Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Chapter 7 The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical Communication in Fishes Brian D. Wisenden Minnesota State University Moorhead, Moorhead, Minnesota, USA 7.1 Introduction Chemical information is ubiquitous and can be a powerful releaser of behavioral responses (Sorensen and Stacey, 1999; Wisenden and Chivers, 2006; Wyatt, 2010). Chemical information in the environment comes from abiotic and biotic sources. Abiotic cues allow fish to navigate to favorable habitat along gradients in pH, dissolved oxygen, or salinity. Chemical cues of biotic origin are called semiochemicals, after the Greek word semion for sign. Semiochemicals provide important information to receivers about every aspect of physiological and ecological function, including spatial and temporal variation in food availability, the diet choice of others, the identity of individual group members on the basis of shared phylogeny, familiarity or kinship, the presence and activity of predators, risk of parasitism, the dominance status of sexual rivals, and the location and reproductive readiness of potential mates and cues that play a role in parent–offspring interactions (Bradbury and Vehrencamp, 2011). The enormous fitness benefits of this information create selection pressure on the sensory biology of fish to favor elaboration of receptors to detect this information and cognitive processes to generate adaptive behavioral responses to this information. Wherever there is production of information by some individuals and exploitation of that information by other individuals, there is also potential for co-evolutionary processes to shape both the sensory biology of receivers to better detect these chemicals and for senders to specialize in production and release of semiochemicals (Stacey and Sorensen, 1991, Wisenden and Stacey, 2005, Wisenden and Chivers, 2006; Stacey, 2015). Odors, chemical cues and signals, signature mixtures, pheromones and “substances” are terms used to describe the enormous diversity of semiochemicals that fish use to inform their behavioral decision-making. The absence of universally accepted standard nomenclature has created confusion because these terms do not necessarily reflect the evolutionary underpinning involved in the Fish Pheromones and Related Cues, First Edition. Edited by Peter W. Sorensen and Brian D. Wisenden. © 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc. 149 0002208146.indd 149 11/22/2014 5:38:57 PM 150 Fish Pheromones and Related Cues production, detection, and processing of this information. To fully understand their ecological function, one needs an understanding of the evolutionary selection behind the origin and maintenance of semiochemical detection and production. Historically, there have been two approaches to the study of fish semiochemicals: (1) by physiologists who study various aspects of the physiology and behavior of sex pheromones (e.g., Stacey and Sorensen, 2009) and (2) by behavioral ecologists who study how chemical cues mediate predator-prey interactions (e.g. Kelley, 2008; Ferrari, Wisenden, and Chivers, 2010). These parallel communities of researchers have developed largely independent literatures, each with its own lexicon for semiochemicals. The best way for the study of semiochemicals in fishes to move forward is for there to be integration of these literatures and with that an acceptance of a common vocabulary. Therefore, this chapter aims at organizing known semiochemicals along a hypothesized evolutionary trajectory from ancestral to derived. This framework will hopefully highlight opportunities for future research to fill in gaps in collective knowledge and to test predictions of this hypothesis. 7.2 A HYPOTHESIS FOR THE EVOLUTION OF SEMIOCHEMICALS Orientation → Contextualization → Specialization of production → Specialization of release A plausible sequence for the evolution of use and production of several broadly defined classes of semiochemicals (Table 7.1) is proposed here. The first and simplest form of behavioral response to external chemical information is orientation. The simplest form of orientation occurs in response to chemicals of abiotic origin, such dissolved oxygen, geological mineral cues and salinity, and so on, which provide important information about the environment. Chemo-orientation is used in the settlement of larvae of marine fishes, orientation cues for long-distance migratory behavior, and for microhabitat use. These are not semiochemicals per se because semiochemicals are only those chemicals that are released by