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Brian D. Wisenden

updated Nov 2009 by Brian Wisenden

Sorensen PW, Wisenden BD (eds). In prep. Fish Pheromones. Wiley-Blackwell Press.

Wisenden BD, Stumbo AD, Self PA, Snekser JL, Brisch E. In prep. Evolutionary development of antipredator competence in larval cichlids under parental care.

Wisenden BD, Martinez JY, Gracia ES. In prep. Incidence and prevalence of Ornithodiplostomum ptychocheilus metacercariae in a population of fathead minnows with tests for behavioral compromise of minnow antipredator behavior.

Wisenden BD. 2009. Quantifying anti-predator response to chemical alarm cues. In: Zebrafish Behavioral Protocols (Kalueff AV, Hart P, LaPorte J, eds). Cambridge University Press. In press

Wisenden BD. 2009. Learned recognition by zebrafish and other cyprinids. In: Zebrafish Models in Neurobehavioral Research (Kalueff AV, Hart P, LaPorte J, eds). Cambridge University Press. In press

Pellegrini AFA, Wisenden BD and Sorensen PW. In Press. Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk. Behavioral Ecology and Sociobiology. Pre-published online at doi 10.1007/s00265-009-0854-y 

James CT, Wisenden BD, Goater CP. In Press. Epidermal club cells do not protect fathead minnows against trematode cercariae: a test of the anti-parasite hypothesis. Journal of the Linnean Society.

Ferrari MCO, Wisenden BD, Chivers DP. In press. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology, 76 manuscript pages.

Wisenden BD, Binstock CL, Knoll KE, Linke AD, Demuth BS. Revised, resubmitted and in review. Risk-sensitive information gathering by minnows following release of chemical alarm cues. 26 manuscript pages.

Wisenden BD, Unruh A, Morantes A, Bury S ,Curry B, Driscoll R, Hussein M, Markegard S. 2009. In Press. Functional constraints on nest characteristics of pebble mounds of breeding male hornyhead chub, Nocomis biguttatus. Journal of Fish Biology. Pre-published online at doi:10.111/j.1095-8649.2009.02384.x

Wisenden BD, Rugg ML, Korpi NL, Fuselier LC. 2009. Estimates of active time of chemical alarm cues in a cyprinid fish and an amphipod crustacean. Behaviour 146: 1423-1442. pdf

Wisenden BD, Alemadi SD, Dye TP, Geray K, Hendrickson J, Rud C, Jensen M, Sonstegard G, Malott ML. 2009. Effects of nest substrate on egg deposition and incubation conditions in a natural population of fathead minnows (Pimephales promelas). Canadian Journal of Zoology 87: 379-387. Abstract pdf

Wisenden BD, Goater CP, James CT. 2009. Behavioral defenses against parasites and pathogens. In: Fish Defenses: Pathogens, Parasites, Predators vol 2 (Giacomo Z, Perrière C, Mathis A, Kapoor B.G. eds). Science Publishers. pp 151-168. Abstract pdf

Wisenden BD, Dye TP. 2009. Young convict cichlids use visual information to update olfactory homing cues. Behavioral Ecology and Sociobiology 63: 443-449. pdf

Wisenden BD, Snekser JL, Stumbo AD, Leese JM. 2008. Parental defense of an empty nest after catastrophic brood loss. Animal Behaviour 76: 2059-2067. pdf

James CT, Noyes KJ, Stumbo AD, Wisenden BD, Goater CP. 2008. Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnows. Journal of Fish Biology 73: 2238-2248 pdf

Wisenden BD. 2008. Active space of chemical alarm cue in natural fish populations. Behaviour 145: 391-407. Abstract. pdf

Wisenden BD, Karst J, Miller J, Miller S, Fuselier L. 2008. Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, Umbra limi (Kirtland 1840). Environmental Biology of Fishes. 82: 85-92.  Abstract pdf

Wisenden BD, Pogatshnik J, Gibson D, Bonacci L, Schumacher A &  Willett A. 2008. Sound the alarm: Learned association of predation risk with novel auditory stimuli by fathead minnows (Pimephales promelas) and glowlight tetras (Hemigrammus erythrozonus) after single simultaneous pairings with conspecific chemical alarm cues. Environmental Biology of Fishes 81: 141-147. Abstract pdf

Chivers DP, Wisenden BD, Hindman CJ, Michalak TA, Kusch RC, Kaminskyj SGW, Jack KL, Ferrari MCO, Pollock RJ, Halbgewachs CF, Pollock MS, Alemadi S, James CT, Savaloja RK, Goater CP, Corwin A, Mirza RS, Kiesecker JM, Brown GE, Adrian JCJr, Krone PH, Blaustein AR, Mathis A. 2007. Epidermal ‘alarm substance’ cells of fishes are maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proceedings of the Royal Society London, Series B. 274: 2611-2620 Abstract pdf

Wisenden BD & Chivers DP 2006. The role of public chemical information in antipredator behaviour. In: Fish Communication (Ladich F, Collins SP, Moller P, Kapoor BG, eds), Science Publisher, NH, pp259-278. Abstract pdf

Wisenden BD & Barbour KA. 2005. Antipredator responses to skin extract of redbelly dace by free-ranging populations of redbelly dace and fathead minnows. Environmental Biology of Fishes. 72: 227-233. Abstract  pdf

Wisenden BD & Stacey NE 2005. Fish semiochemicals and the evolution of communication networks. In: Communication Networks (McGregor PK ed), Cambridge University Press. pp. 540-567. Synthesis section of chapter pdf

Wisenden BD, Klitzke J, Nelson R, Friedl D, & Jacobson, P. 2004. Predator-recognition training of hatchery-reared walleye and a field test of a training method using yellow perch. Canadian Journal of Fisheries and Aquatic Sciences 62: 2144-2150. Abstract  pdf

Wisenden BD, Vollbrecht KA & Brown JL. 2004. Is there a fish alarm cue? Affirming evidence from a wild study. Animal Behaviour 67: 59-67. Abstract  pdf

Pollock MS, Chivers DP, Mirza RS & Wisenden BD. 2003. Fathead minnows learn to recognize chemical alarm cues of introduced brook stickleback. Environmental Biology of Fishes 66: 313-319. Abstract  pdf

Wisenden BD, Pollock MS, Tremaine RJ, Webb JM, Wismer ME & Chivers DP. 2003. Synergistic interactions between chemical alarm cues and the presence of conspecific and heterospecific fish shoals. Behavioral Ecology and Sociobiology 54: 485-490. Abstract.  pdf

Wisenden BD. 2003. Chemically-mediated strategies to counter predation. In: Sensory Processing in the Aquatic Environment (Collin SP & Marshall NJ eds). pp 236-251. Springer-Verlag, NY . Summary table

Alemadi SD & Wisenden BD. 2002. Antipredator response to injury-released chemical alarm cues by convict cichlid young before and after independence from parental care. Behaviour 139: 603-611. Abstract  pdf

Wisenden BD & Thiel TA. 2002. Field verification of predator attraction to minnow alarm substance. Journal of Chemical Ecology 28: 433-438. Abstract  pdf

Wisenden BD & Millard MC. 2001. Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues. Animal Behaviour 62: 761-766. Abstract  pdf

Wisenden BD, Pohlman SG & Watkin EE. 2001. Avoidance of conspecific injury-released chemical cues by free-ranging Gammarus lacustris (Crustacea: Amphipoda). Journal of Chemical Ecology 27: 1249-1258. Abstract pdf

Wisenden BD & Harter KR. 2001. Motion, not shape, facilitates association of predation risk with novel objects by fathead minnows (Pimephales promelas). Ethology 107: 357-364. Abstract  pdf

Wisenden BD 2001. Brood defense and optimal brood size in convict cichlids Cichlasoma (Archocentrus) nigrofasciatum, a species with biparental care.  Journal of Aquariculture & Aquatic Sciences  9:303-320. Abstract

Korpi NL & Wisenden BD. 2001. Learned recognition of novel predator odour by zebra danios, Danio rerio, following time-shifted presentation of alarm cue and predator odour. Environmental Biology of Fishes 61: 205-211. Abstract  pdf

Wisenden BD. 2000. Olfactory assessment of predation risk. Philosophical Transactions of the Royal Society. 355: 1205-1208.  Abstract  pdf

Wisenden BD. 2000. Scents of danger: the evolution of olfactory ornamentation in chemically-mediated predator-prey interactions. in: Animal Signals: Signalling and Signal Design in Animal Communication (Espmark Y, Amundsen T, & Rosenqvist G, eds). Tapir Academic Press, Trondheim, Norway. pp. 365-386. Abstract

Yunker WK, Wein DE & Wisenden BD. 1999. Conditioned alarm behavior in fathead minnows (Pimephales promelas) resulting from association of chemical alarm pheromone with a nonbiological visual stimulus. Journal of Chemical Ecology. 25: 2677-2686. Abstract pdf

Wisenden BD. 1999. Alloparental care in fishes. Reviews in Fish Biology and Fisheries. 9: 45-70. Abstract pdf

Wisenden BD, Cline A & Sparkes TC. 1999. Survival benefit to antipredator behavior in the amphipod Gammarus minus in response to injury-released chemical cues from conspecifics and heterospecifics. Ethology 105: 407-414. Abstract  pdf

Wisenden BD & Smith RJF. 1998. A re-evaluation of the effect of shoalmate familiarity on the  proliferation of alarm substance cells in fathead minnows. Journal of Fish Biology. 53: 841-846. Abstract pdf

Sargent RC, Rush VN, Wisenden BD & Yan HY. 1998. Courtship and mate choice in fishes: Integrating behavioral and sensory ecology. American Zoologist 38: 82-96. Abstract pdf

