The effects of competitor odour on predator choice for grouped prey in blue acara cichlids,...

The effects of competitor odour on predator choicefor grouped prey in blue acara cichlids

Aequidens pulcher (Gill 1858)

Marc S Botham1) amp Jens Krause(School of Biology Miall Building University of Leeds Woodhouse Lane Leeds

LS2 9JT England)

(Accepted 8 February 2005)

Summary

1 Predators are often faced with the choice of various prey groups to attack where individualprey are equally profitable but there is a cost of reduced capture success from overcomingthe confusion effect2 We investigated experimentally preference for a singleton or a shoal of guppies Poeciliareticulata by wild-caught blue acara cichlids Aequidens pulcher and how this was affectedby cues that may indicate both intra- and interspecific competition3 When offered binary choices between single guppies and shoals acaras showed a pref-erence to attack the shoal Faced with a potential competitor they no longer showed such apreference4 We discuss the implications of these results regarding predator-prey interactions in envi-ronments where prey form shoals and multiple predators are present

Keywords Aequidens pulcher predator-prey straggler shoals guppies

Introduction

Many studies to date have looked at prey selectivity in animals in termsof testing models of optimal diet theory (ODT) (Sih amp Christensen 2001)mainly in the context of prey size (eg Johansson et al 2004) or preytype (eg Cooper et al 1985) Due to the various anti-predator mechanisms(morphological and behavioural) associated with their prey many predators

1) Corresponding authorrsquos e-mail address bgymsbleedsacuk

copy Koninklijke Brill NV Leiden 2005 Behaviour 142 441-453Also available online -

442 Botham amp Krause

are faced with numerous other prey choices for example whether to attacksingle or grouped prey (Milinski 1977) armoured or non-armoured prey(Abrahams 1995) Selectivity in predators represents a balance betweennumerous factors such as the capture success experienced when attackingcertain prey types the nutritional value of the prey and the predatorsrsquo abilityto detect the prey in the first place

How does competition affect prey choice in predators Exploitative com-petition typically results in an accelerated depletion of prey and a reduc-tion in encounter rates which can cause decreased or no selectivity (egPlowright amp Landry 2000) Interference competition when the competi-tors directly interact (Hughes 1997) may influence diet selection in variousways For example shifts in prey selectivity may result when there is a riskof predation by competitors (Milinski amp Heller 1978) or when interactionsmay result in injury andor loss of prey through kleptoparasitism (Nilsson ampBronmark 1999)

Of particular interest is how the presence of a competitor will affect apredatorrsquos decision as to whether to attack a single prey item or a groupof prey In this situation choice is unlikely to be influenced by prey energyvalue since all individuals are equally profitable Instead it may be a resultof which prey require less energy expenditure for the predator to completea successful capture The confusion effect of grouped prey may increase en-ergy expenditure since many predators suffer a reduction in capture successwith increasing prey group size (Pitcher amp Parrish 1993) Despite this therehave been mixed results for predator preferences whereby some predatorspreferentially attacked singletons and smaller groups (Milinski 1977 Cress-well amp Quinn 2004) and others preferentially attacked larger groups possi-bly because of shoal conspicuousness (Krause amp Godin 1995) andor dif-ferent predation strategies that overcome the confusion effect in some way(Turesson amp Bronmark 2004) Regardless of what preferences are exhibitedthere have been few studies to see if and how they are affected by competi-tion Milinski amp Heller (1978) found that a model predator induced a shift inprey selectivity towards lower prey densities by hungry three-spined stickle-backs Gasterosteus aculeatus attributed to the problem of overcoming theconfusion effect associated with high densities whilst remaining vigilant tothe predator

In this study we investigated experimentally the effects of olfactory cuesfrom both intra- and interspecific competitors on whether predators choose to

