How many meals a day to minimize cannibalism when rearing larvae of the Amazonian catfish

12 Pages·2011·1.2 MB·English

Aquat.LivingResour.24,379–390(2011) Aquatic
(cid:2)c EDPSciences,IFREMER,IRD2011
Living
DOI:10.1051/alr/2011141
Resources
www.alr-journal.org
How many meals a day to minimize cannibalism when rearing
larvae of the Amazonian catfish Pseudoplatystomapunctifer?
The cannibal’s point of view
EtienneBaras1,a, DustinV. SilvadelAguila2, GraceV. MontalvanNaranjos2,3, Rémi Dugué1,4,
Fred Chu Koo2,4, FabriceDuponchelle1,3,4, Jean-François Renno1,2,4, Carmen Garcia-Dávila2,4
and JesusNuñez1,3,4
1 IRD,UMR226,ISE-M,BP5095,34196MontpellierCedex05,France
2 IIAP-AQUAREC,Av.AbelardoQuiñonesKm7.5,Iquitos,Perú
3 UNFV-FOPCA,350CalleRoma,Miraflores,Lima,Perú
4 LMIEDIA(EvolutionetDomesticationdel’Ichtyofauneamazonienne),Iquitos,Perú
Received30April2011;Accepted28July2011
Abstract– Mealfrequencyisakeyparameterinfishlarviculture,especiallyinhighlycannibalisticspecies.Knowl-
edgeofthebiologicalbasesofcannibalism(growthcapacityofcannibals,morphologicalconstraintsoncannibalism,
preysizepreference)canhelppredictingtherisksofcannibalismfordifferentfeedingschedulesunderculturecondi-
tions.Thisstudyreliedontheday-by-dayanalysisofpreysizepreferenceandbioenergeticsofindividualcannibalsof
thecatfishPseudoplatystoma punctifer (8–65 mmstandardlength,SL,0.5–400 mgdrymass,DM)at28.5◦Cunder
12L:12D.Theresultswereequatedwiththeontogeneticvariationsofmorphological factors(headandmouthwidth)
andfeedefficiencyoflarvaefeedingonArtemianauplii,inordertocalculatetherisksofcannibalismamongfishfed
2–7dailymeals.ThepredationcapacitiesofP.punctiferwerehighestat8mmSLanddecreasedinlargerfish(largest
prey=86%and70%SLinfishof8and>30mmSL,respectively).Cannibalsofincreasingsizepreferredincreasingly
smaller prey relative to their own size, but also to their predation capacities. These morphological and behavioural
constraintswerelargelycompensatedforbybioenergeticsperformance. Cannibalsconsumedhighdailyfoodrations
(ashighas171and29%DMinfish<1and>300mgDM,respectively),exhibitedhighgrossconversionefficiencies
(0.50–0.55andabout0.70,infish<1and>30mgDM,respectively),andgrewrapidly(90and18%DMday−1infish
<1and>300mgDM, respectively). Thegrowth advantage of cannibals over siblingsfedArtemianauplii wasdeci-
sive,exceptforhighmealfrequencies(6–7dailymeals).Thisstudysupportstheviewthattheriskofcannibalismand
adequatefeedingstrategiescanbelargelypredictedinaparticularfishspeciesifthemorphological,behaviouraland
bioenergeticsbasesofcannibalismareexaminedaltogetherinanontogeneticperspective.
Keywords: Aquaculture/Cannibalism/Ontogeny/Growth/Morphology/Behaviour/Siluriformes
1 Introduction technicalconstraints,whichmayvarybetweenproducersand
rearingsystems.Inspecieswithstrongcannibalistichabits,the
The adoption of adequate feeding strategies is frequently penaltyfornotmaximisinggrowthcanbemoresevereinterms
a key to successful larval rearing, as the type of food, mode ofsurvival(HechtandPienaar1993;Folkvord1997;Barasand
ofdistribution,mealsize andmealfrequencyintimatelygov- Jobling2002).Ingeneral,informationontheacceptablenum-
ernfishgrowthandsizeheterogeneity(PallerandLewis1987; bers of daily meals or meal sizes under culture conditions is
FolkvordandOtterå 1993; Kubitzaand Lovshin1999). Meal gainedthroughexperienceandessay-errors(e.g.Katavicetal.
size is generally maximised, otherwise there is a differen- 1989;QinandFast1996).However,thisinformationcanalso
tial food intake, heterogeneousgrowth, greater size dispersal bepredicted,atleastinpart,fromthebiologicalbasesofcan-
andeventuallyhigherrisksofcannibalism(HechtandPienaar nibalismandtheirvariationsduringtheontogenyoffishes.
1993;Kestemontetal.2003).Bycontrast,thenumberofdaily
Most studies aiming at predicting the risk of cannibalism
meals, and thus growth is not always maximised, depending
in fishes focused on the morphological factors that govern
on the objectives of the production, operational schedules or
predation capacities and their ontogenetic variations (Hecht
a Correspondingauthor:[email protected] andAppelbaum1988;QinandFast1996;Parazoetal.1991;
ArticlepublishedbyEDPSciences
380 E.Barasetal.:Aquat.LivingResour.24,379–390(2011)
Sogard and Olla 1994; Hseu et al. 2003, 2004). In general, Loreto,Peru).Hormonallyinducedovulation,eggfertilisation
during the larval and juvenile stages there is a positive allo- andincubationwereperformedfollowingNuñezetal.(2008).
metricgrowthofbodydepth(orwidth)andanegativeallomet- Hatchingtookplace17 h afterfertilization.Duringthe hours
ricgrowthofmouthdimensions,whichaltogetherforcecanni- followinghatching,fishweretransferredin30-Lsquaretanks
balstoselectpreythatareincreasinglysmallerrelativetotheir (40×40×19[h]cm;stockingdensitiesofabout20fishL−1)
own size (Hecht and Pienaar 1993; Baras and Jobling 2002). inanindoorrecirculatingsystemunderanaturalphotoperiod
This information is indispensable for calculating the largest (12L:12D).Watertemperaturewasmaintainedat28.0±0.5◦C
preythatcanbeeatenwholebyacannibalofaparticularsize. with a 2-kW heater connected to a Biotherm 2000 thermo-
However, it is frequent that cannibals do not prefer consum- stat,andoxygenwasnearsaturation(>90%).Fromtheageof
ingpreyaslargeaspossible,asthesepreymightnotguarantee 60 h after hatching(hah)onwards, fish were fed live, freshly
the highest energy return, because of lower capture success, hatchedbrineshrimp(Artemiasp.)nauplii.Agroupoffishwas
longerhandlingtimeorgreaterriskofretaliation(synthesisin fedinexcessfivetimesaday,andfourotheronesonlytwice
BarasandJobling2002).Asforpredationcapacities,preysize a day, in order to produce rapidly a size differential for the
preferencescanvarysubstantiallyduringtheontogeny(Hecht predationexperiments(see below). Two othergroupsof fish,
andAppelbaum1988;FolkvordandOtterå1993;Baras1999; alsofedfivetimesaday,weresparedformorphologicalanal-
Barasetal.2010a).Anyfurtherpredictionoftheriskofcanni- yses. No foodwas distributedat night,anduneatenfoodwas
balismrequiresestimatinghowmanyfisharecannibalisedper removedin the eveningwith a siphon to ensure that fish had
unitoftime,andforhowlongcannibalswillcontinuepreying emptygutswhenpredationexperimentsstartedthe following
uponthestock.Themaximaldailyimpactofcannibalismcan morning.
