Ethology 103, 283-291 (1997) 0 1997 Blackwell ~issenschafts-Verlag,Berlin ISSN 0179-1613

Centerfor Ecology, Evokution and Behavior, 7:H.Morgan .School of Biological Sciencer, riniversio of Kentucb, 13exington

Antipredator Behaviour and Suppressed Aggression by Convict in response to Injury-released Chemical Cues of Conspecifics but not to those of an Mopatric Heterospecific

BM:IN D. WISENUfi;.ni tk R. CRAIG; SARGENT

WISH~D~.:N,B. D. tk SARIXNT, R. C. 1997: Antipredator hchaviour and suppressed aggresyion by convict cichlids in response to injuryreleased chemical cues of conspecifics but not to those of an allopatric heterospecific. Ethology 103, 283-291.

Abstract

In aquatic environments, chemical cues sene as an important source of information for the dctcctron of risk. Here, we investigate the response of convict cichlids, (;lcbIusoma nigr+.rciatum, to injuryrelcased chemical cues. We exposed pairs of juvenile convict cichlids first t~ dechlorinated tap water (control), then hter to one of two test stimuli: 1. chemical cues from injured convict cichlids; or 2. chemical cues from injured mosquito , Gambzisiu uznnir. Gambusiu are allopatric and phylogenetically unrelated to convict cichlids. C~umhusiu?kin was used to control for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of tcst aquaria and time under a shelter object. In rcsponse to (,bm/7usiu skin, convict cichlids tended to increasc ume spent near the tank bottom hut did not increase use of the shelter object. There was a trade-off between antipredator and agonistic behaviours. In response to con\wt cues, there was a significant reduction in the frequency of approaches and bites. Gumhush skin extract had no significant effect on aggressive behaviour. These data sugest a -specific antipredator response to conspecific alarm pheromones in a New World cichlid fish and demonstrate a trade-off between predator avoidancc and intraspecific aggression. Further, the presence of an alarm response in this model species sets the stage for thc use of chemical cues as a research tool to manipulate predation risk in studies of the interaction betwccn predation risk and reproductive bchaviour.

Corresponding author: Brian WISENDJ~N,Center for Hcolo~y,Evolution and Beha\ ior, T H. Morgan Sch(101 of Bi(11ogical Sciences, 101 Morgan Building, Uni\ ersity of Kentucky, Lexington, liY 4050ti-0225, USA. e-mail: [email protected]

Introduction Chemical cues are a rich source of information about the environment. This is particularly true in aquatic habitats where water serves as a good medium for dissolving and dispersing chemical signals (1,Ir.w 2982; HAM 1992). A wide range of aquatic taxa use chemical information to assess predation risk (CHIVERSunpubl. data) including many species of fish (SMITH 1992). Among , attention has focused on the Ostariophysi,

LJ. S. Copyright Clcarancc Ccnter Code Statement: 0179-1~13/97/1034-0283$14.00/0 284 €3. D. Vi’lSt.hDF,N & R. C. S,1RGI‘N’l representing 72% of freshwater fish (NEIXIK 1984), and the role of their specialized pheromone system in mediating predator-prey interactions (MAGL’KR:\S 1989; MA’I’I[IS & ShiI’rti 1992, 1993a,b,c; SMI‘I’H1992; CHI~ERS81 SMITH 1994a,b, 199s; hh‘1’~[1Set al. 1995; W1SHNDF.N et al. 1995a; CHIVtXS et al. 1996a). Injuryreleased alarm cues elicit antipredator behaviour from conspecifics and sympatric heterospecifics. Injuryreleased alarm pheromones are not restricted to spccics within the (ha- riophysi. Recently uncovered examples of alarm reactions to conspecific chemical cues for fish taxa outside of the Ostariophysi include the Gasterosteidae (h~ITl~llS8c S~IITH 1993c), Gobiidae (SMITH 1989; SMITH & I,AWREI\;CE 1991; SMITH et al. 19911, (htidac (HI:<;IE et al. 1991), Cyprinodontidae (REXD 1969), Poeciliidae (GARCLAet al. 1992) and Percidae (SMlTtl 1979, 1982; CHIVERS et al. 1995a). The Cichlidae is a speciose family of fish that occur throughout thr. tropics in the Old and New World (BF,RRA 1981). Only a few cichlid species have been tested for a response to injuryreleased chemical cues. Two African species, Oreochrumis mossan//iczis U.-\IS\X’AL 8c Wt\GtIk%Y 1990) and Elupiu mmwp!du (NOBLE1939) exbillit antipredator behaviour in response to injured conspecifics. One South American species, Ptero/dyllum sculare, showed no response (SCHUTZ1956). In this study, we test the convict cichlid, C2da.roonm n&rqfusczatzm, a cichlid species native to (Bussi~;1987), for the presence of an alarm reaction to chemical cues from injured conspecifics. Convict cichlids are commonl>-used in laboratory experiments for studies of parental care (iIRMITA<;E 1960; W1IHI:R & %’F,BER 1971; MYKBEKG1975; BEKNSTElh 1980; NOON,11\: 1983; T(l\&’NstIF.ND & WiOOTTOK 1984; KF.”.hl.F,YSlDE 1985; I