Wisenden BD. 1998. Frog distress calls attract secondary predator, benefiting the signaler. Herpetological Review 29: 168. Abstract

Wudkevich K, Wisenden BD, Chivers DP & Smith RJF. 1997. Reactions of Gammarus lacustris (Amphipoda) to chemical stimuli from natural predators and injured conspecifics. Journal of Chemical Ecology. 23: 1163-1173. Abstract pdf

Wisenden BD & Sargent RC. 1997. Antipredator behavior and suppressed aggression by convict cichlids in response to injury-released chemical cues of conspecifics but not to those of an allopatric heterospecific. Ethology 103: 283-291. Abstract

Wisenden BD, Chivers DP & Smith RJF. 1997. Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. Journal of Chemical Ecology 23: 135-151. Abstract pdf

Wisenden BD & Smith RJF. 1997. The effect of physical condition and shoal-mate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows. Journal of Fish Biology 50: 799-808. Abstract pdf

Chivers DP, Wisenden BD & Smith RJF. 1996. Damselfly larvae (Enallagma boreale) learn to recognize predators from chemical cues in the predator’s diet. Animal Behaviour 52: 315-320. Abstract  pdf

Wisenden BD, Chivers DP & Smith RJF. 1995. Early warning in the predation sequence: a disturbance pheromone in Iowa darters (Etheostoma exile). Journal of Chemical Ecology 21: 1469-1480. Abstract pdf

Chivers DP, Wisenden BD & Smith RJF. 1995. The role of experience in the avoidance of darter alarm pheromone by fathead minnows (Pimephales promelas). Behaviour 132: 665-674. Abstract pdf

Chivers DP, Wisenden BD & Smith RJF. 1995. Predation risk influences reproductive behaviour of Iowa darters, Etheostoma exile (Osteichthyes, Percidae). Ethology 99: 278-285. Abstract

Wisenden BD, Chivers DP, Brown GE & Smith RJF. 1995. The role of experience in risk assessment: avoidance of areas chemically labelled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Écoscience 2: 116-122. Abstract pdf

Wisenden BD. 1995. Reproductive behaviour in free-ranging convict cichlids. Environmental Biology of Fishes 43: 121-134. Abstract pdf

Wisenden BD, Lanfranconi-Izawa TL & Keenleyside MHA. 1995. Fin digging and leaf lifting: examples of parental food provisioning by the cichlid fish Cichlasoma nigrofasciatum. Animal Behaviour 49: 623-639. Abstract  pdf

Wisenden BD & Keenleyside MHA. 1995. Brood size and the economy of brood defence: testing Lack’s hypothesis in a biparental cichlid fish. Environmental Biology of Fishes 43: 145-151. Abstract pdf

Wisenden BD, Chivers DP & Smith RJF. 1994. Risk-sensitive habitat use by brook stickleback (Culaea inconstans) in areas associated with minnow alarm pheromone. Journal of Chemical Ecology 20: 2975-2983. Abstract pdf

Wisenden BD. 1994. Factors affecting reproductive success of convict cichlids in Costa Rican streams. Canadian Journal of Zoology 72:2177-2185. Abstract

Wisenden BD & Keenleyside MHA. 1994. The dilution effect and differential predation following brood adoption in free-ranging convict cichlids (Cichlasoma nigrofasciatum). Ethology 96: 203-212. Abstract

Wisenden BD. 1994. Factors affecting male mate desertion in the biparental cichlid fish (Cichlasoma nigrofasciatum) in Costa Rica. Behavioral Ecology 5:439-447. Abstract

Fraser SA, Wisenden BD & Keenleyside MHA. 1993. Aggressive behaviour among convict cichlid (Cichlasoma nigrofasciatum) fry of different sizes and its importance to brood adoption. Canadian Journal of Zoology 71:2358-2363. Abstract

Wisenden BD. 1993. Female convict cichlids can adjust gonadal investment in current reproduction in response to relative risk of brood predation. Canadian Journal of Zoology 71:252-256. Abstract

Wisenden BD & Keenleyside MHA. 1992. Intraspecific brood adoption in convict cichlids: a mutual benefit. Behavioral Ecology and Sociobiology 31:263-269. Abstract pdf

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Abstracts

Young convict cichlids use visual information to update olfactory homing cues

Brian D. Wisenden and Thomas P. Dye

submitted to Behavioral Ecology and Sociobiology

In this study, we tested young cichlids for a role of chemical cues in homing toward the safety of parental protection. Convict cichlids have biparental defence of their free-swimming young. If young become separated from their family they must rejoin their family within minutes to have any chance of survival. Here, we used a dichotomous Y-maze to test if displaced convict cichlid young can use chemical cues to orient to their family. First, we showed that young preferentially orient toward water taken from their home tank versus blank water taken from a tank that contained no fish. Second, we showed that young prefer home tank water to water from a tank containing another family of convict cichlids. In a third experiment, we placed young convict cichlids in a small aquarium inserted within a larger aquarium. The large aquarium contained either their parents or no fish. The small insert aquarium contained blank water from a tank that had never contained fish. After 20 min in the insert tank, young convict cichlids were placed in the Y-maze and given a choice between either their home tank water or water from the insert tank. Convict cichlids that did not see their parents during the 20-min conditioning period oriented strongly toward chemical cues of their home tank water. Young that saw their parents during the 20-min conditioning period oriented strongly toward the chemical cues of the insert tank. These data indicate that young convict cichlids use visual cues to learn and re-set the smell of “home” in less than 20 min.

Active space of chemical alarm cue in natural fish populations.

Brian D. Wisenden

Behaviour 145: 391-407

Chemical cues released from injured fish skin during a predator attack provide reliable information about the presence of predation risk. Here, I report estimates of the area avoided by littoral fishes after experimental release of chemical alarm cues in two small lakes in northern Minnesota. Minnow traps were labeled chemically with either water (control) or skin extract (chemical alarm cue) made from 2 cm² of cyprinid skin (redbelly dace in experiment 1, fathead minnows in experiment 2). Traps labeled with water were placed 1, 2, or 8 m from traps labeled with alarm cue. After 2 h, water-traps that were either 1 or 2 m distant from an alarm-trap caught significantly fewer fish than water-traps 8 m distant from alarm-traps. Conspecific and heterospecific skin extract produced similar area avoidance by fathead minnows. Redbelly dace showed a larger active space in response to conspecific than heterospecific alarm cues. Overall, the radius of active space was between 2 and 8 m under lake conditions with average subsurface currents of 0.82 cm / s. These data are the first field estimates of active space of ostariophysan chemical alarm cues. Back to ref list

Epidermal ‘alarm substance’ cells of fishes are maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

Douglas P. Chivers, Brian D. Wisenden, Carrie J. Hindman, Tracy A. Michalak, Robin C. Kusch, Susan G.W. Kaminskyj, Kristin L. Jack, Maud C.O. Ferrari, Robyn J. Pollock, Colin F. Halbgewachs, Michael S. Pollock, Shireen Alemadi,  Clayton T. James, Rachel K. Savaloja, Cam P. Goater, Amber Corwin, Reehan. S. Mirza, Joseph M. Kiesecker, Grant E. Brown, James C. Adrian Jr., Patrick H. Krone, Andrew R. Blaustein and Alicia Mathis.

Proceedings of the Royal Society, London, Series B (In Press)

Many fishes possess specialised epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fish. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water molds: Saprolegnia ferax and S. parasitica), skin penetrating parasites (larval trematodes: Teleorchis sp., Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fish challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialised cells arose and are maintained by natural selection because of selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation. Back to ref list

Behavioral defenses against pathogens and parasites

Brian D. Wisenden, Cam P. Goater, Clayton T. James

In: Fish Defenses (eds. Zaccone Giacomo, Alicia Mathis)

In the extreme, parasites contribute to premature mortality of their hosts. More commonly, parasites exert sublethal effects.  The enormous diversity of parasites that utilize fish at some stage in their life-cycle has been demonstrated to affect virtually every aspect of fish ecology – from foraging to avoiding predators to attracting to mate choice. Here, we review the literature on behavioral defenses of fish against risk of attack from parasites. Our aim is to organize the literature to stimulate future research to fill in the many and large gaps in existing knowledge. We identify three main classes of behavioral avoidance of parasites based on the mode of parasite transmission: (1) avoidance of infective stages, (2) avoidance of contagious conspecifics, and (3) avoidance of infected prey. Post-infection behavioral management of ectoparasite load includes chafing and cleaner-client mutualisms, while management of endoparasites is poorly documented. Early evidence suggests that fish can detect infective stages either directly upon contact, or indirectly via behavioral changes in shoalmates or by chemical cues. Upon detection, some aquatic hosts elicit a series of behaviors to reduce exposure, often involving dislodgement of infective stages from the site of infection, decreased activity, and/or increased use of parasite-free refugia. Although there are early indications that fish can respond to some ectoparasites in a similar manner as they do to predators and other aquatic stressors, there are too few studies to generalize to other types of aquatic parasite. Back to ref list

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, Umbra limi (Kirtland 1840)

Brian D. Wisenden, Justin Karst, Jeffrey Milller, Stacey Miller & Linda Fuselier

Environmental Biology of Fishes in press

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory. Back to ref list

Sound the alarm: Learned association of predation risk with novel auditory stimuli by fathead minnows (Pimephales promelas) and glowlight tetras (Hemigrammus erythrozonus) after single simultaneous pairings with conspecific chemical alarm cues.

