The nose knows: minnows determine predator proximity and density through detection of predator odours

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1 ANIMAL BEHAVIOUR, 26, 72, 927e932 doi:1.116/j.anbehav The nose knows: minnows determine predator proximity and density through detection of predator odours MAUD C. O. FERRARI, FRANÇOIS MESSIER & DOUGLAS P. CHIVERS Department of Biology, University of Saskatchewan (Received 16 December 25; initial acceptance 5 January 26; final acceptance 6 March 26; published online 14 August 26; MS. number: A1326R) Prey often face a behavioural trade-off between fitness-related activities and costly predator avoidance. Individuals that are able to assess their level of risk should maximize their fitness by allocating appropriate amounts of time and energy to avoid predators. The threat-sensitive predator avoidance hypothesis states that prey should respond to a given threat with an intensity that matches their level of risk. Prey fish are known to assess predation risk using predator odours. However, the level of sophistication of risk assessment based on predator odours is not well understood. We conducted two experiments to investigate whether fathead minnows, Pimephales promelas, assess proximity and density of pike, Esox lucius, predators based on pike odours. In experiment 1, we exposed pike-experienced minnows to either 6 ml of pike odour from 12 pike (i.e. 5 ml/pike), 6 ml of pike odour from two pike (i.e. 3 ml/pike) or a control of 6 ml of water. Minnows exposed to odours from two pike showed a more intense antipredator response than did minnows exposed to odours from 12 pike, demonstrating that minnows can detect individual pike in a mixture of odours from several pike. The fact that minnows responded with a greater intensity as the per-pike concentration increased while the overall concentration of pike odour remained constant, indicates that minnows can use odours to determine their relative proximity to predators. In experiment 2, we exposed pike-experienced minnows to either 5 ml/pike from each of 12 pike, 5 ml/pike from each of two pike or a water control. Minnows in the 12-pike treatment showed a stronger antipredator response than did minnows in the two-pike treatment, demonstrating that minnows can assess the relative density of predators using predator odours. These results demonstrate an amazing level of sophistication of predator odour assessment; they are the first to show that prey fish can use odours to determine predator proximity and relative density to respond to predators in a threat-sensitive manner. Ó 26 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Prey animals often face an important trade-off between spending time and energy for fitness-related activities, such as foraging or reproducing, and avoiding predation (Lima & Dill 199). To maximize their fitness, prey should adaptively respond to predation threats by assessing their own level of risk associated with each threat. Helfman (1989) proposed that prey should behave according to the degree of threat posed by their predators (threatsensitive predator avoidance hypothesis). This hypothesis has been tested and validated many times in a wide range of taxa, including freshwater isopods (Holomuzki & Short 199), mayflies (McIntosh et al. 1999), crustaceans (Wahle 1992), amphibians (Kats et al. 1994; Anholt et al. 1996; Puttlitz et al. 1999; Mathis & Vincent 2; Amo et al. Correspondence: M. C. O. Ferrari, Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK S7N 5E2, Canada ( maud.ferrari@usask.ca). 3e 3472/6/$3./ 24) and fish (Williams & Brown 1991; Hartman & Abrahams 2; Chivers et al. 21; Golub & Brown 23). For example, Puttlitz et al. (1999) showed that bigger Pacific treefrog, Hyla regilla, tadpoles display a weaker antipredator response to caged salamanders (Ambystoma macrodactylum) than do smaller tadpoles. Likewise, small American lobsters, Homarus americanus, are more likely to seek refuge than are large lobsters when encountering predatory sculpins (Myoxocephalus aenaeus) (Wahle 1992). These examples illustrate variations in antipredator responses and prey vulnerability due to growth or life histories. Threat-sensitive predator avoidance has also been demonstrated in moment-to-moment assessment of predation threat by prey individuals. For instance, Helfman (1989) demonstrated that three-spot damselfish, Stegastes planifrons, showed more intense antipredator responses to a model trumpetfish (Aulostomus maculatus) as the predator model was closer, larger or in a strike pose. Several studies have also shown that prey use the concentration 927 Ó 26 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

