Behavioral Ecology Advance Access originally published online on June 11, 2004
Behavioral Ecology 2004 15(5):810-815; doi:10.1093/beheco/arh084
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Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues
a Department of Biology, Concordia University, 7141 Sherbrooke St., W. Montréal, Quebéc, H4B 1R6, Canada b Department of Chemistry, Union College, Science and Engineering Center, Schenectady, NY, 12308, USA
Address correspondence to G. E. Brown. E-mail: gbrown{at}alcor.concordia.ca.
Received 17 June 2003; revised 25 November 2003; accepted 17 December 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The ability to accurately assess local predation risk is critical to prey individuals, as it allows them to maximize threat-sensitive trade-offs between predator avoidance and other fitness related activities. A wide range of taxonomically diverse prey (including many freshwater fishes) relies on chemical alarm cues (alarm pheromones) as their primary information source for local risk assessment. However, the value of chemical alarm cues has been questioned due to the availability of additional sensory inputs (i.e., visual cues) and the lack of an overt antipredator response under conditions of low perceived risk. In this paper, we test the hypothesis that chemical alarm cues at concentrations below the point at which they elicit an overt behavioral response function to increase vigilance towards other sensory modalities (i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammus erythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide (the putative Ostariophysan alarm pheromone) did not exhibit an overt antipredator response in the absence of secondary visual cues (not different than the distilled water control). However, when exposed to the sight of a visually alarmed conspecific, they significantly increased the intensity of their antipredator response (not different from shoals exposed to the suprathreshold alarm cue). This study demonstrates that prey may benefit from responding to low concentration alarm cues by increasing vigilance towards secondary cues during local risk assessment, even in the absence of an overt behavioral response. By increasing vigilance towards secondary risk assessment cues in the presence of a low risk chemical cue, individuals are likely able to maximize the threat-sensitive trade-offs between predator avoidance and other fitness related activities.
Key words: Chemical alarm cues, Ostariophysan fishes, predator-prey interactions, antipredator behavior, vigilance, risk assessment, threat-sensitive trade-offs.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Predation is a significant and pervasive selection force, shaping an individual's behavior, morphology, and life history traits (Chivers and Smith, 1998
; Kats and Dill, 1998; Lima and Dill, 1990; Wisenden, 2000). Individuals that can detect and avoid potential predators should be at a selective advantage (Mirza and Chivers, 2001). However, predator avoidance is likely very costly, as it would reduce time and energy available for other fitness related behaviors, such as foraging or mating. Thus, predator avoidance strategies can be viewed as a series of threat-sensitive trade-offs between antipredator benefits and the fitness gain associated with other behavior patterns (Brown, 2003; Lima and Bednekoff, 1999; Wisenden, 2000).
The ability to assess local predation risk requires the presence of spatially and temporally reliable information. Of all potential sensory modalities capable of conveying such information regarding local predation risk, visual and chemical cues have been the most widely studied (Bouwma and Hazlett, 2001; Chivers and Smith, 1998, Hartman and Abrahams, 2000; Kats and Dill, 1998). Visual and chemical cues, however, represent very different levels of risk and information. Visual cues are spatially and temporally reliable, but can be considered very risky, as the prey and predator must be within close proximity (Brown and Magnavacca, 2003; Kats and Dill, 1998). Chemical information, while spatially and temporally less reliable, may have a lower associated risk, as prey and predator need not be in close proximity for prey to acquire information (Brown and Magnavacca, 2003; Kats and Dill, 1998).
A wide range of taxonomically diverse prey fishes, including Ostariophysan fishes, relies on damage released chemical alarm cues (alarm pheromones) as a source of information regarding local predation risk (Brown, 2003; Chivers and Smith, 1998; Smith, 1999). When released, after mechanical damage to the skin, these chemical alarm cues can elicit a dramatic short term increase in species typical antipredator behavior in nearby conspecifics and some sympatric heterospecifics (Chivers and Smith, 1998; Smith, 1999). Such overt behavioral responses (Smith, 1999) have been well documented and include increased shoal cohesion, area avoidance, dashing, freezing, and reduced foraging and mating (Chivers and Smith, 1998). Chemical alarm cues can also elicit a variety of covert behavioral responses (Smith, 1999), including acquired recognition of novel predators, induced morphological and life history changes, and the assessment of local predation risk through predator inspection behavior (Brown and Godin, 1999; Chivers and Smith, 1998).