Effects of competitor odour on cichlid prey preference 443

attack grouped or ungrouped prey using wild caught blue acaras Aequidenspulcher with guppies Poecilia reticulata as prey and pike cichlids Crenici-chla frenata (previously misidentified as C alta (Coleman amp Kutty 2001))as interspecific competitors Acaras and pike cichlids are sympatric guppypredators (Endler 1986) We gave acaras three binary choices between a sin-gleton and a shoal of ten guppies The three choice tests differed as followsone was performed in the absence of a competitor one in the presence of aconspecific (intraspecific competitor) and the other in the presence of a pikecichlid (interspecific competitor) Because domestic acaras have been shownto attack prey shoals because of their greater conspicuousness (Krause ampGodin 1995) we predicted that the wild acaras in this study would directsignificantly more attacks towards and spend more time with the shoal thanthe singleton in the absence of any potential competition In the presence ofolfactory cues from a potential competitor (intra- or interspecific) we pre-dicted a reduced preference for the shoal over the singleton as a result of apossible reduction in attention towards grouped prey (where acaras have toovercome the confusion effect) incurred when monitoring the competitor

Materials and methods

This study was conducted in the laboratory at Simla Research Centre inArima Trinidad during the period of April-May 2003 Previous field studiesinvestigating predator density and behaviour showed acaras and pike cichlidsco-occurred and frequently interacted both within and between species inthe stretch of the Arima river where our test predators were caught from(Botham et al unpubl data)

We used sixteen blue acara cichlids A pulcher (51-70 mm total length(TL)) as test fish in all experiments To investigate the effects of interspe-cific competition we used juvenile pike cichlids C frenata of similar bodylengths (58-65 mm TL) All fish were wild-caught from the Arima riverTrinidad in April 2003 using hand seine nets Acaras were housed indi-vidually in the test tanks (described below) separated by opaque barriers toeliminate visual interaction between them Pike cichlids were housed indi-vidually separate from the acaras in small holding tanks (600 times 300 mm)All fish were fed juvenile guppies daily and maintained at a temperature of25C and a light cycle of 12 h light 12 h dark to replicate conditions in thefield


Wild juvenile guppies (15-18 mm) were caught from the Arima river inTrinidad using hand seine nets They were housed in several small aquaria(300 times 300 mm) where they were fed dry flaked food ad libitum daily

Procedure

Experimental set-up

Figure 1 shows the set-up used throughout all experiments in this study Testtanks were divided into two sections (predator and prey) using a black markeron the underside The predator section contained the test predator and thesecondary predator (representing a competitor) A rock was positioned cen-

Figure 1 Plan view of the experimental set-up used


trally in the test tank to give the test predator a refuge from which it wasable to see both the left and right stimulus prey containers The secondarypredator was housed in an opaque 70 mm cylinder which was perforated toallow the transmission of olfactory cues An opaque cylinder was used be-cause with visual contact the test predator would often attack the secondarypredator Whilst the use of olfactory cues signalled the presence of a poten-tial competitor it did not result in the test fish attacking the competitor Forexperiment 1 this cylinder was empty to test the acarasrsquo prey choice in theabsence of a competitor A second acara was placed in the cylinder for exper-iment 2 (intraspecific competitor) and a pike cichlid for experiment 3 (inter-specific competitor) The order in which these three competition treatmentswere conducted was randomised To ensure chemical cues from competitorswere introduced to the test acara water from their holding tank was pouredinto their cylinder In experiment 1 (no competitor) fresh water free of com-petitor odour was added To reduce the chance of olfactory cues residing inthe test tanks after competition treatments acaras were only tested once ina 24 h period and after each trial we carried out a 50 water change Anygreater exchange of water caused too much disturbance to the test fish Inaddition secondary predators were only contained in the test tank for up to15 minutes and in most trials this time rarely exceeded 5 minutes Acarasregularly investigated the secondary predator container in competition trialsbut did not so when there was no secondary predator in the container duringno-competition trials

The prey section contained the stimulus prey shoals in two perforatedtransparent cylinders (to allow both olfactory and visual cues) positioned tothe left and right rear (Figure 1) The space in-between the left and rightstimulus containers was greater than 100 mm to reduce the possibility ofleft and right prey being perceived as one large shoal (Pitcher amp Parrish1993) The prey section was subdivided into left and right zones of attack(Figure 1) These zones were the areas in which a predator was recordedas attacking the left and right stimulus containers respectively (the zonein-between represents the area where a predator was not attacking eithercontainer over the other)

