The influence of temperature and presence of predators on growth, survival and energy allocation for...

The influence of temperature and presence of

predators on growth, survival and energy allocation

for reproduction in the Catarina scallop

Argopecten ventricosus

Citlali Guerra1,2, Alfonso Nivardo Maeda-Mart|¤ nez2, Alfredo Hernandez-Llamas2, MariaTeresaSicard-GonzaŁ lez

2, Stefan Koenigstein1, Doris Abele1 & Eva E R Philipp3

1Department of Functional Ecology, AlfredWegener Institute for Polar and Marine Research, Bremerhaven, Germany2Centro de Investigaciones Biolo¤ gicas del Noroeste, La Paz, Baja California Sur, Me¤ xico3Institute of Clinical Molecular Biology, Christian-Albrechts University Kiel, Kiel, Germany

Correspondence: DAbele, Department of Functional Ecology, AlfredWegener Institute for Polar and Marine Research, Am Handelsha-

fen12, 27570 Bremerhaven, Germany. E-mail: [email protected]

Abstract

Environmental factors are known to modify the lifehistory of marine ectotherms. In a16-month labora-tory experiment, we investigated the in£uence oftemperature and presence of predators on life-his-tory parameters including shell growth, survivaland the energy investment in reproduction and bodymass of the short-lived (2^3 years) scallopArgopectenventricosus. In parallel,A. ventricosuswasmaintainedin the ¢eld at the Paci¢c coast of Baja California, Me¤ x-ico, to compare growth, survival and reproductive ef-fort under natural conditions. For the laboratorytreatments, scallops were reared at simulated ¢eldtemperatures (SFT), 5 1C above SFT and in the pre-sence of predators. Elevated water temperaturescaused higher growth and gonad production,although at the cost of increased mortality. Presenceof predators induced energy allocation to musclerather than gonad growth, deferred spawning andextended survival. Field scallops exhibited highergrowth, higher reproductive investment and wereable to reproduce twice, whereas all laboratory scal-lops died after the ¢rst spawning. The natural varia-bility of environmental parameters such as food andtemperature may thus support optimal growth in the¢eld, andwhenanimals are protected frompredators,reproduction in the second year of life.

Keywords: Argopecten ventricosus, temperature,predation, energy allocation

Introduction

Bivalves o¡er a rich diversity of lifestyles and adapta-tions to environmental conditions and are ideal mod-el organisms to study the in£uence of intrinsic andextrinsic variables on life-history parameters suchas growth, reproduction, ¢tness and senescence(Abele, Brey & Philipp 2009; Philipp & Abele 2010).The short lifespan of 2^3 years (Pen� a 2001) and thelong-standing use of the Catarina scallop (Argopectenventricosus) in aquaculture (Felix-Pico 1993; Maeda-Mart|¤ nez, Reynoso-Granados, Monsalvo-Spencer,Sicard-GonzaŁ lez, Mazo¤ n-SuaŁ stegui, Hernandez,Segovia & Morales 1997; Sicard-GonzaŁ lez, Maeda-Mart|¤ nez, Reynoso-Granados, Ormart-Castro, & Car-valho1999; Steller & CaŁ ceres-Mart|¤ nez 2009) renderthis species an ideal model to investigate the in£u-ence of environmental factors on life-history para-meters in laboratory experiments covering thespecies lifespan.Di¡erences in food levels and water temperatures

have been suggested to cause di¡erential maturity,growth and survival of A. ventricosus populationswhen cultivated at di¡erent sites on the coast of theBaja California Peninsula, Me¤ xico (Cruz, Ramirez,Garcia & Ibarra 1998; Cruz, Rodriguez-Jaramillo &Ibarra 2000). Villalaz (1994) found that gametogen-esis in A. ventricosus maintained in controlledlaboratory conditions occurs primarily at low phyto-plankton densities, whereas high phytoplanktonconcentrations increased muscle growth. However,