living organisms. Behavioral responsiveness to semiochemicals is a significant transition because it creates an opportunity for selection to act on the chemical nature of the cue itself. The simplest forms of semiochemicals provide information about the presence of conspecifics (competitors, prospective mates) and heterospecifics (prey, predators, competitors). The second stage of evolution of semiochemicals is contextualization. Semiochemicals become contextualized when they are reliably released during specific ecological or physiological interactions. Context allows selection to shape behavioral responses in sophisticated ways. Contextualized semiochemicals are still cues (i.e., not yet signals) because responses to semiochemicals are driven entirely by selection on receivers. Receiver response to a chemical cue does not contribute to fitness of the sender (Fig. 7.1). The first step toward elevating semiochemicals from cues to signals and, thus, true chemical communication, is the elaboration of tissues specialized for production of messenger chemicals, even if at first these chemicals are released for benefits other than manipulating receivers (Wisenden and Stacey, 2005). The ultimate category of semiochemicals is when there is the elaboration of tissues and behavioral mechanisms to produce and control release of specialized semiochemicals. Examples from fishes can be described for each of these stages in the evolutionary trajectory from chemical cues released passively as public information to chemical signals that are part of a co-evolved communication system (Sorensen and Stacey, 1999; Wisenden and Stacey, 2005). 7.3 ORIENTATION TO ENVIRONMENTAL SEMIOCHEMICALS The simplest, and presumably most ancestral, form of chemical cues that reveal information about habitat suitability are chemicals that are released from the decay of organic matter and the geochemical makeup of the watershed, spatial and temporal variation in dissolved oxygen, and exposure to salinity (e.g., Leggett, 1977; Kramer, 1987; Odling-Smee and Braithwaite, 2003; Maes, Stevens, and Breine, 2007). An example of this phenomenon is diadromous fish that spend part of their life in 0002208146.indd 150 11/22/2014 5:38:57 PM 151 The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical Table 7.1. Summary of a hypothesis for the evolution of semiochemicals used by fishes on the basis of the presence (1) or absence (0) of various selection pressures on sender (S) and/or receiver (R). The Cue/signal transition to communication occurs when senders show evidence of specialization for cue release. Specialized issues Semiochemical Environmental cues Environmental parameters (pH, salinity, etc.) Migratory cues (geochemistry) Semiochemical cues Food odors (amino acids) Odor of prey, predator, and conspecifics Injury-released alarm cues Recognition of familiarity and kinship (signature mixtures) Sex steroids Semiochemical signals (pheromones) Bile acids Conspecific cues about social hierarchy Sex pheromones Selection on Sender/ receiver Biotic Contextual Production Release 0 0 0 0 R 0 0 0 0 R 1 1 0 0 0 0 0 0 R R 1 1 1 1 0 0 0 0 R R 1 1 1 0 R 1 1 1 1 1 1 0/1 0/1 1 1 1 1 R/S + R R/S + R S + R freshwater and part of their life in salt water. Anadromous salmonids mature in salt water and orient to chemical cues of their natal streams during the migration back to freshwater to spawn (Scholz et al., 1976), which include organics and odors from plant, animals, and amino acids from biofilms (see Sorensen and Baker, 2015). Some catadromous fishes such as bull sharks spawn in salt water and orient to low salinity gradients to find freshwater to grow to adulthood (Heupel and Simpfendorfer, 2008). Eels returning to freshwater orient to organic compounds released by biofilm organisms (Sorensen, 1986, see Sorensen and Baker, 2015). The evolution of this kind of orientation results from selection on receivers to elaborate receptors and neural wiring to detect and respond adaptively to environmental chemicals of value to the fitness of the receiver (Table 7.1; Fig. 7.1). 