Brian D. Wisenden, Julie Pogatshnik, Danfee Gibson, Lucia Bonacci, Adam Schumacher &  Allison Willett

Environmental Biology of Fishes 81: 141-147

Fathead minnows (Ostariophysi, Cyprinidae, Pimephales promelas) and glowlight tetras (Ostariophysi, Characidae, Hemigrammus erythrozonus) were tested for their ability to associate predation risk with novel auditory stimuli after auditory stimuli were presented simultaneously with chemical alarm cues. Minnows and tetras gave a fright response when exposed to skin extract (alarm cue) and an artificial auditory sound stimulus, but no response to water (control) and sound, indicating that they did not have a pre-existing aversion to the auditory stimulus. When retested with sound stimuli alone, minnows and glowlight tetras that had previously been conditioned with water and sound showed no response, but those that had been conditioned with alarm cues and sound exhibited antipredator behaviour (reduced activity) in response to the auditory cue. This is the first known demonstration of learned association of an auditory cue with predation risk, and raises questions about the role of sound in mediating predator-prey interactions in fishes. Back to ref list.

The role of public chemical information in antipredator behaviour

 Brian D. Wisenden, & Douglas P. Chivers

In: Fish Communication (Ladich F, Collins SP, Moller P, Kapoor BG, eds), Science Publisher, NH. (2006) pp. 259-278

Predators stalk, attack, capture and ingest prey. At each stage chemical cues are released passively as a natural by-product of this behavioural interaction. These chemical cues are not signals in the strict sense because their production and release are not shaped by natural selection by benefits to the sender that accrue from receiver responses. However, predation exerts steep selection on receivers to detect and respond adaptively to these cues because doing so reduces the receiver’s risk of predation. Here, we discuss briefly disturbance cues, predator odours, alarm cues and dietary cues that are released during predation. We then consider elaborations of these basic responses in behavioural ecological interactions with visual indicators of risk and the role of learning in greatly expanding the range and complex combinations of stimuli in which prey use chemical public information for mediating risk. Back to ref list

Antipredator responses to skin extract of redbelly dace by free-ranging populations of redbelly dace and fathead minnows.

Brian Wisenden & Kamil Barbour

Environmental Biology of Fishes (2005) 72: 227-233

Fishes in the superorder Ostariophysi possess specialized epidermal cells that contain a chemical alarm cue. The alarm cue is released when the skin is damaged during a predatory attack. Therefore, the cue serves as a reliable indicator of predation risk to nearby conspecifics and ecologically similar heterospecifics with which it shares predators. Antipredator behaviour in response to these alarm cues has been demonstrated in numerous studies in confined spaces (laboratory aquaria, field traps, a fluvarium). When tested on a natural field population however, behavioral response has been inconsistent. Here, we expose free-ranging redbelly dace and fathead minnows to skin extract of redbelly dace and record their behavioral response with an underwater video camera. We observed avoidance of areas in which skin extract was introduced, but no avoidance of areas in which water (control) was introduced. These data confirm the ecological function of skin extract in mediating predator-prey interactions in aquatic habitats, and argue against the hypothesis that alarm reactions are an artifact of confined spaces. Back to refs

Predator-recognition training of hatchery-reared walleye and a field test of a training method using yellow perch.

Brian Wisenden, Josh Klitzke, Ryan Nelson, David Friedl, & Peter Jacobson

Canadian Journal of Fisheries and Aquatic Sciences (2004) 62: 2144-2150.

Chemical alarm cues from injured conspecifics reliably indicate the presence of an actively foraging predator and serve as a releaser of recognition learning of correlated indicators of predation risk. Novel cues are recognized as indicators of predation risk after a single pairing of novel stimuli and chemical alarm cues. Fishes reared in captivity are predator-naïve and suffer large predation mortality when stocked into lakes with a full complement of predators. Here, we tested the potential of releaser-induced recognition learning to enhance post-stocking survival of hatchery-reared walleye (Stizostedion vitreum). In the first part of this study, we found that walleye 1) use chemical cues for assessment of predation risk, 2) do not have innate recognition of the odor of northern pike, Esox lucius (dominant predator in most lakes in Minnesota) as an indicator of predation, and 3) associate predation risk with pike odor after a single simultaneous encounter of pike odor and chemical alarm cues from walleye skin. In the second part of this study, we tested if efficient mass training of fingerlings could be conducted in rearing ponds before fingerlings are harvested and stocked. We attempted to train a natural population of yellow perch, Perca flavescens (as a surrogate for walleye) to fear pike odor. Initially, perch avoided traps scented with perch skin extract (alarm cues) but not those scented with pike odor or water. We attempted to confer recognition learning by placing sponge blocks containing pike odor and perch alarm cues around the perimeter of the lake. When we repeated the trapping protocol of the first day we found that perch avoided traps scented with perch alarm cues, but did not avoid traps labeled with pike odor or water. We conclude that recognition learning offers potential as a management tool for walleye, but significant logistic challenges must be solved before it can be implemented. Back to refs

Fish semiochemicals and the evolution of communication networks. 

In: Communication Networks (McGregor PK ed), (2005) Cambridge University Press. pp. 540-567.

Brian D. Wisenden & Norm E. Stacey  

Current theory about the function of animal communication networks (e.g. McGregor & Peake, 2000) has been heavily influenced by studies of acoustic and visual systems, where it seems clear that true communication between specialised signallers and receivers has arisen through the bilateral benefits resulting from their reciprocal interactions. Although studies of fish semiochemicals also provide evidence of specialisations indicative of communication, the specific functions of such specialised semiochemicals within networks are not well understood.

In sea lamprey, for example, both the large active space of the proposed male sex pheromone 3-keto-PS and apparent male-specific gill structure facilitating its release (Li et al., 2002), suggest specialisations for increased amplitude of a specialised tonic signal. The proposed function of this male lamprey signal appears analogous to the aggregate signal produced by chorusing male anurans (Grafe, this volume), insofar as the combined odour of many males induces the upstream movement of many females. However, it remains to be determined if attracted female lamprey also use the male pheromone in mate choice, and if this might have been the pheromone's original function.

Also, in the black goby, non-spermatogenic portions of the testes appear specialised for synthesis of a steroid pheromone, etiocholanolone-glucuronide (Etio-G), originally proposed simply to attract ovulated females to the male's nest (Colombo et al., 1980). In the round goby Neogobius melanostomus, however, both males and females respond behaviourally to Etio-G (Murphy et al., 2001), suggesting that the pheromone functions in a more complex network involving both intra- and intersexual communication. 

Given that semiochemical communication appears to have evolved in sea lamprey and gobies, and perhaps in some other fish such as blennies (Laumen et al., 1974; Gonçalves et al., 2002) and African catfish Clarias gariepinus (Van Den Hurk & Resink, 1992), these species may communicate in semiochemical networks analogous to those seen in terrestrial systems involving acoustic and visual signals. However, other fish semiochemicals such as the alarm cues of ostariophysans and the sex pheromones of goldfish appear to function not in communication, but rather in spying, where specialisation for information transfer evidently is restricted to receivers. Nonetheless, these semiochemical cues also operate in complex information networks in which semiochemicals can influence several conspecifics both directly (through exposure) and indirectly (through changes induced in exposed individuals) (e.g. Figs. 2, 4b)

Because such fish semiochemical networks based on unspecialised cues have the potential to give rise to true communication networks, they should not only extend the scope of current network theory but also raise important issues relevant to the evolutionary processes by which such communicatory networks evolve. To cite just one example, when discussion of information networks is restricted to those that involve communication, it might seem reasonable to assume that eavesdropping arises only after communicative interaction has been established. However, the ability of male goldfish to indirectly derive information about female cues by spying on the responses of exposed males (e.g. Figs. 2, 4b) demonstrates that a process analogous (and possibly homologous) to eavesdropping can precede the origin of communication.

To promote discussion of the functional and evolutionary relationships among spying, eavesdropping, and communication, we propose two hypothetical schemes. One is based on the intraspecific interactions induced by the goldfish preovulatory steroid pheromone (Fig. 5A), the second involves both intra- and interspecific predator-prey interactions in ostariophysan fishes (Fig. 5B), and both are derived from our general model for the evolution of communication (Fig. 1).

In goldfish, spying by male receivers (R) on an unspecialised steroid cue released by female originators (O; Fig. 5A-1) could lead to communication (Fig. 5A-2) if male response to heritable variation in cue production leads to differential female fitness. If this occurs, females would then be signallers (S) releasing a specialised pheromonal signal, and the male's role would change (R¹), as he now influences, and is influenced by, signal evolution. As we emphasize in this paper, however, the goldfish preovulatory pheromone mediates more than the simple dyadic spying event depicted in Figure 5A-1. The pheromone directly stimulates behavioural and endocrine/testicular responses in more than one male (R) and also induces a distinct response (ovulation) in females (Fig. 5A-3). In addition, the pheromone indirectly stimulates males (R²) via cues released by pheromone-exposed males (Fig. 5A-4).

In the ancestral condition of predator-induced prey chemical alarm cues, predator (P) attack releases general cues from the originator (O) that can be received both as an alarm cue by conspecific prey (R) and as a feeding cue by secondary predators (P²; Fig. 5B-1). If interference by secondary predators benefits originators and leads to alarm cue specialisation, originators become signallers (S), the secondary predator's role changes (P³), and receiving conspecific prey become interceptive eavesdroppers (IE) in a communication network (Fig. 5-B2). As with the goldfish pheromone (Fig. 5-A3,4), predator-induced alarm cues can exert complex effects prior to the evolution of communication. For example, alarm cues are used to associate risk with stimuli (C) correlated with predation that later serve as indicators of predation risk (Fig. 5B-3). This latter system may become elevated to that of a communication network without involvement of a secondary predator if an originator's shoalmates learn to recognise a novel indicator of risk and later alert the surviving originator to the presence of risk through early response to danger (Fig. 5B-5). And of direct relevance to the evolution of eavesdropping, alarm cues can also affect predator-prey interactions indirectly through social facilitation (social spying?) of alarm behaviour both in conspecifics (R²) and in heterospecifics (r; Fig. 5B-4).