\Ve obtained juvenile convict cichlids from a commercial tropical fish dealer. \Ye placcil two con\ ict cichlids into each of tcn, 9-1 tcst aquaria (30.5 x lS x 20 cm high). Fach tat contained a >!km laycr of gravel Alarm Reaction by (:onvicr (:ichlids ti? Chemical Cues 285

and a small shelter ohject composed of a hlacl, plcviglass roof (8 x 12 cm) raised 5 cm above the suhst~itui~ihy three legs cif transparent rigid plastic tubing. The tanks were filled to a depth of IOcni above the gravel with dcchlorinated tap water. A horizontal line 5 cni above the gravel was drawn across the fronr IJF wcti t:inL. Thc tank water was aerated hut not filtered. Test stimuli were inlected through a second line of .~qi.a:iuni airline tubing atrached to the airline supplying air to the airstonc in each tanh. Tcsr stiinuh, dischargcd into the upward stream of bubbles from the airstone, dispersed quickly thrwgh~~utthe test aquarium Fish were allo~ved24h to acclimate to test aquaria hchc trials licgan. Each pair of iirh wa., iested twice using the sanie protocol, with the exception of the stimulus used (wucr control <>rsLin eXti-;ict). In tnc morning (0900L1200 h), each pair of fish was tested for a response to 5 ml of dechlorinatcd rap wirer, to coptrd for the effect of stimulus injection. In the afternwn (1400L1700 h), each pair of lich was retested \vith ow of two test stimuli: (1) 5 ml of rinse water from an iniured ciimict cichlicl, or (2) 5 ml of rinsc water frim an inltircd mosquito fish, Gumhusza afinbr. \Ve uscd Gunihusiu skin to tect for a general response to injureii tish. Xlrrsquirr, hvh arc tion- ostariophysan species in the family Poccihidac and arc phylr~geneticallyunrehted ti>cichlidc. Gunhriodo not co- occur with convict cichlids in the rearing ponds from which wc ohtarncd our fish (,I. Rc )IwRFS, pcr:;. comni.) Test stimuli were prepared as follciws. Iminediatel! hefim each trial, a tisli was killed in\tantls lx its vcrtebral column behind the head with a scalpel hlade. Then I0 \ertical cuts were inade nitli ii dpclon cach side of the hod). The fish was then rinsed with Sin1 r~fdechlvrinatedtap \Later. Rinsc writer w:is sollcctecl in :I beaker and uscd immediately. Time between stimulus collection and injcctiiin in a trial was 2 - niin (hi! female Gunh& wcre used to prepare stimuli ro ensure that thc hdy size of stimulus fish \vas approvini it,:l! equal to that of fish uscd in the cichlid treatment. Mean (+ SD) standard Icngth (mm) of ctimulur firh \\'as 3') 6 + 3.8inm and 38.9 + 3.7 mm for convict cichlids and C;iifih&, respcctivcly (t = 0.3l. df = 26, p = 0.623). \Ye ran a total of 28 trials, each lasting for 11 min: 14 trials using water in rhe morning followed by Gum/i//.riu skin in the afternoon, and 14 trials using water in the morning and convict cichlid skin in the afternoon. I3efore each trial, we prepared test stimuli (5 ml water, <;urn/hrio or cichlid cues). We then wirhdrcw 60 nil of water through the injection tube froin the test tank inti, a 6Ohi syringe, discarded it to rcmmc st:ile \v.itcr from the injecrion tube, and withdrew another 60 ml iif tank water and saved it for later use. ;It l(1-s iiitenalq for i inin, we scored the numhcr of fish (0, 1, 2) positioned below the horizontal line on the front panc of ttic aquariuin, and the numhcr of fish under rhe shelter ohicct. ;\t the 3 min mark, we slowly injected the .5 nil ik test stimuli fiillowcd hy the 60 ml of tank water. 