7.4 Passively Released Biotic Semiochemicals without Ecological Context The sum of biochemical processes occurring within aquatic animals generates a chemical profile, that is, a characteristic bouquet or mosaic of compounds that can uniquely identify the species (Sorensen and Baker, 2015). These chemical profiles can also provide information about the internal state of the animal such as hunger state, recent diet, and habitat use (Csanyi, 1985; Licht, 1989; Brown and Godin, 1999; Webster et al., 2007; Ferrari, Wisenden, and Chivers, 2010). Molecules are often passively released from the mucus, gills, urine, and feces of fishes as a result of diffusion gradients and natural 0002208146.indd 151 11/22/2014 5:38:57 PM 152 Fish Pheromones and Related Cues Sender Receiver Semiochemicals from sender Production and release of semiochemical Physiological mechanisms - Hypertrophy of secretory tissues Specialized gill cells Conjugated steroids for release in urine Bladder control Ecological function - Species identification Signal social status Attract mates Reproductiion Differential reproductive success - Promotion of genes for Production of semiochemicals Controlled released of semiochemicals Response Physiological mechanisms Ecological function - Olfactory receptor specificity, sensitivity - Neural wiring - Cognitive processing of information - Navigation Find food Avoid predators Reproduction Differential reproductive success - Promotion of genes for Detection of semiochemicals Cognitive processing of chemical information Figure 7.1. The evolution of signal production and release in senders and behavioral responses to semiochemicals in receivers. In receivers, genes that give rise to the proximate mechanisms of behavior (anatomical and physiological aspects of receptors, neural wiring of cognitive processes—the capacity and inclination to behave) are promoted when an individual responds adaptively to information contained in a semiochemical released into the environment. The semiochemical provides information about the context and timing for when a particular behavioral response will be most effective. When a response to semiochemicals is executed at the correct time and in the correct place, it is effective in achieving the ecological function (migration, foraging, predator avoidance, reproduction). Responses to semiochemicals evolve when individuals that are best at exploiting chemical information achieve greater reproductive success than individuals that do not respond as adaptively to semiochemicals. Genes for the production and contextual release of semiochemical signals by senders are promoted when the response of receivers confers a fitness benefit to senders. In a co-evolved communication system, natural selection promotes specialization for production and controlled release of the chemical signal (pheromone) to make the signal more detectable to receivers whose responses benefit the sender. metabolic clearance. Detection of these molecules in the chemical profile reveals presence/absence information about specific organisms of fitness value to predators (odor of prey), to prey (odor of predators; Ferrari, Wisenden, and Chivers, 2010), species identification mating and migration (e.g. Scholz et al., 1976; Fine and Sorensen, 2005; Sorensen et al., 2005; Keefer et al., 2006; Sorensen and Hoye, 2007), and settling site selection by larval coral reef fishes (Sweatman, 1988). Because these semiochemicals provide useful information, there is selection on receivers to detect and respond adaptively to these semiochemicals. However, because senders do not benefit from the response of receivers, there is no opportunity for selection to act on production of cues or control of their release (Fig. 7.1; Table 7.1). 7.5 Passive, Contextual Release of Semiochemicals When release of semiochemicals occurs only during a limited range of ecological contexts, then there will be opportunity for selection on receivers to tailor behavioral responses to those contexts. For example, fish respond to semiochemicals released from damaged conspecifics (alarm cues) that 0002208146.indd 152 11/22/2014 5:38:58 PM The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical 153 are released when a predator damages prey tissues in the process of attack and consumption of prey (Wisenden and Chivers, 2006; Kelley, 2008; Ferrari, Wisenden, and Chivers, 2010; Wisenden, 2015). Injury-released chemical cues are typically released only in the context of predation, and therefore reliably indicate the presence of predation risk. Responses to alarm cues are innate. Labreared minnows show full response intensity to conspecific extract (e.g., Wisenden et al., 2010). Fishes are also adept at detecting injury-released cues from injured conspecifics in the diet of unfamiliar predators (Mathis and Smith, 1993; Wisenden, 2015). Although the chemical nature of alarm cues is not yet fully characterized for any species (Mathuru et al., 2012), there is no evidence linking the source of alarm cues to a specialized structure for synthesis and release of an alarm cue. Even the much-discussed epidermal club cells of Ostariophysi and Percid