be estimated by multiplyingthe numberof fish that are large
enoughtoexercisecannibalismandthenumbersofdailyvic-
tims percapita,whichcan be obtainedbyequatingthe max- 2.2 Morphology
imal food intake of cannibals and their maximalor preferred
prey size. The duration of cannibalism depends on how fast Fish were sampled every 12 h until 96 h after hatching
cannibalsgrowrelativetotheirpotentialvictims,inparticular (hah), at daily intervals until the age of 7 days after hatch-
on whether the immediate growth advantageprovidedby the ing (dah) and less frequently afterwards, until they attained
exerciseofcannibalism(KubitzaandLovshin1999)sufficesto 60–70 mm in standard body length (SL). At every sampling
compensatefortheincreasingmorphologicalconstraintsupon time,fishwereanaesthetised(2-phenoxy-ethanol,0.4mlL−1)
cannibalisminfish ofincreasingsize (Baras1999;Barasand andphotographedunderthestereomicroscopebyreferenceto
Jobling2002). a graduatedmark. The study focused on mouth width (MW)
This study precisely analysed the ontogenetic variations and head width (HW), which are the key morphologicalfac-
of the maximal size ratios enabling cannibalism, prey size torsforcannibalisminthisspecies,andonheadlength(HL),
preference,foodintake,conversionefficiencyandgrowthina whichvariessubstantiallyduringthelarvalandjuvenilestages
specieswithreputedcannibalistichabits.Theseperformances of P. punctifer. All dimensions were measured from digital
and constraints are compared with the growth rates of sib- photographs(nearestpixel),expressedinproportionofSLthen
lings fed Artemia nauplii at different meal frequenciesto es- equatedtoSL,usingsimpleorpolynomialregressionmodels.
timate the risks of cannibalism associated to different feed- Thelargestprey(SLPmax)thatcouldbeingestedbyacannibal
ing schedules. The target species is an Amazonian catfish, of particular size was deduced from the comparisonbetween
thesurubiPseudoplatystomapunctifer(Castelnau)(Pimelodi- modelledvaluesofMW (forcannibals)andHW (forprey).
dae;formerlyP. fasciatum(L.) forfish of the AmazonRiver, Additional samples were collected to document the rela-
see Buitrago-Suárezand Burr 2007). This piscivorouscatfish tionships between SL, wet body mass (WM) and dry body
is a candidate to the diversification of aquaculture in South mass (DM) in fish with empty guts. Following the measure
America (Kossowski 1996; Nuñez 2009), and its spineless of WM (nearest 0.1 mg), fish were euthanized (2-phenoxy-
tastyflesh hasalsoraisedinterestforitscultureoutsideofits ethanol,2.0mlL−1),placedat105◦C for12hthenweighed
original distribution area (e.g. USA, Dabrowski et al. 2008). againforthemeasureofDM(AOAC1995).WMwasindivid-
Asinmanyotherpiscivorousfishspecies,cannibalismismost uallymeasuredinfish>10mgandingroupsof5–20individ-
frequentduringits larvalandjuvenilestages, and haslargely uals of homogenoussize for smaller specimens.For DM, the
compromised the developmentof its aquaculture for a while measurementsweredoneongroupsoffishproducingatleast
(Padilla Pérez et al. 2001; Arslan et al. 2008; Nuñez et al. 30mgofDM(tensoffishforlarvae,atleastthreefishforlarge
2008). juveniles).
2.3 Predationexperiments
2 Methods
Design
2.1 Fishandrearingenvironment
The design of predation experiments in this study was
Fishwerehalfsiblingsproducedfromtheartificialrepro- almostreplicatedfromBarasetal.(2010a).Allpredationex-
duction of captive broodfish (one female, three males) in the perimentstookplaceincagesimmersedat90%inanindepen-
Aquaculture Research Station of the Instituto de Investiga- dentwaterrecirculatingsystemwheretemperaturewasmain-
cionesdelaAmazoniaPeruana(IIAP)atQuistococha(Iquitos, tainedat28.5±0.2◦C(mean±SD)undernaturaldaylength.
E.Barasetal.:Aquat.LivingResour.24,379–390(2011) 381
Two sizes of predation cages were used: 0.5 L (12.5×8.0× cages,and(2)inthecontrolgroupafter24hoffooddepriva-
5.0 [h] cm) and 2.5 L (17 × 17 × 11 [h] cm), for cannibals tion,soastodeterminethelossofDMover24h.Theprecise
< and >21 mm SL, respectively. In each cage, a single large timing of cannibalistic bouts was unknown. For the sake of
fish(i.e.thefuturecannibal)wasplacedtogetherwithsmaller simplicity,itwasassumedthatpreyfishwereonaverageeaten
siblings(potentialprey)ofknowndimensions.Nootherfood atmidofeach24-hperiodandthereforethattheylostweight
was provided.The amountof preyfish per cage (n = 15–20, over12 h. The daily foodration(cid:2)of the cannibal(R, mg DM)
depending on fish size) was in large excess of the presumed was thus calculated as R = 0.01(1−0.5WC − 0.5WC)
f i
cannibal’sfoodintake(seereasonsinBarasetal.2010a),ex- (0.5WM +0.5WM),whereWCisthewatercontent(%WM),
f i
ceptonsomeoccasions(n = 0–5prey)soastodocumentthe WMisthewetmass(mg)ofeatenpreyfish,andsuffixesfand
relationships between growth and food intake over a broader i stand for final and initial, respectively.WM was calculated
f
range. The latter situations were not retained in the analyses as WM = WM(1−WML),whereWML is theproportionof
f i
ofpreysizepreference.Preyfishwereselectedonthebasisof WM lostduring24hofstarvation,asmeasuredinthecontrol
two criteria: (1) all prey had to be small enough to be eaten group.WhentheSLofpreyfishwasmeasured,theirWMatthe
whole by the cannibal (based on the results of the morpho- startofeach24-hperiodwasback-calculatedfromtheWM-SL
logical study), and (2) their size distribution had to be broad modeldocumentedinthemorphologicalstudy.