Overt antipredator behaviors in response to chemical alarm cues can function as secondary visual alarm cues, allowing for rapid propagation of an antipredator response through shoals (Smith, 1992). Upon detection of a chemical alarm cue, the starry goby (Asterropteryx semipunctatus) engages in ‘head-bobbing’ behavior (a conspicuous visual display) that elicits increased antipredator behavior in nearby conspecifics (Smith, 1989). Glowlight tetras (Hemigrammus erthrozonus), on detecting a conspecific chemical alarm cue, significantly increase their frequency and intensity of fin-flicking behavior (Brown et al., 1999). Fin-flicking in glowlight tetras is a conspicuous visual alarm signal that only occurs when they are frightened (Brown et al., 1999). This entails rapid ‘flicking’ of the dorsal and caudal fins without changing the position of the fish in space. Nearby individuals that have not detected a chemical cue will significantly increase their antipredator behavior in response to a visually displaying (fin-flicking) conspecific. In both fathead minnows (Pimephales promelas) and European minnow (Phoxinus phoxinus), an alarm response can rapidly spread through a shoal based on visual cues (Magurran and Higham, 1988; Mathis et al., 1996).
Magurran et al. (1996) and Hartman and Abrahams (2000) have recently argued that the Ostariophysan alarm ‘pheromone’ system is of limited value to prey under natural conditions due to the availability of additional information (i.e., visual cues) and the lack of an overt antipredator response under conditions of low perceived risk (but see Smith, 1997). However, Brown et al. (2001a) have shown that fathead minnow are able to detect and learn to recognize the chemical identity of a previously novel predator paired with concentrations of chemical alarm cues well below the concentration required to elicit an overt behavioral response. Mirza and Chivers (2003) have further demonstrated that juvenile rainbow trout (Oncorhynchus mykiss) gain significant survival benefits when exposed to concentrations of conspecific skin extracts below that which elicits an overt behavioral response. Thus, individual prey appear to attend to conspecific alarm cues below the concentration required to elicit observable behavioral responses. Furthermore, these data suggest that individuals are trading off immediate antipredator benefits in favor of other fitness related activities (i.e., foraging). Individuals could maximize these trade-offs by increasing their reliance on secondary predator cues (i.e., visual cues) in the presence of low concentration chemical alarm cues. By doing so, they could reduce the potential loss of antipredator benefits while still gaining fitness associated with other activities (Smith, 1997, 1999).
To determine if subthreshold concentrations of conspecifics chemical alarm cues function to increase vigilance towards secondary predator cues, we exposed shoals of glowlight tetras (Charicidae, Ostariophysi) to supra- and subthreshold concentrations of hypoxanthine-3-N-oxide (H3NO, the putative Ostariophysan alarm pheromone; Brown et al., 2000, 2001b, 2003) or a distilled water control, in the presence or absence of a conspecific stimulus fish displaying a visual alarm signal. We predicted that if subthreshold concentrations of chemical alarm cues increased vigilance towards visual information, test shoals initially exposed to subthreshold concentrations of H3NO should respond to the presence of a visually alarmed conspecific: (1) more intensely than those initially exposed to distilled water controls, and (2) with a similar intensity to those initially exposed to a suprathreshold concentration of H3NO.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Glowlight tetras were obtained from a commercial supplier and were held in a 110 l holding aquarium equipped with a gravel substrate and filled with continuously filtered, dechlorinated tap water (28°C). Mean (±SE) length at time of testing was 2.99 ± 0.24 cm. All fish were fed ad libitum twice a day with commercial fish food and exposed to a 12:12h light:dark cycle.