If it is reasonable to assume that sex and alarm pheromone communication evolves from spying, as depicted in Figures 1, 5A-1,2 and 5B-1,2, then it also seems reasonable to ask whether and how communication networks evolve from spying networks. We therefore propose two general scenarios that differ primarily in the evolutionary origins of eavesdropping. In the first scenario, a simple dyadic communication (Figs. 5A-2 and 5B-2) could lead to the evolution of interceptive or social eavesdropping (Peake, this volume) if receivers evolve adaptive responses either to the signalling behaviour per se (interceptive eavesdropper; IE; Figs. 5A-5 and 5B-6) or to the signalling interaction (social eavesdropper, SE; Figs. 5A-6 and 5B-6). In this scenario, where the evolution of communication precedes that of eavesdropping, eavesdropper functions (IE and SE) are analogous to the various receiver functions in spying networks (Figs. 5A-3,4 and 5B-3,4). In the second scenario, incipient eavesdropping arises in spying networks, either as direct (Figs. 5A-3 and 5B-4) or indirect (Figs. 5A-4 and 5B-4) spying by receivers on originators, and is retained as interceptive and social eavesdropping, respectively, following the evolution of communication. In this scenario, receivers in spying networks are homologous to eavesdroppers in communication networks.

In all the scenarios shown in Figure 5, we depict eavesdropping in its proposed initial state: i.e. spying via a cue that is not specialised for transmission to eavesdroppers, despite being a signal specialised for information transfer to the primary target (Peake, this volume). At this early stage, the network functions of eavesdropper and primary target differ in kind. However, if subsequent selection by eavesdroppers leads to signal specialisation specific to the eavesdropping interaction, and thus forming a communicative relationship between eavesdropper and signaller, functions of eavesdroppers and receivers will come to differ only in degree. Studied examples of eavesdropping (Peake, this volume) typically appear to involve costs or benefits to signallers that would be expected to modify signal function; thus, it will be important to determine whether, as has been suggested for sex pheromone function in fish (Fig. 5A-1), various forms of eavesdropping in communication networks (Figs. 5A-5,6 and 5B-2,5,6) can persist as spying. Moreover, it will be important to document covariance in the relative proportions of spying versus communicative eavesdropping and the ecological and social factors that lead to the spying-communication transition. Back to refs

Fathead minnows learn to recognize chemical alarm cues of introduced brook stickleback. 

Pollock, M.S., Chivers, D.P., Mirza, R.S. and Wisenden, B.D. 

Environmental Biology of Fishes (2003) 66: 313-319.

In four experiments conducted over a 6-year period, we investigated whether fathead minnows, Pimephales promelas, could acquire the ability to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. A laboratory experiment documented that stickleback-naïve minnows did not exhibit an anti-predator response when exposed to the chemical alarm cues of stickleback. In a laboratory experiment conducted 5 years after the introduction of stickleback to the pond, minnows exhibited an antipredator response to stickleback cues. Moreover, in a field experiment the minnows exhibited avoidance of areas labelled with stickleback alarm cues. Minnows raised from eggs taken from the test pond did not exhibit an anti-predator response to stickleback cues while minnows from the test pond that had experience with stickleback cues did respond to stickleback cues. Our results provide clear evidence that cross-species responses to chemical alarm cues of fishes can be learned. Learned recognition of alarm cues has important implications for predator/prey interactions. Back to refs

Synergistic interactions between chemical alarm cues and the presence of conspecific and heterospecific fish shoals

Wisenden BD, Pollock MS, Tremaine RJ, Webb JM, Wismer ME, and Chivers DP.

Behavioral Ecology and Sociobiology (2003) 54: 485-490

Chemical and visual sources of information are used by aquatic prey during risk assessment. Here, we test the behavioral response of littoral prey fishes to combinations of chemical alarm cues (skin extract) and the visual presence of a fish shoal. We scented minnow traps with either alarm cues or water (control), placed inside the trap a jar that contained either a fish shoal or nothing (control), and recorded the number and species of fish captured. We predicted that chemical alarm cues would reduce the number of fish captured and that a fish shoal would increase the number of fish captured. The predicted effect of chemical and visual cues combined depended on the nature of the interaction. We found that the lowest catch rate was for the combination of alarm cue + no shoal but the highest catch rate occurred for the combination of alarm cue + shoal. Fish shoal + water had the second highest catch rate and no shoal + water had the second lowest catch rate. We conclude that chemical alarm cues induce area avoidance in the absence of a shoal but a strong behavioral proclivity to increase shoal cohesion in the presence of a shoal. The presence of a shoal in the traps induced alarmed fish to shoal with them and thus, enter the traps. This occurred even though traps were the source of the alarm cue. Back to refs.

Is there a fish alarm cue? Affirming evidence from a wild study

Brian D. Wisenden  Keith A. Vollbrecht & Jason L. Brown 

Animal Behaviour (2004) 67: 59-67

Chemical alarm cues released from injured tissue are not released under any other context and therefore reliably inform nearby prey of the presence of a predator. Laboratory and field studies have demonstrated that most aquatic taxa show antipredator responses to chemical alarm cues from injured prey. Magurran, Irving & Henderson (1996) were the first to use underwater video to carefully document the behavioural response of free-ranging wild populations of minnows to minnow alarm cues. They found no evidence of an antipredator response and proposed that alarm responses are context dependent in that they occur only in the context of enclosed environments of laboratory aquaria and field traps. Here, we repeat their experiment and report a significant decrease in the number of minnows in areas where chemical alarm cues were released. The effect of the chemical cues was equal in magnitude to the effect of the presentation of a model predator. The response to the approach of a model predator (visual cue) was intensified by pre-exposure to chemical alarm cues. We corroborated this interaction between chemical and visual indicators of predation risk in a laboratory study using glowlight tetras (Ostariophysi: Characidae). Response to the visual stimulus of a predator was significantly intensified by previous exposure to conspecific chemical alarm cues. We conclude that Ostariophysan skin indeed contains an alarm cue that 1) informs nearby prey of imminent predation risk, 2) induces some form of antipredator behaviour in most contexts, and 3) affects subsequent behavioural responses to stimuli in other sensory modalities. Back to refs.

Antipredator response to injury-released chemical alarm cues by convict cichlid young before and after independence from parental protection

  Shireen D. Alemadi & Brian D. Wisenden

Behaviour (2002) 139: 603-611

 Injury-released chemical alarm cues are released when predators attack aquatic prey. These cues are generally released only in this context and as such, conspecific alarm cues form an important component of risk assessment. Minnows (Ostariophysi, Cyprinidae) possess a well-developed chemical alarm system. However, minnows do not respond to conspecific injury-released alarm cues until 30 to 50 d post-hatch. Non-ostariophysan fishes respond to chemical alarm cues with antipredator behavior but the ontogeny of this behavior is not known for any species. Here, we test convict cichlids (Acanthopterygii: Cichlidae), a species known to respond to alarm cues as adults. Convict cichlid parents care for their eggs and defend their developing young from predators for 4 to 6 weeks. In our experiment, we tested the ontogeny of antipredator response to chemical alarm cues in young convict cichlids well within and just beyond the size range typically defended by parents. We found that small convict cichlid young of a size typically defended by parents engaged in area avoidance and grouping behaviors in response to alarm cues and did so as effectively as young that would typically be independent of parental care. Back to refs

Field verification of predator attraction to minnow alarm substance

Brian D. Wisenden and Travis A. Thiel

Journal of Chemical Ecology (2002) 28: 433-438

Abstract -- Fishes such as minnows in the superorder Ostariophysi possess specialized alarm substance cells (ASC) that contain an alarm pheromone. Alarm substance can only be released by damage to the epidermis thus, the release of alarm substance is a reliable indicator of predation risk. When nearby minnows detect the pheromone they adopt a range of antipredator behaviors that reduce their probability of predation. For many years ASCs puzzled evolutionary ecologists because it was not apparent how these cells are maintained by natural selection. Recent laboratory experiments showed that ASCs provide a selfish benefit to individuals that possess them by signaling to predators, not conspecifics. Many predators have long handling times during which alarm substance is released. Additional predators attracted by alarm substance interfere with the first predator giving the minnow an opportunity to escape. Here, we present data from a simple field experiment verifying that fish predators are attracted to minnow alarm substance. Fishing lures were baited with sponge blocks scented with either 1) water (control for sponge odor and appearance), 2) skin extract from non-Ostariophysan convict cichlids (superorder Acanthopterygii, Archocentrus “Cichlasoma” nigrofasciatus) to control for general injury-released cues from fish, or 3) skin extract from fathead minnows (superorder Ostariophysi, Pimephales promelas). Predator strike frequency on each sponge type was 1:1:7 for water, cichlid and minnow cues respectively. These data provide the first field test using fish predators of the predator-attraction hypothesis for the evolution of Ostariophysan alarm substance cells. Back to refs

Chemically-mediated strategies to counter predation. 