General protocol

Observations were made using a digital video camera (Sony DSR-PD100AP)placed above the test tanks with a small monitor allowing the observer to


watch the proceeding activity without disturbing the test fish Sixteen testacaras were presented with the following binary choices of a single juvenileguppy (straggler) and a shoal of juvenile guppies differing in group size1 vs 2 1 vs 6 and 1 vs 10 For each of the three different competitionexperiments the stimulus prey choices given were the same therefore eachacara was tested a total of nine times Before a trial started an opaque barrierwas placed between the predator and prey sections of the test tank Stimulusprey fish were then placed into the respective prey cylinders with water fromtheir holding tanks to enhance olfactory cues After the guppies were givenfive minutes to acclimatise the barrier was lifted and the trial began Werecorded latency to first approach (defined as the time taken to leave therefuge and cross the approach line) first choice (defined as which stimuluswas first attacked (bitten at)) and attack duration for each prey compartment(calculated as percentages of the total duration of that attack) An attack wasconcluded when the acara swam back over the approach line and returned toits refuge

We randomised the order of the three prey choice treatments (1 vs 21 vs 6 1 vs 10) and the side assignment of the prey stimuli Guppies weretaken randomly from their holding tank and used repeatedly for subsequenttrials before being returned

Data analysis

Kolmogorov-Smirnov tests showed the data to be non-normally distributedtherefore multiple non-parametric tests were carried out on the data To re-duce the chances of finding Type I errors we applied a Bonferroni correction(α1 = αN where N = number of tests) to lsquofamiliesrsquo of tests (Chandler1995) Reduced α1 levels are listed with the test values

Results

Experiment 1 mdash predator choice in the absence of competition

Latency to first approach

We found no significant difference in the time it took acaras to approacheither the single guppy or the shoal across shoal size treatments when nocompetitor was present (Friedman test (α1 = 0008) χ2 = 0375 p =0829 N = 16)


First choice and attack duration

In the absence of any competitor acaras directed significantly more firstattacks at the shoal (Binomial test (α1 = 0006) p lt 0001 N = 16)when offered a choice between a single guppy and a shoal of ten (Figure 2a)but not when offered a choice between 1 vs 2 fish and 1 vs 6 fish (Binomialtest (α1 = 0006) 1 vs 2 p = 0454 1 vs 6 p = 0021) Attack durationwas significantly greater for the shoal in the 1 vs 6 and the 1 vs 10 treatments(α1 = 0006) 1 vs 6 z = minus3294 p = 0001 1 vs 10 z = minus3442p = 0001 Figure 3a) but not in the 1 vs 2 treatment (Wilcoxon matchedpairs test (α1 = 0006) z = minus1931 p = 0053) The acaras showedno significant increase in attack duration with increasing shoal size acrosstreatments in the absence of competition (Friedman test (α1 = 0008) χ2 =3042 p = 0219)

Experiments 2 and 3 mdash predator choice in the presence of a con- andheterospecific competitor


As in experiment 1 we found no significant difference across shoal sizetreatments with an intra- or interspecific competitor present for the timetaken to approach either the single guppy or the shoal by acaras (Friedmantest (α1 = 0008) intra- χ2 = 3500 p = 0174 inter- χ2 = 3375p = 0185 N = 16)


In the presence of a competitor acaras showed no significant preference toattack either the singleton or the shoal in any shoal size treatment (Binomialtest (α1 = 0006) intra- 1 vs 2 p = 1000 1 vs 6 p = 0077 1 vs 10p = 0454 N = 16 inter- 1 vs 2 p = 1000 1 vs 6 p = 0210 1 vs 10p = 0454 N = 16) However attack durations were greater with the shoalfor 1 vs 6 and 1 vs 10 treatments with an intraspecific competitor present andfor the 1 vs 6 treatment with an interspecific competitor present (Wilcoxonmatched pairs test (α1 = 0006) intra- 1 vs 6 z = minus3493 p lt 00011 vs 10 z = minus3225 p = 0001 N = 16 (Figure 3b) inter- 1 vs 6z = minus3468 p = 0001 N = 16 (Figure 3c)) but not significantly greaterfor the remaining treatments (Wilcoxon matched pairs test (α1 = 0006)


Figure 2 The frequency of first attacks directed at the single fish or the shoal by acaras forthree treatments differing in shoal size difference under (a) no competition (b) intraspecific

competition and (c) interspecific competition (lowastlowastlowastp lt 0001)