fishes (Smith, 1992) are not directly linked to alarm cues (Chivers et al., 2007; Carreau-Green et al., 2008; Ferrari, Wisenden, and Chivers, 2010). Another example of a contextual semiochemicals is those released from familiar individuals (Ward, Axford, and Krause, 2002, 2003; Ward and Hart, 2003; Ward, 2015). These cues are contextual because they provide information in addition to the simple presence/absence of a conspecific. The ability to discriminate familiar individuals leads to differential behavioral responses to these groups (Dugatkin and Wilson, 1993; Ward and Hart, 2003; Ward et al., 2005; Webster et al., 2007). This class of semiochemical is considered a signature mixture by Wyatt (2010) because responses result from learning either during a sensitive period early in development or based upon self-matching (e.g., Ward and Hart, 2003; Gerlach and Lysiak, 2006; Mehlis, Bakker, and Frommen, 2008; Le Vin, Mable, and Arnold, 2010; Green, Mirza, and Pyle, 2011; Ward, 2015). Consistent with the types of semiochemicals discussed thus far in this chapter, information gathering of passively released contextual semiochemicals imposes selection pressure on receivers to detect and respond adaptively to chemical information, but it does not exert any selection pressure on senders to produce or regulate the release of semiochemicals. 7.6 Passive, Contextual Release from Tissues Specialized for the Production of Semiochemicals Chemical compounds that regulate internal physiological processes for cell–cell communication are produced and secreted by specialized tissues and detected by specialized receptors on target tissues within the same individual. Having specialized tissues to produce a chemical compound(s) is the first step in interindividual chemical communication. Bile is produced by specialized tissues in the liver, and many of the acids in bile are potent odorants for which there is low-threshold olfactory sensitivity in many species, including bile of conspecifics and heterospecifics (cross reactions among phylogenetically disparate species of European eel, Anguilla anguilla; goldfish, Carassius auratus; and Mozambique tilapia, Oreochromis mossambicus; Huertas et al., 2010). Adult sea lamprey (Petromyzon marinus) use derivatives of larval bile acids as a migratory cue to find locations that contain larvae as an indicator of suitable nursery habitat for spawning (Sorensen et al., 2005; Sorensen and Hoye, 2007; Fine and Sorensen, 2010). In fishes, hormones produced by specialized tissues in the gonads regulate reproductive maturation. These hormones subsequently leak into the external environment where they reliably inform nearby conspecifics of the reproductive status of that individual (Sorensen and Scott, 1994; Sorensen and Stacey, 1999). Studies on phylogenetically disparate fish taxa suggest that hormonally based semiochemicals are more the rule than the exception (see Stacey, 2015). For example, male tilapia, O. mossambicus, distinguish between preovulatory and postovulatory females on the basis of chemical cues (Miranda et al., 2005). Redfin shiners (Notropis umbratilis) spawn in the nests of green sunfish (Lepomis cyanellus). Spawning aggregations, territorial behavior, and courtship by redfin shiners can be induced by chemical cues associated with gamete 0002208146.indd 153 11/22/2014 5:38:58 PM 154 Fish Pheromones and Related Cues release (milt, ovarian fluids) of the host sunfish even when these cues are experimentally released over substratum unsuitable for spawning (Hunter and Hasler, 1965). In this case, redfin shiners exploit publicly released sexual cues of a heterospecific to cue the context and timing of their own reproductive behaviors (Fig. 7.1). The absence of species specificity in these examples underscores how conspecific exploitation of these same semiochemicals could lead to specialization to control the quantity and context of release, and thus the evolution of pheromonal systems of communication. Although there is once again selection on receivers to detect and respond adaptively to chemical information, there is only incipient selection on senders to elaborate mechanisms of synthesis and control of semiochemical release. Although the semiochemicals discussed thus far are passively released by-products of endogenous physiological processes, they set the stage for the evolution of specialized production and release of these cues because of the opportunity for receiver responses to confer fitness benefits to senders. Control of release by senders is necessary if exploitation of semiochemical cues is to become a component of a co-evolved communication system where receivers benefit from information in the semiochemical (and elaborate receptors and cognitive processes to respond adaptively) and senders benefit from manipulating receivers (and elaborate mechanisms to control production and release of the semiochemical signal). 