'llic volume of the injection tube was 25 inl, thus thy test stiniuli \%ere flushed out of the injection tube. Stimulus inlcction lasted for 60 s. ;It the 6 min mark we resumed scoring the fish's behaviour for another 5 min noting, as bcforc, the numhcr of fish below the line and under rlie shelter. To obtain our measure of timc spent near the tank hortom and timc spent undcr the shelter object, wc summed the number of fish (0, 1, 2) exhibiting cach hchaviour during point samples in each of the prc- and post stimulus periods. Mean (+ SLI) standard kngh (mm) of response used in this study \v:is 30.4+ 4 2 inm. 'I'hcrc was no significant difference in the size of firh tested with ~,u~hhskin :id thosc tcstcd n,itli c,)ii\-ict cichlid skin (t = 1.55,df = 56,p = 0.126). K'e videotaped the final 18 trials to score changes in agonistic Ixha\-iour between inenibers 14cach pair. We scored three bchaviours relating to intraspccific aSgrcssion: approaches, hite.; and chases. An :ippriiach u-as scored when one fish approached to within one hody length of the other. A bite was scored whcn one fish mnde oral contact with ihe other. I\ chase was scured each timc one fish pursued the other for at last onc lwdy Icngth. \Ye alsu noted thc prcscnce of freezing, an antipredator response, consiclcretl prcscnt if horh iish iii a trial remained motionless simultancously for more than 60 consecutive s. \Ye used K'ilciixon matched-pairs signed-rank tests (SlI,<;F~,l.& (AsTI-,I,I .)\\ 19x8) to compare thc magnitude of the changc in hchaviour of each pair of fish in rcspcinsc to i ml of dcchlormared water (po\r-stiiiiulus minus prc-stimulus), to the magnitude of the changc in hehaviiiur in rezponx to 5 ml of test srimulus (post-stimulus minus pre-stimulus). Movement to the bottom, use of refuge and reduction in activin .ire :ill cimiponcnts of crypsis, a common antipredator strategy uscd hy pry to avoid predators (1.1\f/\ & DII I 1090). l'urtlici, ;iggrcssioti is ncgatircly associated with predation rish (tlr h'~'lv~FoRl>1'182). Thus, we used fine-tailed iccts because we prcdictcd an antipredmir rcspi)iisc to injury-released chemical cues, rhat is, an incrucc in tinic >pent at the bottom, an increase in timc spent under the shelter, and a dccrcasc in agr Any effect of time of day (control trials in the muming, expcrimcntal t or aggressive behaviour applied equally to trials tckting the effects of C,un//mrzuand convict cichlid Am. Therefore, testing water in the morning and skin estract in the afternoon do not confound the ci)nclusii~nsot tiiis crud!. Results Convict cichlids sig~ificantlyincreased the amount of time they spent in the bottom 5 cm of the tank in response to chemical stimuli from conspecifics ('I' = 6?.:i, n = 12, 286 Near tank Under bottom shelter 40 1 I 30