enough to give the cannibal the opportunity of selecting be- The daily relative growth rate of cannibals (G, %
tweenpreyofdifferentsizes,butnotexcessivelybroadother- DM day−1)wascalculatedasG =100(DM –DM )DM−1,
ci cf ci ci
wise preyfish couldeateach other.To test whetherthe latter whereDM andDM arethedrymassesofthecannibalat1-
cf ci
situationcouldhappen,acontrolgroup,consistingofpreyfish dayinterval.Thegrossconversionefficiency(GCE,DM:DM)
with a similar size distribution as in the predation cages, but was calculatedas GCE = GR−1, whereG is thedailygrowth
withoutanylargecannibal,wasinstalledinanadditionalcage rateandRisthedailyfoodration(bothin%DM ).
ci
andofferednofood.Theoperationwasrepeatedeveryday. Thereafter, the values of R, G and GCE were equated to
Every 24 h, fish were collected and cages were cleaned the cannibal’s DM. Simple (R and G) or polynomial (GCE)
to remove faeces. The cannibal was anaesthetised, weighed power regression models were constructed from the highest
(nearestmg),revivedandreturnedrapidlytothesamecageas valuesinfishofdifferentsizes, withtheobjectiveoftracking
onthepreviousday,togetherwithanewsetofpreyfish.Sur- thetopperformancesofcannibals.Inparallel,G wasequated
viving prey fish were anaesthetised and measuredagain. The withR forcalculatingthe(negative)growthduring24-hstar-
methodforidentifyingthevictimsofcannibalismdependedon vation(G )andthemaintenancefoodration(R )producing
s maint
whetherSLorWMwasmeasured.SLwasmeasuredpreferen- zero growth. The latter calculations were made on a discrete
tially in fish <14 mm SL (<30 mg WM), and WM in larger basis,usingsevensizecategoriesofcannibal(seeresults).The
fish, because of size-dependentaccuracy and risk of injuring sevenvaluesofG andR wereequatedtothemeanDMof
s maint
fish upon weighing. The identification of missing prey was cannibalsineachcategory.
straightforwardwhenSLwasmeasured,asthisdimensiondid For each category of cannibals, prey size preference was
notvaryin fish deprivedoffoodover24h. By contrast,WM calculatedintwocomplementaryways.Thesizeofeacheaten
decreased during this interval, thereby requiring a two-step preySL wasexpressedasaproportionofthecannibal’ssize
P
back-calculationprotocolfor the identification of eaten prey: SL ,andofthelargestpreySL thatcouldbeeatenwhole
C Pmax
(1) the WM of prey fish after 24 h of food deprivation was by the cannibal, with the objective of testing whether canni-
estimated by subtractingfrom the initial WM the weightloss balsofdifferentsizesshowedsimilarpreysizepreferencesin
that was measured in the control group;(2) missing cases in respect to their predation capacities. For both ways of calcu-
theactualfinaldistributionofWM weremovedbysuccessive lations, size ratios were categorized,using 4% intervals. The
iterations,inordertodetermine(withsimplelinearregression preference index I of cannibals for each class of prey size
p
tests)thebestfit(i.e.thecombinationwiththehighestr2 and wascalculatedasI = N N−1,whereN andN arethenum-
p c a c a
aslopeof1.00;furtherdetailsinBarasetal.2010a). bersofeatenandavailablepreyinthissizeclass.Classeswith
Nomorethansevenpredationcageswerestudiedperday, N <5werenottakenintoaccountforthecalculationofI .In
a p
in order to reduce the monitoring period to 30 min. Canni- order to enable direct comparisonsbetween cannibalsof dif-
bals were studied over a maximum of five consecutive days. ferentsizes,I valueswerenormalized(i.e.,thehighestvalue
p
Surviving prey fish were never used again in any subsequent wassetat1.00).
experiment.
2.4 GrowthoflarvaefedArtemianauplii
Dataanalysis
AllbioenergeticsdatawereexpressedintermsofDM.For For logistic reasons, it was not possible measuring the
cannibals,whichwerestudiedseveraldaysinarow,DM was growth of groups of larvae fed Artemia nauplii at all possi-
deducedfromtheWM-DM modelsthatweredetermineddur- blemealfrequenciesthroughoutthelarvalstage.Additionally,
ingthe morphologicalstudyofwell-fedfish (Table1).These different frequencieswould have resulted in variable rates of
models were not used for prey fish, which had been fed less cannibalism,whichwouldhaveskewedgrowthestimates.In-
frequently,asfeedingrestrictionsresultinlowerDM:WM ra- stead,thesegrowthrateswereestimatedindirectlyasfollows.
tios.Hence,oneachdayofexperiment,theDM:WMratiowas Two-dayold larvae of P. punctifer (n = 10)were housed
measured (1) at the start of each period of 24 h, in an addi- in individual enclosures and offered freshly hatched Artemia
tional group of prey fish of similar size as in the predation nauplii four times a day, using a maximal meal size, i.e.
382 E.Barasetal.:Aquat.LivingResour.24,379–390(2011)
Table1.Morphological relationshipsinlarvaeandjuvenilesof P.punctifer (fishof4–66mmSL;0.5–2560mgWM).SL=standardbody
length; HL=headlength;HW =headwidth; MW =mouthwidth;SL =largestpreythatcanbeconsumedbyacannibalofaparticular
Pmax
SL,WM =wetbody mass;DM =drybody mass.Allmassesareexpressedinmgand otherdimensions inmm, except forSL (%SL),
Pmax
p< 0.0001forallmodels,*indicatesthatthismodeliscalculatedfrommodelleddata,usingthemodelsbetween MW andSL,andbetween
HWandSL(seeFig.1).
Equation Sizerange(mmSL) r2 F df
HW =0.140+0.0275SL+0.0252SL2−0.00077SL3 <20 0.996 2090 31
HW =1.508+0.165SL >20 0.991 1618 15
MW =−0.113+0.0994SL+0.0104SL2−0.00031SL3 <20 0.993 1364 31
MW =0.970+0.134SL >20 0.984 862 15
HL=0.375−0.0504SL+0.0386SL2−0.00141SL3 <13 0.994 1153 25
HL=1.693+0.363SL >13 0.999 8631 21
SL =−254.4+1074.7(logSL)−1209.2(logSL)2+571.3(logSL)3−97.2(logSL)4 4–66* 0.993 2651 84
Pmax
logWM=1.731−10.472logSL+14.721(logSL)2−5.010(logSL)3 <11.5 0.988 2403 91
logWM=−1.823+2.875logSL >11.5 0.992 26564 211
log(DM:WM)(%)=1.0459+0.01492logSL+0.01003(logSL)2 4–66 0.979 459 22
M (%WM) = 14.14+8.07logWM−2.36(logWM)2 (Baras which is probablythe most variablecomponentof the canni-
max
etal.,inpress).Intheevening,about30minutesafterthelast balistic dynamics,asit dependson a series ofcomplexinter-
meal, water was renewed and uneaten nauplii were counted. actionsbetweenbiologicalandenvironmentalvariables(Baras
Fishweremeasuredat4,8,12,16,20and24dahtodetermine and Jobling 2002). Here, an estimate of this proportion was
theirGandGCE.InthecalculationofGCE,nocorrectionwas obtainedbyexaminingat 13dahthe size distributionsof lar-
madeforuneatennauplii,whichwerealwaysinlowamounts vae stocked at 4 dah in sixteen 30-L tanks (25 fish L−1) and
(always<10%andonaverage3%ofthefeedinglevel).Inpar- fed in slight excessfourtimes a day.It was assumed thatthe
allel,fishofvarioussizes(1–110mgWM,n = 35)wereheld “jumpers” had gained their larger size through cannibalism,
inisolationanddeprivedoffoodover24htomodeltherela- andinallinstancestheywerelargeenoughtocannibalisesib-
tionship between WM andG . For each period in the growth lingsintheirrespectivetanksonthedayofmeasurement.