7.7 Active, Voluntarily Released Chemical Compounds from Tissues Specialized for Production, Storage, and Release of Semiochemicals There are several clear examples of hyperdeveloped (beyond the immediate needs of intercellular communication) tissues for the synthesis and release of semiochemicals. Male sea lamprey possess specialized glandular gill cells to facilitate the release of the bile acid-derived sex pheromone 7α, 12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (also known as 3keto-petromyzonol sulfate, or 3ketoPZS) (Li et al., 2002). Immunocytochemical experiments showed that 3ketoPZS is located in cells in the interlamellar region of the gills of prespermiating males and moves to the gill lamellae when males enter the spermiating phase of reproductive readiness (Siefkes et al., 2003). Seasonal fluctuations in the size of the seminal vesicles in Clarias catfish coincide with the release of compounds that attract females (Resink et al., 1989). In gobies, the mesorchial region of the testes associated with the mesenteries, is hypertrophied and laden with Leydig cells that actively secrete conjugated steroids (a variety of 5β-reduced steroids, chiefly 17-oxo-5β-androstan-3α-yl, also known as etiocholanolone glucoronide, or ETIO-g) that attract females (Colombo, Bekvedere, and Pilati, 1977; Colombo et al., 1980; Murphy, Stacey, and Corkum, 2001; Arbuckle et al., 2005). Interestingly, the black goby has both territorial and sneaker male mating tactics, but only the territorial males possess a hypertrophied mesorchial gland (Locatello, Mazzoldi, and Rasotto, 2002). The absence of a mesorchial gland in sneaker males suggests selection for chemical crypsis (i.e., secondary loss of pheromone-producing tissue). Fish that do not show obvious tissue specialization for production and release of sex pheromones may nevertheless have an intersexual cascade of pheromonal communication that governs gonadal maturation and spawning behavior that ensures simultaneous gamete release. For example, the release of 17, 20β-dihydroxy-4-pregen-3-one (17, 20βP), sulfated (17, 20βP-20S) and androstenone by pre-ovulatory female goldfish stimulate male reproductive behaviors and sperm production (Sorensen and Stacey, 1999). While 17, 20βP is released via the gills, 17,20βP-20S is released in pulses of urine, giving females voluntary control over its release (Sorensen et al., 1995). Ovulation is accompanied by a 100-fold increase in prostaglandin F2α (PGF2α) (Sorensen et al., unpublished results). PGF2α and a related metabolite 15-keto-PGF2α are released primarily with pulses of urine, which increase in frequency when in the presence of a male, especially at the time of entering 0002208146.indd 154 11/22/2014 5:38:58 PM The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical 155 vegetation where oviposition occurs (Appelt and Sorensen, 2007). In other species, such as the Mossambique tilapia, O. mossambicus, and swordtail (Xiphophorus birchmanni), it is the males that increase the rate of urine release when in the presence of a pre-ovulatory female (Almeida et al., 2005; Rosenthal et al., 2011). Interestingly, anosmic male tilapia did not increase rate of urination in the presence of pre-ovulatory females indicating that the urination of males is based solely in response to pheromones released by pre-ovulatory females (Miranda et al., 2005). Males in another cichlid, Astatotilapia burtoni, showed a similar urinary response to visual stimuli alone, with low rates of urination when presented with mouth-brooding (nonreceptive) females but increasing urination rate when presented with non-mouth-brooding females (Maruska and Fernald, 2012). Urine containing sex pheromones are released by O. mossambicus in contexts other than reproduction. Socially dominant males increase concentrations of urinary sex steroids (Oliveira, Almada, and Canario, 1996) and frequency of urine pulse release (Barata et al., 2007) in male–male social interactions. Taken together, these studies provide evidence from disparate phylogenies for selection on context and timing of release of behaviorally active chemical compounds by both sexes. By commonly accepted communication theory (e.g., Bradbury and Vehrencamp, 2011), these chemical cues should be considered signals in a co-evolved communication system, and thus, qualify as true pheromones. 