Aquaculture Research, 2011, 1^11 doi:10.1111/j.1365-2109.2011.02885.x

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the author did not observe a relationship between re-productive condition and water temperature.The presence of predators can also in£uence

growth, reproductionand physiological performanceof a species. Anti-predator responses, includingchanges of shell morphometrics (length and width)and thickening of di¡erent shell sections, such as theumbo or the lid, are observedwhen exposing bivalvesor gastropods to waterborne predator cues or cagedpredators (Leonard, Bertness & Yund 1999; Delgado,Glazer & Steward 2002; Cheung, Lam, Gao, Mak &Shin 2004). Lafrance, Cliche¤ , Haugum and Guderley(2003) observed wild scallops (Placopecten magellani-cus) to have stronger shells and perform a moreintense escape response compared with culturedindividuals, which they attributed to the presence ofstar¢sh in the natural environment. If the energybudget does not su⁄ce for the mechanical and phy-siological arms race with the predator, reproductioncan be altered. Hoverman, Auld and Relyea (2005)showed that the occurrence of predators deferred re-production and accelerated growth of the freshwatersnail Helisoma trivolvis.Although many studies have shown the e¡ect of

one or more environmental factors on physiologicalparameters in laboratory experiments, most investi-gations are limited to short periods of time.These stu-dies miss the in£uence of environmental factors overlonger time periods and through di¡erent ontoge-netic stages. Our study presents a long-term investi-gation of the e¡ects of elevated temperature and thepresence of predators on growth and survival rates,and on the alternating energy investment into repro-duction and body mass over the lifetime of Catarinascallops. For a better understanding of the naturalconditions, scallops produced in the same cohortwere reared in the ¢eld and investigated in parallelto the laboratory experiment.

Material and methods

Brood stock and larvae culture

Sixty mature adult A. ventricosus were purchasedfrom local ¢shermen in August 2007 in Bah|¤ a Mag-dalena. Animals were transported as described byMaeda-Mart|¤ nez, Sicard and Reynoso-Granados(2000) to the hatchery station of CIBNOR. Spawningof mature scallops was induced by the thermal shockmethod, following Uriate, Guilherme and Abarca(2001). Larvae settlement in the tanks occurred natu-rally. Larvae were maintained at 25 � 1 1C in1500 L

tanks and fed a1:1 ratio of Isochrisis galbana and Pav-lova lutheri during their ¢rst 13 days. On day 14, thediatoms Chaetoceros calcitrans and Chaetoceros graci-lis were added to the food mix to an end concentra-tion of 3:1:2:1 respectively. After 47 days, the scallopswere transferred to tanks with a continuous upwel-ling £owof 5000 L day�1using the same microalgaespecies for feeding. In October 2007, the animalsreached the harvest size of 5^7mm shell height(Maeda-Mart|¤ nez et al.1997). At the time, the spat wasdivided into two groups one of whichwas returned tothe ¢eld, whereas the other group was kept for labora-tory treatments (temperature and predation).

Field study

Approximately10000 scallops of 5^7mm shell heightwere transported to Rancho Bueno estuary, in the vi-cinity of Bah|¤ a Magdalena in October 2007 (geogra-phical position: 24119017.300N, 111125037.300W). The¢eld site chosen in the present study represents a ben-e¢cial environment forA. ventricosuswith high chlor-ophyll concentrations and the optimal temperaturewindow for growth (Acosta-Ruiz & Lara-Lara 1998;Sicard-GonzaŁ lez 2006). Scallops were kept in ¢nemesh bags (2mm) ¢tting within 20 nestier trays(55 � 55 � 8 cm) suspended in a long-line systemfor 2 months, until reaching an average size of24mm (December 2007). Subsequently, animalswere kept without bags in the trays. Initial stockingdensity was set at 500 animals tray�1 (equivalent to1700 animals m�2) for optimal growth (Maeda-Mar-t|¤ nez et al. 1997) and adjusted to 150, 90 and 60 ani-mals tray�1 (495, 297 and 198 animalsm�2) after187, 337 and 480 days (February, July and December2008) in order to keep densities optimal for growth.