20

.-e 10 Q) 0

IU Garnbusia Cichlid Gambusia Cichlid Skin stimulus I,<$. I: Median (+ 25 and 75?'oilcs) change (post-stiniulus minus pre-stimulus) in the number (itfich near the tank bottom and undcr the shcltcr object for pairs of con\-ict cichlids prcsentcd with 5 ml of &chlorinated tap nater (open bars) and 5 rnl of skin extract (hatched bars). Skin extract was prepared from either Lrirr/bii.rdu or convict cichlidr

p = 0.032) and showed a tendency to move to the bottom in response to CMmhusia skin (T' = 79, n = 14, p = 0.052; Fig. 1). Pre-post differences of zero are omitted from matched- pairs signed-rank tests (SIEGFL & Cr\srm,r,Aw 1988), resulting in sample sizes of less than 14 in some cases. The shelter object was monopolized by the dominant individual within each pair in the pre-stimulus period. However, in the post-stimulus period of expcrimental trials both members of each pair often shared the shelter. Compared with the response to dechlori- nated water, the number of fish occupying the shelter increased significantly in response to conspecific alarm cues (T' = 91.5, n = 14, p = 0.007) but not in response to Gumhusia skin ('I?= 72.5, n 14, p = 0.121; Fig. 1). Freezing behaviour occurred in 3 of the 10 videotaped trials using Ganhszu skin as the stimulus, and in 5 of the 8 videotaped trials using convict cichlid skin as a stimulus (Fisher's exact test, p = 0.248). Freezing did not occur in any of the water-control trials. There was a significant reduction in the frequency of aggressive behaviour in response to injured conspecific skin, but not in response to injured Gam/~usirrslan, rclative to the water control (Fig. 2). In response to injured conspecific skin, there was a significant reduction in the number of approachcs (T' = 3.5, n = 7, p = 0.047) and number of bites

(T' = 4, n = S, p = 0.027) but not in the number of chases (T' = 7, n = 6, p 1: 0.281). There was no reduction in any of the measures of aggression in response to Ghh.riu skin; approaches (T' = 23.5, n = 9, p = 0.500), bites p' = 15, n = 7, p = 0.469) and chases v' = 15, n = 7, p = 0.469). /\larm Reaction by bnvict Cichlids to (:hernical Cues 287 Approach Chase 0t U

Gambusia Cichlid Gambusia Cichlid Gambusia Cichlid Skin stimulus I?<. 2: Median (+ 25 and ii'%des)change (post~stimulusminus pre-stimulus) in the frequency of approachca, bites and chases for pairs of convict cichlids presented with 5 in1 of dechlorinated tap \T attr (open bars) and 5 ml of skin extract (hatched bars). Skin extract was prepared from either Gumh.rzo or ccinmct cichlids

Discussion

Convict cichlids clearly showed antipredator behaviour and suppressed aggression in response to injuryreleased chemical stimuli from conspecifics, but not to injuryreleased chemical stimuli from allopatric heterospecifics. Injury-released cues from conspecifics arc a reliable source of information about predation risk. Antipredator 1xh:n iour in response to these cues significantly reduces the risk of predation (SNYDER1967; HEWS 1988;

1~~~~~ & SMITH 1993a). Confirmation of an alarm reaction to injuc-released alarm pheronioncs in convict cichlids adds another to the list of non-ostariophysans with similar antipredator systems. Of the 94 non-ostariophysan species considered by PI.I

Acknowledgements

This prolcct was supportcd hy the University of licntuchy and a posthct"d fellinchip to 13. 11. W. trom the hatiiral Scieiices and Ikgincering Kcscarch Council of Canada.