7.8 Discussion: Evolution of Semiochemicals from Cues to Signals This book on fish pheromones covers a range of semiochemicals released by conspecifics that can be arranged across the evolutionary spectrum from cues to signals, showing an incremental transition from basic information gathering to the elaboration of specialized receptors and mechanisms for production and release of pheromones. The term “pheromone” was first coined by Karlson and Lüscher (1959), as a form of chemical communication between conspecifics. Karlson and Lüscher (1959) defined pheromone using examples from insects (social Hymenoptera, Isoptera, Lepidoptera), sexual attractants in Crustacea, alarm pheromone [which we are now careful to call alarm cues because senders do not benefit from the response of receivers (Ferrari, Wisenden, and Chivers, 2010; Wisenden, 2015)] in minnows and territorial marking substances of carnivorous mammals. Wyatt (2009, 2010, 2013) reviewed 50 years of research on pheromones across many taxa and updated the definition: “Pheromones are molecules that are evolved signals which elicit a specific reaction, for example, a stereotyped behavior and/or a developmental process in a conspecific.” (Wyatt, 2010). Clearly, fish produce and respond to semiochemicals that qualify as pheromones as per Wyatt’s definition of the term. However, the majority of semiochemicals used by fishes are not pheromones by this definition. Most fish “pheromonal” systems are in fact precommunication processes in which receivers exploit chemical forms of public information while providing no selection on senders to specialize in production or release of semiochemicals. Future work on fish communication should emphasize the demonstration of evidences of specialization for detection, production, and contextspecific active release of semiochemicals. To do that, we must first acquire much more information about the chemical nature of the compounds, often comprising mixtures of compounds, which fish use to inform their behavioral decision-making for migration, foraging, predator avoidance, and reproduction. References Almeida, O.G., Miranda, A., Frade, P. et al. (2005) Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). Chemical Senses, 30 S1, i309–i310. Appelt, C.W. and Sorensen, P.W. (2007) Female goldfish signal spawning readiness by altering when and where they release a urinary pheromone. Animal Behaviour, 74, 1329–1338. Arbuckle, W.J., Bélanger, A.J., Corkum, L.D. et al. (2005) In vitro biosynthesis of novel 5β-reduced steroids by the testis of the round goby. Neogobius melanostomus. General and Comparative Endocrinology, 140, 1–13. 0002208146.indd 155 11/22/2014 5:38:58 PM 156 Fish Pheromones and Related Cues Barata, E.N., Hubbard, P.C., Almeida, O.G. et al. (2007) Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus). BMC Biology, 5, 54. Bradbury, J.W. and Vehrencamp, S.L. (2011) Principles of Animal Communication, 2nd Edn, Sinauer, Sunderland, MA. Brown, G.E. and Godin, J.-G. (1999) Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Animal Behaviour, 57, 475–481. Carreau-Green, N.D., Mirza, R.S., Martinez, M.L., and Pyle, G.G. (2008) The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. Journal of Fish Biology, 73, 2390–2401. Chivers, D.P., Wisenden, B.D., Hindman, C.J. et al. (2007) Epidermal “alarm substance” cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proceedings of the Royal Society Series B, 274, 2611–2619. Colombo, L., Bekvedere, P.C., and Pilati, A. (1977) Biosynthesis of free and conjugated 5β-reduced androgens by the testis of the black goby, Gobius jozo L. Bollettino di Zoologia, 44, 131–134. Colombo, L., Marconato, A., Belvedere, P.C., and Friso, C. (1980) Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Bollettino di Zoologia, 47, 355–364. Csanyi, V. (1985) Ethological analysis of predator avoidance by the paradise fish (Macropodus opercularis L.) 1. Recognition and learning of predators. Behaviour, 92, 227–240. Dugatkin, L.A. and Wilson, D.S. (1993) Fish behaviour, partner choice experiments and cognitive ethology. Reviews in Fish Biology and Fisheries, 4, 368–372. Ferrari, M.C.O., Wisenden B.D., and Chivers, D.P. (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology, 88, 698–724. Fine, J.M. and Sorensen, P.W. (2005) Biologically relevant concentrations of petromyzonal sulfate, a component of sea lamprey migratory hormone, measured in stream water. Journal of Chemical Ecology, 31, 2205–2210. Fine, J.M. and Sorensen, P.W. (2010) Production and fate of the sea lamprey migratory