s
study (2–4,4–8,...20–24dah),the netconversionefficiency
(NCE, WM:WM) was calculated as NCE = (G −G ) R−1,
o s
where G is the observed growth, G is the negative growth 2.6 Statisticalanalyses
o s
duringstarvation,andRisthemeandailyfoodrationoverthe
rearing period (all variables in mg WM day−1; mean WM of Contingency tables analyses were used to test for ran-
0.015 mg for Artemia nauplii). Thereafter,NCE was equated dom prey selection in each size category of cannibals, and
to the geometric mean WM of fish over each period so as to whether cannibals of different sizes exhibited different pref-
describeitsontogeneticvariationsinP.punctifer. erences with respect to predation capacities. Simple (linear,
OnemajoradvantageofNCEisthatitcanservetoestimate logarithmic,power)andpolynomialregressionanalyseswere
thetheoreticalgrowthoffishfedndailymealsofknownvol- used to model the relationships between morphologicalvari-
ume,providedthattheontogeneticvariationsofG and M ablesandfishsize,andbetweenbioenergeticsdescriptors(see
s max
are known, which is the case for P. punctifer. Based on data above).Nullhypotheseswererejectedat p<0.05.
of gut evacuation rate in young P. punctifer (Baras et al., in
press),andcurrentpracticesinthelarvicultureofthisspecies,
growth trajectorieswere calculated for fish fed ad libitum up 3 Results
toseventimesaday.
3.1 Morphology
2.5 Impactofcannibalism Athatching,embryosofP.punctiferwere3.2±0.1mmin
totallength(TL;mean±SD).Thenotochordwasbentat16–
Theriskofcannibalismamongfishfeddifferentmealfre- 18hah,themouthwasopenat24hah,andexogenousfeeding
quencies can be estimated by equating the data collected in commencedat48–60hah,whenlarvaewere4.4±0.1mmSL
the different parts of the study, i.e. the growth trajectories of (5.2±0.2mmTL).Atthisstage,headwidth(HW)andmouth
fish fed Artemia nauplii (2.4), the growth and food ration of width(MW)averaged15.3and10.5%SL,respectively(Fig.1;
cannibalsfeedingmaximally(2.3)andthemorphologicalcon- modelsinTable1).Bothdimensionsexhibitedapositiveallo-
straintsuponcannibalism(2.2).Thesedataenablethecalcula- metricgrowthandattainedtheirlongestextension(relativeto
tion of the number of daily victims of an individualcannibal thefishSL)at16.5mmSLforMW(18%SL)andat18mmSL
at a particular age, and their iteration over time gives an es- for HW (23.5% SL). Thereafter, they exhibited a period of
timate of how fast the stock is depleted by cannibalism. The negative allometric growth, followed by isometric growth in
finalinformationthatisneededtoestimatetheimpactofcan- fish >50 mm SL. By contrast, head length increased steadily
nibalism is the proportion of fish that exercise cannibalism, throughoutthisontogeneticinterval,from18%SLatthestart
E.Barasetal.:Aquat.LivingResour.24,379–390(2011) 383
Preysizeselectivity
The hypothesis of random prey selection was rejected at
p < 0.05 in all size categories (Table 2). Cannibals of in-
creasing sizes preferred eating prey of decreasing sizes rela-
tive to their own (Fig. 2a), which was expected as predation
capacitiesdecreaseinfish>8mmSL(Fig.1).However,size-
dependent differences persisted after prey size was equated
to SL (Fig. 2b), thereby indicating that cannibals of in-
Pmax
creasingsizepreferredincreasinglysmallerpreybyreference
totheirpredationcapacities.Thesize-dependentmodelscon-
structedfromthisanalysiswerehighlysignificant(r2 > 0.97,
p<0.0001;seecaptionofFig.2).Theypredictthateachtime
thecannibalSLdoubles,therelativesizeofitspreferredprey
decreasesby20%byreferencetoitsbodylength,andby14%
byreferencetoitspredationcapacities.
Bioenergetics
Fig.1.Variationsofmouthwidth,headwidth,headlength(thinlines, In every size categories of cannibals, the relationship be-
right vertical axis), andthelargest preySL that canbeingested tweengrowth(G)andfoodration(R)wassystematicallybest
Pmax
whole by the cannibal, thick line, left vertical axis) during the on- described by a simple linear regression model (p < 0.0001;
togeny of P. punctifer. All dimensions are expressed in percents of Table3).Theweightlossduringstarvation(Gs)andthemain-
thefishstandardbodylength(SL).Curvesconstructedfromthemod- tenance food ration (R ) were high in larvae <1 mg DM
maint
elsinTable1. (6.5% DM day−1 and 12.2% DM, respectively). The values
ofbothvariablesdecreasedrapidlyuntilcannibalswereabout
30 mg DM, and stabilised around 2.8% DM day−1 (G ) and
s
of exogenous feeding to about 34% SL in fish >50 mm SL 3.9% DM (R ) in larger fish (Table 3). The value of the
maint
(Fig.1). highestfoodrationconsumedbythecannibal(R )decreased
max
Throughoutthe larval and early juvenile stages, HW was rapidlywithincreasingfishsize(Fig.3a),passingfrom171%
the largest cross-sectional body dimension, and the morpho- DM in fish <1 mg DM to 29% DM in fish >300 mg DM.
logicalconstraintsuponcannibalismweregovernedbythera- The value of G (i.e. the growth at R ) also decreased
max max
tio between the MW of the cannibaland the HW of the prey. in fish of increasing size (90 and 18% DM day−1 in fish <1
At the start of exogenous feeding (4.4 mm SL), the largest and >300 mg DM, respectively; Fig. 3b), but at a slower
preythatcouldbeingestedwholebyacannibal(SL )was ratethanforR (log-logrelationships,slopesof–0.265and
Pmax max
about73%SL.Itincreasedrapidly,peakedat86%at8mmSL, –0.292, respectively;Table 3). Thisdifferencereflectedonto-
thendecreasedandattainedaplateauatabout70%SLinfish genetic variations of GCE, which passed from 0.50–0.55 in
>30mmSL(modelinTable1).Remnantsofincompletecanni- fish <1 mg DM to 0.65–0.70 in fish >30 mg DM (Fig. 3c).
balism,inwhichthevictimisingestedtailfirstanditscephalic ThiscurvilinearincreaseofGCEparalleledthecurvilinearde-
region is discarded by the cannibal, were occasionally ob- creaseoftheirR andG duringtheontogenyofP.punctifer
maint s
servedintherearingtankssparedforthemorphologicalstudy. (Table3).