Laboratory study

The laboratory study started in November 2007. Scal-lops of 7^9mm shell height were kept in a £ow-through system of 12 aquaria (70 � 60 � 16 cm)with a constant water £ow of 210 L day�1, using� 630 scallops aquarium�1. Initial stocking densitywas � 1500 animalsm�2 in order to keep similarinitial densities as in the ¢eld. No densityadjustmentswere carried out in the laboratory, as densities werealways lower than in the ¢eld. Incoming seawaterwas ¢ltered over a sand ¢lter (Jacuzzi 225 L, LittleRock, AR, USA) and a1 mm gaft ¢lter. Of the12 aqua-ria, eight were held at simulated ¢eld temperature

In£uence of temperature and predation on Argopecten ventricosus C Guerra et al. Aquaculture Research, 2011, 1^11

2 r 2011 Blackwell Publishing Ltd, Aquaculture Research, 1^11

(SFT) and four at 5 1C above SFT (SFT15 1C). Simu-lated ¢eld temperature values were deduced from¢eld measurements. A temperature logger recordedwater temperature at 60min intervals (WTA32-5137, Onset Computer, Bourne, MA, USA) attachedto one of the nestier trays. The temperature loggerwas collected and replaced during ¢eld trips atmonthly intervals; in addition, the water tempera-ture in the SFT treatments was adjusted to monthlyaverage ¢eld temperature (FT) and controlled usingaquarium heaters (Hagen Aquaclear 22952). Thus,the temperature in the SFT treatments representsthe mean FTof the previous month (Fig.1).Temperatures in the laboratory £uctuated daily by

about 3 1C with1peakday�1. In the ¢eld, two distinctpeakswithina daywere recorded andawider thermalwindow of oscillation of about 5 1C (Fig. 2) was

observed. In fall (August 2008^October 2008), FTsranged close to the species-speci¢c lethal temperatureof 29 1C (Sicard-GonzaŁ lez et al.1999). During this peri-od, the temperature limit in the laboratory was set at27 � 1 1C in the SFT15 1C treatment to limit mortal-ities linked to high-temperature exposure. The SFTtreatment was kept at 5 1C below the SFT15 1C treat-ment throughout the experiment, except in November2007 and May and June 2008, where only 3^4 1Cdi¡erence could be adjusted (Fig.1).The SFT1predator experiment started in April

2008. Predators were introduced in four SFTaquaria(1crabaquarium�1). Crabs were kept in the aquaria6 hday�1 for 5 days week�1. The crabs’pincers wereheld together by rubber bands to prevent them fromeating scallops. Crabs were fed squid every thirdnight in a separate aquarium.

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Figure 1 Argopecten ventricosus. Mean values of temperatures during the experimental period. The monthly average FTwas simulated in the laboratory1month later (see ‘Material and methods’). SFT, simulated ¢eld temperatures; SFT15 1C,5 1C above SFT; SFT1predator, SFT with the presence of predator; and FT, ¢eld temperatures.

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Figure 2 Argopecten ventricosus. Example of daily temperature £uctuations in the laboratory (black line) and in the ¢eld(grey line) during 2 weeks in June 2008. Each vertical line represents1day.

Aquaculture Research, 2011, 1^11 In£uence of temperature and predation on Argopecten ventricosus C Guerra et al.

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The scallops were fed ad libitum throughout theexperiment usinga1:1mixture ofC. calcitransand I. gal-bana delivered by an automated system containing amixing tankandaturbidimeter-controlled pump (Hach1720, Loveland, CO, USA). Cell concentrations weremonitored using a Coulter Cell Counter (Multisizer 3,Beckham, Coulter, Fullerton, CA, USA). Concentrationvaried between 60000 and 250000 cellsmL�1 in themixing tank and between 20 and 50 cellsmL�1 ineach aquarium throughout the experimental time,ensuring that scallops were fed at satiety. Salinity waskept at 33^36 p.p.t., similar to values found in the ¢eldsite (SaŁ nchez-Montante, Zaitsev&Saldivar-Reyes2007).