pheromone. Fish Physiology and Biochemistry, 36, 1013–1020. Gerlach, G. and Lysiak, N. (2006) Kin recognition and inbreeding avoidance in zebrafish is based on phenotype matching. Animal Behaviour, 71, 1371–1377. Green, W.W., Mirza, R.S., and Pyle, G.G. (2011) Kin recognition and cannibalistic behaviours by adult male fathead minnows (Pimephales promelas). Naturwissenshaften, 95, 269–272. Heupel, M.R. and Simpfendorfer, C.A. (2008) Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquatic Biology, 1, 277–289. Huertas, M., Hagey, L., Hofmann, A.F. et al. (2010) Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a “broad range” sensitivity not confined to those produced by conspecifics. Journal of Experimental Biology, 213, 308–317. Hunter, J.R. and Hasler, A.D. (1965) Spawning association of the redfin shiner, Notropis umbratilis, and the green sunfish. Lepomis cyanellus. Copeia, 1965, 265–281. Karlson, P. and Lüscher, M. (1959) “Pheromones”: a new term for biologically active substances. Nature, 183, 55–56. Keefer, M.L., Caudill, C.C., Peery, C.A., and Bjornn, T.C. (2006) Route selection in a large river during the homing migration of chinook salmon (Oncorhynchus tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences, 63, 1752–1762. Kelley, J.L. (2008) Assessment of predation risk by prey fishes, in Fish Behaviour (eds Magnhagen, C., Braithwaite, V.A., Forsgren, E., and Kapoor, B.G.), Science Publishers, Enfield, pp. 269–301. Kramer, D.L. (1987) Dissolved oxygen and fish behavior. Environmental Biology of Fishes, 2, 81–92. Le Vin, A.I., Mable, B.K., and Arnold, K.E. (2010) Kin recognition via phenotype matching in a cooperatively breeding cichlid, Neolamprologus pulcher. Animal Behaviour, 79, 1109–1114. Leggett, W.C. (1977) The ecology of fish migrations. Annual Review of Ecology and Systematics, 8, 285–308. Li, W., Scott, A.P., Siefkes, M.J. et al. (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science, 296, 138–141. 0002208146.indd 156 11/22/2014 5:38:58 PM The Cue–Signal Continuum: A Hypothesized Evolutionary Trajectory for Chemical 157 Licht, T. (1989) Discrimination between hungry and sated predators: the response of guppies (Poecilia reticulata) from high and low predation sites. Ethology, 82, 238–243. Locatello, L., Mazzoldi, C., and Rasotto, M.B. (2002) Ejaculate of sneaker males is pheromonally inconspicuous in the black goby, Gobius niger (Teleostei, Gobiidae). Journal of Experimental Biology, 293, 601–605. Maes, J., Stevens, M., and Breine, J. (2007) Modelling the migration opportunities of diadromous fish species along a gradient of dissolved oxygen concentration in a European tidal watershed. Estuarine, Coastal and Shelf Science, 75, 151–162. Maruska, K.P. and Fernald, R.D. (2012) Contextual chemosensory urine signaling in an African cichlid fish. Journal of Experimental Biology, 215, 68–74. Mathis, A. and Smith, R.J.F. (1993) Chemical labelling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). Journal of Chemical Ecology, 19, 1967–1979. Mathuru, A.S., Kibat, C., Cheong, W.F. et al. (2012) Chondroitin fragments are odorants that trigger fear behavior in fish. Current Biology, 22, 1–7. Mehlis, M., Bakker, T.C.M., and Frommen, J.G. (2008) Smells like sib spirit: kin recognition in three-spined stickleback (Gasterosteus aculeatus) is mediated by olfactory cues. Animal Cognition, 11, 643–650. Miranda, A., Almeida, O.G., Hubbard, P.C. et al. (2005) Olfactory discrimination of female reproductive status by male tilapia (Oreochromis mossambicus). Journal of Experimental Biology, 208, 2037–2043. Murphy, C.A., Stacey, N.E., and Corkum, L.D. (2001) Putative steroidal pheromones in the round goby, Neogobius melanostomus: olfactory and behavioral responses. Journal of Chemical Ecology, 27, 443–470. Odling-Smee, L. and Braithwaite, V.A. (2003) The role of learning in fish orientation. Fish and Fisheries, 4, 235–246. Oliveira, R.F., Almada, V.C., and Canario, A.V.M. (1996) Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus. Hormones and Behavior, 30, 2–12. Resink, J.W., Voorthuis, P.K., Van Den Hurk, R. et al. (1989) Steroid glucoronides of the seminal vesicle as olfactory stimuli in African catfish, Clarias gariepinus. Aquaculture, 83, 1–2. Rosenthal, G.G., Fitzsimmons, J.N., Woods, K.U. et al. (2011) Tactical release of a sexually-selected pheromone in a swordtail fish. PLoS ONE, 6, e16994. Scholz, A.T., Horrall, R.M., Cooper, J.C., and Hasler A.D. (1976) Imprinting to chemical cues: the basis for home stream selection in salmon. Science, 192, 1247–1249. Siefkes, M.J., Scott, A.P., Zielinski, B. et al. (2003) Male sea lamprey, Petromyzon