Thisbehaviourwasnolongerobservedbeyond8–9dah(fish
>8–9mmSL),supportingtheview thatcompletepreyinges-
tionwasthemainmodeofcannibalisminthisspecies. 3.3 Growthadvantageofcannibalsandimpact
ofcannibalism
Aswas the case for measurementson cannibals,the rela-
3.2 Predationexperiments
tionshipbetweentheweightlossduring24-hstarvation(G ,%
s
WM day−1) andWM was curvilinear(Fig. 4a). Larvaeraised
Cannibals ranging from 8 to 65 mm SL (corresponding inisolationandfedArtemianaupliifourtimesadayaveraged
body masses of 4 to 2437 mg WM, and 0.5 to 397 mg DM) 159 ± 12 mg WM (25 ± 1 mm SL) at 24 dah. Their GCE
werestudiedover147days×fish(Table2).Intotal,2337prey (WM:WM) at 2–4 dah (0.8 mg WM, 4.8 mm SL) averaged
(5–32mmSL)wereoffered,ofwhich581(25%)wereeaten. 0.24 (Fig. 4b). It increased rapidly in fish of increasing age
This proportionsuggests that food availability was always in and size, and attained a plateau at 0.38–0.39in fish >10 mg
excessofthecannibals’needs.Onlytwo(outof300)fishdied WM (10 mm SL).The value ofNCE fora particularfish size
in the control groups, and none of them had been consumed wascalculatedfromthemodelledvaluesofG andGCE,and
s
in partor totality, which suggests that the missing fish in the servedtomodelthegrowthoffishfedtwotosevendailymeals
predation cages had been eaten by the large cannibalsexclu- (seeSect.2.4).Theresultinggrowthtrajectoriesareshownin
sively, and that naturalmortalitywas low and did notimpact Figure5,togetherwiththoseofcannibalsgrowingmaximally,
substantiallyonpreysizeselectivity. and those of their largest and preferred prey. The proportion
384 E.Barasetal.:Aquat.LivingResour.24,379–390(2011)
Table2.CharacteristicsoftheexperimentsforstudyingthebioenergeticsandpreysizepreferenceinlarvaeandjuvenilesofP.punctifer.WM
isthefishwetbodymass,DMisitsdrybodymassandSLisitsstandardbodylength.IndicesciandPrefertotheinitialsizeofcannibaland
preyatthestartofeach24-hcycle.PreysizeexpressedbyreferencetothecannibalsizeSL ortothelargestpreythatcanbeeatenwholeby
ci
thecannibal(SL ,seeFig.1).Preysizepreferencetestedbycontingencytableanalyses:Symbols***,**and*standfor p<0.001,<0.01
Pmax
and<0.05,respectively,andNSfor p>0.05.
Cannibalsizecategories 1 2 3 4 5 6 7
Cannibal WM (mg) mean 6.2 15.7 47.8 147.7 358.2 1145 1967
ci
range 4.0−8.2 9.5−24.0 26.9−77.2 83.9−212.4 252.1−537.7 687−1572 1611−2437
DM (mg) mean 0.7 1.9 6.0 19.8 50.7 175.9 314.8
ci
range 0.5−1.0 1.1−3.0 3.3−9.9 10.9−29.0 34.8−78.0 101.4−246.9 253.4−396.6
SL (mm) mean 8.9 11.2 16.5 24.5 33.3 49.9 60.2
ci
range 8.0−9.6 9.9−13 13.5−19.5 20.1−27.8 29.5−38.4 41.8−55.7 56.2−64.9
Nobservations(day×fish) 16 20 19 21 16 36 19
npreyoffered 225 209 210 302 179 503 128
npreyeaten 72 90 69 69 45 179 57
PreySL (mm) range 5.0−7.8 6.3−8.8 7.3−11.6 9.9−17.6 13.0−19.8 15.6−30.6 18.1−32.6
P
Preference(4%SL class) *** *** *** *** ** *** **
ci
Preysize(%SL ) range 63−103 64−93 58−89 51−95 51−80 43−82 42−72
Pmax
Preference(4%SL class) *** *** *** *** NS *** **
Pmax
Table3.BioenergeticsofcannibalisminP.punctifer.Upperpart:relationshipsbetweengrowthGanddailyfoodrationR(bothinDM day−1)
ci
inthesevensizecategoriesofcannibals(seeTable2).DM isthedrybodymass(mg)ofthecannibalatthestartofa24-hperiodoverwhich
ci
growthismeasured. Lowerpart:size-dependent variationsofmaximumdailyfoodration(R ),maximumgrowth(G ),maximumgross
max max
conversionefficiency(GCE ,DM:DM),maintenancefoodration(R ,%DM )andnegativegrowthduring24hoursoffooddeprivation
max maint ci
(G ,%DM day−1).ThemodelsforR andG areconstructedfromthesevenmodelsintheupperpartofthetable.ThemodelsforR ,
s ci maint s max
G and GCE are deduced from the highest scores observed in cannibals of different sizes (Fig. 3). Symbols ***, ** and * stand for
max max
p<0.001,<0.01and<0.05,respectively.