Data collection and analysis

Shell height growth

Shell height (distance from hinge to distal shell mar-gin) was measured monthly using calipers: forSFT scallops, measurements were undertaken fromOctober 2007 to October 2008, for SFT15 1C fromNovember 2007 to October 2008, for SFT1predatorfrom April 2008 to October 2008 and for the ¢eldscallops (FT) from October 2007 to October 2008.Scallops were randomly selected at each samplingdate: Field: 2 animals nestier tray�1 (a total of 40animals); Laboratory: 10 animals aquarium�1 (atotal of 40 animals). The growth of scallops wassubsequently calculated using the model proposedby Ratkowsky (1986), which is an alternate parame-terization of the von Bertalan¡y growth model withclose to linear behaviour. This model was shown tobemore reliable than the conventional von Bertalanf-fy equation, because it allows nonlinear regressionsto converge easily and to conduct tests for parameterinvariance more precisely (Hernandez-Llamas & Rat-kowsky 2004):

Ht ¼ hi þ ðhf � hiÞð1� km�1Þ=ð1� kn�1Þ ð1Þ

whereHt is the calculated height of scallops at time t,hi the initial height, hf the ¢nal height, k the growthcoe⁄cient, n the number of data points and m thetime modi¢ed according to:

m ¼ 1þ ðn� 1Þðt� tiÞ=ðtf � tiÞ ð2Þ

where ti is the initial time and tf the ¢nal time.

Shell weight to shell height ratio

In order to investigate whether the scallops developheavier shells under predation pressure, shells of the

SFTand SFT1predatorgroupwere used to determinethe shell weight/shell height ratio.

Survival

Animal survival in the laboratory was measured bymonthly counts of dead animals in each experimen-tal aquarium over scallop lifetime: SFT from Decem-ber 2007 to October 2008 (150^410 days of age),SFT15 1C from December 2007 to December 2008(150^480 days of age) and SFT1predator from May2008 to February 2009 (280^540 days of age). Survi-val in the ¢eld was recorded in February, Julyand De-cember 2008 when scallops’ number had to beadjusted in the nestier trays (see ‘Field study’).

Tissue indices

For gonadosomatic, muscle, mantle, gill and condi-tion indices, scallops were sacri¢ced and tissue freshweight, total freshweight, as well as shell weight wasdetermined using a digital balance (Precisa XT320M, Precisa Instruments AG, Dietikon, Switzer-land). The indices were calculated as follows:

Tissue index ¼ ðweight of component tissue=

total tissueweightÞ100

Condition index ¼ ðtotal tissueweight=

shell weightÞ100

Statistical analysis

Di¡erences in shell growth parameters between thedi¡erent treatmentswere calculatedwith nonlinear re-gression analysis using GRAPHPAD PRISM (version 5.0 forWindows, GraphPad Software, San Diego, CA, USA).Signi¢cant di¡erences indicate di¡erences in growthamong treatments using the least restrictive invar-iance test, analysing the parameters hi 5 initial height,hf 5¢nal height and k5growth coe⁄cient actingtogether (for references of the method, see also:Hernandez-Llamas, Magallon-Barajas, Lechuga-Devez,Bustillos-Guzman & Lopez-Cortes1995; Osuna-Garc|¤a,Hernandez-Llamas & Mazo¤ n-SuaŁ stegui 2008).Di¡erences in survival between laboratory treat-

ments were assessed with the Kaplan^Meier method.Kaplan^Meier survival curves were constructedusing the known birth and death dates of each indi-vidual. This method allows comparison of two ormore survival curves over time and the calculationstake into account censored observations because ofsamplings for analysis. The log-rank test (log), as im-



plemented in the program PASW STATISTICS 18 version18.0.0 (SPSS, Chicago, IL, USA), was used (for refer-ences of the method see also Motulsky 1995). One-way analysis of variance (ANOVA) and Tukey’s post hoctest (unequal sample size) or the Student t-test wasused for analysis of indices after testing for normalitywith the Kolmogorov^Smirnov test (GraphPad Prism5.0 Software). Index values were arcsine transformedand are presented as back-transformed means.

Results

Shell growth

Treatment a¡ected ¢nal shell height (hf) (Fig. 3,Table1). Applying Eqn (1) to growth datayielded signi¢cantdi¡erences between SFT and SFT15 1C as well asbetween SFT and FT treatments (Po0.0001,Table 1).Exposure to predators did not in£uence shell growth,but resulted in signi¢cantly heavier shells inOctober 2008 after exposure to predators for 6months (Table 2).

