%. TierpTychol.. 52, 347-354 (1980) @ 1980 Vcrl.ig Paul P x e y , I k r l i n u n d H a m h u i g ISSN 0044-3573 / ASTM-Codel l : ZI:TIAC;

Dcpixrtmetit of Biological Sciences, The Universi ty of Gezira, Sudan

The Discrimination of and Reactions towards Predatory and Non-predatory Species of Fish by Humbug Damselfish,

Dascyllus aruanws (Pisces, Pomacentridae)

Received: FcLir rL i , y 11, 1980

Accrptet i : April 8, 1980

Abstract L).,rrrcavrts retrc.it in to their home jite (coral) 011 the approach of a p rcda to r o r u n -

familiar o b j c c t . T h i s csc.ipc re\ponsc occupie\ time that could otherwise be spent on o the r x t i v i t i e s a n d rcsponws to iiiappropri.ite stimuli may penalize U. UI-uunus. T h e ahility of 1). rirumius t o discriminate v.iriou\ species of fish tow'irds which responses and no response \hould he m.iJc W.I\ ii1vestig.itc.d i n the f i e l d . 1:ivc predatory and five lion-predatory species o f fish wcrc prcsctitcd to social groups .it either o f t w o presentation dis tmces. D. a r u m u s ckh i l i t an .ibilitv r o discriniinate t h e t w o categories of f i s h and react t o the predatory species by rem.iining closer t o o r within thc protection of their hoine s i t e . These effects were more m.irked .it the closcr prcsentation dist'itice. 11. ~ ~ J - U J ~ Z U S did not react significantly in thcsc rcqpccts tow.irdr q w c i e s of noii-prcd.itor\ f ish. Interspecific nggres\ivc bchaviour is described ;ind was e\;liibitcd t o w a r d s species of prcd.itory fish only. The funct ion of this beh.iviour is briefly discussed.

Introduction

The Humbug Damselfish, L)ascyllus aruanus, is a small pomacentrid coral-reef fish. This species has recently been subject to study (COATES 1977). D. a~uixnus live in social groups in association with branched acroporan and pocilloporan corals which are used for protection against predators. The nor- mal activity in undisturbed social groups in the field is for most individuals to be swimming some distance aw;iy from their coral, orientated into the cur- rent and feeding on plankton as this drifts by (COATES 1980). Individuals rarely leave their home site by more thmi 1 m (SALE 1971; COATES 1977). Fish released away from their home site (coral) are often swiftly taken by pisci-

348 DAVID COATES

vorous species of fish such as Pavapevcis cylindvica, Pavacivvhites fosteri, Ce- phalopholis avgus and Thalassoma sp. whereas a predator has never been observed to take a D. uvuanus from an undisturbed social group (COATES 1977).

When predators approach a social group the fish swim nearer and nearer to their coral until they eventually remain safe from attack within its branches. The same behaviour is exhibited towards unfamiliar objects such as the author. Sudden movement by a predator, an unfamiliar object or by other large creatures within the vicinity of social groups results in the simultaneous with- drawal of the social group members nearer to or within the protection of their coral. Subsequently social group members either remain within the coral or venture out again to distances from the coral dependent upon the relative danger (e.g. closeness) of a particular threat. This escape response is very similar to that described and investigated for Chromis cyaneus (HARTLINE et al. 1972; HURLEY and HARTLINE 1974).

Response to inappropriate stimuli (e.g. non-predatory fish) may penalize D. avuanus since escape responses occupy time which could otherwise be spent on activities such as feeding. There is thus likely to be a selective advantage to the ability to discriminate the species towards which appropriate responses should be made. To this effect D. avuanus can be observed to give no ap- Farent response to the presence of species of fish presenting no threat to them. For example, members of the families Chaetodontidae, Scaridae, Balistidac, Labridae (smaller specimens) and Acanthuridae can frequently be seen swim- ming through and amongst social groups of D. arumus . None of such fish are piscivorous (pers. obs.; HIATT and STRASBURG 1960; RANDALL 1967; HOBSON 1974; ORMOND 1980a). This ability of D. avuanus to discriminate predatory and non-predatory species of fish is investigated further in the present report.