Literature Cited hKhllTh~;l~,,K. H. 1961): Obsemations of parental behavior of C,7ch/u,romu mpfi.rc/u/t~m((>bnt?cr). Trans. lianqas kad. Sci. 63, 269-275. /\rb:hl A, 1. & SI'I:N%I ,f;K, D 1977: ;\]arm suhstaiicc of thc marine mud snail, .\'or,ior///i ci%ro/t.in.r, hir)logical characterization and posslhle evolution. J. (:hein. t.cd 3, 1'3-1 87. I~I:RXSI'F IK, \x. 1980: Parental care heharior in the cichlid fish C,i&mmu qqmfir~;utw,/. (:(~pci;i 1980, 682- 686. HIIRKA, T. M. 1981: An Atlas of Distribution of thc Ireshwater Fish Families of the \Torld. L'niv. of Nebraska Press, Imcoln. tlk bSlh(;, \X . i\. 1987: l'cces dc ias )\pas Continentales dc Costa Kica. Lrnkersidad de (.octa Kica, Sail Jose, 271 PP. (~liIL'I:Kb, D. P.. RHOLY'U,G. E. & SAIIT-II,K 1. I' 1?96a: The cvolution of chemical al:irm iignds: attracting predators hencfits alarm signal senders. Am. Nar., 148, 649-659. --. & Shrmi, R. J. I;. 1994a: Intra- and intcrspecitic avoidance of arcas marked aith shin cxtract from brcmk sticklel~acLs((,dm inmmfuns) in a natural habitat. J. (:hem. Ihl. 20, 1517-1 524. _- & -- 1994h: Fathcad minnows, l'Niiepliubprnmrlu.r, acquire predator recognition \vhcn alarm substance is assnciated with the sight of unfamiliar fish. hnim. Kchav. 48, 59-605. Alarm Reaction by Convict Cichlids to Chemical (:ues 289

-- & -- 1995: Free-living fathead minnows rapidly learn to recogni7e pike as predators. J. t?sh Bid. 46, 949-954.

--, WISLNDEN, B. D. & SMITH, R J. I: 1995a: The role of experience in the response oi- tathead minnoars (I~i~/~hul~spr~melus)to skin extract of Iowa dartrrs (l:tiieustomu wile). Behaviiiur 132, 665- 674.

--, -- & -- 1995h: Predation risk influences repniductix e behanour of Iowa darters. /:th~o~/omuode (Osteichthyes, Percidae). Ethology 99, 278-285. -- __ & -- 1996b: Damselfly larvae learn to recognize predators from chemical cue; in rhe predator's diet. i\nim. Hehav. 52, 315-320. CVI.P, J. hl. & CAStl, l<. J. 1994: i\nti-prcdator responses of mayfly larvae to conspecific and predator stimuli. J. N. /\m. Benthiil. Six. 13, 299-309. ,T. J. 1996: Gender contests in a simultaneous hermaphrodite snail: a size-advantage nigxlel for behaviour. Anim. Hehav. 51, 345-351. FoRSGREN, E 1992: Predation risk affects mate choice in a gobiid fish. Am. Nat. 140, 104--1049.

-- & ~~AGNHAGFX,C 1993: Conflicting demands in sand gobics: predators influence reproductil e behaviour. Behamtur 126, 125-135. FR,w.R, S. A. & Ki?,r;.iw,r

