Research Papers

Shoals Receive more Attacks from the Wolf-Fish (Hoplias

malabaricus Bloch, 1794)

Marc S. Botham & Jens Krause

School of Biology, University of Leeds, Leeds, UK

Abstract

We investigated whether the piscivorous wolf-fish, Hoplias malabaricus(Bloch, 1794), showed preferences for attacking a �straggler� or a shoal usingguppies, Poecilia reticulata (Peters, 1860), as prey. Predators should show apreference to attack single prey items rather than grouped prey to overcome theconfusion effect, which has been shown to negatively affect their capture success.However, they may attack groups more frequently because they are more likely todetect them because of their greater conspicuousness. In our study we looked atpredator choice for grouped or single prey and whether this was affected by largershoals being more conspicuous. We offered Hoplias binary choices of a singleguppy (straggler) and shoals of 2, 6 and 10 fish. Hoplias preferred to attack theshoal over the straggler with regards to both frequency of attacks (initial andsubsequent) and attack duration. The implications for predator–prey interactionsof such a preference are discussed.

Correspondence: Marc S. Botham, School of Biology, Miall Building,University of Leeds, Woodhouse Lane, Leeds LS2 9JT, UK. E-mail: bgymsb@leeds.ac.uk

Introduction

In aquatic ecosystems predatory fish are often in close proximity to multipleshoals of their predominant prey species (Pitcher et al. 1983). As a consequencethey have to continuously make choices regarding which shoal to attack tomaximize capture efficiency. The anti-predator benefits of grouping have beenwell studied and suggest that per capita predation risk decreases with group size(Krause & Ruxton 2002). A reason for this is predator capture success has beenshown to decrease with prey group size for a selection of predators, for example:blue acara cichlids, Aequidens pulcher (Krause & Godin 1995); squid, Loligovulgaris, cuttlefish, Sepia officinalis, perch, Perca fluviatilis, and pike, Esox lucius(Neill & Cullen 1974); largemouth bass, Micropterus salmoides (Landeau &

Ethology 111, 881—890 (2005)

� 2005 Blackwell Verlag, Berlin

Terborgh 1986); lions, Panthera leo (Scheel 1993; Funston et al. 2001) (but seeKrause et al. 1998b for an exception). In conjunction with this many predatorsenjoy higher capture success when attacking single prey or stragglers from a group(for example; Major 1978; Morgan & Godin 1985; Nshombo 1994). When facedwith multiple prey shoals that vary in group size, predators might therefore beexpected to attack stragglers and/or the smallest shoals available. What choicespredators make have received little attention. Instead there has been more focuson the consequences of their attacks to investigate further the adaptive anti-predator function of grouping behaviour in prey species. Yet such choices areimportant in defining the relative importance of the various benefits associatedwith grouping behaviour in prey species.

Cresswell & Quinn (2004) showed that sparrowhawks, Accipiter nisus,attacked the most vulnerable group of redshanks, Tringa totanus, in two-thirds oftheir attacks with group size an important factor determining vulnerability, assmaller groups were more vulnerable than large ones. Conversely, Krause &Godin (1995) showed blue acara cichlids, Aequidens pulcher, preferred to attacklarger shoals of guppies, Poecilia reticulata, when given a choice between twoequidistant shoals of different size. Morgan & Godin (1985) found that whiteperch, Morone americana, directed more attacks towards stragglers than shoals ofbanded killifish, Fundulus diaphanus, and satiated three-spined sticklebacks,Gasterosteus aculeatus, preferentially attacked stray water fleas, Daphnia magna,over the swarm despite initially approaching the swarm first (Milinski 1977).However, Turesson & Bronmark (2004) found that despite the resultant lowercapture success, perch, Perca fluviatilus, directed multiple attacks towards largergroups of prey where they split the shoal and successfully captured individuals.

A potentially confounding factor on such choices may be that of detection.Detection of prey is fundamental as predators have to locate their prey first beforethey can instigate any attack. Larger shoals are more conspicuous both becausethey are physically larger and also because there are likely to be more individualsmoving about at any given time. Krause & Godin (1995) demonstrated theimportance of shoal conspicuousness by manipulating the activity of groups byusing temperature. Blue acaras attacked smaller shoals when the prey activity wasgreater than in the larger shoals. In Milinski’s (1977) study, sticklebacks initiallydirected more attacks at the swarm of Daphnia before switching their preferencetowards the stragglers. Sticklebacks are likely to get the chance to continuouslyattack such prey, but for piscivores feeding on mobile prey with good escaperesponses (Pitcher & Parrish 1993) the importance of the first stages of an attackmay possibly be greater.