Method The experimental work was undertaken i n the lied Sc.1 .it Port Sudan where D. aruunus

are common in the shallow water to the inside of thc fringing reef. 10 species of fish that were comnion within the study are.1 were selected. These were

divided into two groups of 5 predatory and 5 tion-predatory species. The predatory species were Cephalopholis argus , Pterois volituns, Grumistes scxlinc~atus, Purapercis cylindricu and Epinephrlus J ~ ~ o g ~ t r a t ~ s . All these .ire pixivorous prcdators that slowly approach unsuspect- ing prey and capture them by suddm rapid advances (pcrs. obs.: HIATT and STRASBUKC 1960; FISHELSON 1973; ORMOND 1980'1). The non-predatory species were Acunthurus sohul, Rhinc- canthus assasi , Chat,rodon ' u r i g a , Scarus sordidus and Zebrasoma velijerum. None of these species are piwivorous (pers. obs.; HIATT and STRASUUKC 1960: RANDALL 1967: VINE 1974; ORMONU 1980,i) and hence present no immediate threat to D. a r u m u s .

Two specimens of each of the above 10 species were caught within the study area either by netting them or by using the anaesthetic Quinaldine. It was difficult to obtain fish of equivalent size,, especially taking into consideration the different s h a p e of the species selected but all the fish used were considered to be of a comparable size, ranging from 17.5 to 23.0 cm total length. These f i s h were kept alive and healthy during the course of this work in individual cages submerged on the reef.

8 isolated social groups of D . u r u u w s ( i .c . those occupying corals surrounded by a flat sandyirubble substrate) were located within the 5tudy arcd and their positions marked

L, i scr i 111 in .it i on of .I nd I< c.ic t i on s t o \v .I r ci \ 1' re d ,i to ry .I nd Non -pred ,I t o ry Spec i es of Fish 3 4 9

with buoys. l:or c.ich g r o u p , t w o transp.irent polythcne bags each mc.i\uring 40 x 60 cm were fillccl \v i th \v.iter, \vcighcd dorm w i t h le.id t \ .itid placeJ 7 0 c m f rom, and \vith one b.ig .it e.ich \ ide of t h e coral occupied. l ' h e \ c remained at nppro i ima tc ly the s,ime lcvel .I\ t h e cor.iI\. i t i i t i , i l l y , L). , i r u m i i s \vould re t he presence of these b q s alone. Hence they were left i n po\ition for four J. iy \ a f t c r which their presence did not nppenr t o have . iny c f fcc t on t h e hch. iv iuur of D. , i r u d > / ~ . Tlicse b ~ g s were left in position, except for the p ti rposc of e i pc r i m en t ,I t i on. t h ro u gli o u t t I1 i \ \vo r h .I nd .I re t c rni ed pc r ma lien t bags.

roup.; tverc tc.;ted to t h e pi.c\cncc o f one of the 10 test \pecies of f i s h prcsentcd A tri.11 c o i i \ i s t c d of removing o n e of t h e perm.incnt bag\ and replaciiig it with ,ig conta in ing one indiv idu . i l (chosen altern.itcly f rom the two .ivailable) of the

10 tc \ t \pccicr. Ilccordings n c r c made every 10 \ for 10 inin of 1) the number o f I ) . aruanus o u t of thcir c o r a l .itid 2) t h e c\tim.itcd .i\cr.igc di\ t . ince f rom their coral of those outside it. I n .iddition, t h e occurrence o f interspecific .re\\ ive bchaviour (scc results) was recorded during the ob\erv.i t ioii period. A t the e n d o lie tri.il t h e bag containing t h e tes t f ish was rcmoved .ind rcpl~secl b y t h c perm.inent Lug. T w o trisl l \ were undert,ikcn for e.ich test and t h e wcond t r ia l o f t he test, undertaken 3 Ii .iftcr the f i r \ [ , w.15 J repeclt of the above procedure except th . i t t h e test f i s h within .i b,ig m .I \ pl.iced 011 t h e opposite side o f the social group.