--, WISENDEiX, A. D. & K~.~PI;LI;YSII~~.,h1. H. A. 1993: Aggressive behaviour among con\ ict cichlid (('khIu.sofnu nijr~usciutm~)fry of different sizes and its importance in brood adoption. Can. J. Zoo1 71, 23.58-2362. GARCIA,C., ROI,~~X-/\~.\,AR€~,~,E.& Shn~ 1k.2, L 1992: r\larm reaction and alert state in (7u~iib,~.siuuif1iis (Pisccs, Poeciliidae) in response to chemical stimuli from inlured ciinspecifics. J. Ethol. 10, 11-+(I. GRAKD,T. C. & GRANT, J.\Y. A 1994 Spatial predictahilit! of resources and the icie:il free distribution in convict cichltds, Cichlasomu ngrofi.suu/zin/. him. Hehav. 48, 909--919. k[AIb\, T. J. 1992: Ovc and introduction. In: I%h Chemrjrcception (I O'+Kh, T. J.. ed.). ('hapman & Hall, hew k'ork. pp. 1-12. HIui.r:m, B A. 1994: r\larm resprinses in the crayfish 0rcanecte.r r;irilir and Onunectrs propnpinpus. J. (:hem. Fcol. 20, 1i25-1535. Ht.u,s, D k;. 1988: Alarm response in larval western toads, Hu/i boreas: release of lard chcniicd by a natural predator and its effect on predator capture efficiency. hnim. Hehai. 36, 125-133. HI:)\?'^:,, N.R. & stlk,lh, 'I' hl. 1975: Anthopleurine: a sea anemtme alarm pheriimime. Science 189, 386-388. HVGII~.,D. M., TI IL'RINC;Io inter- and intraspecific aggression vary in relation to prcd:itim pressure in sticklebacks? him.Bchav. 30, 909-916. JI\IS\Y'AI,, S. l<. & W~(;HRAY,S. 1990: Quantification of defence reactions of cichlid fish, Orwchrott/i.snio.ssuwh~iw (Peters) Trewavas, in response to warnlng chemicals. Ind. J. ,\nim. Sci. 60, 1137-111.5. tihEl.t.,Y, H R. & GRA~T,J. \Y. A. 19932: Visual informat~~n,resource valuc, and scqucnt!al assessment in convict cichlids (~.ichLz.sumn

-- &-- 199%: j\cymmetries in the expected value of food dc not predict the iiutrimc (if iontests hetwvcen convict cichlids. Anim. Hehav. 45, 1035-1037. KEI.~xI.I..YSIDT:, hf El. A. 1985: Ripmy and mate choice in thc biparental cichlid fish C/chhsomi titp~uciutum. Behav. Ecol. Sociobiol. 17, 285-290. .- -, K,\>u(;I:I.~~',R. W. & KL'PP~,Rs,B. LT. 1985: 1:emale mate choice and male parental defence bchariiir in the cichlid fish CXhmmu nz;rroiasriatum. Can. I. Zed. 63, 2489-2493. tioo~s,hl I\. 8: GRANT,J. W, A 1993: X'eight asymmetry and sequential assessment in ccinvx: cichlid contests. Can. J. Zool. 71, 47Sd79. LAVKRY, R. J. 1995: Past reproductive effort affects parental lxhmiour in a cichlid tidi, C/fhL7smc7 ri&/usczu//vt/: a comparison of tnexperienced and experienced hreeders with normal and expcrinientally reduced broods. col. Sociohiol. 36, 19.%199. -- ~.hYslDk.,M H,A. 1990: Parental investment uf a biparental cichlid hh, C ich:cl.ortm @r~~usciuir,m (Pisces, Cichlidae) in response to brood size and past in\,estmerit. Anim. Hehav. 40, 1 128--1117.

-- & REEUS,S G. 1994: F.ffect of mate removal on current and subsequent parental carc in the con\-ict cichlid (Pisces: Cichlidae). Ethology 97, 265-277. LIl.t:,Y, N R. 1982 Chemical communicatiim in fish. Can. J. Fish. hquat. Sci. 39, 22-35 LIhi,A, S. L. & DiI.]., L M. 1990: Behavioral decisions made under the risk of prcdatiim: a rcvicw and prospectus. <:an. J. hid. 68, 619-640. MAGNHAGIX;,C. 1991: Predation risk as a cost of reproduction. Trends Ecol. Evd. 6, 183--186.