Survival

Using the Kaplan^Meier model, lower survival ratesfor the SFT15 1C treatment compared with SFT ani-mals were detected (log, wdf51

2 � 71.247, Po0.001)(Fig. 4a). Around October 2008 (410 days of age), al-most all scallops in the SFTand SFT15 1C laboratorytreatments died after a massive spawning event. Theremaining scallops in the SFT15 1C treatment livedfor another 2 months and the last individuals (2.6%of initial population) were sacri¢ced in December2008 for analysis (480 days of age). Individuals inthe SFT treatment had a lower survival rate com-pared with individuals of the SFT1predator treat-ment (log, wdf51

2 � 30.193, Po0.001, Fig 4b). The

di¡erence was due to the high mortality followingthe spawning in October 2008 in the SFT treatment.Survival rates before the spawning event did not dif-fer between both treatments (wdf51

2 � 0.4, P50.5).The last scallops of the predator-exposed group weresacri¢ced in February 2009 (540 days of age). Wecould not compare survival rates of SFT vs. FT withthe Kaplan^Meyer model because of the small num-ber of samplings in the FT treatment. However, in De-cember 2008, when all SFT animals were alreadydead,10% of the initial population in the ¢eldwas stillalive and ¢eld scallops lived up toAugust 2009.

Tissue indices

Tissue indices were determined to evaluate thealternating energy investment into reproduction[gonadosomatic index (GSI)] and other body mass

Table 1 Growth parameters of Argopecten ventricosus using Eqn. (1)

Treatment hi hf k P Time period

SFT 6.9 � 1.5 31.9 � 4 0.93 � 0.01 o0.0001 October 2007–October 2008

FT 6.9 � 1.5 51.2 � 4.4 0.89 � 0.01

SFT 8.5 � 1.4 31.9 � 4 0.98 � 0.03 o0.0001 November 2007–October 2008

SFT15 1C 8.5 � 1.4 37.2 � 1.7 1.0 � 0.02

SFT 18.3 � 1.6 31.9 � 4 0.97 � 0.1 0.672 April 2008–October 2008

SFT1predator 17.9 � 2 32.5 � 2 0.92 � 0.07

Signi¢cant P-values indicate di¡erences in growth among treatments using the least restrictive invariance test (i.e. testing the para-meters acting together). N540 for each treatment.SFT, simulated ¢eld temperatures; SFT15 1C, 5 1C above SFT; SFT1predator, SFT with presence of predator; FT, ¢eld; hi, initial height(mm); hf, ¢nal height (mm); k, growth coe⁄cient.

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Figure 3 Argopecten ventricosus. Shell growth � SEM (inheight) in di¡erent treatments.N540 for each treatment.Fitted growth curves correspond to Eqn. (1). SFT, simu-lated ¢eld temperatures; SFT15 1C, 5 1C above SFT;SFT1predator, SFT with the presence of predator; andFT, ¢eld temperatures.



components (muscle, mantle and gill) over time.Gonadosomatic index di¡ered signi¢cantly between¢eld-reared and laboratory SFTanimals (Fig.5a). Thehighest GSI within the ¢eld treatment was measuredin August 2008 (ANOVA, Po0.0001) after meantemperatures rose from 22 to 27 1C in only 1month.The scallops spawned thereafter, which is indicatedby the decrease in GSI. In the SFTgroup, the highestGSI was observed 2 months later in October2008 (ANOVA, P 50.0026) simultaneously with theSFT15 1C scallops (ANOVA, Po0.0001). After reach-ing the maximum gonad index, SFT and SFT15 1Cscallops spawned, and almost all animals died. Peakgonad indices in FT, SFT15 1C and SFT were12.57 � 2.4%, 10.15 � 1.5% and 7.09 � 1.31%,respectively, and signi¢cantly higher for FT andSFT15 1C individuals compared with SFT scallops