Test tanks
The testing apparatus consisted of a 37 l test tank (filled with 35 l dechlorinated tap water) and a 20 l stimulus tank (filled with 17.5 l dechlorinated tap water) adjacent to each other, separated by a sheet of one-way mirror. We positioned an incandescent lamp (40 W) 25 cm above the stimulus tank. When the stimulus tank was illuminated, fish in the test tank could see into the stimulus tank, but fish in the stimulus tank could not see into the test tank. When not illuminated, fish in either tank could not see into the neighboring tank. Both stimulus and test tanks contained a gravel substrate, an airstone, and were maintained at 28°C. We fixed an additional length of airline tubing near the airstone (of both test and stimulus tanks), allowing us to introduce the chemical stimuli (see below) remotely, from behind a black plastic observation blind. All trials were videotaped for later behavioral analysis.
Experimental stimuli
To investigate the potential effects of subthreshold concentrations of chemical alarm cues, we manipulated two independent variables (chemical cues and visual cues) in a repeated measures design. Two concentrations of hypoxanthine-3-N-oxide (the putative Ostariophysan alarm pheromone; Brown et al. 2000, 2001b, 2003) were tested: suprathreshold (0.4 nM) and subthreshold (0.1 nM), in addition to a distilled water control. H3NO was synthesized as in Brown et al. (2000). Stock solutions of H3NO were prepared by dissolving H3NO in glass-distilled water to concentrations of 2.9 and 0.7 µM. Thus, when injected into the test tank, a final concentration of 0.4 or 0.1 nM was obtained (Brown et al., 2001c).
In order to verify that these concentrations were indeed above and below the minimum behavioral response threshold (Brown et al., 2001c), shoals of four tetras were exposed to a distilled water control and H3NO at a concentration of either 0.4 nM or 0.1 nM. Paired control and experimental trials (N = 10 for each concentration) consisted of a 5 min prestimulus and a 5 min post-stimulus injection observation period. During both the pre- and post-stimulus observation periods, we recorded: (1) vertical area use and shoaling index (see below) every 15 s. We then calculated the difference between pre- and post-stimulus observations and compared these difference scores (distilled water control versus H3NO at either 0.4 or 0.1 nM) using paired t tests. We found a significant increase in shoaling and a significant decrease in vertical area use (indicating an alarm response; Brown et al. 2001b) for tetras exposed to H3NO at 0.4 nM, but not at 0.1 nM (Figure 1).
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These concentrations were then paired with a visual alarm cue (presence of a single stimulus tetra exhibiting an overt visual alarm display; Brown et al., 1999
) or a visual non-alarm cue (presence of a single tetra not exhibiting any overt visual alarm display). In the visual non-alarm treatments, the stimulus fish was exposed to distilled water immediately before its exposure to the test shoal. In the visual alarm treatments, the stimulus fish was exposed to 0.4 nM H3NO. In all visual alarm trials, the stimulus fish were observed to exhibit an overt antipredator response (i.e., visual alarm display). Ten replicates of each treatment combination were performed.
Experimental protocol
A test shoal of four fish (matched for size) was placed within the test tank and a single stimulus fish in the stimulus tank. Prior to the start of trials, all fish were given a 24 h acclimation period in the testing apparatus and fed 30 min prior to testing. At the start of all trials, five min of prestimulus baseline behavior were recorded. At the end of the prestimulus observation period we injected 5 ml of 0.4 nM H3NO (Full), 0.1 nM H3NO (Sub), or distilled water (DW) into the test shoal tank. The test shoal behavior was recorded for another five min. At the 10-min mark, the stimulus fish was exposed to either 5 ml of suprathreshold H3NO (visual alarm) or distilled water (visual non-alarm). Full strength H3NO induced the visual alarm condition and distilled water induced the visual non-alarm condition. The light was turned on and behavior recorded for another five min.
During each observation period, we recorded, every 15 s: (1) vertical area use, (2) horizontal area use, and (3) shoaling index. We recorded vertical area use as the sum of location scores for each tetra (1 = bottom third of the tank, 3 = top third of the tank). For any given scan, possible vertical area use scores ranged from 4 (all tetras near substrate) to 12 (all tetras near surface). Similarly, we recorded horizontal area use (1 = section furthest from the stimulus tank, 3 = section closest to the stimulus tank). Possible horizontal area use scores ranged from 4 (all tetras away from the stimulus tank) to 12 (all tetras near the stimulus tank). Shoaling index scores (modified from Mathis and Smith, 1993) ranged from 1 (no tetras within one body length of each other) to 4 (all tetras within one body length of each other). Test and stimulus tetras were used only once and the order of stimulus was randomized.