I so te\tcd t o the pre\cncc of bag\ .ilone b y u\ ing the \n ine procedurc but

11 \ i 11 g p r c J t o ry spec i cs \verc 'i It c r t i .I t cd \v i t h t c t s ti s i i i g ti o t i - pred a t ory species. The sequence o f t c \ t \ \v.I\ A . ~ o / M / , Ce. ~ v , y m , I<. a s c , ~ s i , I't. v o l i t ~ m , C/7. arrrigu, bag alone, G. sexlinc~,itr4s, S . $ o r d 1 d u ~ , P' i . c>flrntirrc,i. %. veiijeruni and I:. fuscoguttatus for f o u r groups, tlii.; order hcing rcvcr\ecI f o r t h e i-em.iining f o u r g r o u p . Tests were undertLiken on separate d a y s b u t . i lw, iys during the s.iiiie tiiiic periocl f o r e x h g roup , bctwccn Y.CO and 15.00 h.

The whole e\pcr imental procedure W J S rcpc.itcd, on t he wimc soci.11 groups, w i n g the lmjis .it the clojer ili\t.incc of 35 cm from rhcir cor,Il\.

Tc \ t

Results

Mean values (i.e. per 10 s observation, including both trials for each prcsentation distance) were considered for each separate group and each ..;cpr;ite presentation distance. Results were analysed statistically using in all c x c s the Wilcoxon matched pairs test ( 2 tailed), this test being sensitive to the behaviour of separate social groups.

Social groups of D. UEYULEY~ZIS behaved quite differently to the presence of the predatory species of test fish than they did to the presence of the b a c ~ 'I' alone (Figs. 1 arid 2 ) . Sigiiificaiitly fewer individuals ventured out of their corals in the presence of predatory species compared to the presence of the bag alone (p < 0.05 for each of the 5 predatory test species and for each distance c f presentation, 35 o r 70 cm).

The D. L E Y U ~ U S t ha t did venture out of their corals tended to remain closer to their home site when the predatory species were presented than they did when the bag was presented alone ( p < 0.05 for each of the 5 predatory species and each distance of presentation).

This behaviour exhibited towards the predatory species was more marked when these species were presented 'it the closer distance of 35 cm compared t o 70 cm. Significantly fewer fish remained outside their coral and those that did remained significantly closer to it when these S predatory species were presented a t the closer distance ( p < 0.05 for each of the 5 predatory species).

350 DAVID COATES

Predatory species

Non-Predatory species

(a) Ce.argus (b) Pf. volitans (c) G. sexlineatus (d) Po. cylindric0 ( e ) E. fuscoguftatus ( f ) Polythene bag

(9) A . sohol (h) R. assosi ( i ) Ch. ourigo

( j ) S. sordidus (k) Z. veliferum

I ig. 2: Mean values (between all 8 social groups) for the mean distance (cm) of indivi- dual D. a r u a n u ~ from their coral, per observation, during the presence of various species of fish housed within poly- thene bags and to the presence of such bags alone ( f ) . Bags were presented a t 70 cm (shad- ed areas) and 35 cm (non- \haded areas) from the corals

Predatory species

' h m Non-Predatory species

Fig. 1: Mcnn values (between a11 8 social groups) for the mean number of individual D. a w a m s per observation re- corded outside of their coral during the presence of various species of f i s h housed within polythene bags and to the pre- .sence of such bags presented Jlone (f). Bags were presented at 70 cm (shaded areas) and 35 cni (noii-shaded areas) from the cor.ils occupied by social

groups

(a) Ce. orgus (b) Pt. volitons ( c ) G.sex1ineotu.s (d) Pa. cylindric0 (e) E. fuscoguftatus ( f ) Polythene bag ( g ) A . sohal (h)R.assosi ( i ) Ch.aurigo

( j) S. sordidus (k) Z. vel i ferum

Discrimin.ition of .ind Kcactions towards P rcda to ry and N o n - p r c d ~ t o r y Species of Fish 351

70 cm

Na Ng

Ce. argus L1 5 P I . volitans 3 1 G. sexlineatus 17 L Pa. cylindrica 19 5 E. fuscoguttatus L7 6

Predatory Species

The behaviour of I ) . aruunus towards non-predatory species of test fish was not different from their behaviour towards the bag alone (Figs. 1 and 2). No significant differences exist in either the numbers of individuals outside their coral, or in the niean distance of individuals from their coral, when the rextions of D. a r u m u s to each separate test species of non-predatory fish are compared to their reaction to the bag alone (p > 0.05 in all cases). Similarly, differences i n the behaviour towards non-predatory test fish presented at 70 cm compared to 35 cm are not significant ( p > 0.05 in all cases).