Figure 3 The median percentage time (s) spent by acaras on front of the single stimulusfish and the stimulus shoal for three treatments differing in shoal size difference under (a) nocompetition (b) intraspecific competition and (c) interspecific competition Error bars show

quartiles (lowastlowastlowastp lt 0001 lowastp lt 005)


intra- 1 vs 2 z = minus1424 p = 0154 inter- 1 vs 2 z = minus1267p = 0205 1 vs 10 z = minus2514 p = 0012) We found no significantdifference in attack duration with increasing shoal size across treatmentswith a competitor present (Friedman test (α1 = 0008) intra- χ2 = 4179p = 0124 N = 16 inter- χ2 = 3111 p = 0211 N = 16)

Comparison between experimental (competition) treatments


All acaras attacked the shoal for the 1 vs 10 treatment with no competitorpresent (Figure 2) but less than two-thirds did with a competitor presentA significant difference in the frequency of first attacks directed at theshoal was found between competition treatments for the 1 vs 10 treatment(Cochran Q test (α1 = 0016) Q = 9000 p = 0011 N = 16) butnot other shoal size treatments (Cochran Q test (α1 = 0016) 1 vs 2Q = 0667 p = 0717 1 vs 6 Q = 0667 p = 0717) Further analysisshowed that there was a significant difference in the frequency of first attackson the shoal of ten over the singleton between experiments 1 (no competi-tion) and 2 (intraspecific competition) (McNemar change test (α1 = 0016)p = 0014) and between experiments 1 and 3 (interspecific competition)(McNemar change test (α1 = 0016) p = 0014) but not between ex-periments 2 and 3 that involved secondary predators (McNemar change test(α1 = 0016) p = 1000) (see Figure 4) We found no significant differencein attack duration between competition experiments for any of the shoal sizetreatments (Friedman test (α1 = 0008) 1 vs 2 χ2 = 0900 p = 06381 vs 6 χ2 = 1111 p = 0574 1 vs 10 χ2 = 2739 p = 0254)

Discussion

Acaras showed a preference for a shoal over a single fish in the absence ofany potential competition whereby they directed significantly more first at-tacks towards the shoal over the singleton when the shoal size was ten Inthe presence of olfactory cues from both an intra- and inter-specific competi-tor they no longer showed this preference We found no effect of competitorodour on attack duration Attack duration itself may not be a useful measureof preference since acaras could spend more time with a stimulus and yetnever attack it


Figure 4 The proportion of first attacks directed towards the shoal of ten guppies in the1 vs 10 treatment by acaras under different competition treatments (lowastp lt 005)

Preference for attacking shoals

These results suggest that singly foraging acaras prefer to attack shoals oversingle fish Studies on predator choices for grouped prey have yielded vary-ing results Whilst some have shown preferences for single preysmallergroups (Milinski 1977 Cresswell amp Quinn 2004) others have found the op-posite (Krause amp Godin 1995 Turesson amp Bronmark 2004) Some preda-tors adopt strategies that overcome or are unaffected by the confusion ef-fect of grouped prey and hence attack groups (Turesson amp Bronmark 2004)Many of these strategies involve predators attacking as groups Competitorodour resulted in reduced preference for shoals in acaras which along withfield observations on their behaviour (Holliday 2003) suggests it is unlikelythat acaras hunt cooperatively Acaras may have simply attacked groups onthe basis of greater conspicuousness (Krause amp Godin 1995) However wefound no differences in either approach latency or number of first attacksdirected at the shoal across group size treatments Possible benefits to at-tacking groups over a single prey include decreased individual vigilanceof group members compared to solitary individuals increasing some preyrsquosvulnerability to predation (Cresswell et al 2003a but see Cresswell et al2003b) more individuals may be engaged in activities which make themmore vulnerable (Krause amp Godin 1996) the likelihood of groups contain-ing individuals that are phenotypically odd that use the group as protectionbut are more easily captured (see Pitcher amp Parrish 1993) If group size aidsdetection through greater conspicuousness and the confusion effect can be


overcome for any of the mentioned reasons then it may be advantageous toattack groups

How does competition affect predator choice

The loss of preference for the shoal by acaras with competitor cues presentsuggests a reduction in selectivity rather than an active change in preferencesPredators may lose their selectivity broadening their diet by attacking anyprey to avoid being out-competed For example pigeons Columbia livia in-cluded more of their less preferred food items in the presence of competitors(Plowright amp Landry 2000) This may be especially prominent where domi-nance hierarchies exist since there may be better competitors that can depletethe best prey (Hughes 1997) What causes this reduction in selectivity