In this study we investigated whether predators prefer to attack grouped preyor single prey (representing a straggler) and whether this is confounded by preyconspicuousness. We used a major guppy predator found in the Arima river, theWolf fish, Hoplias malabaricus which despite being generally regarded as anocturnal predator, is active and readily feeds on guppies, by day, both in thelaboratory and the field (Botham & Krause, pers. obs.). We offered Hopliaschoices between a single guppy (straggler) and a shoal of two, six and 10 guppies,

882 M. S. Botham & J. Krause

respectively, and recorded their first attack and subsequent attack preferences. Weexpected one of two possible behavioural outcomes. First, based on captureefficiency being greatly increased by attacking stragglers, Hoplias might preferen-tially attack the straggler rather than the shoal both in first choice and subsequentattacks, in each treatment. The second possible outcome, based on the concept ofshoal conspicuousness, is that Hoplias might preferentially attack the shoal overthe straggler in their first choice, but that in subsequent attacks this preference mayswitch towards the straggler. In terms of the effects of shoal conspicuousness, wealso expected to see a difference in approach latency between shoal size treatmentswhereby Hoplias approached the largest shoal (10) more quickly.

Materials and Methods

Study Organisms

Predators

We used 22 Hoplias which were wild-caught from the Arima and Guanaporivers in Trinidad between Apr. and May 2003, using hand seine nets. Theymeasured 58–125 mm TL. We housed the predators individually in the test tanksdescribed below. All predators were maintained on a diet of earthworms,minnows and guppies. Temperature was maintained at 25–27�C and the lightcycle was maintained at 12 h light:12 h dark to replicate conditions in the field.

Prey

Wild guppies were caught from the Arima river in Trinidad, Jun. 2001, usinghand seine nets. Female guppies were used as stimulus fish in all experimentsrather than males as males have variable colour patterns. All guppies were housedin large holding tanks where they were fed dry flaked food ad libitum daily.

Procedure

Figure 1 shows the experimental set-up. We constructed a mobile stimulustank that could be positioned in front of the test tanks. The stimulus tank wassplit into three compartments with one side made of one-way glass to prevent theprey from visual contact with the predators whilst allowing visibility of the prey tothe predators. Each compartment measured 10 · 10 cm. Stimulus shoals wereplaced in the two outer compartments where the space between was greater thanfour body lengths to reduce the chance of the two shoals being perceived as one(Pitcher & Parrish 1993). Predators were guided behind an opaque screen (seeFig. 1) before experimental trials. The opaque screen was designed with aremovable gate in the centre which was lifted to release the predator in a centralposition in the test tank. From here the predator could see both stimuluscompartments. We placed a black plastic triangle on the tank bottom at the frontof the tanks to mark out zones where the predator could be defined as

883Hoplias Preference for Guppy Shoals

approaching one or the other stimulus shoal (see Fig. 1). The stimulus tank wasbrightly illuminated whilst the test tanks were covered to create the low lightconditions necessary to make the one-way glass barriers operational (Botham &Krause, pers. obs.).

Observations were made with a digital video camera from a hide at the sideof the tanks (see Fig. 1). A removable opaque barrier was placed between the testand stimulus tanks before trials started. For each trial, a single female guppy anda shoal of female guppies of 25 mm (±5 mm SD) were placed into the two outercompartments in the stimulus tank and positioned in front of the test tank.Guppies had no visual or olfactory contact with the predators, but had bothvisual and olfactory contact with one another between stimulus compartments.We observed no differences in prey activity or behaviour between single andgrouped guppies in their respective compartments. Twenty-two Hoplias werepresented with the following binary choices of a single guppy (straggler) and ashoal of guppies differing in size: 1 vs. 2, 1 vs. 6, and 1 vs. 10. After the guppieswere given 5 min to acclimatize the removable barrier was lifted making themvisible from within the test tank. We then lifted the gate to the predatorcompartment to allow the predator to enter the test tank.

Digital video camera

10 cm

Predator

Approach line

Opaque barrier

Stimulus shoals (single fish or shoal of 2, 6 or 10)

One-way glass

Test tank (45 x 30 cm)

Stimulus tank (10 x 30 cm)

Left shoal zone of attack

Right shoal zone of attack

Triangle marking zones of attack

Opaque screen with a central gate to release predator

Fig. 1: Plan view of the experimental set-up used, showing the separate test and stimulus tanks holdingpredator and prey, respectively

884 M. S. Botham & J. Krause

An attack on a shoal was defined as when the predator made a bite at astimulus compartment. The measurement of attack durations was initiated whenthe predator crossed the approach line (see Fig. 1) which was positioned 1.5 bodylengths from the stimulus tank (based on the average body length of all Hopliasused) and entered either the left or right shoal zone of attack. The variables werecorded were as follows: (1) latency to first attack (defined as the time(s) taken byHoplias to attack a stimulus compartment after release); (2) first choice (whichprey compartment was first attacked); (3) subsequent attacks (all attacks made ateither stimulus compartment after the first choice where Hoplias remainedorientated towards the stimulus tank); and (4) attack duration with each preycompartment (defined as time(s) spent in either the left or right shoal zone ofattack). Hoplias were allowed to attack for a maximum of 3 min. Trials wereterminated earlier if predators were considered to be in danger of injuringthemselves through intense repetitive attacks at a stimulus compartment. Theattack durations with each compartment were calculated as percentages of thetotal time the predator spent attacking overall.

