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Chapter 6 Chemical Cues That Indicate Risk of Predation

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Chapter 6 Chemical Cues That Indicate Risk of Predation Chapter 6 Chemical Cues That Indicate Risk of Predation Brian D. Wisenden Minnesota State University Moorhead, Moorhead, Minnesota, USA 6.1 INTRODUCTION Chemical cues released passively as a by-product of ecological interactions provide a rich and reliable source of public information to guide behavioral decision-making. Predation is an omnipresent and unforgiving agent of selection that is reliably correlated with context-specific chemical cues. Consequently, natural selection has led fish to evolve finely tuned mechanisms to first detect chemical information about predation risk and then execute adaptive behavioral responses to minimize exposure to these risks. The regular interval of reviews of this topic (Smith, 1992; Chivers and Smith, 1998; Wisenden, 2003; Wisenden and Stacey, 2005; Wisenden and Chivers, 2006; Ferrari, Wisenden, and Chivers, 2010; Chivers, Brown, and Ferrari, 2013) reflects the pace and volume of new research on how fish and other aquatic animals use chemical information to ameliorate predation risk. In this chapter, the principal sources of chemical information about predation risk and the large and active literature on how injury-released chemical alarm cues from conspecifics mediate these interactions are briefly reviewed. Alarm cues are chemicals released by cells and tissues of prey dam- aged in the process of a predator attack. Because alarm cues are released only in the context of predation, they reliably inform nearby receivers of the presence of an actively foraging predator. Thus, there is strong selection on receivers to elaborate mechanisms to detect and discern the quality of this information and to respond accordingly. I focus on these interactions because conspecific chemical alarm cues are the class of compounds and mixtures that come closest to the concept of pheromone. From there, what little is known about the chemistry of these cues and the anatomical and physiological mechanisms that detect them are summarized. 6.2 CHEMICAL INFORMATION ABOUT PREDATION RISK In addition to damage-released chemical alarm cues, predator odor and disturbance cues are chemical cues that relay information about predation risk, and provide information about position in the predation sequence (Fig. 6.1A). The predation sequence parses predation events into discrete steps, each of which produces stage-specific chemical cues. Predator odor is the most obvious chemical by which prey detect the presence of predation risk. From the perspective of prey, predator odor is a 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. 131 0002208145.indd 131 11/22/2014 5:37:26 PM 132 Fish Pheromones and Related Cues (A) (B) Predation Cue types availabel to prey for risk Kairomone sequence assissment Damage-released alarm cue Detection Kairomones Disturbance cues Alarm cues O Attack x ! o ! o Capture Dietary alarm cue Ingestion Dietary cues Disturbance cue Figure 6.1. Sources of chemical information about predation risk come from the odor of the predator (kairomone), disturbance cues released by startled prey, damage-released alarm cues from predation in progress, and postingestion cues released from the predator’s diet. (A) Ecological context of when each cue type becomes available in the predation sequence; (B) source of each cue type. kairomone, that is, a chemical that is released by one species that can provide benefits­ to heterospecific receivers without providing benefits to the sender. A second type of chemical cue used by prey for detecting risk are chemicals released by disturbed but uninjured prey (herein termed “disturbance cues”). Both of these cues are used at the detection stage of the predation sequence. Kairomones and disturbance cues cause prey to increase frequency of vigilance behaviors and prepare for evasive maneuvers. Chemical alarm cues are released from damaged conspecific tissues during the attack and capture stages and indicate clear and present danger from an actively foraging predator. These cues invoke intense antipredator behavioral responses. A type of cue related to an alarm cue is a dietary cue, which are chemicals of ingested prey released from the digestive tract of predators (Fig. 6.1). Thus, kairomones comprise multiple chemical constituents; the background species-specific signature odor of the predator with additional components from the predator’s diet. 6.2.1 Cues Associated with Pre-Attack Detection of Predation Risk At the detection stage of predation, chemicals passively released from predators (kairomones) or disturbance cues released by startled or distressed (but otherwise uninjured) prey can serve to inform prey about the