In: Sensory Processing in the Aquatic Environment (Collin SP & Marshall NJ eds). Springer-Verlag, NY. (pp. 236-251)

Brian D. Wisenden

Table 1. Summary of literature survey of chemically mediated predator-prey interactions in aquatic environments, published 1985-2000. Fr = freshwater habitats, Mar = marine habitats. Back to ref list

Back to ref list

Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues

Brian D. Wisenden & Melissa C. Millard

Animal Behaviour (2001) 62: 761-766

A growing number of aquatic organisms have been shown to exhibit antipredator behaviour in response to injury-released chemical cues from conspecifics. Here, we demonstrate a clear antipredator response in the form of avoidance behaviour by a free-living flatworm Dugesia dorotocephala to chemical cues from injured conspecifics. This is the first demonstration of an alarm pheromone in a platyhelminth. In a second experiment, we exposed planaria to combined cues of sunfish odour and water or sunfish odour and planaria alarm cue. Planaria avoided the sunfish + alarm cue but did not avoid the sunfish odour alone, indicating no prior aversion to the odour of sunfish. When these same planaria were subsequently retested two days later with sunfish odour only, planaria that had previously received sunfish odour + alarm cue avoided the cue but planaria that had previously received sunfish odour only did not. These data indicate that planaria learned to recognize sunfish odour as an indicator of danger based on a single simultaneous exposure to conspecific alarm cue and the novel cue. This is the first demonstration of this phenomenon in a platyhelminth and the simplest nervous system known to be capable of learned risk association. Back to ref list 

Brood defense and optimal brood size in convict cichlids Cichlasoma (Archocentrus) nigrofasciatum, a species with biparental care

Brian D. Wisenden 

Journal of Aquariculture & Aquatic Sciences (2001) 9:303-320 

The question of optimal brood size in taxa other than birds has received little attention. In this paper I consier optimal brood size for convict cichlids Cichlasoma (Archocentrus) nigrofasciatum, a fish with biparental care of the eggs and free-swimming young. A model is presented that optimizes the tradeoff between the fitness benefit of fecundity with the behavioral cost of defending young. I then use field data from natural populations in Costa Rican streams to test some predictions from the model. Consistent with the model, field data showed (1) a positive correlation between number of young eaten per day and the number of young in the brood, in some cases independent of the age of the brood; (2) the number of young at the end of the period of parental care (start of life independent of parents) increased at a decelerating rate with initial brood size, converging upon an asymptote set by the maximum number of young that two parents can defend economically; (3) a negative correlation between number of young and growth rate of the young, suggesting that as brood size increases, the young respond to declining efficiency of parental brood defense by crowding under the parent, thereby increasing brood density and reducing foraging rates of the young. The tradeoff between fecundity and the behavioral constraints imposed by brood defense result in stabilizing selection on clutch size in this species. Future work needs to be directed at the three-way tradeoff among egg number, egg size, and the cost of parental care. Back to refs.

Avoidance of conspecific injury-released chemical cues by free-ranging Gammarus lacustris (Crustacea: Amphipoda). 

Brian D. Wisenden, Scott G. Pohlman & Erin E.Watkin

Journal of Chemical Ecology (2001) 27: 1249-1258.

Behavioral responses to chemical cues have been demonstrated for a range of aquatic animals. Injury-released chemical alarm cues from conspecifics are released when a predator is actively foraging. Detection of these cues elicits antipredator behaviors that reduce the probability of predation. Amphipod crustaceans in the genus Gammarus are widespread denizens of ponds and streams. Antipredator responses by Gammarus to conspecific alarm cues, and subsequent reduction of predation risk, are known from experiments in the laboratory. Here, we verify earlier laboratory findings with a field experiment in which we demonstrate an avoidance response to alarm cues in a field population of G. lacustris. We used small traps baited with sponge blocks containing either water (control) or injury-released cues from Gammarus. We repeated the experiment twice. In the both experiments significantly fewer Gammarus were captured in traps with alarm cue sponges than in traps with water sponges. Predatory leeches Dina parva were attracted to Gammarus traps in the first experiment but not the second experiment. In the second experiment, we measured the weight of individual amphipods captured in each trap type to the nearest mg. Two size classes were present; small (1-5 mg) and large (35-108 mg). Both sizes contributed to the avoidance response to alarm cue. Within the large size class, small individuals were significantly less effective at avoiding the alarm cue than large individuals, implying that small adult Gammarus may have different cost/benefit decision criteria for risk assessment than large Gammarus. Back to ref list.

Motion, not Shape, Facilitates Association of Predation Risk With Novel Objects by Fathead Minnows (Pimephales promelas)

Brian D. Wisenden & Katherine R. Harter 

Ethology (2001) 107: 357-364

Injury-released chemical cues are reliable indicators of predation risk among many aquatic taxa. When a novel, neutral stimulus is presented in tandem with chemical cues from an injured conspecific, an association is formed between the novel stimulus and apparent risk. Learned recognition of predation risk is well documented for fathead minnows, Pimephales promelas. When minnows detect alarm cues in nature they are also potentially exposed to multiple environmental stimuli, few of which are likely to be relevant indicators of risk. How do minnows discern among candidate stimuli potentially associated with predation risk? Two possibilities are shape and motion. In this study, individual piscivore-naïve minnows were presented simultaneously with conspecific chemical alarm cues and two stimulus objects. One object was a darkened tube with its long axis in the horizontal plane (fish-like). The second object was a black disk. Following introduction of chemical alarm cues, one of the objects was raised and lowered repeatedly. After a single conditioning trial, minnows associated risk significantly more with the previously moving object than the previously stationary object, as indicated by reduced activity. Object shape had no significant effect on response intensity in test trials. Our data suggest that minnows have been selected to form aversive responses to moving objects at a site of recent predation because movement is a more predictable indicator of predator identity than shape. Back to ref list.

Learned recognition of novel predator odour by zebra danios, Danio rerio, following time-shifted presentation of alarm cue and predator odour. 

Nichole L. Korpi  & Brian D. Wisenden  

Environmental Biology of Fishes (2001) 61: 205-211.

Fishes in the superorder Ostariophysi possess specialized epidermal cells that contain an alarm cue. Fish associate novel odours, such as the odour of a predator, with predation risk after a single, simultaneous exposure to the novel odour and alarm cue. Thereafter, the novel cue is recognized as an indicator of risk and its presence induces antipredator behaviour. Two common antipredator behaviours are reduction in activity and movement to the bottom. This phenomenon has been demonstrated many times in the laboratory setting for a variety of aquatic taxa. In nature however, the detection of novel predator odour may be time-shifted with respect to the detection of alarm cues. Is there a critical period immediately upon the detection of alarm cue in which associative learning can occur? We presented zebra danios (Ostariophysi, Cyprinidae: Danio rerio) with the odour of northern pike (Esox lucius) 5 min after presenting them with either alarm cue or water (control). During a predation event, 5 min is a long time. When later retested with pike odour alone, zebra fish conditioned with alarm cue significantly increased antipredator behaviour in terms of decreased activity (p = 0.001) and movement toward the bottom (p = 0.001). Control fish did not recognize pike odour as dangerous when retested (activity: p = 0.335, bottom: p = 0.447). These data show that learned recognition of predation risk is sufficiently robust to accommodate ecologically realistic temporal shifts in stimulus presentation. Back to ref list

Conditioned alarm behavior in fathead minnows (Pimephales promelas) resulting from association of chemical alarm pheromone with a nonbiological visual stimulus.

Warren K. Yunker, Dan E. Wein & Brian D. Wisenden

Journal of Chemical Ecology (1999) 25, 2677-2686.

Fathead minnows (Pimephales promelas) adopt antipredator (alarm) behavior when they detect alarm pheromone released from an injured conspecific. This is an adaptive response since alarm pheromone is generally released only in the context of a predation event. Alarm reactions may also occur in response to chemical and visual stimuli that minnows learn to associate with release of alarm pheromone. Here, we tested if fathead minnows can learn to associate a nonbiological, visual stimulus with predation risk. Minnows were simultaneously exposed to red light and conspecific alarm pheromone, inducing an alarm reaction.  When retested using red light alone, small shoals of minnows displayed an antipredator response: dashing movements and disorganized swimming followed by decreased height in the water column and increased shoal cohesion. This resulted from a single-trial exposure to the combined cues and demonstrates a robust ecological mechanism by which minnows learn to recognize indicators of risk that may vary in space and time. However, learning to associate risk with biologically irrelevant stimuli may be an ecological liability. How minnows discern between relevant and irrelevant stimuli in nature is now known. back to ref list

Olfactory assessment of predation risk

Brian D. Wisenden

Philosophical Transactions of the Royal Society (2000) 355, 1205-1208

The aquatic environment is well suited for the transmission of chemical information. Aquatic animals have evolved highly sensitive receptors for detecting these cues. Here, I review behavioural evidence for the use of chemical cues by aquatic animals for the assessment of predation risk. Chemical cues are released during detection, attack, capture and ingestion of prey. The nature of the cue released depends on the stage of the predation sequence in which cues are released. Predator odours, disturbance pheromones, injury-released chemical cues and dietary cues all convey chemical information to prey. Prey use these cues to minimize their probability of escalating to the next stage of the sequence. The evolution of specialised epidermal alarm substance cells in fishes in the superorder Ostariophysi represent an amplification of this general phenomenon. These cells carry a significant metabolic cost. The cost is offset by the fitness benefit of the chemical attraction of predators. Attempts of piracy by secondary predators interrupt predation events allowing prey an opportunity for escape. In conclusion, chemical cues are widely used by aquatic prey for risk assessment and has resulted in the evolution of specialized structures among some taxa. back to ref list

Alloparental Care in Fishes

Brian D. Wisenden

Reviews in Fish Biology and Fisheries (1999) 9, 45-70.