(FT vs. SFT: t-test, Po0.001; SFT vs. SFT15 1C: t-test,P50.006). In the SFT1predator group, the maximalgonad index was measured in December 2008(5.83 � 1.2%) (ANOVA, Po0.0001) and was signi¢-cantly lower than the maximal GSI in the SFTgroup(SFT vs. SFT1predator: t-test, P50.02). Scallopsspawned thereafter (pers. obs.), which caused adecrease in GSI.Muscle and condition indices followed an inverse

pattern to the GSI in all treatments (Fig. 5b and c).Peak muscle and condition indices were higher inFT individuals compared with SFT scallops (t-test,Po0.0001) and occurred in June 2008 in FT and inAugust 2008 in SFT scallops. In the SFT1predatorgroup, the highest muscle index was observed inAugust 2008 and condition index in October 2008and both were higher than peak indices in the SFTgroup (SFT vs. SFT1predator: muscle index: t-test,Po0.0001; condition index: t-test, P 50.005). No dif-ferences in peak muscle index between SFT andSFT15 1C were found (t-test, P50.2) but the lattergroup displayed higher maximal condition index(t-test, Po0.0001) in August 2008.In the SFT15 1C group, the mantle index in-

creased signi¢cantly between April and August2008 and decreased in October 2008 (ANOVA,Po0.0001, Fig. 5d). The mantle index did not varywith time in SFT, SFT1predator and FT group (SFT:ANOVA, P50.22; SFT1predator: ANOVA, P50.09; FT:ANOVA, P50.44). This index was signi¢cantly higherfor SFT15 1C and the SFT1predator individualscompared with SFT scallops in August and October

(b)(a)

Figure 4 Argopecten ventricosus. Survival analysis using the Kaplan^Meier method and the log-rank test for comparisonof curves. (a) SFT (solid line) vs. SFT15 1C (dashed line) (initialN5635). (b) SFT (solid line) vs. SFT1predator (dashed line)(initialN5250). SFT, simulated ¢eld temperatures in laboratory; SFT15 1C, SFT 5 1C above SFT; SFT1predator, SFTwiththe presence of predator.

Table 2 Argopecten ventricosus. Shell weight to shell heightratios

Treatment April 2008 August 2008 October 2008

SFT 0.144 � 0.008 0.14 � 0.009 0.13 � 0.012

SFT1predator 0.15. � 0.009A 0.16 � 0.01 0.2 � 0.015�

�Indicate signi¢cant di¡erences between treatments in the re-spective month (t-test, Po0.05).AIntroduction of predators. Means � SEM (N510^16). Di¡erentletters indicate signi¢cant di¡erences between treatments (t-test,Po0.05).SFT, simulated ¢eld temperature in the laboratory; SFT1preda-tor, SFT with presence of predator.



2008 (SFT15 1C vs. SFT August 2008: t-test,Po0.0001; October 2008: P50.0036; SFT vs.SFT1predator August 2008: t-test, P50.01; October2008: P50.003). Field scallops tended to have lowestmantle indices compared with SFT, but was only sig-ni¢cantly di¡erent in August 2008 (Fig.5d).Di¡erences in gill index were signi¢cant when

comparing SFT and SFT15 1C scallops in Augustand October 2008 (t-test in August: t-test, P50.001;October: t^test, P50.0045) and between SFTand FTin April and August 2008 (t-test, Po0.0001, Fig.5e).

Discussion

Growth and survival

In this long-term experiment, we observed increasedshell growth (height) in scallops exposed 11monthsto 5 1C elevated temperatures (SFT15 1C: 22.1^27.5 1C) compared with scallops grown at SFT (17.2^23.0 1C). This contrasts results obtained by Sicard-GonzaŁ lez et al. (1999), who observed decreasedgrowth in juveniles from the same population accli-mated for 55 days to higher temperatures (25 and

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Figure 5 Argopecten ventricosus. Gonadosomatic (a), muscle (b), condition (c), mantel (d) and gills (e) indices in the di¡er-ent treatments.Values are means � SEM (N 58). Details of statistical di¡erences are given in the text. SFT, simulated ¢eldtemperatures in laboratory; SFT15 1C,5 1C above SFT; SFT1predator, SFT in the presence of predator; and FT, ¢eld.