Each individual predator was tested with each shoal size treatment. Nopredator was tested more than twice in a day and we randomized the order of thetreatments and the side assignment for the stimulus shoals. Guppies were takenrandomly from their holding tank and used repeatedly for subsequent trialsbefore being returned. Video recordings were scored blind as to the nature andlocation of the shoal.

Data Analysis

Not all 22 Hoplias made attacks (some only approached the stimulus tank) inall treatments. Those that made no attacks at all were excluded from the analysis.Fifteen Hoplias made attacks in all three shoal size treatments and were used inanalysis between treatments for attack latency, first choice and attack duration.For within treatment analyses we included data from all Hoplias that attacked fora given treatment.

Kolmogorov–Smirnov tests showed the attack data to be non-normallydistributed. As a result multiple non-parametric tests were carried out on some ofthe data, thus increasing the chances of finding type I errors (Chandler 1995). Toadjust for this we applied a Bonferroni correction (a1 ¼ a/N, where N ¼ numberof tests) to �families� of tests (Chandler 1995). The reduced a1 level for each groupof tests is listed with the test values where appropriate.

Results

Latency to First Approach

There was no significant difference between shoal size treatments in thelatency to attack either stimulus compartment (one-way anova, d.f. ¼ 2; F ¼0.008, p ¼ 0.992).

885Hoplias Preference for Guppy Shoals

First Choice, Subsequent Attacks and Attack Duration

Hoplias directed significantly more of their first attacks at the shoal ratherthan the single fish in the 1 vs. 10 treatment [Binomial test (a1 ¼ 0.017): N ¼ 16,p ¼ 0.001 (Fig. 2)] but not in the 1 vs. 2 and 1 vs. 6 treatments [Binomial test(a1 ¼ 0.017): 1 vs. 2; N ¼ 17, p ¼ 0.332, 1 vs. 6; N ¼ 16, p ¼ 0.021] where wefound no significant difference between first attacks directed at either the shoal orthe single fish. First choice did not significantly differ between shoal sizetreatments (Cochran’s Q-test: p ¼ 0.453, N ¼ 15).

There was no significant difference in the attack duration with the single fishor shoal for the 1 vs. 2 treatment [Wilcoxon matched pairs test (a1 ¼ 0.017): Z ¼)1.002, N ¼ 17, p ¼ 0.355]. However, Hoplias showed significantly longer attackdurations with the shoal than the single fish for the other treatments [Wilcoxonmatched pairs test (a1 ¼ 0.017): 1 vs. 6; Z ¼ )2.580, N ¼ 16, p ¼ 009, 1 vs. 10;Z ¼)3.599, N ¼ 16, p < 0.001 (Fig. 3)]. Hoplias showed no significant increasein attack duration with increasing shoal size across treatments (Friedman test:v2 ¼3.244, N ¼ 15, p ¼ 0.215).

As with first choice, Hoplias directed significantly more subsequent attackstowards the shoal than the single fish for the 1 vs. 10 treatment [Wilcoxonmatched pairs test (a1 ¼ 0.017): Z ¼ )0.948, N ¼ 12, p ¼ 0.002 (Fig. 4)] butnot for the other shoal size treatments [Wilcoxon matched pairs test (a1 ¼ 0.017):1 vs. 2; Z ¼ )0.673, N ¼ 12, p ¼ 0.108, 1 vs. 6; Z ¼ )0.036, N ¼ 9, p ¼ 0.051].

Hoplias Body Size

Smaller fish have higher metabolic demands than larger fish and thereforerequire to feed more often (Wootton 1998). This affects their behaviour as itincreases the cost of lost feeding opportunities associated with remaining in arefuge (Krause et al. 1998a, 2000). Smaller Hoplias may therefore make attacks

0

10

20

30

40

50

60

70

80

90

100

1vs.2 1vs.6 1vs.10

Treatment

% f

irst

ch

oic

e at

tack

s

Single f ish

Shoal

**

Fig. 2: First choice: percentage of first attacks directed at the single fish or the shoal by Hoplias forthree treatments differing in shoal size difference. **p < 0.01

886 M. S. Botham & J. Krause

more quickly. However, we found no significant correlation between predatorbody size and average attack latency (Pearson correlation: r ¼ 0.227, N ¼ 18,p ¼ 0.365).

