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Brian D. Wisenden

updated Apr 2008 by Brian Wisenden

Wisenden BD, Snekser JL, Stumbo TD, Leese JM. Submitted. Post-predation parental hope: defense of an empty nest after catastrophic brood loss.

Leiser J, Gagliardi J, Itzkowitz M, Wisenden BD. Submitted. Promiscuous mating does not preclude mate choice by female Leon Springs Pupfish, Cyprinodon bovinus.

James CT, Noyes KJ, Stumbo AD, Wisenden BD, Goater CP. Submitted. Cost of exposure to trematode cercariae and learned recognition and avoidance of parasite risk by fathead minnows.

Wisenden BD, Dye TP. Submitted. Young convict cichlids use visual information to update olfactory homing cues. Abstract

Wisenden BD. 2008. Active space of chemical alarm cue in natural fish populations. Behaviour 145: 391-407. 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. doi:10.1098/rspb.2007.0709 Abstract pdf

Wisenden BD, Goater CP, James CT. In Press. Behavioral defenses against parasites and pathogens. In: Fish Defenses (Giacomo Z, ed). 28 manuscript pages. Abstract

Wisenden BD, Karst J, Miller J, Miller S, Fuselier L. 2007. Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, Umbra limi (Kirtland 1840). Environmental Biology of Fishes  Abstract pdf

Wisenden BD, Pogatshnik J, Gibson D, Bonacci L, Schumacher A &  Willett A. 2007. 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

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

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

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

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

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

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