Equation r2 F df pintercept pslope
Sizecategory1:G=−6.458+0.531R 0.980 697 15 ** ***
2:G=−5.160+0.571R 0.979 852 19 * ***
3:G=−4.482+0.606R 0.990 1737 18 *** ***
4:G=−3.142+0.697R 0.983 1123 20 ** ***
5:G=−2.692+0.715R 0.994 2303 15 *** ***
6:G=−2.662+0.693R 0.964 924 35 *** ***
7:G=−2.799+0.688R 0.988 1431 18 *** ***
logR =2.190−0.292logDM 0.969 1231 40 *** ***
max ci
logG =1.930−0.265logDM 0.943 647 40 *** ***
max ci
logGCE =−0.267+0.085logDM −0.021(logDM )2 0.832 94 40 *** ***,***
max ci ci
logR =1.051−0.391logDM +0.082(logDM )2 0.963 52 6 *** **,*
maint ci ci
log(–G )=0.784−0.281logDM +0.055(logDM )2 0.966 56 6 *** **,*
s ci ci
ofjumpersat13dahamonggroupsof750fishfedfourmeals twoorthreemealsadaywouldgrowataslowerratethanthe
a dayvariedverylittle betweenexperimentaltanksandaver- preferredpreysizeofcannibals.Thenumberofdailyvictims
aged 0.5±0.3%(mean ± SD). Calculationsof the impactof wouldincreaserapidly,and90%ofthestockwouldhavesuc-
cannibalismweredoneonthebasisofthisproportion(Fig.6). cumbedtocannibalismattheagesof14or21dah,fortwoor
Based on these models, fish fed seven daily meals would three daily meals, respectively (Fig. 6). Fish fed four or five
alwaysgrowfastenoughtoescapecannibalism(Fig.5),except daily meals would alwaysfall between the maximaland pre-
possiblyduringthe veryfirst rearingdays,whencannibalism ferred prey size of cannibals (Fig. 5) and for both situations
consistsin theincompleteingestionoftheprey,anddoesnot the number of daily victims would decrease rapidly beyond
requireanysizedifferentialforitsexercise.Infishfedsixdaily 10–12dah(Fig.6).However,thetotalimpactofcannibalism
mealscannibalismwouldbecomevirtuallyimpossibleafter12 at21dahwithfourdailymealswouldbealmosttwiceashigh
dahandthetotallosseswouldbe<15%.Bycontrast,fishfed aswithfivedailymeals(48versus25%).
E.Barasetal.:Aquat.LivingResour.24,379–390(2011) 385
Fig.2.PreysizepreferenceincannibalisticP.punctifer ofdifferent
sizes(categories1–7,Table2).Foreachcategory,thepreferencein-
dex (I ) is normalized so that the maximum is 1.00. Prey size ex-
p
pressedasaproportionofthecannibal’sstandardbodylength(SL ,
ci
a), and of thelargestprey that canbe ingested wholeby thecanni-
bal (SL , b). The relationships between SL and preferred prey
Pmax ci
size (P ), using the modes shown in graphs a and b, stand as: log
P
P (% SL ) = 2.107–0.336 log SL (r2 =0.983, F =293, df = 6,
P ci ci
p<0.0001forbothinterceptandslope),logP (%SL )=2.065–
P Pmax
0.219 log SL (r2 = 0.974, F = 188, df = 6, p < 0.0001 for both
ci
interceptandslope). Fig. 3. Size-dependent variation of daily food ration (R), growth
(G)andgrossconversionefficiency(GCE,DM:DM)incannibalistic
P.punctifer.DM isthedrybodymass(mg)ofcannibalsatthestart
ci
4 Discussion of the24-hcycleover whichgrowthandfoodintake aremeasured.
Datapointsrefertoindividualmeasurements.Polynomial(GCE)or
4.1 Morphologicalconstraintsoncannibalism simple(RandG)powerregressionmodelsareconstructedfromthe
andpreysizepreference highestpointsonly(darkcircles;equationsandstatisticsinTable3).
This study highlighted that young P. punctifer suffered
from little morphological restrictions for cannibalising sib-
lings, although their mouth width never exceeded 17% SL WMratiosof57and40%respectively).Thesescorescompare
(Fig.1),whichisquitelowbyreferencetomanypiscivorous to those of highly cannibalistic species such as barramundi
fishspecies(Shirota1970).However,throughoutthelarvaland Latescalcarifer(Parazoetal.1991),northernpikeEsoxlucius
earlyjuvenilestages,thebodyshapeofP.punctiferremained (Bryetal.1992;ZiliukieneandZiliukas2006),tunas(Sawada
slender, thereby facilitating cannibalism (SL of 86% at etal.2005)andgroupersEpinephelusspp.(Hseuetal. 2003,
Pmax
8mmSL,andaround70%infish>30mmSL,corresponding 2004,2007).
386 E.Barasetal.:Aquat.LivingResour.24,379–390(2011)
Fig.5.GrowthofyoungP.punctiferfedArtemianaupliitwotoseven
timesadaywithamaximalmealsize(thinplainlines),incomparison
tocannibalsfeedingmaximally(thickplaincurve),theirlargest(thick
dashedcurve)andpreferredpreysizes(thickdottedcurve).
Fig.4.Size-dependent variationofthenegativegrowthduring24-h
starvation(G ,a)andofthegross(GCE,WM:WM)andnetconver-
s
sionefficiency(NCE,WM:WM)inyoungP.punctiferfedfourmeals
aday(b).TheNCEcurveiscalculatedfromthevaluesofGCEand
G infishofdifferentwetbodymass(WM;seemethods).Themod-
s
els stand as: log (-G ) = 0.821–0.216 log WM + 0.040 (log WM)2
s
(R2 = 0.843, F = 85,df = 34, p < 0.0001,<0.0001and0.0410for Fig.6. Theoreticalvariationinthenumbersofvictimsofcannibal-
intercept,firstandsecondorderpolynomials).GCE=0.266+0.189 isminP.punctifer,dependingonfishageandnumberofdailymeals
logWM–0.102(logWM)2+0.019(logWM)3(R2=0.925,F=230, (plain thin curves). The intersection with a dotted thick curve indi-
df = 59, p < 0.0001,except for3rdorder polynomial, p = 0.013). catestheageoffishwhencannibalismhaseliminatedagivenpropor-
NCE=0.394+0.124logWM–0.080(logWM)2+0.017(logWM)3 tion(10,25,50,75or90%)oftheinitialstock,consideringthat0.5%
(calculatedfromthetwomodelsabove). ofstockedlarvaebecomecannibals(seeresults).
Cannibals of P. punctifer in the present study never con- correspondingWMratiosare31,22and16–17%,respectively,
sumed prey as large as allowed by their mouth dimensions, in goodconcordancewiththemaximalstomachcapacitiesof
possibly because stomach capacity was limiting. This factor youngP.punctifer(i.e.20–21%WMin fish<16mmSL,and
is rarely invoked for large-sized piscivores, the stomach of slightlylessinlargerfish;Barasetal.,inpress).
which is several times as large as their maximum daily food The preferred prey size of P. punctifer was always well
ration (e.g. Essington et al. 2000 for largemouth bass Mi- below their predation capacities. It is not frequent that can-
cropterus salmoides), but it can apply to larvae or small ju- nibals or piscivores prefer prey as large as possible, because
veniles that consume much larger amounts of food relative suffocationisfrequentwhenthepreyisslightlytoolarge,es-
to their size. Here, the largest prey fish ingested whole by pecially in species with spiny fin rays that preventregurgita-
cannibalistic P. punctifer were about 85, 75 and 70% SL , tion(EurasianperchPerca fluviatilis,Brabrand1995;brown-
C
in fish of 10, 25 and >40 mm SL, respectively (Fig. 2). The marbledgrouperEpinephelusfuscoguttatus,Hseuetal.2007).