2 928 ANIMAL BEHAVIOUR, 72, 4 of chemical cues present in water to assess the level of danger in their environment. Kusch et al. (24) demonstrated that pike (Esox lucius)-experienced fathead minnows, Pimephales promelas, increased the intensity of their antipredator responses when exposed to increased concentrations of pike odour. These results suggest the possibility that minnows can determine either the relative proximity or relative density of predators based on predator odours. Kusch et al. (24) also demonstrated that experienced fathead minnows could determine the relative size of the pike using pike odours. We conducted two experiments to further investigate the level of sophistication of olfactory risk assessment by prey fish. METHODS Hypotheses and Predictions We tested the hypothesis that pike-experienced fathead minnows could use pike odour to determine proximity and relative density of predators. In experiment 1, we exposed pike-experienced fathead minnows to 6 ml of a mixture of pike odour made from either two pike (3 ml/pike) or 12 pike (5 ml/pike) or a water control. Given that the overall concentration of pike stimulus was constant between the two treatments (same mass of fish/litre/day), any difference observed must reflect that minnows can detect either a difference in density (2 versus 12 pike) or a difference in relative proximity. A higher-intensity response to the 12-pike stimulus over the two-pike stimulus would indicate that minnows show a stronger response to an increased density of predators irrespective of the overall concentration. A greaterintensity response to the odour of the two-pike stimulus however, would indicate that the minnows can determine relative predator proximity. Indeed, given that the overall concentration is the same but the per-pike concentration is higher (3 ml/pike versus 5 ml/pike), this can only reflect that the two pike are in closer proximity than the 12 pike. Results of experiment 1 provided evidence to support the hypothesis that minnows respond to predator proximity. Consequently, we performed a second experiment, where we kept predator proximity constant (i.e. same per-pike concentration between the two treatments) and manipulated predator density alone. We exposed minnows to either 5 ml of predator odour from each of two pike, 5 ml of predator odour from each of 12 pike or a water control. A greater-intensity response to the 12-pike stimulus would indicate that the minnows can determine the relative predator density, while no difference between treatments would indicate that minnows do not respond to differences in predator density (when proximity is constant). in four 15-litre tanks filled with dechlorinated tap water at about 15 C on a 14:1 h light:dark cycle. Minnows were fed with commercial fish flakes (Nutrafin basix, Rolf C. Hagen, Inc., Montreal, Quebec, Canada) ad libitum twice a day. Fish were kept in their holding tank for at least 1 days before testing to acclimate them to their new environment. In July 25, we seined northern pike from Pike Lake, where fathead minnows and pike co-occur. Juvenile pike (<1 year of age) and fathead minnows were always caught in the same seine. Several times, we caught as many as 1 juvenile pike in a single seining attempt, which encompassed approximately 15 m of shoreline, indicating that juvenile pike can be found at high density even though they are solitary predators. Pike were housed in the R. J. F. Smith Center for Aquatic Ecology at the University of Saskatchewan in a 6-litre flow-through pool filled with dechlorinated tap water maintained at about 12 C on a 14:1 h light:dark cycle. Pike were fed with live fathead minnows. To avoid cannibalism among the pike, we ensured that some minnows always remained in the pool. Pike Odour Collection Twelve juvenile pike of similar size ðx standard length SD ¼ 16:5 1:5 cmþ were transferred from the holding facility to the laboratory and housed individually in 37-litre tanks. Each tank contained dechlorinated tap water, an air stone and a corner filter, and was maintained at 18 C. Pike remained in these conditions for 7 days until odour stimulus collection. Prey animals often respond to predators based on the presence of conspecific cues in the predator s diet, so we fed pike red swordtails, Xiphophorus helleri, which lack the alarm substance recognized by minnows (Brown et al. 1995; Mathis & Smith 1993a), to eliminate diet cues as a factor in minnow antipredator responses (Korpi & Wisenden 21; Mirza & Chivers 23; Leduc et al. 24). We fed each pike two adult swordtails of similar size (ca. 4.5 cm standard length) once per day on days 2 and 4. According to Bevelhimer et al. (1985), the gut evacuation of a meal in juvenile pike takes 5 days at a temperature of 5 C. On day 8 (i.e. 4 days after pike were last fed), individual pike were rinsed and transferred into clean 37-litre tanks containing dechlorinated tap water and an air stone but no filter. Pike remained in their collection tank for 24 h and were then removed and returned to their initial holding pool. Stimulus bags were filled and frozen at 2 C until required (Mathis & Smith 1993a). Stimulus bags contained either 6 ml of pike odour from 12 pike (i.e. 5 ml from each of the 12 tanks) or 6 ml of pike odour from only two pike (i.e. 3 ml from two randomly chosen tanks, the two tanks being different for each bag). Test Fish For both experiments, pike-experienced fathead minnows were captured from Pike Lake, Saskatchewan, Canada, in September 25 (experiment 1) and October 25 (experiment 2) using seine nets. They were housed Experiment 1 We tested whether predator proximity or predator density is the overriding variable that minnows use to assess their level of risk by exposing minnows to the same overall volume of pike odour (6 ml), but varying the