28 1C) compared with a control group maintained atlower temperature (19 and 22 1C). This discrepancyarises from comparing short-term with long-terminvestigations such as the present study, in whichhigher growth for SFT15 1C scallops occurredonly after 7 months of exposure (from June 2008on). We propose that the higher mortality in theSFT15 1C group from April 2008 on (250 days ofage) possibly selected for scallops of better physiolo-gical condition and stronger growth in this laterperiod of the long-term experiment.Within the laboratory treatments, we observed an

increase in condition index in SFTand SFT15 1C be-tween April and August 2008. Thus, scallops in bothlaboratory treatments gained in tissueweight relativeto shell weight indicating good general growth con-ditions. This index was higher in survivors of theSFT15 1C scallops. Higher tissue weight gain wasdue to higher mantle and gill growth, whereas mus-cle and gonad grew less. Higher mantle andgill indices in the SFT15 1C group in August 2008may a¡ord better oxygen uptake (gill and mantle)and food absorption (gill) at the higher temperature,where oxygen solubility is decreased and scallopmetabolism is higher. Indeed, food absorption rateswere higher in SFT15 1C animals in April andAugust 2008 (data not shown).The higher condition index in ¢eld scallops before

maturation, the strikingly higher shell growth overthe entire study period and longer survival comparedwith laboratory SFT animals imply that controlledconditions (e.g. temperature control and normalizedmicroalgal mixture) are not optimal to sustain phy-siological status. Sicard-GonzaŁ lez (2006) found thatoscillating night and day temperatures led to fastergrowth of the scallopNodipecten subnodosus, and thatindividuals exposed to thermal £uctuations livedlonger, in spite of earlier onset of reproduction whencompared with animals maintained permanently atan experimentally determined optimum tempera-ture. In our study, the in£uence of the tides in the ¢eldresulted in more pronounced thermal £uctuationscompared with the day and night oscillations in thelaboratory (Fig. 2). In addition, food quality and com-positionat the scallop experimental ¢eld site (RanchoBueno in Bah|¤ a Magdalena) are more variable inalgal species composition (GaŁ rarte-LizaŁ rraga, Band-Schmidt,Verdugo-D|¤ az, Mun� eto¤ n-Go¤ mez & Fe¤ lix-Pico2007) compared with the uniform control feedingregime in the laboratory. Under ¢eld conditions,scallops preferentially allocated energy into muscleand gonad rather than in mantle and gill growth

compared with SFT and SFT15 1C scallops. Thisdi¡erential energy investment into tissues in ¢eldand laboratory scallops may have important implica-tions for growth, reproduction and survival. Appar-ently, ad libitum feeding with a standardizedplankton mixture does not present the same foodquality as the natural algal community of the habitatand indicates variability and diversity to be more im-portant for the scallops’ physiological conditionsthan the food quantity.Scallops reared in the presence of predators in-

vested signi¢cantly more energy into muscle thangonad growth (Fig. 5a and b) and developed heaviershells (Table 2). Similarly, blue mussels, Mytilusedulis, develop stronger byssal attachments, thickershells and larger adductor muscles in the presenceof star¢sh and crab predator signals (Reimer &Tedengren 1996; Reimer & Harms-Ringdahl 2001).Thus, predator-exposed animals appear to investmore energy into defensive mechanisms, which maydelay reproduction.

Reproduction

Argopecten ventricosus grown in the ¢eld as well as inall laboratory treatments displayed a conservativegametogenic cycle, meaning that gametogenesis isfueled by energy stored in tissues, mainly the adduc-tor muscle (Luna-Gonzalez, Caceres-Martinez, Zun� i-ga-Pacheco, Lopez-Lopez & Ceballos-Vazquez 2000).Dependence of the gonad energy allocation onmuscle mass was con¢rmed even for the older ¢eldanimals (data not shown) and corroborates earlierstudies of A. ventricosus from di¡erent sites of BajaCalifornia Sur (Felix-Pico1993). Epp, Bricelj and Mal-ouf (1988) suggested that mantle tissue mayalso playa role as energy storage site for gonad development,and mantle mass declines as gonads mature.We ob-served a slight decrease in mantle index in maturescallops in all treatments, which was, however, onlysigni¢cant in SFT15 1C scallops.Field animals reached maturation in August 2008

concomitantly with a pronounced increase in tem-perature by 5 1C between July and August 2008. Inmarine po|« kilotherm species, temperature plays animportant role throughmodulation of most physiolo-gical processes, including reproduction (Clarke1987;Lubet 1983; Jalabert 2005). In Bah|¤ a Magdalena, A.ventricosus is known to reproduce throughout theyear with two main spawning peaks in March^Apriland August^September when water temperatures