Statistical analysis
For each behavioral measure, we used a two-way repeated measure ANOVA to assess the effects of chemical (DW, Full, and Sub) and visual cues (visual non-alarm vs. visual alarm), using treatment (prestimulus, chemical only, and chemical + visual) as the repeated measure. To further assess the effects of chemical cues, we conducted separate one-way repeated measures ANOVAs on visual non-alarm and visual alarm conditions. To assess differences within each treatment block, we conducted planned contrast using one-way ANOVAs and multiple comparisons using Fisher's Protected Least Square Difference tests.
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RESULTS |
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Overall comparisons
For each of the three behavioral measures recorded, we found significant interactions between the repeated measures effect (treatment) and the presence or absence of a visually signaling stimulus fish (shoaling index: F(2,108) = 15.01, p < 0.0001; vertical area use: F(2,108) = 6.08, p < 0.004; horizontal area use: F(2,108) = 4.51, p < 0.02). Thus, these interactions demonstrate that shoals of tetras were exhibiting increased antipredator behavior in the visual alarm conditions (i.e., responding to a visual alarm cues; Brown et al., 1999
), but not in the visual non-alarm condition. Hence, we further examined the main treatment effects using separate one-way repeated measures ANOVAs (see above).
Visual non-alarm conditions
We found a significant interaction between the repeated measure (treatment) and chemical condition for shoaling index (Table 1; Figure 2A), but not for vertical area use (Table 1; Figure 2C) or horizontal area use (Table 1; Figure 2E). In the case of vertical area use, we found a marginally significant effect of chemical condition (DW vs. Full vs. Sub: Table 1; Figure 2C). Test shoals exposed to suprathreshold alarm cues (0.4 nM H3NO) significantly increased shoaling index and decreased vertical area use relative to shoals exposed to distilled water or subthreshold concentration of alarm cues (0.1 nM H3NO) (Table 2; Figure 2A,C). There was no difference among the three chemical conditions during prestimulus observations (Table 2). In the absence of a visual alarm cue, test shoals exposed to distilled water or subthreshold concentration of alarm cues did not increase antipredator behavior during the chemical + visual treatment (Figure 2).
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Visual alarm conditions
For shoaling index and vertical use, we found significant interactions between the repeated measure (treatment) and chemical conditions (Table 1; Figure 2B,C). While we did not find significant interaction for horizontal area use, we did see a significant repeated measures effect (Table 1; Figure 2F). During the chemical uses only observation period, test shoals significantly increased shoal cohesion and decreased vertical area use when exposed to suprathreshold alarm cues versus either distilled water or subthreshold concentration of alarm cues (Table 2; Figure 2B,D). However, during the chemical + visual observation period, tetras initially exposed to subthreshold concentrations of H3NO increased shoaling and decreased vertical area use to similar levels of those exposed to full concentrations of H3NO (Table 2; Figure 2B,D). During the chemical + visual observation period, tetras significantly increased their horizontal area use scores (i.e., approached the stimulus tetra; Table 2, Figure 2F). This increase was significantly greater for tetras initially exposed to supra- and subthreshold concentration of H3NO versus those initially exposed to distilled water (Table 2; Figure 2F).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our data demonstrate that even in the absence of an immediate overt antipredator response, subthreshold concentrations of conspecific alarm cues function to increase vigilance towards secondary (visual) alarm cues. Thus, contrary to the arguments of Magurran et al. (1996)
and Hartman and Abrahams (2000), prey fishes appear to detect and respond to conspecific chemical alarm cues at thresholds well below that required to elicit an ‘overt’ behavioral response. By increasing vigilance towards additional sensory information, individuals could continue to engage in some fitness related behavior (i.e., foraging, territorial defense or mating) while gaining crucial information regarding local predation risk (Brown and Magnavacca, 2003). In the absence of visually displaying conspecifics, only test shoals exposed to the suprathreshold concentration of H3NO exhibited an overt antipredator response. However, in the presence of a visually alarmed stimulus fish, test shoals exhibited an overt antipredator response during the chemical + visual observation period, regardless of which chemicals stimulus they were exposed to during the chemical only observation period. Shoals exposed to the subthreshold concentration of H3NO, which were not different from the distilled water controls during the chemical only period, exhibited a significantly stronger antipredator response than did those exposed to distilled water in the presence of a visually alarmed conspecific. Furthermore, test shoals exposed to either supra- or subthreshold concentrations of H3NO did not differ in the presence of a visually signaling tetra. Thus, our data strongly suggest that subthreshold concentrations of conspecific alarm cues significantly increase vigilance towards secondary (visual) alarm cues.