35 cm

Na Ng

6 3 0 0 7 3 L 1 9 L

Interspeci f ic aggressive behaviour During the course of these observations a curious behaviour pattern was

occasionally exhibited by certain individuals withiii social groups. Such behav- iour usually involved an individual slowly approaching a test fish to a distance of u p to two thirds of the test fish to home site distance. The fish would then suddenly dart back to the home site. This behaviour was only exhibited towards predatory species of test fish and more so when such fish were prescnted a t 70 cm compared to 35 cm (Table 1).

TJLIc I : Tot.11 nuniber\ of occurrcncc\ of ioterspecific aggressive behaviour (N.1) and the tot.11 number of soci.il groups of D. clrt(a?/t(( in which t h i s bchaviour was observed (Ng) when prescnted with species of prcd'itory fish housed withiii polythcne bags. Bags were presented .it either 70 cm o r 3 5 em .I< i n d i c ~ t e d . Thi! behaviour was not exhibited tow.irds non-prcdatory

\pccic\ o n any occasion

Discussion

D. azyua~zus behave differcntll. to different species of fish placed within the proximity of their home site. The results clearly indicate an ability in this species to discriminate certain predatory and non-predatory species of fish. Similar results have been obtained in many avian species (e.g. CURIO 1963).

Individuals within social groups of D. aruunus exhibited interspecific aggressive behaviour towards the predatory species presented to them. Similar behaviour has been observed in a number of other specics of coral-reef fishes (c.g. Low 1971; MYRBERG and THKLSHER 1974; VINE 1974; ROBERTSON et al. 1976). These reports suggest that this type of behaviour may be associated with the defense of resources contained within a territory. EBERSOLE (1977) in .I detailed study on the pomacentrid Eupomacentrus leucost ic tus discussed many theories on the significance of interspecific aggressive behaviour and concluded that such behaviour is adaptive by reducing the loss of food in the

3 5 2 DAVID COATICS

territory to competitors and protects the nest from egg predators. Such a11 explanation is difficult to consider in D. avuanus as it is not known what resources, if any, are being defended by this species nor is it certain whether the predators tested presented any threat to any such resources. I t is more probable that this behaviour is associated with an attempt by D. aruanus to drive off those species that are threatening to prey on them directly. All of the predatory species of test fish were quite large enough to eat even the largest D. arumus. However, such predators may only be able to efficiently catch prey if these are taken unawares as HIATT and STRASBURG (1960) suggest specifically for Cephalopholis argus and Ptevois volitans. The tendency for L). aruanus to associate with corals in fairly isolated positions (SALE 1970; COATES 1977) presumably enables them to be more vigilant of the approach of predators. Provided that D. avuanus are aware of the presence and threat of a predator they may exhibit behaviour that may appear to render them more vulnerable. In this context i t is interesting to note that iiiterspecific aggression was observed less frequently when the predatory test fish were presented a t the closer range. At such close quarters these fish may present too much of a threat for this behaviour to be exhibited safely by D. aruanus. Furthermore, the comparatively few observations of this behaviour directed towards Pt. volitans may be due to the unusual appearance of this species pro- duced by a combination of its colouration and patterning, body shape and the form of its pectoral fins which makes the recognition of its pertinent features (e.g. mouth, eyes) difficult (LORENZ 1966; ORMOND 1972). D. avuanus may be confused by these factors aiid react with caution.