Alloparental care, care directed at non-descendant young, presents a potential challenge to evolutionary ecologists because investment in non-descendant eggs and young gives the appearance of maladaptive behaviour. Yet wherever there is parental care in fishes, there is usually alloparental care. As such, alloparental care is an integral part of care in fishes. Alloparental care appears to have arisen independently many times in disparate taxa. The chief reason for this is the low cost of care, relative to homeotherms, both in terms of low post zygotic investment to nourish young, and low risk of predation to the parent during brood defence. In some cases, alloparenting is misdirected parental care and maladaptive. A celebrated example of brood parasitism in fish is that of the catfish Synodontis multipunctatus that parasitizes broods of mouthbrooding cichlids. Previously unpublished data on the reproductive biology of S. mulitpunctatus are reported here. However in the majority of cases, particularly for the widespread phenomena of zygote dumping (nest associates) in the Cyprinidae and adoption of non-descendant free-swimming young in brood-guarding Cichlidae, alloparental care is a mutualistic relationship maintained by natural selection. This review describes broad patterns of known examples of alloparental care, the pathways to adoption, and highlights the ways in which alloparents derive fitness benefits. By caring for non-descendant young, an alloparent may benefit by one or more of the following phenomena: acquisition of mates, confusion effect, dilution effect, selfish herd effect, selfish shepherd effect, kin selection, and reciprocal altruism. Although the breadth and diversity of examples of alloparental care in fishes is growing, to date these accounts have been largely descriptive. Future research should be directed at careful documentation of the fitness consequences for both donor and alloparent. These are the data that are needed to fully understand the evolutionary underpinnings of alloparental care, and by extension, parental care. back to ref list

Scents of danger: the evolution of olfactory ornamentation in chemically-mediated predator-prey interactions

Brian D. Wisenden

(2000) Chapter in: Animal Signals: Signalling and Signal Design in Animal Communication (Espmark Y, Amundsen T, & Rosenqvist G, eds). Tapir Academic Press, Trondheim, Norway. pp. 365-386. 

Aquatic environments favour the elaboration of chemical signals and the evolution of receptors to detect them. Encounters between predators and prey escalate from initial detection to attack, capture, and finally ingestion. Chemical cues released at each stage in the predation sequence serve as public information about predation risk and allow prey to assess risk, reduce the probability of predator attack and to learn the chemical identity of unfamiliar predators. Discussed here are disturbance pheromones, predator odours and chemical cues released upon injury from predator attacks on fellow conspecifics or heterospecific prey with which habitat and predators are shared. Following prey ingestion, injury-released chemical cues are released from the predator’s digestive tract. Diet-related cues make injury-released chemical cues available at the detection stage of the predation sequence. Each of these chemical cues represents a reliable form of public information. Prey that detect these cues can initiate steps to avoid detection or attack and reduce their probability of predation. Publicly available chemical cues are not signals because they do not necessarily benefit the sender. Fishes of the superorder Ostariophysi (minnows, catfish, characins, etc) possess specialised epidermal cells containing an alarm pheromone. This pheromone amplifies injury-released chemical cues and attracts (signals) secondary predators that interfere with the primary predator, allowing the prey (signaller) to escape. Alarm substance cells (ASC) are metabolically expensive and allocation of resources to these cells is facultative. As such, ASCs of the Ostariophysan fishes may be considered as olfactory ornaments that have been selected as signals to predators (receivers) for the benefit of individual prey (senders). back to ref list

Survival Benefit to Antipredator Behavior in the Amphipod Gammarus minus (Crustacea: Amphipoda) in response to Injury-Released Chemical Cues from Conspecifics and Heterospecifics

Brian D. Wisenden, Alecia S. Cline & Timothy C. Sparkes

Ethology (1999) 105, 407-414. 

A wide range of aquatic taxa use environmental chemical cues for the assessment of predation risk. We examined whether Gammarus minus (Crustacea: Amphipoda) exhibit antipredator behavior in response to injury-released chemicals from conspecifics or heterospecifics (Crustacea: Isopoda). We then examined whether behavioral responses to these cues conferred survival benefits to the amphipods. In the first part of this study, we tested the behavioral response of G. minus to the following treatments: 1) water containing injury-released cues of conspecifics; 2) water containing injury-released cues of a sympatric isopod crustacean, Lirceus fontinalis; or 3) water containing no cues (control). Relative to the control, Gammarus responded to the conspecific cue by moving to the substratum and decreasing activity. In contrast, Gammarus responded to the heterospecific cue by moving up into the water column and increasing activity. In the second part of this study, we tested if the behavioral response to these cues confers a survival benefit to Gammarus when exposed to a predator. A green sunfish (Lepomis cyanellus) was retained behind a partition in the test tanks. Two minutes after the introduction of the chemical cues in the first test, the barrier was lifted and predation events recorded. Relative to the control, time to first attack increased for Gammarus exposed to conspecific cues and decreased for those exposed to heterospecific cues. These data indicate that Gammarus distinguish between chemical cues from conspecific and heterospecific crustaceans, and that the antipredator response to conspecific cues confers a fitness benefit (i.e., increased survival due to increased time to first attack). back to ref list

A re-evaluation of the effect of shoalmate familiarity on the proliferation of alarm substance cells in ostariophysan fishes

B. D. Wisenden and R. J. F. Smith

Journal of Fish Biology (1999) 53, 841-846.

A re-examination of data from Wisenden & Smith (1997) that suggests that fathead minnows Pimephales promelas adjust investment into epidermal alarm substance cells (ASCs) facultatively based upon the level of perceived risk. When placed into a container with non-familiar shoalmates (relatively high risk) ASC production increased. This allows these individuals to attract a secondary predator better. When placed into a container with familiar shoalmates (relatively low risk) ASC production decreased. This may reflect increased effectiveness of a group antipredator response by familiar individuals, and/or the cost to inclusive fitness of attracting additional predators to the vicinity of their kin. back to ref list

CTENOSAURA SIMILIS (Ctenosaur, Garrobo, Iguana Negra). BEHAVIOR. Brian D. Wisenden. Herpetological Review (1998) 29, 168. Recently I observed a predation event involving a frog distress call that attracted a large ctenosaur, presumably by the opportunity to pirate a meal, allowing the frog to escape from its original predator (a colubrid snake). Although anecdotal, this observation is one of only a few examples in the herpetological literature of predator attraction to distress calls, and the second example of a selfish benefit to distress calling in an amphibian. back to ref list

Courtship and mate choice in fishes: integrating behavioral ecology and sensory ecology

Robert Craig Sargent, Victor N. Rush, Brian D. Wisenden & Hong Y. Yan

American Zoologist (1998) 38, 82-96. 

Sexual selection theory predicts a coevolution between male sexual ornamentation and female preference. The implication of this prediction for sensory ecology is that there should be a tight coupling between the physiology of male signal production and the physiology of female reception. Indicator models of sexual selection predict that male ornamentation is correlated with male condition, and that female preference is correlated with male ornamentation. Indicator models of sexual selection have a conceptual overlap with resource acquisition and investment models of behavioral ecology. Empirical studies with fishes, particulary with guppies (Poecilia reticulata) and threespine sticklebacks (Gasterosteus aculeatus), suggest a strong connection between aqcuired resources, male condition, male ornamentation, male courtship and female preference. back to reflist

Predation risk influences reproductive behaviour in Iowa darters, Etheostoma exile (Osteichthyes, Percidae)

Douglas P. Chivers, Brian D. Wisenden & R. Jan F. Smith

Ethology (1995) 99, 278-285

In this study, we tested the effects of predation risk on reproductive behaviour of Iowa darters (Etheostoma exile). We recorded the frequency of courtship behaviour (head shaking) and spawning acts for 30 min before and after removing an opaque barrier to expose groups of darters to (1) an empty tank (the before-pike treatment), then (2) a tank containing a pike (the pike treatment), and finally (3) an empty tank (the after-pike treatment). In response to the pike, darters peformed significantly less reproductive behaviour than before exposure to the pike. Furthermore, darters performed proportionately less reproductive behaviour in the area in the immediate vicinity of the pike where risk of predation was highest. However, darters continued to occupy the risky area while exposed to pike. Removal of the barrier in the absense of the pike (the before- and after-pike treatments) had no effect on the overall level of repoductive behaviour, the proportion of reproductive behaviour performed in the immediate vicinity of the pike tank (the risky area), or use of the risky area. back to reflist

Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues

Brian D. Wisenden, Douglas P. Chivers & R. Jan F. Smith

Journal of Chemical Ecology (1997) 23, 135-151.

We studied two populations of damselfly larvae (Enallagma boreale): one population co-occurred with a predatory fish (northern pike, Esox lucius), the other did not. Damselflies that co-occurred with pike adopted antipredator behavior (reduced activity) in response to chemical stimuli from injured conspecifics, and to chemical stimuli from pike, relative to a distilled water control. Damselflies from an area where pike do not occur responded only to chemical stimuli from injured conspecifics. In a second set of experiments, we conditioned pike-naive damselflies to recognize and respond to chemical stimuli from pike with antipredator behavior. Damselfly larvae that were previously unresponsive to pike stimuli, learned to recognize pike stimuli after a single exposure to stimuli from pike and injured damselflies or pike and injured fathead minnows (Pimephales promelas). The response to injured fathead minnows was not a general response to injured fish because damselfly larvae did not respond to chemical stimuli from injured swordtails (Xiphophorus helleri), an allopatric fish. Taken together, these data suggest a flexible learning program that allows damselfly larvae to rapidly acquire the ability to recognize local predation risk based on chemical stimuli from predators, conspecifics and heterospecific members of their prey guild. back to ref list

Reactions of Gammarus lacustris (Crustacea: Amphipoda: Gammaridae) to chemical stimuli from natural predators and injured conspecifics

Karen Wudkevich, Brian D. Wisenden & R. Jan F. Smith

Journal of Chemical Ecology (1997) 23, 1163-1173

When exposed to chemical stimuli from pike (Esox lucius), and larval dragonflies (Aeshna eremita), Gammarus lacustris significantly reduced its activity compared to activity recorded in response to distilled water control. In response to chemical stimuli from pike, G. lacustris also tended to reduce its time active in the water column, spending more time near the bottom of the aquarium. However, no such trend was seen in response to chemical stimuli from dragonfly larvae. The differences in response to chemical stimuli from pike and larval dragonflies, suggests that G. lacustris may possess the ability to detect and react differently to different classes of natural predators. A decrease in activity by G. lacustris was also observed in response to exposure to crushed conspecifics. The similarity in responses to chemicals associated with predators and predatory danger and to injured conspecifics suggests the presence of an alarm pheromone within the body tissues or fluids of G. lacustris. back to ref list

The effect of physical condition and shoal-mate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows

Brian D. Wisenden & R. Jan F. Smith

Journal of Fish Biology (1997) 50, 799-808.