Discussion

In this study Hoplias directed more first attacks towards the shoal than asingle fish. Although this trend was evident for all shoal size treatments it was onlystatistically significant when a shoal size of 10 was offered. First choice maysimply be a consequence of detection during the encounter phase of the predationcycle. However,Hoplias showed no difference in approach latencies between shoalsize treatments and when we analysed subsequent attacks and attack duration we

0

20

40

60

80

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1vs.2 1vs.6 1vs.10

Treatment

% d

ura

tio

nSingle f ish

Group

****

Fig. 3: The median percentage time (s) spent by Hoplias on front of the single stimulus fish and thestimulus shoal for three treatments differing in shoal size difference. Error bars show quartiles.

*p < 0.05; ***p < 0.001

0102030405060708090

100

1vs.2 1vs.6 1vs.10

Treatment

% s

ub

seq

uen

t at

tack

s

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Fig. 4: Percentage of subsequent attacks directed at the single fish and shoal by Hoplias for threetreatments differing in shoal size difference. **p < 0.01

887Hoplias Preference for Guppy Shoals

found the same trends as with first choice whereby Hoplias directed significantlymore subsequent attacks towards the shoal and also spent significantly longerwith the shoal than the single fish. These results suggest that Hoplias showed anactive preference, independent of shoal conspicuousness, to attack the shoal overthe straggler. In all variables measured there was an increase in the magnitude ofthis preference as the shoal size offered increased. Although non-significant, thissuggests that larger shoals may receive greater predator attention.

Why do Hoplias Prefer to Attack Shoals?

We expected that Hoplias should prefer to attack a single guppy rather thanthe shoal, but that this may be initially confounded by detection of the moreconspicuous shoal because predators are not only faced with the problem ofcapturing their prey, but they must also first locate it. Cresswell & Quinn (2004)found that sparrowhawks, Accipiter nisus, preferentially attacked smaller flocks ofredshanks, Tringa totanus. Sparrowhawks had no problem detecting their preyand were able to monitor a large number of groups to assess vulnerability beforeinitiating an attack. Similarly, lions in Funston et al.�s (2001) study are likely tohave had little trouble detecting prey and therefore other factors such asvulnerability probably affected their prey choice. Hoplias are faced with far moreof a problem when locating prey in the aquatic environment where visibility is notas good and where their prey is highly cryptic. Large groups are more likely to bedetected by a predator as they are more conspicuous (Turner & Pitcher 1986;Pitcher & Parrish 1993; Krause & Godin 1995). Although we found that Hopliasdid direct more attacks towards the shoal in each treatment, we concluded this tobe a preference independent of shoal conspicuousness. Attacking groups of preymay not be such a constraint as it seems. First, certain predator strategies may beless sensitive to the anti-predator benefits of group size than others (for example,Krause et al. 1998b). Secondly, shoaling is a highly dynamic behaviour with manyexchanges involving shoals joining and breaking up (Hoare et al. 2000; Croftet al. 2003). This means that any given shoal is unlikely to remain that size forlong. Added to this, more individuals are likely to be non-vigilant in larger groupsas reduced individual vigilance is a benefit associated with grouping (Pitcher &Parrish 1993). Less vigilant individuals that are involved in activities such asforaging are often targeted by predators as they are more vulnerable (Fitzgibbon1989; Krause & Godin 1996). For this reason it may be more advantageous for apredator to seek large shoals as they are more easily detected and are likely tofrequently break down into smaller groups and straggling individuals wherecapture success increases. Major (1978) found that predatory jacks, Carynxignobilis, initially attacked large shoals of Hawaiian anchovy, Stolephoruspurpureus. Initial attacks were not successful, but subsequent attacks on smallergroups and straggling individuals resulted in higher capture success. Similarly,Turesson & Bronmark (2004) found that perch regularly attacked shoals of preywith low success, but followed these initial attacks with highly successful attackstowards prey splitting from the group.

888 M. S. Botham & J. Krause

Conclusions

In this study, we found that H. malabaricus preferred to attack the shoalrather than the single fish regardless of conspicuousness. We have discussed thepossible benefits of attacking a shoal, but information on Hoplias� capture successwhen attacking groups of different sizes and composition is required for a betterunderstanding of their attack preferences and the mechanisms underlying them.However, that they show such a preference has important implications regardingthe weighting of different benefits and costs associated with shoaling by their preyand for our understanding of observed shoal sizes in the wild.

Acknowledgements

We would like to thank Darren Croft, Nicholas McLetchie and Geoff Moxon for their helpcollecting the study organisms and Scott Fawcett for his continual help in the aquarium. We wouldalso like to thank the editor, Will Cresswell and an anonymous referee for their valuable comments onthis manuscript. M.B. was funded by a University of Leeds Scholarship.

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Received: May 7, 2004

Initial acceptance: October 20, 2004

Final acceptance: December 8, 2004 (M. Bateson)

890 M. S. Botham & J. Krause