate that both C. typicus and C. kroyeri are capable ofproducing diapause eggs.

The hatching success of C. typicus showed high fluctuationsduring seasons in the North Sea (Wesche et al., 2007) and also inthe Gulf of Naples (Carotenuto et al., 2006). In these studies thehatching success rates of C. typicus were much higher than thosereported in our study for C. kroyeri. It is impossible in our case todistinguish between subitaneous and diapause eggs (if they areproduced), but other environmental factors, such as the direct orindirect negative effects of the diatom dominated diet in the field,can also explain the low hatching success observed here and itshigh variability at both daily and weekly scales. Chaudron et al.(1996) showed that the process of inhibition is food density-dependent. The higher the density of diatoms and the longer theyare ingested by copepods, the lower the hatching success. Indeed,all maxima recorded for the hatching success rate occurred in July,which was characterized by maximum abundances of chloro-phytes, dinoflagellates or cryptophytes, and also the first period ofzero hatching success rate coincided with the maximum ofdiatoms. We noticed that when diatom densities decreased, aprogressive increase in egg hatching success occurred. During thisperiod the dominant diatom species wereChaetoceros curvisetus,Dactyliosolen fragilissimus, Pseudo-nitzschia delicatissima andPseudo-nitzschia seriata. The second zero period seems to bethe logical consequence of the yield of the other reproductive traits(percentage of spawning females and egg production). At thesame time, we also noted an increase in diatom density, withdominance of the speciesP. delicatissima,Rhizosolenia delicatulaand D. fragilissimus. Between these two zero periods, thehatching success rate was slightly enhanced, coinciding with alower abundance of Pseudo-nitzschia.

The diatom species that have an inhibitory action on egghatching success of copepods contain compoundswith deleteriouseffects (Ban et al., 1997; Miralto et al., 1999, 2003; Ianora et al.,2003). The responsible agents are secondary metabolites (e.g.,aldehydes) that represent chemical defenses of the diatoms againstthe herbivorous copepods by potentially sabotaging their futuregenerations (Miralto et al., 2003; Cebellos and Ianora, 2003).Aldehyde production occurs following the damage in diatom cellsdue to feeding, in a process similar to the wound reaction in higherplants (Pohnert, 2000).

P. delicatissima produces these reactive unsaturated alde-hydes that have deleterious effects on copepod embryogenesis(Miralto et al., 1999). Therefore, we can suppose that such aphenomenon occurred during our study, and was responsible forthe sharp reduction to zero of the hatching success rate.

Several studies on the action of the aldehydes produced byD. fragilissimus on copepod embryogenesis have shown that thisspecies may not produce the unsaturated aldehydes described forP. delicatissima, or produce others with less toxic effects oncopepod embryogenesis and hatching success (Miralto et al.,1999, 2003). However, two strains of diatoms from different

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135A. Souissi et al. / Journal of Experimental Marine Biology and Ecology 355 (2008) 125–136

geographical zones can have different inhibitory effects oncopepod hatching success (Miralto et al., 2003). Therefore, in ourfield study, we can hypothesize that D. fragilissimus may haveinhibited the egg hatching success of C. kroyeri.

4.4. The nauplii survival rate

In order to assess the quality of the hatched eggs, the survivalrates of larval stages of C. kroyeri after 24 h and 48 h ofhatching were estimated. Actually, these rates were very low.The nauplii survival rate after 24 h followed very closely thehatching success, and the rate after 48 h was low in comparisonwith survival after 24 h. This parameter followed closely thevariations of the other reproductive traits, but showed somedifferences owing to the influence of environmental factors onembryogenesis (Carotenuto et al., 2002; Devreker et al., 2004).In fact, this rate was negatively correlated with temperature(rp=−0.36; pb0.01), suggesting that high temperatures wereresponsible for the naupliar mortality and that low temperaturesencourage their survival. Indeed, the maximum of 62.5%observed for the nauplii survival rate after 48 h occurred whenthe temperature reached its minimum of 15.1 °C.

Ianora et al. (2004) showed that maternal diatom diets affect notonly egg hatching success but also the development of nauplii thatemerge. They suggested the existence of amechanismof transfer ofaldehydes via feeding and accumulation of toxins in the oocytesduring vitellogenesis. Also, early naupliar stages of copepods donot feed and rely on maternal yolk reserves (Marshall and Orr,1955; Devreker et al., 2004; Carotenuto et al., 2006). Therefore, theproduction of nonviable or deformed nauplii seems to be the resultofmaternal consumption of diatoms that induce teratogenesis in thedeveloping embryo and have insidious effects on larval postem-bryonic growth (Carotenuto et al., 2002; Ianora et al., 2003).

The low survival rate may either be due to abnormal naupliithat were unable to develop, or to unfavorable field conditions.In fact, on the basis of the suggestion that nauplii are capable ofdrinking, Carotenuto et al. (2006) concluded that high naupliarmortality may be related not only to poor maternal diets but alsoto the quality of the water in which the nauplii emerge. Inaddition to these studies, our results showed that this rate maybe impaired by high temperatures; indeed, temperature can be alimiting factor for nauplii survival or for copepod reproductivebiology (Halsband-Lenk et al., 2002).

5. Conclusion

Our results quantified for the first time the high variability ofthe key environment factors affecting copepod reproduction andrecruitment in an understudied area in the southern Mediterra-nean Sea. Among planktonic copepods, C. kroyeri is the mainspecies during the second half of the year (July–December).During the study period,C. kroyeri showed population dynamicsthat followed a daily and seasonal variability, and seemed to begoverned by summer environmental factors (e.g., temperature)and was characterized by a dominant presence of females.

The maturation of C. kroyeri females and their reproductivetraits were linked both to temperature variations and food

availability in the field, which consisted mainly of diatoms. Femalefecundity was closely dependent on the presence of males; indeedtheir absence in autumn caused a very low reproductive output.

The egg production rate (EPR) and female's body size differedsignificantly between summer and autumn, with larger femalesand higher EPR observed in autumn. These results suggest thatC. kroyeri undergoes the density-dependence effect and that theegg production rate is influenced by the female body size. It wasnot possible to distinguish in this study between subitaneous anddiapause eggs. However, the low hatching success observedduring the study period and particularly during autumn can be dueto the production of diapausing eggs. The conditions in which thefemales lived were reflected in the quality of the spawned eggsand in their viability. Indeed, food ingested especially when it isconstituted by some diatom species with inhibitory effects, canalso be responsible for hatching failure at certain dates and for thelow survival rate of nauplii. The influence of temperature was alsoimportant for nauplii survival. However, the verification of thesehypotheses requires careful studies in the future with adequateexperimental protocol.

Acknowledgements

We thank J.C. Molinero and P. Elayaraja for their commentson the manuscript. G.A. Boxshall and C. Razouls are thankedfor their verification of the taxonomy of C. kroyeri. J.W. Reidrevised the English text. This work was presented during the 9thInternational Conference on Copepoda, Hammamet, Tunisia,July 11–15, 2005. It was partially funded by the TunisianMinistry of Research through its program of collaboration withTunisian Competences Abroad. We are deeply grateful toAbderrahmene Ben Radhia for his precious help during all stepsof this study and for his assistance during sampling. [SS]

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