Ostariophysan fishes have specialised epidermal alarm substance cells (ASC's). In this study a metabolic cost to the production and maintenance of these cells is demonstrated. Fathead minnows Pimephales promelas were maintained on high or low food rations and, to test for the effect of social context on the number of ASC's, they were held with either no shoal-mates or two shoal-mates. Shoal-mates were familiar (from the focal fish's shoal), or unfamiliar (from a shoal separated by 1 km from the focal fish's shoal). After 16 days, epidermal thickness, number of mucus cells and number of ASC's were all significantly greater for minnows on the high ration than for those on the low ration. Within the high ration group, physical condition was positively correlated with epidermal thickness and ASC number. The shoal-mate treatment had no measurable effect on the epidermis. It was concluded that food availability determines investment into ASC's, inferring a tradeoff between the cost of ASC's and the fitness benefits they accrue. back to ref list

The role of experience in the response of fathead minnows (Pimephales promelas) to skin extract of Iowa darters (Etheostoma exile)

Douglas P. Chivers, Brian D. Wisenden & R. Jan F. Smith

Behaviour (1995) 132, 665-674.

Detection of an alarm pheromone may allow conspecifics to lower their risk of predation if they avoid areas where alarm pheromones are detected. Similarly, individuals that learn to recognoze and avoid alarm signals produced by heterospecifics of their prey guild (i.e. those with which they share common predators) will likely receive similar benefits. In two separate field studies we tested whether fathead minnows (Pimephales promelas) avoid areas labelled with Iowa darter (Ethoeostoma exile) skin extract (which contains an alarm pheromone). One population of minnows tested was sympatric with darters while the other was allopatric from darters. Swordtails (Xiphophorus helleri) are allopatric from fathead minnows in both populations tested. Swordtail skin lacks ostariophysan and darter alarm pheromones, and was used to control for a general response to damaged skin of an unfamiliar fish. In the darter-sympatric population we captured significantly fewer and smaller minnows in traps marked with darter skin extract (experimental traps) than traps marked with a control of swordtail skin extract. Given the correlation between age and size, and therefore experience, these data suggest that less experienced fish do not avoid darter skin extract to the same extent as do older more experienced fish. in the darter-allopatric population there was no difference in the number of minnows or the size of minnows captured in control versus experimental traps. Taken together, these results demonstrate that fathead minnows recognize and avoid areas where darter alarm pheromone is detected and that this is a learned response. Use of heterospecific alarm pheromones to assess predation risk may be a widespread phenomenon within communities of small fishes. back to reflist

Factors affecting mate desertion by males in free-ranging convict cichlids (Cichlasoma nigrofasciatum).

Brian D. Wisenden

Behavioral Ecology (1994) 5, 439-447.

Convict cichlid fish have biparental care for about a 6 week period lasting from egg laying until the young (fry) have grown to about 10mm. However, the young can sometimes survive with care from only one parent, and desertion of the mate and offspring by males has been observed. I tested a theoretical model modified from Lazarus (1990) which predicted that mate and offspring desertion by male convict cichlids should be promoted by low predation pressure on fry, high remating opportunities for males, increasing age of fry and decreasing number of fry. Males deserted 7.8% of 334 broods studied during two breeding seasons in Costa Rican streams. As predicted, males deserted their broods most frequently at sites with the highest brood survivorship (lowest brood predation pressure), when fry were close to independence and when brood size was smaller than average. Sex ratios and interspawning intervals did not indicate any relationship between mate desertion and opportunities for remating for males. The reuse of spawning caves may favor fidelity to the mate and brood, and defending the young from predators at the same time as defending the cave from conspecifics may favor biparental care in this species. back to ref list

Antipredator behavior and suppressed aggression by convict cichlids in response to injury-released chemical cues of conspecifics and heterospecifics

Brian D. Wisenden and R. Craig Sargent

 Ethology (1998)103, 283-291. 

Chemical information is an important source of information in aquatic environments. A number of aquatic taxa use chemical cues to detect predation risk. Here we investigate if convict cichlids Cichlasoma nigrofasciatum, use injury-released chemical cues to detect predation risk. We exposed pairs of juvenile convict cichlids to one of three test stimului: 1) distilled water, 2) chemical cues from injured convict cichlids, or 3) chemical cues form injured mosquito fish Gambusia, an allopatric and phylogenetically unrelated fish. Gambusia skin was used to test for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of test aquaria and time under a shelter object. In response to Gambusia convict cichlids tended to increase spend time near the tank bottom but did not increase use of the shelter object. There was a tradeoff between antipredator behavior and the level of agonistic behaviors between each pair of juvenile cichlids. In rsponse to convict cichlid cues, there was a significant reduction in approaches and bites. Gambusia skin extract had no significant effect on agressive behavior. Theses data suggest a species-specific antipredator response to conspecific alarm pheromones in a cichlid fish and demonstrate a variable tradeoff between predator avoidance and intraspecific aggression. back to ref list

Damselfly larvae learn to recognize predators from chemical cues in the predator's diet

Douglas P. Chivers, Brian D. Wisenden & R. Jan F. Smith

Animal Behaviour (1996) 52, 315-320. 

Chemosensory recognition of predators by naive prey may be facilitated if the predator's diet chemically 'labels' the predator. In a laboratory experiment, behavioiur patterns were quantified in individual damselfly larvae, Enallagma spp., that had never been exposed to pike, Esox lucius, before and after exposing the damselflies to one of three chemical stimuli: water from a tank that held pike fed a diet of (1) damselflies, (2) fathead minnows, Pimephales promelas, or (3) mealworms, Tenebrio molitor. Damselflies decreased their frequency of feeding bites, head bends and moves in response to stimuli from pike fed damselflies and pike fed fathead minnows, but not to stimuli from pike fed mealworms. Damselflies are sympatric with fathead minnows in the population tested, and probably have many of the same predators. A response to stimuli from pike fed fathead minnows indicates that damselflies associate predation risk with stimuli from injured minnows. In a second experiment, responses of damselflies previously exposed to stimuli from pike fed one of the three treatment diets (damselfly, fathead minnow or mealworm) were tested for a response to stimuli from pike fed mealworms. Damselflies that had been exposed to stimuli from pike fed damselflies or fathead minnows in the first experiment responded to stimuli from pike fed mealworms in the second experiment, but damselflies exposed to pike fed mealworms in the first experiment did not. Thus (1) pike-naive damselflies may initially respond to chemical stimuli from pike based on stimuli of conspecifics or familiar heterospecifics in the pike's diet, and (2) damselflies can learn to recognize chemical stimuli of pike irrespective of the pike's recent feeding regime based on the initial association with damselflies or minnows in the pike's diet. back to ref list

Early warning in the predation sequence: a disturbance pheromone in Iowa darters (Etheostoma exile)

Brian D. Wisenden, Douglas P. Chivers & R. Jan F. Smith

Journal of Chemical Ecology (1995) 21, 1469-1480.

The probability of prey avoiding a predator's attack should increase if the predator's presence is detected at an early stage in the predation sequence. In this study, we tested whether threatened Iowa darters (Etheostoma exile) release disturbance pheromones that warn conspecifics of the presence of predation threat. Pairs of aquaria were visually isolated from one another, but connected chemically by water circulating between them. Darters in one aquarium were observed before and after darters in the other aquarium were chased with a model predator. In control tests, the model was moved in the same manner but there were no darters in the upstream tank. Darters receiving water from threatened fish increased vigilance behavior and decreased movement. Vigilant fish raised their head above the substratum, propping themselves up on their pectoral fins and/or arching their neck dorsally, pointing the snout upward. Exposure to water from disturbed darters suppressed exploratory behavior and resulted in movement by short rapid hops that ended abruptly in a rigid, alert posture. This study suggests that Iowa darters release a disturbance pheromone that can provide conspecifics with an early warning of predation risk. back to ref list

Brood size and the economy of brood defence: examining Lack's hypothesis in a biparental cichlid fish

Brian D. Wisenden & Miles H. A. Keenleyside

Environmental Biology of Fishes (1995) 43, 145-151.

We tested the explanatory value of two hypotheses reviewed by Lack (1954) in the maintenance of brood size in free-ranging convict cichlids (Cichlasoma nigrofasciatum): (1) physiological constraints on egg production, and (2) behavioural constraints imposed by brood defence. Number of free-swimming young in 13 experimental (E) broods was augmented to the upper limit of the size distribution of natural broods (150 young); 18 control (C) broods were handled in the same way but brood size was not changed (mean + SE = 69.5 + 11.0). E and C brood sizes were measured at 5 day intervals. At day 20 (just before independence from parental care), 50.3 + 9.4 (n = 9) young remained in E broods and 30.8 + 7.8 (n = 8) young remained in C broods (P > 0.05). Offspring number did not differ significantly (P > 0.05) between C and E broods after day 10. Mean growth rate of offspring was significantly lower in E broods than in C broods, perhaps in response to increased density of young in the former. Both the convergence of offspring number in E and C broods and suppression of growth in E broods support a behavioural constraint; that two parents are unable to successfully defend large broods from predators during the first 10 days that their young are free-swimming. A trade-off exists in parental investment between current and future reproduction. Extra parental investment in current reproduction (eggs) does not result in an increased number of young at independence, therefore a behavioural constraint during brood defence should stabilize the evolution of clutch size. back to ref list

The Dilution Effect and Differential Predation Following Brood Adoption in Free-ranging Convict Cichlids (Cichlasoma nigrofasciatum)

Brian D. Wisenden & Miles H. A. Keenleyside

Ethology (1994) 96, 203-212.