3 FERRARI ET AL.: CHEMOSENSORY ASSESSMENT OF RISK 929 number of predators used to prepare the stimulus. The experiment consisted of trials where minnows were exposed to 6 ml of pike odour made from 12 pike (i.e. containing 5 ml/pike, 12 PO), 6 ml of pike odour made from two pike (i.e. containing 3 ml/pike, 2 PO) or 6 ml of dechlorinated tap water. All pike conditioned the water for the same time (24 h), so the 6 ml of pike odour had the same overall concentration (same mass of fish/litre/day). A greater response to the 12-pike treatment over the two-pike treatment would indicate that minnows adjust the intensity of their response using predator density. A greater-intensity response to the two-pike treatment over the 12-pike treatment would indicate that minnows rely primarily on relative proximity of predators to adjust the intensity of their responses. Remember that the overall concentration of pike odour was the same and hence the difference in per-pike concentration (3 ml/pike versus 5 ml/pike) must reflect a change in predator proximity. A total of 144 minnows ðx fork length SD ¼ 3:7 :4 cmþ were used. There were 16 replicates in each of the three treatments (48 trials), with three fish used per trial. The order of the treatments was randomized and the experimenter was blind to the treatments (i.e. the experimenter recording the fish s behaviour was blind to the identity of the stimulus injected in the tank). Procedure Twenty-four hours prior to testing, groups of three minnows, from the same holding tank, were transferred into 37-litre tanks ( cm). The tanks were filled with dechlorinated tap water and each contained a gravel substrate and an air stone, to which a 2.5- m-long piece of plastic tubing was attached to inject the stimulus. Fish were fed 1 h after their transfer and 1 h before testing. All trials were conducted between 12 and 153 hours. Observations consisted of an 8-min prestimulus and an 8-min poststimulus injection period. Before the prestimulus period, we withdrew and discarded 6 ml of water from the injection tubes (to remove any stagnant water) and then withdrew and retained an additional 6 ml. Following the prestimulus period, we injected 6 ml of either the 2 PO solution, the 12 PO solution or dechlorinated tap water. We used the retained tank water to slowly flush the stimuli into the tank. Once the stimuli were fully injected, we began the poststimulus observation period. We used a well-established protocol to quantify the antipredator behaviour of the minnows (e.g. Mathis & Smith 1993b; Ferrari et al. 25) based on the following three behavioural measures. Shoaling index. The shoaling index of the three fish every 15 s; 1: no fish within a body length of another; 2: two fish within a body length of each other; 3: all three fish within a body length of each other. Line crosses. The number of line crosses (using the 3 3- grid pattern drawn on the side of the tank) made by one of the three minnows (randomly chosen) during the conditioning period, using a click counter. Dashing. The presence or absence of dashing behaviour (a rapid burst of apparently disoriented swimming). An increase in shoaling index, a decrease in activity level and the presence of dashing are typical antipredator responses in minnows (review Chivers & Smith 1998). Experiment 2 In experiment 1, we found evidence to support the hypothesis that minnows rely primarily on predator proximity to adjust the intensity of their response to predator odours. Therefore, we conducted a second experiment to investigate whether minnows would respond to changes in predator density when predator proximity remained constant. We exposed minnows to 5 ml of pike odour from each of 12 pike (12 PO) or 5 ml of pike odour from each of two pike (2 PO), or 6 ml of dechlorinated tap water. To control for volume injected in the tank, an extra 5 ml of tank water was withdrawn and injected in the 2 PO treatment. If minnows show a greaterintensity response to the 12 PO treatment over the 2 PO treatment, we would have strong evidence for the ability of minnows to respond to relative predator density. However, the lack of a difference between treatments would indicate that minnows do not adjust their antipredator intensity in response to predator density. Indeed, the presence of predator cues alone might be enough to elicit a maximal response for a given proximity. The procedure used was the same as in experiment 1. A total of 144 minnows ðx fork length SD ¼ 3:2 :6 cmþ were tested; three fish were tested in each trial and there were 16 replicates in each treatment. Statistical analysis For both experiments, we calculated the change in shoaling index and