marinus L. excrete a sex pheromone from gill epithelia. Biology of Reproduction, 69, 125–132. Smith, R.J.F. (1992) Alarm signals in fishes. Reviews in Fish Biology and Fisheries, 2, 33–63. Sorensen, P.W. (1986) Origins of the freshwater attractant(s) of migrating elvers of the American eel, Anguilla rostrata (LeSueur). Journal of the Environmental Biology of Fishes, 17, 185–200. Sorensen, P.W. and Baker, C. (2015) Species-specific pheromones and their roles in shoaling, migration and reproduction: a critical review and Synthesis, in Fish Pheromones and Related Cues (eds Peter W. Sorensen and Brian D. Wisenden), John Wiley & Sons, Inc., Hoboken. Sorensen, P.W. and Hoye, T.E. (2007) A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey, Petromyzon marinus L. Journal of Fish Biology, 71 (supplement D), 100–114. Sorensen, P.W. and Scott, A.P. (1994) The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiologica Scandinavica, 152, 191–205. Sorensen, P.W. and Stacey, N.E. (1999) Evolution and specialization of fish hormonal pheromones, in Advances in Chemical Signals in Vertebrates (eds Johnston, R.E., Müller-Schwarze, D., and Sorensen, P.W.), Kluwer Academic/Plenum Publishers, New York, pp. 15–47. Sorensen, P.W., Fine, J.M., Dvornikovs, V. et al. (2005) Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nature Chemical Biology, 1, 324–328. 0002208146.indd 157 11/22/2014 5:38:58 PM 158 Fish Pheromones and Related Cues Sorensen, P.W., Scott, A.P., Stacey, N.E., and Bowdin, L. (1995) Sulfated 17,20β-dihydroxy-4-pregen-3one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. General and Comparative Endocrinology, 100, 128–142. Stacey, N. (2015) Hormonally-derived pheromones in teleost fishes, in Fish Pheromones and Related Cues (eds Peter W. Sorensen and Brian D. Wisenden), John Wiley & Sons, Inc., Hoboken. Stacey, N.E and Sorensen, P.W. (2009) Hormonal pheromones in fish, in Hormones, Brain and Behavior, 2nd edn, vol. 2 (eds Pfaff, D.W., Arnold, A.P., Etgen, A., et al.), Elsevier Press, San Diego, pp. 639–681. Stacey, N.E. and Sorensen, P.W. (1991) Function and evolution of fish hormonal pheromones, in Biochemistry and Molecular Biology of Fishes, vol. 1 (eds. Hochachka, P.L. and Mommsen, T.P.), Elsevier, Amsterdam, pp.109–135 Sweatman, H. (1988) Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemicals. Journal of Experimental Marine Biology and Ecology, 124, 163–174. Ward, A.J.W. (2015) Intraspecific social recognition in fishes via chemical cues, in Fish Pheromones and Related Cues (eds Peter W. Sorensen and Brian D. Wisenden), John Wiley & Sons, Inc., Hoboken. Ward, A.J.W. and Hart, P.J.B. (2003) The effects of kin and familiarity on interactions between fish. Fish and Fisheries, 4, 348–358. Ward, A.J.W., Axford, S., and Krause, J. (2002) Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice. Behavioral Ecology and Sociobiology, 52, 182–187. Ward, A.J.W., Axford, S., and Krause, J. (2003) Cross-species familiarity in shoaling fishes. Proceedings of the Royal Society of London Series B, 270, 1157–1161. Ward, A.J.W., Holbrook, R.I., Krause, J., and Hart, P.J.B. (2005) Social recognition in sticklebacks: the role of direct experience and habitat cues. Behavioral Ecology and Sociobiology, 57, 575–583. Webster, M.M., Goldsmith, J., Ward, A.J.W., and Hart, P.J.B. (2007) Habitat-specific chemical cues influence association preferences and shoal cohesion. Behavioral Ecology and Sociobiology, 62, 273–280. Wisenden, B.D. (2015) Chemical cues that indicate risk of predation, in Fish Pheromones and Related Cues (eds Peter W. Sorensen and Brian D. Wisenden), John Wiley & Sons, Inc., Hoboken. Wisenden, B.D. and Chivers, D.P. (2006) The role of public chemical information in antipredator behavior, in Fish Communication (eds Ladich, F., Collins, S.P., Moller, P. et al.), Science Publisher, Enfield, pp. 259–278. Wisenden, B.D. and Stacey, N.E. (2005) Fish semiochemicals and the evolution of communication networks, in Communication Networks (ed. McGregor, P.K.), Cambridge University Press, Cambridge, pp. 540–567. Wisenden, B.D., Binstock, C.L., Knoll, K.E., et al. (2010) Risk-sensitive information gathering by cyprinids following release of chemical alarm cues. Animal Behaviour, 79, 1101–1107. Wyatt, T.D. (2009) Fifty years of pheromones. Nature, 457, 262–263. Wyatt, T.D. (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. Journal of Comparative Physiology A, 196, 685–700. Wyatt, T.D (2013) Pheromones And Animal Behavior: Chemical Signals And Signature Mixtures, 2nd edn, Cambridge University Press, Cambridge. 0002208146.indd 158 11/22/2014 5:38:58 PM