Overcoming the confusion effect mdash the trade-off between performingmultiple tasks

In the presence of a competitor acaras face a possible trade-off betweena competitive interaction and overcoming the confusion effect of attackinggrouped prey When feeding on high prey densities sticklebacks were lessaware of a potential predator (Milinski 1984) Similarly atlantic salmonSalmo salar lost their ability to discriminate between edible and inediblefood items in the presence of a predator and attacked both with equal fre-quency (Metcalfe et al 1987) Thus there may be a cost associated withlsquomulti-taskingrsquo because of information overload (Milinski 1990) which mayin part explain the loss of preference shown in this study

Variation in competitive abilities

Behavioural observations in the wild showed that acaras are extremely ag-gressive both towards conspecifics and pike cichlids (Holliday 2003) Ob-servations both in the field and laboratory suggest dominance differencesmay occur in acaras Dominance hierarchies may affect foraging decisionswhereby subordinates show a reduction in prey selectivity through eitheraggressive exclusion by dominants or avoidance of competitive interactions(Whiteman amp Cote 2004) More information on interactions between acarasand individual competitive differences are required to test the possibilitiesof dominance effects which may contribute to the observed reduction in se-lectivity by acaras in this study


In summary the presence of olfactory cues from a potential competitorcaused a loss of preference for grouped prey in acaras though further studiesare required to determine the precise mechanism(s) underlying this reducedselectivity Our results highlight the importance of predator density regardingthe benefits and costs associated with antipredator behaviours of prey

Acknowledgements

We thank Ronnie Hernandez for technical support in the laboratory and provisioning offacilities at Simla Research Station Trinidad We also thank Ashley Ward Darren Croft theeditor and two anonymous referees for their comments on the manuscript MB was fundedby a University of Leeds Scholarship

References

Abrahams MV (1995) The interaction between antipredator behaviour and antipredatormorphology Experiments with fathead minnows and brook sticklebacks mdash Can JZool 73 2209-2215

Chandler CR (1995) Practical considerations in the use of simultaneous inference formultiple tests mdash Anim Behav 49 524-527

Coleman RM amp Kutty V (2001) The predator of guppies on Trinidad is the pike cichlidCrenicichla frenata not Crenicichla alta A caution about working with cichlids mdashJ Aquaricult Aqu Sci 9 89-92

Cooper S Smith D amp Bence J (1985) Prey selection by freshwater predators with differ-ent foraging strategies mdash Can J Fish Aqu Sci 42 1720-1732

Cresswell W Lind J Kaby U Quinn JL amp Jakobsson S (2003a) Does an opportunisticpredator preferentially attack nonvigilant prey mdash Anim Behav 66 643-648

Cresswell W amp Quinn JL (2004) Faced with a choice sparrowhawks more often attackthe more vulnerable prey group mdash Oikos 104 71-76

Cresswell W Quinn JL Whittingham MJ amp Butler S (2003b) Good foragers can alsobe good at detecting predators mdash Proc Roy Soc London B 270 1069-1076

Endler JA (1986) A preliminary report of the distribution and abundance of fishes andcrustaceans of the northern range mountains Trinidad mdash Unpubl data

Holliday K (2003) Time budgets of two coexisting cichlid species Crenicichla alta andAequidens pulcher in the Arima river Trinidad mdash MSc University of Leeds

Hughes RN (1997) Diet selection mdash In Behavioural ecology of teleost fishes (GodinJ-GJ ed) Oxford University Press New York p 134-158

Johansson J Turesson H amp Persson A (2004) Active selection for large guppies Poeciliareticulata by the pike cichlid Crenicichla saxatilis mdash Oikos 105 595-605

Krause J amp Godin JGJ (1995) Predator preferences for attacking particular prey groupsizes mdash Consequences for predator hunting success and prey predation risk mdash AnimBehav 50 465-473


Krause J amp Godin JGJ (1996) Influence of prey foraging posture on flight behavior andpredation risk Predators take advantage of unwary prey mdash Behav Ecol 7 264-271

Metcalfe N Huntingford FA amp Thorpe JE (1987) Predation risk impairs diet selectionin juvenile salmon mdash Anim Behav 35 931-933