line crosses from the prestimulus baseline. An increase in shoaling index as well as a reduction in line crosses would indicate an increase in antipredator responses. For experiment 1, the data were normally distributed but the variance was not homogeneous among treatments. For this reason, we performed a nonparametric KruskaleWallis test followed by nonparametric two-tailed ManneWhitney U tests for the three comparisons between treatments. The level of rejection (a) was modified following the Bonferroni correction and set to.17. For experiment 2, the data were normally distributed and the variance was homogenous among treatments. Thus, we performed a one-way ANOVA followed by three Bonferroni post hoc comparisons. For both experiments, the presence of dashing was analysed using a two-tailed Fisher s exact test. RESULTS Experiment 1 There was a significant effect of treatment for shoaling index (KruskaleWallis test: c 2 2 ¼ 34:1, N ¼ 16, P <.1)

4 93 ANIMAL BEHAVIOUR, 72, 4 and line crosses (c 2 2 ¼ 38:2, N ¼ 16, P <.1; Fig. 1). Fish exposed to the 2 PO treatment showed a more intense antipredator response than fish exposed to the control water treatment for shoaling index (ManneWhitney U test: U ¼ 3., N 1 ¼ N 2 ¼ 16, P <.1), line crosses (U ¼., P <.1) as well as dashing (Fisher s exact test: P <.1). Similarly, fish exposed to the 12 PO treatment showed a more intense antipredator response than fish exposed to the control water treatment for shoaling index (ManneWhitney U test: U ¼ 13.5, N 1 ¼ N 2 ¼ 16, P <.1), line crosses (U ¼ 6., P <.1) and dashing (Fisher s exact test: P ¼.176). Interestingly, fish exposed to the 2 PO treatment showed a more intense antipredator response than fish exposed to the 12 PO treatment (shoaling index: U ¼ 31., N 1 ¼ N 2 ¼ 16, P <.1; line crosses: U ¼ 17., N 1 ¼ N 2 ¼ 16, P <.1; dashing: P ¼.91). Experiment 2 There was an overall effect of treatment for shoaling index (ANOVA: F 2,45 ¼ 36.3, P <.1) and line crosses (F 2,45 ¼ 49.9, P <.1; Fig. 2). As in experiment 1, fish (a) (b) (c) Change in shoaling index Change in line crosses Proportion of fish dashing PO 12 PO Water 2 PO 12 PO Water 2 PO 12 PO Water Figure 1. Mean SE change in (a) shoaling index, (b) line crosses, and (c) proportion of fish dashing for minnows exposed to 6 ml of pike odour from 12 pike (12 PO), 6 ml of pike odour from two pike (2 PO) or 6 ml of dechlorinated tap water (water). N ¼ 16. exposed to the 12 PO treatment showed a stronger alarm response than fish exposed to the control water treatment for both shoaling index (Bonferroni post hoc comparison: difference ¼.5, N ¼ 16, P <.1) and line crosses (difference ¼ 35.9, N ¼ 16, P <.1). Fish exposed to the 2 PO treatment also showed a stronger alarm response than fish exposed to the control water for both shoaling index (difference ¼.29, N ¼ 16, P <.1) and line crosses (difference ¼ 2.4, N ¼ 16, P <.1). More interestingly, fish exposed to the 12 PO treatment displayed a stronger antipredator response than fish exposed to the 2 PO treatment (shoaling index: difference ¼.22, N ¼ 16, P ¼.2; line crosses: difference ¼ 15.4, N ¼ 16, P <.1). Dashing behaviours were observed only in the 12 PO treatment. Fish in the 12 PO treatment also dashed more than fish exposed to the control water treatment (Fisher s exact test: P ¼.68) and to the 2 PO treatment (P ¼.68). DISCUSSION The results of experiment 1 demonstrate that pikeexperienced fathead minnows have the ability to differentiate individual pike in a mixture of odours of several pike, and moreover, can assess the relative concentration of the odour from each pike. Indeed, when given the same volume of two pike solutions that had the same overall concentration, minnows showed a stronger antipredator response to the odour made from two pike than the one made from 12 pike. The per-pike concentration was higher in the 2 PO treatment (3 ml/pike) than in the 12 PO treatment (5 ml/pike). The 2 PO solution containing the higher per-pike concentrations almost certainly represents the odour of two pike being in closer proximity to the minnows, hence representing a bigger threat for the minnows. The 12 PO solution did not seem to represent a bigger danger than the 2 PO solution, despite the high number of pike used to make the solution. Thus, minnows must have been able to assess each pike s odour concentration and hence responded with a higher intensity to predators that were in closer proximity. The results of experiment 2 showed that minnows also respond to the number of pike detected. Indeed, when the per-pike concentration was kept constant (i.e. 5 ml/pike in both 12 PO and 2 PO treatments), minnows showed a more intense antipredator response to the 12 PO treatment than to the 2 PO treatment. This demonstrates the ability of minnows to show stronger antipredator responses when the relative density of the predator increases. Minnows, and probably many prey animals, have an amazing ability to gain information about their predators using chemical information. Kusch et al. (24) already demonstrated that minnows could assess the size of a pike based on the pike s odour. Indeed, they found that minnows showed a more intense antipredator response to small pike than to larger pike and they ruled out the use of concentration in the assessment of size, given that bigger pike would release more odour than would smaller ones. However, a small pike represents a bigger threat for small minnows, since bigger pike actually