presence and nature of predation risk. Detecting and learning to recognize kairomones confer demonstrable survival benefits in encounters with predators (Berejikian et al., 1999; Mirza and Chivers, 2000, 2002; Gazdewich and Chivers, 2002). Adaptive use of fish ­kairomones is also well studied in zooplankton (Tollrian and Harvell, 1999) and amphibia (e.g., Schoeppner and Relyea, 2009). In fishes, some salmonid species have innate recognition of odors of their predators (Berejikian, Tezak, and LaRae, 2003; Vilhunen and Hirvonen, 2003; Hawkins, Magurran, and Armstrong, 2007; Scheurer et al., 2007; see Section 3.3); however, the majority (dozens of studies on minnows, characins, salmonids, gobies, cichlids, centrarchids, percids— see Chivers and Smith, 1998; Ferrari, Wisenden, and Chivers, 2010 for recent reviews) do not have innate recognition of predator odors and must acquire recognition of predator odor through associative learning. Fish learn to associate correlates of predation events, such as predator odor, when those novel stimuli are paired with the release of chemical alarm cues. Consequently, a single pairing­ of 0002208145.indd 132 11/22/2014 5:37:26 PM Chemical Cues That Indicate Risk of Predation 133 novel neutral stimuli (e.g., odor of an unfamiliar predator) with damage-released chemical alarm cues (e.g., skin extract of a conspecific) is sufficient to impart near-permanent association of danger with the novel predator odor. Thereafter, encounters with the novel predator odor invoke the same suite of antipredator behaviors as the behavioral response to skin extract. Göz (1941) and Magurran (1989), both working with European minnows (Phoxinus phoxinus), were the first to record this form of learning. Suboski (1990) coined the label “releaser-induced recognition learning” to describe the critical role that damage-released alarm cues have in trig- gering the formation of association between predation risk and a novel stimulus. Because predation is such a common occurrence, particularly during early life stages, surviving fishes have ample opportunity to acquire recognition of novel odors associated with predators in their area (Chivers and Smith, 1994a, 1995a; Pollock et al., 2003). Fish can also learn to associate danger with habitat-specific chemical signatures (Chivers and Smith, 1995b), visual appearance of the predators (Chivers and Smith, 1994b), or the sound of predators (Wisenden et al., 2008). The selective advantage of this learning paradigm is that fish quickly arm themselves with the ability to detect early indicators of predation risk through multiple sensory modalities. From the viewpoint of natural selection, early detection of predator presence allows prey the opportunity to execute antipredator responses and completely evade detection by the predator. Another route by which prey detect the presence of a predator is by chemical stimuli released from the digestive system of the predator (Chivers and Mirza, 2001) (Fig. 6.1). This mechanism allows prey to recognize novel fish as dangerous even if they have no previous experience with that species of predator (Mathis and Smith, 1993a) and use these dietary cues to associate that predator with predation risk in future encounters (Mathis and Smith, 1993b; Brown and Godin, 1999; Mirza and Chivers, 2003). Notable exceptions to this general rule are two studies that found no evidence that prey can detect dietary cues. Feminella and Hawkins (1994) showed that tadpoles of tailed frogs (Ascaphus truei) respond to dietary alarm cues from predatory giant salamanders (Dicamptodon spp.), cutthroat trout (Salmo clarkii) and brook trout (Salvelinus fontinalis) but not to the dietary alarm cues of shorthead sculpin (Cottus confusus). Similarly, Maniak, Lossing, and Sorensen (2000) found no evidence that Eurasian ruffe (Gymnocephalus cernuus) can detect conspecific dietary cues that had passed through the gut of northern pike (Esox lucius). Thus, it appears that some predators, such as shorthead sculpin, have the ability to mask or breakdown recognizable components of alarm cues, or perhaps that some fish, such as ruffe, do not have the ability to detect alarm cues after they have been processed in the gut of a predator. In a comparison of digestion efficiency between two predators, the mudminnows (an esociform, Umbra limi) and bluegill sunfish (a centrarchid, Lepomis macrochirus), fathead minnows (Pimephales promelas) were equally able to detect dietary alarm cues suggesting that either the more derived predator (sunfish) were no better at masking dietary cues than ancestral ones or that minnows have evolved the ability to detect dietary cues from multiple predator types (Sutrisno et al., 2014). 6.2.2 Cues Associated with Post-Attack Detection of Predation Risk When a predator
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