Parental investment in unrelated offspring is potentially maladaptive but may be promoted by natural selection if the presence of foreign young enhances the survival of the parents' own young. We experimentally augmented broods of free-ranging convict cichlids (Cichlasoma nigrofasciatum) to test (1) if survival of the adopting parents' young (fry) increases, in relation to that of control broods, after the addition of smaller foreign fry, and (2) if such an increase can be attributed to the effect of brood dilution acting alone or in combination with the effect of differential predation on adopted young. Total fry survival did not differ between experimental (E) broods and control (C) broods, but E broods had significantly more large (host) fry after 5 d and 10 d than C broods did. In E broods, small (foreign) fry suffered higher rates of predation than large fry, indicating differential predation. In E broods starting at 7.0 and 7.5 mm SL, observed fry mortalities did not differ significantly from mortalities expected from the effect of brood dilution. However, E broods starting at 8.0 mm SL had significantly lower mortalities than expected, indicating that parents that adopt smaller foreign fry can increase the survival of their own fry by the combined effects of brood dilution and differential predation. Within E broods, growth of smaller foreign fry was significantly slower than that of larger host fry, suggesting that intra-brood agonistic behaviour affects access to food for smaller fry. Therefore, increased predation and reduced growth are two costs acting on fry of donor parents. back to ref list

Fin digging and leaf lifting by the cichlid fish Cichlasoma nigrofasciatum: examples of parental food provisioning

Brian D. Wisenden, Tanya L. Lanfranconi-Izawa & Miles H. A. Keenleyside

Animal Behaviour (1995) 49, 623-639

In fishes, the predominant form of parental care is brood defence. The convict cichlid, a biparental fish native to Central America, engages in two types of brood provisioning: fin digging and leaf lifting. These behaviour patterns were studied in the field, outdoor experimental ponds and in laboratory aquaria. In outdoor experimental ponds, females fin dug 51 times more often when guarding fry than when unmated; males fin dug three times more frequently when guarding fry than when unmated. Fin digging frequency was influenced by sex of the parent, brood age and substrate quality in the field. After the young became free-swimming, females performed four times (field) and two times (pond and laboratory) more fin digging and twice as many leaf lifts (field) as males. Females in the field increased leaf lifting with brood age but males did not. Fin digging frequency by parental females and males increased with brood age. Frequency of adult feeding bites at the substrate did not change with brood age except in the field, where female feeding bites increased with brood age. In the field, females performed more feeding bites than males but in the laboratory males fed more often than females. Thus changes in fin digging frequency with brood age do not seem to be strongly linked to the feeding requirements of the parents. Taken together, these data provide a description of changes in this parental behaviour with sex of parent, stage of brood development, food ration and substrate type and support the hypothesis that these patterns of behaviour help increase food availability to their young. back to ref list

Risk-sensitive habitat use by brook stickleback (Culaea inconstans) in areas associated with minnow alarm pheromone

Brian D. Wisenden, Douglas P. Chivers & R. Jan F. Smith

Journal of Chemical Ecology (1994) 20, 2975-2983. 

Brook stickleback (Culaea inconstans) share habitat and predators with cyprinid species and they exploit the alarm pheromone of fathead minnows (Pimephales promelas) to avoid areas of high predation risk. In this field experiment, we measured the retention and duration of area avoidance by brook stickleback from areas marked with alarm pheromone of fathead minnows. Area avoidance was greatest during the first two hours after the source of the alarm pheromone was removed (p < 0.05) but after four hours area use was not significantly different from pre-marking levels. This study shows that brook stickleback: (1) use the alarm pheromone of fathead minnows to avoid high risk areas, (2) continue to avoid locations associated with predation risk after the source of the pheromone has gone, and (3) avoid risky areas temporarily, and resume use of risky areas after two to four hours. This behavioral response by stickleback to minnow alarm pheromone could serve to minimize risk of predation. back to ref list

Reproductive behaviour of free-ranging convict cichlids, Cichlasoma nigrofasciatum

Brian D. Wisenden

Environmental Biology of Fishes (1995) 43, 121-134.

Cichlids are unusual among fishes because they have prolonged care of their young. Convict cichlids (Cichlasoma nigrofasciatum) are monogamous and have biparental care of their young. This species has been studied extensively in the laboratory, however, little is known of their reproductive habits in nature. Four populations of convict cichlids were studied in Costa Rican streams during the long dry season in 1990 and 1991. Basic physical and chemical parameters of the study sites are described. In the study area breeding fish paired size assortatively; large males with large females and small males with small females. A comparison of the size distribution of breeding fish to that of non-breeding fish showed that small males and in some cases, small females were excluded from breeding. This suggests competition among males for nest sites and mates or female-female competition. Further evidence of intrasexual competition in females is provided by the black colour phase adopted by some females. Some of these females were active in courtship and had mature ova. Cave guarding behaviour and reuse of caves show that a ready-made spawning site is an important resource shaping the mating system of this species. This description of basic natural history can serve as a source of testable hypotheses for future research and allow the results from laboratory studies on this and related species to be interpreted within the ecological context of the natural habitat. back to ref list

Factors affecting reproductive success in free-ranging convict cichlids (Cichlasoma nigrofasciatum)

Brian D. Wisenden

 Canadian Journal of Zoology (1994) 72, 2177-2185.

This study examines the effect of parent size, fry growth rate, and habitat-related brood predation pressure on two measures of reproductive success (percent brood survival and fry number at independence from their parents) of free-ranging convict cichlids (Cichlasoma nigrofasciatum). Four populations in Costa Rican streams were studied, two in 'pool' habitat and two in 'stream' habitat. The number of fry that emerged from the spawning site (as free swimming young) was positively correlated with female standard length (SL) for sites with a relatively wide size range of breeding females. Male SL had no effect on fry number at emergence nor did size of either parent affect the probability of a brood reaching fry independence. Large parents reared more fry to independence than small parents in stream habitat but not in pool habitat. There was a significant difference among sites in fry number at emergence but not at independence (mean = 27 fry), suggesting a maximum number of fry two parents can economically defend. Fry growth rate had no effect on either measure of reproductive success. Reproductive success was largely determined by the effect of habitat. Adult Cichlasoma dovii in pool habitat may have reduced mean brood survival from 47% (n = 126 broods) in stream habitat to 14.9% (n = 141 broods) in pool habitat. Predators such as juvenile C. dovii, may be more effective in the dim ambient light in pool habitat, overwhelming the effect of parent size on brood defence. back to ref list

The role of experience in risk assessment: avoidance of areas chemically labelled with fathead minnow alarm pheromone by conspecifics and heterospecifics

Brian D. Wisenden, Douglas P. Chivers, Grant E. Brown & R. Jan F. Smith

 Écoscience (1995) 2, 116-122.

In two field experiments, we investigated risk avoidance behaviour by individual fathead minnows (Pimephales promelas Rafinesque) and brook stickleback (Culaea inconstans Kirtland) in response to release of fathead minnow alarm pheromone. There was an initial decrease in the number of fish caught in areas labelled with alarm pheromone (risky areas) relative to areas labelled with distilled water (safe areas), after the source of the pheromone was removed. Numbers of minnows or stickleback caught in risky and safe areas were no longer different 4 hours after the pheromone source was removed. For minnows, there was no significant difference in the immigration rates of individuals into risky and safe areas from neighbouring locations. For minnows, and probably stickleback, new individuals, naive to the association of an area with alarm pheromone, immigrated into risky areas before the return of experienced fish. Fish present at the time of pheromone release did not return for 7 or 8 hours after the source of the pheromone was gone. This raises the possibility that the chief beneficiaries of chemical alarm signals may be only those individuals present at the time of pheromone release. back to ref list

Aggressive behaviour among convict cichlid (Cichlasoma nigrofasciatum) fry of different sizes and its importance to brood adoption

Shannon A. Fraser, Brian D. Wisenden & Miles H. A. Keenleyside

Canadian Journal of Zoology (1993) 71, 2358-2363.

Convict cichlids (Cichlasoma nigrofasciatum) exhibit extended biparental care of their young. Parents will adopt unrelated (foreign) conspecific young of similar size or smaller than their own but reject larger foreign young. Adoption of smaller foreign young may benefit the parents by reducing loss of their own young to predators by the dilution effect, which maybe enhanced by differential predation on the smaller young. Another factor influencing adoption is that larger foreign young may pose a direct predatory threat to the host parent's young. Measures of aggression among free-swimming young of different sizes showed that there was at least 1 mm (standard length) size difference before larger young attacked smaller, a 3 mm difference before injury occurred, and a 4 - 5 mm difference before predation occurred. Parents were initially more discriminating than their young with respect to the size of foreign young accepted. As their young grew and became stronger swimmers, parents less actively rejected larger foreign young; however, they continued to reject them before they were large enough to pose a direct predatory threat. Parental rejection of relatively large foreign young is therefore based more on protecting their own young from differential predation than from aggression by larger adoptees. back to reflist

Female convict cichlids adjust gonadal investment in current reproduction in response to relative predation risk of brood predation

Brian D. Wisenden

Canadian Journal of Zoology (1993) 71, 252-256. 

Parental investment theory predicts that investment in current reproduction should be increased when the prospects of success in current reproductive effort are relatively high, and reduced when they are poor relative to expected success from future reproductive effort. A number of studies have shown that levels of postspawning parental investment (brood defence, parents' willingness to risk predation) increase when the brood is augmented. However, few studies have shown a change in prespawning (gonadal) investment in response to indirect indicators of reproductive success, such as nest site quality. Convict cichlids (Cichlasoma nigrofasciatum) are small feshwater fish that have b