5 FERRARI ET AL.: CHEMOSENSORY ASSESSMENT OF RISK 931 (a) (b) (c) Change in shoaling index Change in line crosses Proportion of fish dashing ' PO 12 PO Water 2' PO 12 PO Water 2' PO 12 PO Water Figure 2. Mean SE change in (a) shoaling index, (b) line crosses, and (c) proportion of fish dashing for minnows exposed to 6 ml of pike odour from 12 pike (12 PO), 1 ml of pike odour from two pike (2 PO) or 6 ml of dechlorinated tap water (water). N ¼ 16. consume bigger prey species (Kusch et al. 24). Mathis & Smith (1993a) and Brown et al. (1995) showed that minnows know the diet of a pike based on the presence of conspecific alarm cues in the predator odour. This information also allows minnows to label unknown fish as potential predators. The information carried by predator odours allow prey to accurately assess their level of risk and respond to predation threats in a threat-sensitive manner. It is adaptive for prey fish to respond more to a size class of predator that is more likely to prey on them. Similarly, it is adaptive to display a stronger antipredator response to close-range predators than to more distant ones, and to display a stronger antipredator response when detecting a large number of predators versus a few. Many aquatic organisms, including fish, do not show an innate recognition of their predators (Mathis et al. 1993; Chivers & Smith 1994). Thus, learning is a necessary step for those prey species to respond to predation threats. Ferrari & Chivers (26) showed that experience to different predation situations shaped the intensity of the fright responses displayed by fathead minnows. But, in order to display adaptive antipredator responses to predation threat, prey must survive each predatory encounter. Thus, predation represents a strong evolutionary force shaping the efficiency and content of learning. Predator odours seem to be the messengers of information that prey have been shaped to decrypt and learn, to increase their survival. Fathead minnows are known to use predator odours to gain information about a predator s diet (Mathis & Smith 1993a) and size (Kusch et al. 24). The results of the present study also show that minnows can detect their proximity to predators and the relative density of predators using odours alone. What else is left for us to discover on the amount of information acquired by prey species in predator odours? The fathead minnow/ pike predator/prey system has become the model system for studying predator odour recognition (Chivers & Smith 1993; Mathis & Smith 1993a, b; Mathis et al. 1993; Brown et al. 1995; Kusch et al. 24). Indeed, a look at the latest review on chemosensory assessment of risk by prey animals published by Kats & Dill (1998) indicates nothing that comes close to this level of sophistication. To our knowledge, minnows are no better at chemosensory assessment than are other fish or other vertebrates, particularly mammals. Researchers studying antipredator behaviour need to consider how important chemosensory assessment of risk may be in their systems. Acknowledgments The Natural Sciences and Engineering Research Council of Canada and the University of Saskatchewan provided financial support to D.P. Chivers, M.C.O. Ferrari and F. Messier. All work reported herein was conducted in accordance with the University of Saskatchewan Committee of Animal Care and Supply protocol number References Amo, L., Lopez, P. & Martin, J. 24. Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Animal Behaviour, 67, 647e653. Anholt, B. R., Skelly, D. K. & Werner, E. E Factors modifying antipredator behavior in larval toads. Herpetologica, 52, 31e313. Bevelhimer, M. S., Stein, R. A. & Carline, R. F Assessing significance of physiological differences among three esocids with a bioenergetics model. Canadian Journal of Fisheries and Aquatic Sciences, 42, 57e69. Brown, G. E., Chivers, D. P. & Smith, R. J. F Localized defecation of pike: a response to labelling by cyprinid alarm pheromone? Behavioral Ecology and Sociobiology, 36, 15e11. Chivers, D. P. & Smith, R. J. F The role of olfaction in chemosensory-based predator recognition in the fathead minnow, Pimephales promelas. Journal of Chemical Ecology, 19, 623e633. Chivers, D. P. & Smith, R. J. F The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas. Journal of Fish Biology, 44, 273e285. Chivers, D. P. & Smith, R. J. F Chemical alarm signaling in aquatic predator/prey interactions: a review and prospectus. Ecoscience, 5, 338e352. Chivers, D. P., Mirza, R. S., Bryer, P. J. & Kiesecker, J. M. 21. Threat-sensitive predator avoidance by slimy sculpins: understanding

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