Milinski M (1977) Experiments on the selection by predators against spatial oddity of theirprey mdash Z Tierpsychol 43 311-325

Milinski M (1984) A predatorrsquos costs of overcoming the confusion-effect of swarmingprey mdash Anim Behav 32 1157-1162

Milinski M (1990) Information overload and food selection mdash In Behavioural mecha-nisms of food selection (Hughes RN ed) Springer-Verlag Berlin p 721-737

Milinski M amp Heller R (1978) The influence of a predator on optimal foraging behaviourof sticklebacks (Gasterosteus aculeatus L) mdash Nature 275 642-644

Nilsson PA amp Bronmark C (1999) Foraging among cannibals and kleptoparasites effectsof prey size on pike behavior mdash Behav Ecol 10 557-566

Pitcher T amp Parrish J (1993) Functions of shoaling behaviour in teleosts mdash In Behaviourof teleost fishes (Pitcher T ed) Chapman amp Hall London p 363-439

Plowright CMS amp Landry F (2000) A direct effect of competition on food choice bypigeons mdash Behav Process 50 59-64

Sih A amp Christensen B (2001) Optimal diet theory when does it work and when and whydoes it fail mdash Anim Behav 61 379-390

Turesson H amp Bronmark C (2004) Foraging behaviour and capture success in perchpikeperch and pike and the effects of prey density mdash J Fish Biol 65 363-375

Whiteman EA amp Cote IM (2004) Dominance hierarchies in group-living cleaning gobiescauses and foraging consequences mdash Anim Behav 67 239-247


are faced with numerous other prey choices for example whether to attacksingle or grouped prey (Milinski 1977) armoured or non-armoured prey(Abrahams 1995) Selectivity in predators represents a balance betweennumerous factors such as the capture success experienced when attackingcertain prey types the nutritional value of the prey and the predatorsrsquo abilityto detect the prey in the first place

How does competition affect prey choice in predators Exploitative com-petition typically results in an accelerated depletion of prey and a reduc-tion in encounter rates which can cause decreased or no selectivity (egPlowright amp Landry 2000) Interference competition when the competi-tors directly interact (Hughes 1997) may influence diet selection in variousways For example shifts in prey selectivity may result when there is a riskof predation by competitors (Milinski amp Heller 1978) or when interactionsmay result in injury andor loss of prey through kleptoparasitism (Nilsson ampBronmark 1999)

Of particular interest is how the presence of a competitor will affect apredatorrsquos decision as to whether to attack a single prey item or a groupof prey In this situation choice is unlikely to be influenced by prey energyvalue since all individuals are equally profitable Instead it may be a resultof which prey require less energy expenditure for the predator to completea successful capture The confusion effect of grouped prey may increase en-ergy expenditure since many predators suffer a reduction in capture successwith increasing prey group size (Pitcher amp Parrish 1993) Despite this therehave been mixed results for predator preferences whereby some predatorspreferentially attacked singletons and smaller groups (Milinski 1977 Cress-well amp Quinn 2004) and others preferentially attacked larger groups possi-bly because of shoal conspicuousness (Krause amp Godin 1995) andor dif-ferent predation strategies that overcome the confusion effect in some way(Turesson amp Bronmark 2004) Regardless of what preferences are exhibitedthere have been few studies to see if and how they are affected by competi-tion Milinski amp Heller (1978) found that a model predator induced a shift inprey selectivity towards lower prey densities by hungry three-spined stickle-backs Gasterosteus aculeatus attributed to the problem of overcoming theconfusion effect associated with high densities whilst remaining vigilant tothe predator

In this study we investigated experimentally the effects of olfactory cuesfrom both intra- and interspecific competitors on whether predators choose to








Procedure

Experimental set-up






General protocol





Data analysis


Results






















Discussion
















Acknowledgements


References

































Procedure

Experimental set-up






General protocol





Data analysis


Results






















Discussion
















Acknowledgements


References





























General protocol





Data analysis


Results






















Discussion
















Acknowledgements


References





























Data analysis


Results






















Discussion
















Acknowledgements


References












































Discussion
















Acknowledgements


References








































Acknowledgements


References


























The effects of competitor odour on predator choice for grouped prey in blue acara cichlids,...

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