I t is not known whether D. ayuaiius are able to recognize each predator and each harmless neighbour in their vicinity. This ability would give D. U Y U -

anus the maximum opportunity to opimise their behaviour in each case. It is possible that they recognize a few key stimulus characteristics of the classes of dangerous intruders. In various animals sign stimuli invoking escape respon- ses may be visual (e.g. TINBERGEN 1951; SCHLEIDT 1961; DILL 1974a, 1974b; HURLEY and HARTLINE 1974) chemical (e.g. VON FRISCH 1941; PFEIFFER 1963) or auditory (e.g. STRUHSAKER 1967). HUKLEY and HARTLINE (1974) suggest that cues such as sound, vibration, aiid details of shape, colours and motion

anti-predator behaviour a t length i n the bird Ficedula hypoleuca and suggests that predator recognition may involve the use of a t least two and possibly more perceptual channels. I t is also possible that D. U Y U U ~ U S (and other species) discriminate predators by reacting to the less common fish on the reef, or conversely that they become “habituated” to the presence of the more com- mon species. The dangerous piscivorcus species will be higher up the food chain and are unlikely to be as common on the reef as the harmless species which are usually lower order consumers. EBEKSOLE (1977) demonstrated that Eupoma- centyus leucostictus can discriminate a considerable number of fish species. Enemy recognition is undoubtedly a complex procedure in many cases.

It is interesting to note the reciprocal effects on predator hunting strate- gies of such predator discrimination by prey. A variety of strategies are used

play a role in triggering escape in Chvomis cyaneus. CURIO (1975) d’ lScUSSeS

I) i scr i 111 i 11 .1ti on of .I 11 d Kc JC‘ t i o II s t (1 w .I r ds I’ red a t o ry ,111 d N 011 -pr cd .I tory Spec i cs of Fish 3 5 3

by piscivorous specie5 to capture prey (ORMOND 1980 a). Certain species such as CLtrunx spp. swim rapidly along the side of the reef, accelerating around outcrops of coral to surprise small fish before the former can be recogniscd and the prey can retreat to hiding places. Other species of predators may avoid recognition by potential prey through aggressive mimicry and disguising their approach through interspecific feeding associations (ORMOND 1980 b).

Summary

The reactions of social groups of D. uruanus to the presence of species of predatory and non-predatory fishes were recorded. D. uruunus exhibit an iibility to discriminate these two categories cf fish. Fewer individuals remained outside their home site and those that did so remained closer to it during the presence of predatory species compared to the control situation. This behav- iour was more marked when the predatory species were presented a t a closer range. Reactions of individuals to the presence of lion-predatory species were not significantly different from their reactions in the control situation a t either presentation distance. Some possible mechanisms of this discrimination ‘ire discussed.

D. Ltrmnus also exhibited interspecific aggressive behaviour towards predatory species of fish and the significance and function of this behaviour :ire discussed.

Zusammenfassung

Untersuchungen uber die Reaktionen von Dascyllus uruanus auf die An- wesenheit von Rauber- und Nichtriuberarten wurden angestellt. D. aruunus vcrmochte hierbei zwischen den beiden Fischkategorien zu unterscheiden. In Gegenwart von Riiubern hielten sich wcniger Individuen auflerhalb ihres Ver- stcckplatzes auf - und selbst jene hielten die Ruckzugsdistanyen kurrer als Individuen in Kontrollsituationen. Dieses Verhalten war urn so ausgepragtcr, je usher die FreRfeitide waren. Die Reaktioiien von Einzelindividuen auf die Gegenwart von Nichtr3uberarten unterschieden sich tiicht wesentlich von Reaktionen in der Kontrollsituation bei beliebigcr Darbietungsentfertiuiig. Einige miigliche Mechanismen dieser Unterscheidungsfahigkeit werden dis- kutiert.

I). u r u m u s zcigte Aggressionsverhaltcn gegenuber rauberischen Fischen. Dic Bedeutung dieses Verhaltens wird diskutiert.

Acknowledgements

Thir studv w.i\ supportcd by .I grant from the Universi ty o f Gciira. T. A. REI)I)ING- COATES, I<. 1:. G. OKMONI) and P. .I. V I N I g.ive vdu. ible .issist.ince wi th various manuscripts. I am indcbtcd to the Dep,irtmcnt of Zoology, The Universi ty o f Khar toum, for the use of t 11 c i r rc se .I r cli I .I bo r ‘1 t o ry &it S u ,I k i 11.

24

354 COATES, Discrimination of and Reactions towards Predatory and Non-predatory Fish

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Author's address: David COATES, Department of Biological Sciences, The University of Gezira, P. 0. Box 20, Wad Medani, Sudan.