are 19^23 1C and 27^28 1C respectively (Felix-Pico1993). However, in a laboratory study,Villalaz (1994)found no evidence for a direct e¡ect of water tem-perature on scallop reproductive condition. Instead,temperature, together with food abundance as a sec-ond important parameter, modulates gonad develop-ment in mature animals. The authors suggested thattemperature could be important as both, an initiatorof gametogenesis and as a spawning cue. In thelaboratory, the delay in maturation in SFT andSFT15 1C could be linked to the more modestincrease in temperature by 2 1C between July andOctober 2008, and could further re£ect the delay inwater temperature change in the laboratory, whichwas lagged by 1 month compared with FT. Despitehigher investments in reproduction of ¢eld comparedwith SFTscallops, (shown by the higher GSI) scallopsin the ¢eld survived and reproduced again in the sec-ond year. In contrast, the SFTand SFT15 1C animalsreproduced virtually to death in October 2008, whenalmost all individuals died after the ¢rst spawning.Exposure to predators under laboratory conditions

delayed maturation for 2 months. The e¡ect was notrelated to temperature, which was the same in theSFTas in the SFT1predator treatment. Scallops livedlonger, but at the costs of a decrease in reproductiveoutput, deduced from a lower GSI compared withscallops reared without predators. This con¢rms thatpredators can modulate prey life-history traits suchas age and size at maturation, reproductive outputand mean lifespan (Abrams 1993, Abrams & Rowe1996, Stearns 2000, Beckerman, Wieski & Baird2007). The optimal investment into life history traitswill depend on the environmental conditions that or-ganisms experience during lifetime (Alonso-Alvarez,Bertrand, Devevey, Prost, Faivre, Chastel & Sorci2006). When A. ventricosus scallops are su⁄cientlyprotected from predators, and when food and tem-perature conditions are favourable, investment notonly in growth but also in reproduction is possible.In the present study, ¢eld animals were protected innestier trays against direct predator attack and hadoptimal and diverse feeding conditions. All para-meters together apparently a¡ord higher growthand repeated reproduction in the ¢eld groupcompared with all laboratory treatments. The resultscorroborate previous studies on energy allocation inP. magellanicus (MacDonald & Bayne 1993) and thefreshwater clam (Anodonta piscinalis) (Jokela &Mutikainen 1995). The authors suggest that underfavourable conditions, animals invest energy intoreproduction without cutting on growth or mainte-

nance. However, under energy-limited conditions,energy investments are prioritized for growth andmaintenance (P. magellanicus) or for reproduction(A. piscinalis) depending on the species. Our resultssuggest that under limited conditions, such as in thelaboratory and in presence of a predator, A. ventrico-sus prioritizes energy allocation into muscle growthat the cost of reproduction.

Conclusions

Environmental factors shape life-history parametersin scallops. Animals experimentally exposed to pre-dators allocate energy to muscle growth and protractspawning. As spawning means a major energeticdrainage, late spawning simultaneously extends sur-vival compared with animals kept without predators.In contrast, higher temperatures induce highergrowth and enhance investment in gonad produc-tion, but at the costs of population survival. Further,standardized conditions, such as ad libitum feedingwith even a mixed plankton culture, cannot appro-priately substitute for the natural food quality in the¢eld, which apparently reduced the physiological ¢t-ness of arti¢cially fed animals held under ‘optimized’laboratory conditions. Thus for optimal scallop cul-ture with high market yield (high muscle index),rearing with £uctuating environmental conditionsas well as predators is recommended.

Acknowledgments

The authors would like to thankMario Osuna, Ernes-to Leo¤ n and Carmen Abundis for the technical sup-port, the students Max Ostendorf and BelisamaCarmona for assistance in the hatchery and animalmaintenance and Edouard Kra¡e for suggestions onthemanuscript. Furthermore, wewould like to thankthe Cooperativa del Puerto de San Carlos, Baja Cali-fornia Sur, for the supply of scallops. This researchwas supported by the DAAD grant D/06/47197 andthe SAGARPA-CONACYT project11947.

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