During the visual negative trials, we found no significant difference over the three observation periods (prestimulus, chemical only, chemical + visual) in the horizontal area use. Significant changes in horizontal area use were only observed in the presence of the visually displaying stimulus tetra. Given the relatively small volume of the test tanks, the chemical stimuli would have been rapidly dispersed throughout the tank. As a result, there would have been no concentration gradient present. The observation that when test shoals were exposed to the visual positive conditions they significantly increased horizontal area use (i.e., approached the stimulus tetra) supports our findings that the behavior of the stimulus tetra was indeed functioning as a visual alarm cue. Such a response would result in larger shoal sizes, potentially conferring increased antipredator benefits to individuals (Brown et al., 1999; Pitcher, 1992).
The response to predation threats under natural conditions is likely the product of threat-sensitive trade-offs (Lima and Bednekoff, 1999; Lima and Dill, 1999). Responding to chemical alarm cues of both conspecifics and sympatric heterospecifics significantly increases individual survival (Chivers et al., 1996; Mathis and Smith, 1993; Mirza and Chivers, 2000, 2003). However, such responses are costly, reducing the time spent engaged in other fitness related behaviors such as foraging or mating. As such, the ability to accurately assess local predation risk should be selected with prey populations (Brown, 2003; Wisenden, 2000). Our current results suggest that individuals may be able to maximize these trade-offs by not immediately responding to chemical alarm cues and increasing vigilance towards secondary cues. This would allow individuals to, for example, continue foraging and only respond when secondary cues are detected.
The relative concentration of a chemical alarm cue detected by an individual may provide information regarding immediate predation threats (Brown et al., 2001a; Lawrence and Smith, 1989; Mirza and Chivers, 2003). Individuals detecting relatively low concentrations of chemical alarm cues may continue to forage in a risk sensitive fashion. For example, juvenile convict cichlids switch from a profitable, but risky, foraging strategy to one of lower profitability but lower risk in the presence of lower concentrations of conspecific alarm cues (Brown GE, Harvey MC, and Foam PE, unpublished data). Our current results suggest that an individual may be able to further maximize this form of risk sensitive trade-off by increasing vigilance towards secondary information (Treves, 2000).
Brown et al. (2001c) demonstrated that fathead minnows do not show a graded response to decreasing concentrations of conspecific chemical alarm cues. They report no difference intensity by minnows exposed to H3NO above a population specific minimum behavioral response threshold. Similar results have been demonstrated for juvenile rainbow trout (Mirza and Chivers, 2003). Our results suggest, however, that a more accurate characterization would be to describe the response as graded. Individuals exposed to concentrations above some level will exhibit a strong, overt behavioral response. Individuals below this point still attend to the cues, but they trade-off the overt response in favor of covert responses and continued activity (i.e., foraging or mating). We would predict that below some minimum detectable level, no overt or covert response would be present (Brown et al., 2001a). However, the minimum concentrations at which overt and/or covert behaviors are seen should be dependent on the individual's current physiological and/or motivation state. In addition, environmental conditions such as habitat complexity and ambient predation pressure would likely influence these threshold concentrations (Brown et al., 2001a,c; Marcus and Brown, 2003).
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ACKNOWLEDGEMENTS |
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We thank Antoine Leduc, Justin Golub, Patricia Foam, Isabelle Désormeaux, and James Grant for comments on earlier versions of this manuscript. All work reported herein was conducted in accordance with Concordia University Animal Care and Use Committee protocol #AC-2002-BROW. Funding was provided by Concordia University and the Natural Sciences and Engineering Research Council (NSERC) of Canada to G.E.B.
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