~~ & VHSTERGAARD,K. 1991: Risk taking in relation to reproductive investments and future reproductive opportunities: field experiments on ncst~guardingcommon gobies, Ponmto.rchi.iiw.r mzmp Reha\-. Ecol. 2, 351-359. __ & -- 1993: Brood size and offspring age affect risk-taking and aggression in nest-guarding common gobies. Behaviour 125, 233-243. MAGLIRRAN, A. E. 1989: Acquired recognition of predator odour in the European minnow :Pho.YinMsphoz/nllr). Ethohh~82, 216-233. ~-& No~~ti:,M. A. 1991: Another battle of the sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poeidiu reticdata. Proc. R. Soc. Lond. 246B, 31-38. -~& SbGIiERS, B. H. 1990: Risk sensitive courtship in the guppy (Pods reticdata). Hehavimu 112, 194-201. SfATtIIS, A., CtIIVERS, D P.& SMITH,R. J. F. 1995: Chemical alarm signals: predator dctcrrents or predator attractants? Am. Xat. 145, 9961005. __ tk SMITH, R. J. F 1992: Avmdance of areas marked with a chemical alarm substance by fathead minnows (f~z~n~~a/e~~r~rn~/as)in a natural habitat. Can. J. Zool. 70, 1373-1476. ~-& -- 19931: Chemical alarm signals increase the sunisal time of fathead ininnow (I~1IMYPIIN/~sprome/as) during encounters with northern pike (Esox brrrrr). Achav. Ecol. 4, 260-265.

~~ & -~1993h: Fathead minnows, PimcphalrJ promeius, learn to recognize northern pike, f2so.Y Iuiiiis, as predators on the basis of chemical stimuli from minnows in the pike’s diet. Anim. Behav. 46, 645-656.

~~ & -- 1993~:Intraspccific and cross-superorder responses to alarm signals by brook stickleback. Ecolog3. 74,2395-2404. ~IYKHERG,A. A. Jr 1975: The rolc of chemical and visual stimuli in the preferential discrimination of young hy the cichlid fish C-ichilasoma n~ra/asriafmz(Gunther). 7,. Tierpsychol. 37, 274-207. Nii~.soK,I.S. 1984: Fishes of the World (2nd Ed.). New- York: VC’ilcy-Interscience. N<)BI.K,G. K. 1939: The experimental animal from the naturalist’s point of view. Am. Kat. 73, 113-126. MIONAN, K. (1. 1983: Female mate choice in the cichlid fish Czch/a.iomu n&ro/a.icra/irm. ,him. Behav. 31, 1005- 1010. YSIDTi, hl. H. A. 1993: Mate choice by thc male crmvici cichlid (Cichiasomu idae). Etholok~95, 247-256. Oi.IVt.lKA, R. P. & AI.MADA, D C. 1996: Dominance hierarchies and social structure in cxptire groups of the Oreoihromzs mossurnhiccls peleostei Cichlidae). Ethol. F,col. Cvol. 8, 39-55. pEl+.hl?,H. V. S., HER%, MJ. 8c G/\lLAGt IER,J. E. 1971: Change.; in aggressivc interaction in adjacently territurial consict cichlids (C’irhiasontu @rofi.rizu/mi): a study of habituation. Bchaviour 40, 33-53. -- & PFEG-., S. C. 1982: Parental factors in the sensitizauon and habituation of territorial aggqession in the convict cichlid (Cichlusoma ngro/usciutt/m).J. Comp. Physiol. Psychol. 96, 955-966. PPEIFFIX,W. 1977: The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977, 653- 66.5 Rj\XC;t;,1,EY, R. W. & GoDh,J.-G.J 1992: The effects of a trade-off between foraging and brood defensc on a parental hehaviour in the convict cichlid fish, Ciciilasornu nzgr~fi.iiiatnm.Behaviour 120, 12.3-137. REEHS, S. G. 1993: A test of time-place learning in a cichlid hsh. Behav. Proc. 30, 273-2232. -. - l994a: The anticipation of night hy fry-retrieling convict cichlrds. him. Behav. 48, 89--9.5.

~~ 1994b: Nocturnal mate rccqgnition and nest guarding by fmiale convict c~chlids(Picccs, Cichlidac: Cicldarmma q~r~fasciatum)).F,tholokT 96, 3U3-312. RFED, J. R. 1969: Alarm substances and fright reaction in some fishes of the Southeastern Cnitcd States. Trans. Am. Fish. SOC.98, 66k668. SC:lI( T%, F. 1956: Vergleichende LJntersuchungcn uber die Schreckreakrion bei Fischen und cleren Verbreitung. Z. Vergl. Physiol. 38, 84-135. SIt,GEI., S & CASTEI.I.AK, N. J. Jr 1988: Nonparametric Statistics for the Behavioral Scienccs (2nd Ed.).