E.Barasetal.:Aquat.LivingResour.24,379–390(2011) 387
Inthevastmajorityoffishspecies,thesizepreferencecurveis strategies,consistinginmaximisingeitherfoodintakeorGCE.
dome-shapedanditsmodewellbelowthemaximalingestion The present results on P. punctifer suggests that the antago-
capacities of cannibals (review in Baras and Jobling 2002). nism betweenfoodrationandGCE doesnotapplyto allfish
Thisgeneralpatternisthoughttoreflecttheconflictinginflu- speciesorsituations,atleastwhenthedietishighlydigestible,
encesofdifferentfactorswithinthecontextofoptimalforag- asisnormallythecasewhenpreyingonfishlarvae.
ingtheory(StephensandKrebs1986):theenergyreturnispro-
TheGCEvaluesinlargercannibalsofP.punctiferfeeding
portionaltopreysize,butcapturesuccessdecreasesandrisks maximally (about 0.70 in fish >30 mg DM) were also much
ofretaliationincreasewithincreasingpreysize(e.g.Lundvall
higher than in most species documentedto date (e.g. 0.42 in
et al. 1999). In P. punctifer, capture (or ingestion) success
nase Chondrostoma nasus of 60–80 mg DM, Keckeis et al.
mightrefertotheincreasingdifficultyofswallowinglargeprey 2001;(cid:2)0.46in50-mgDM graysnapperLutjanusgriseusfed
growinglongbonypectoralspines,inadditiontothegenuine
livefish prey,Wuenscheletal. 2004).SuchhighGCE values
difficultyof capturingfish with faster swimmingspeeds. Itis
typicallycomparewiththoseinjuvenilesoftoppiscivoresor
alsopossiblethatpreysizepreferenceincannibalisticP.punc- otherreputedlyefficientspecies,suchasthetambaquiColos-
tiferwasinfluencedbytheirdegreeofsatiation(Turessonetal.
somamacropomum(vanderMeeretal.1997).Theremightbe
2006).Theexactmomentofcannibalisticboutswasunknown
at least threereasonsforwhycannibalistic P. punctifer hada
inthepresentstudy,sowasthedegreeofsatiationofcannibals
highGCEfromtheearlylarvalstageonwards.(1)Byanalogy
bythen.Ifthecannibal’sstomachwasnotemptyuponanew
with other species, it is likely that digestion and assimilation
cannibalistic attempt, this mighthave been another incitation are more efficient after gut coiling. In P. punctifer, the stom-
forselectingasmallerprey,especiallyifthepreyingestedfor-
achpouchisformedandapyloricsphincterisconspicuousat
merlywaslarge. 48 hah (<4.5 mm SL), before the start of exogenousfeeding
Itcannotbeexcludedthatthepatternsofpreysizeprefer-
(Baras et al., in press). (2) Except possibly during the early
ence documentedhere were stronglycontextual,as predation
larval stage, P. punctifer behave as ambush predators, which
cages were small, prey were abundant and could not escape.
generally have higher GCE than active swimming foragers
In these circumstances, cannibals might trade off immediate
(AdamsandBreck1990;HoudeandZastrow1993).(3)Dur-
energy return against capture success and risk of retaliation,
ingtheontogenyofP.punctifer,headlengthpassesfrom20%
therebygivingpreferencetorelativelysmallprey.Similarpref- SLat 8mm SLto about34%SLin fish >50mm SL(Fig.1).
erencesforsmallpreysizehavebeenobservedincannibalistic
Ingeneral,alongsnoutfacilitatesthecaptureandhandlingof
Pangasiusdjambalin similar experimentalconditions(Baras
large prey (see a parallel in the family Lepisosteidae, which
et al. 2010a). Hence,the curvesin Figure2 can probablynot comprises species with different dynamics of snout elonga-
be used to predict prey size preference of young P. punctifer
tion during the ontogeny; Echelle and Riggs 1972; Aguilera
inthewild.Thisisnomajorshortcoming,asthepresentstudy
et al. 2002). The observation that R decreased rapidly as
maint
aimedatestimatingtheriskofcannibalismunderculturecon-
theheadofP.punctiferelongated,andcametoaplateauthere-
ditions,wherepotentialpreyarenumerousandcannotescape,
after,supportsthelatterinterpretation.
aswasthecasehere.
The combination of high food rations and high GCE in
P. punctifer produced a fast growth, similar to the perfor-
mances of tunas exercising piscivory ad libitum (e.g. Pacific
4.2 Foodration,conversionefficiency
bluefin tuna Thunnus orientalis, Sawada et al. 2005) or fast
andgrowthperformance
growingcatfishes(sharptoothcatfishClariasgariepinus,Ver-
reth and Den Bieman 1987; vundu catfish Heterobranchus
YoungcannibalsofP.punctiferconsumedlargedailyfood
longifilis,Legendre1992;IndonesiancatfishPangasiusdjam-
rations (155 and 40% DM at 1 and 100 mg DM, respec-
tively),theyhadahighfoodconversionefficiency(0.50–0.70), bal, Legendre et al. 2000; striped catfish Pangasianodon
and grew at a fast rate (85% and 25% DM day−1, at 1 and hypophthalmus, Baras et al. 2011). Based on the slope of
the (log-log) relationship between growth and body mass
100 mg DM, respectively). Similar or higher food consump-
(–0.265),thedeclineofgrowthcapacitywithincreasingbody
tion rates have been reported in other fish species, although
size in P. punctifer is less dramaticthan in manyfish species
generallyatamuchsmallersize(dailyrationsof120%DMat
0.15mgDMinspottedseatroutCynoscionnebulosusat28◦C, (slopesfrom–0.30to–0.45;Jobling1994),butnotexception-
allyshalloweither(slopeof–0.28inC.gariepinus,Conceição
Wuenschel and Werner 2004; 170% DM at 0.10 mg DM in
etal.1998;–0.25inP.djambal,Barasetal.2010a).