SIH, A. 1986: Antipredator responses and the perception of danger by mosquito larvae. EcoIofl67, 43-41,

~~ & KRLIPA,J. J. 1995: Interacting effects of predation risk and malc and female drnaity on male/female conflicts and mating dynamics of stream water striders. Behav. F,col. 6, 316-325. SlllTl I, c. & WOO’rTON, R. J. 1995: Experimental analysis of some factors affecting parental expenditure and investment in ~icbiasomanz@o/usciatum (Cichlidac). knv. Biol. Fishes 42, 289-302. S~I~TII,R J. F. 1979: Alarm reaction of Iowa and johnny darters (Etheosfoma, Percidac, Pisces) to chemicals from injured conspecifics. Can. J. Zool. 57, 1278-1282. Alarm Reaction by Convict Cichlids to Chemical (:ucs 291

-__ 1982: Reaction of Prrcinu n;Xro/sciulu, An/mocy;ptu hrunz, and ktheosfomu s/uui~ii(Pcrcidae, Pisces) to conspccific and congeneric skin extracts. Can. J. Zool. 60, 1067-1072.

-- 1989: The response of ,4stmoptc~xremipuncfotnr and Gwufholupis unyerenw (Pisces, Gobiidae) to chemical stimuli from injured conspecifics, an alarm response in gobies. i3hoIogy 81, 279-290. -- 1992: Alarm signals in fishes. Rcv. Fish Hid Fish. 2, 33-63. _- & LAWRENC~,B.J. 1991: The response of a bumblebec goby, Bruc,&uIins .ruhuntci, to chmi:c.il stimuli from injured conspecifics. Enr.Biol. Fishes 15, 147-149. --, __ & SMITH,M. J. 1991: Cross-reactions ti) akin extract bcnveen two gobies, .-lstrtr.nopf,vya, .s~rmp1/i7rtatus and Hrucbj;phi/dssulianns. J. Chem. EcoL 17, 2252-2259. SNYDER, N. R. F. 1967: An alarm reaction of aquatic gastropods to intraspecific extract. Cornell I'niv., Apcult. Exp. Station, New York State College of Agric., Ithaca, Memoir 403. -- & SM'I>t-X, H 1970: Alarm response of Il~ademuuntillutzm. Scrcncc 168, 276-278. TOWNWEND,T. J. & WOCTITON, R. J. 1984: Effects of food supply on the reproduction of the convict cichlid, (;irhlusomu n~;imlsciutum.J. Fish BioL 24, 91-104. WI:AER, I? G. & WEBER, S P. 1971: Choice of site in C,?chfusomu ngrofisciutum (Gunthcr) (l'isces: Cichlidae). %. Tierpsychol. 28, 475478. \T'ISI:NDEN, B. D. 1994: Factors affecting reproductive success in free-ranging convict cichlids (Cichlusuim u&ro/isczufum).Can. J. Zool. 72, 2177-2185.

__ - 1995: Reproductive lichaviour of frcc-ranging convict cichlids, Cii/~iusonlan~ro/u.rciutum. Env. l3id Iishcs 43, 121-134. __, CIIIVERS, D. P. 8c SAIITII, R. J. 1:. 1997: I>earnedrecognition of prcdation risk by i:nul/qmu d;imselfly lanw optera) on the basis of chcmical cues. J. Chcm. Ecol. 23, 135-149 , G. E. & SMlTi 1, R. J. F. 1995a: Thr role of experience in risk assessment: avoidance (If areas chemically labellcd with fathead minnow alarm pheromonc by conspecifics and heterospccifics. f?coscience 2, 116-122. ___, I.,~N~R~~N.~~'O~\I-~~~~~A, T I.. & K I.P.YSIDF, M. H. A. 1995b: Fin digging and leafliftirig by the cichlid fish Cichlusomu niX+ufsciutum: examples of parental food provisioning. Anim. Bchav. 49, 623--631.

Recriiad Aprd 17, 1996