SenegalsoleSoleasenegalensis,and242%DMat0.23mgDM
in gilthead seabream Sparus aurata, Parra and Yúfera 2001; Theremightbeseveralreasonswhytheslopeofthe(log-
over 300% DM in Anchoa mitchilli <0.05 mg DM, Houde log) G-M relationship in P. punctifer was not as steep as in
and Schekter 1981). When taking into account the effect of most other studies on fishes. (1) Most data on bioenergetics
body mass, P. punctifer consumes higher food rations, and come from studies of large juvenile fish, which also invest
neverthelessexhibitsbetter GCE (>0.50)than larvae of most some energy into the construction of gonads. (2) In contrast
fishes(Houde1994).HighGCEvalueswereobservedinother to juveniles, larvae do not systematically incur a regular de-
fishes, but generally for low daily ration or meal size, as crease of theirexchangesurfaces(gillsandintestine) relative
large meals have shorter gut residence time and are gener- to their body mass, thereby resulting in lower constraints of
ally associated with lower assimilation (syntheses in Houde increasing body mass on metabolism and growth (synthesis
1994;Keckeisetal.2001).ParraandYúfera(2001)suggested in Kamler 1992). (3) There is increasing evidence that the
that fish species have evolved towards diametrically opposed cost of growth in young larvae is lower than in juvenile fish,
388 E.Barasetal.:Aquat.LivingResour.24,379–390(2011)
possibly because the cost of proteinsynthesis decreases with a day was 20%, with about half of the fish dying from can-
increasing growth rate (Smith and Houlihan 1995; review in nibalism(R.Dugué,unpublisheddata),whichcompareswell
Pedersen 1997). (4) The present study was conducted at a with ourpredictions(Fig.6).Likewise,whenlarvaewereof-
constanttemperatureof28.5◦C.Byanalogywithothertropi- feredfivedailymeals,lossestocannibalismamountedto21%
calspecies(bluetilapiaOreochromisaureus,Barasetal.2002; at24dahandwerenegligibleamongolderfish(E.Baras,un-
P.hypophthalmus,Barasetal.2011),itislikelythatthether- publisheddata),alsoingoodconcordancewiththeprediction
maloptimumforgrowth(T◦ )inyounglarvaeofP.punctifer forthisfeedingschedule.
opt
iswarmerthan28.5◦Canddecreasesinlargerfish.Ifitwere Finally, it is worth remembering that during the larvicul-
thecase,thenP.punctiferofincreasingsizewouldhavebeen ture of P. punctifer, fish die from causes other than canni-
raisedattemperaturescloserto theirT◦ ,andcouldhaveex- balism, in particular from bites associated with unsuccessful
opt
pressed their growth capacities to a greater degree than did cannibalistic attempts or aggressive behaviours. The severity
small fish. Hence, rearing fish at constant temperature in the of bites depends on the relative size of oral teeth, which is
presentstudypresumablyproducedaG-Mrelationshipwitha maximalduringtheearlylarvalstageanddecreasesrapidlyin
shallower slope than if fish of differentsizes had been raised fish >9–10mm SL (authors’ unpublishedobservations).This
attheirrespectiveT◦ .Informationonthethermalbiologyof isafurtherencouragementtofeedyounglarvaeofP.punctifer
opt
P. punctifer is currently too scarce to speculate any further. maximallyandgrowthemrapidlythroughthisdevelopmental
Anyhow,cannibalsofP.punctifercangrowatveryfastrates, interval,inadditiontogrowingbeyondthereachofcannibals.
andthisaccountsforwhytheirgrowthadvantagecanbesub- Similar recommendations were proposed for the Asian cat-
stantialordecisivewhereverfeedingstrategiesareinadequate fishP.hypophthalmus,whichalsogrowslongoralspinesand
undercultureconditions. is subjected to a major risk period during its early ontogeny
(Barasetal.2010b,2011).
4.3 Impactofcannibalsandselectionofadequate
mealfrequencies
4.4 Synthesis,conclusions,perspectives
The models produced here suggest that cannibalism be
verylowinP.punctiferfedmaximallyatleastsixtimesaday,
but increase almost exponentiallyfor any missing meal. This This study highlighted the morphological, bioenergetics
accountsforwhymassivelossestocannibalismwereobserved and behavioural bases of cannibalism during the ontogeny
in earlystudieswhere thefoodrationandgrowthof P.punc- of P. punctifer, and indicated how this information could be
tiferwerestronglyunderestimated(Padilla-Pérezetal.2001). used to mitigate cannibalism with adequate feeding strate-
Thereareseveralreasonsforwhytheimpactofcannibal- gies. This implies feeding fish outside of normal working
ismundercultureconditionscoulddifferfromourpredictions. hoursandthushigheroverallproductioncosts,buteventually
(1) The proportionof jumpers that was used for calculations lower costs per fish produced. In a broader context, there is
wasestimatedat0.5%,basedonexperimentalevidence.How- one particular question that was not addressed in the present
ever,thisproportioncanvary,asitdependsonfoodavailabil- study, i.e. whether the fish that become cannibals under cul-
ity, temperature, initial size heterogeneity, proportion of de- tureconditionshavegenuineadvantagesoverothers,interms
formedhatchlingsor other family effects (synthesesin Baras of growthpotential,conversionefficiencyorpossiblyaggres-
1998;BarasandJobling2002;forP.punctifer,seeNuñezetal. siveness.Here,thefishusedascannibalswereselectedatran-
2011).(2)Theproportionofcannibalswasestimatedfromthe dom, but nevertheless grew faster than ever reported for this
occurrence of jumpers, which is a minimalist view, as other species. This suggests that most siblings of P. punctifer, ex-
fish having exercised cannibalism infrequently, and gained a cept for those suffering from deformities, enjoy similar high
lowergrowthadvantagewouldnothavebeenidentifiedascan- growthpotentialsandcanbecomecannibalsifgiventheoppor-
nibals/jumpersonthedayofmeasurement.(3)Thegrowthof tunity. Nevertheless, this “lottery-winner” hypothesis (Baras
potential victims of cannibalism was calculated here for iso- and Lucas 2010), remains to be tested experimentally in P.
latedfish,whichissoundfromtheviewpointofbioenergetics punctifer.
(see methods), but overlooks the issue of dominance hierar-
chiesthatcandepressgrowth,enhancesizedispersalandthus
Acknowledgements. This study was supported by an INCAGRO
increase the number of daily victims of cannibals. (4) In the
(concurso 03-2007-PIEA) funding to a project coordinated by
presentstudy,cannibalscouldselectadlibitumbetweenprey
Carmen Garcia-Dávila. Collaboration between research teams was
that were all small enough to be eaten, whereas under cul-
facilitated through the network RIIA (Red de Investigación sobre
ture situations, not all siblings might have the adequate size, laIctiofaunaAmazónica;http://www.riiaamazonia.org/).Theauthors
thereby resulting in greater difficulties for exercising canni-
wishtothankSalvadorTello,DirectoroftheAQUARECDepartment
balism, fewer daily victims, slower growth of cannibals and
ofIIAPforfruitfuldiscussions, CarlosChavez(IIAP)andtheIIAP
eventuallyloweroveralllossestocannibalism. technicalstaffinQuistococha(EdwinAgurtoGarcia,HugoMarichin
Basedonfactors2and3,thepredictedriskofcannibalism Ayambo,CherryYahuarcaniTamincheandAsunciónApuelaGuerra)
is underestimated, whereas it is exaggerated on the basis of for technical assistance. Mrs. Dominique Baras-Caseau contributed
factor4.Factor1couldproduceeithersituation.Thereissome toimprove theEnglishstyleof themanuscript. EtienneBarasisan
evidencehoweverthatourpredictionsarenotunrealistic.Ina honoraryresearchassociateoftheBelgianFNRS.ThisisISEMpub-
recentstudy,themortalityat11dahoflarvaefedseventimes lication2011-104.