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Certainty and the cognitive ecology of generalization of predator recognition
Animal Behaviour 111 (2016) 207e211
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Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
Certainty and the cognitive ecology of generalization of predator recognition Maud C. O. Ferrari a, *, Adam L. Crane b, Douglas P. Chivers b a b
Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, Canada Department of Biology, University of Saskatchewan, Saskatoon, Canada
a r t i c l e i n f o Article history: Received 23 June 2015 Initial acceptance 18 August 2015 Final acceptance 17 September 2015 Available online MS. number: A15-00541R Keywords: antipredator behaviour generalized predator recognition predatoreprey interaction risk assessment tadpole uncertainty
Prey exposed to unknown species have the ability to label them as predatory if they are closely related to a predator already known to the prey. This phenomenon is coined generalization of predator recognition. While increasing the threat level of the known predator widens the generalization window (i.e. prey respond to species that are more distantly related), nothing is known about whether or not certainty associated with the identity of the known predator affects the generalization window. Here, we compared the generalization of tadpoles that were conditioned once (low certainty) or five times (high certainty) to recognize the odour of a rainbow trout, Oncorhynchus mykiss, and subsequently tested them for their response to rainbow trout, brown trout, Salmo trutta (closely related), brook trout, Salvelinus fontinalis (more distantly related) or goldfish, Carassius auratus. We found that the window shifted in two opposite ways, with high-certainty tadpoles responding more to brown trout but less to brook trout, when compared to their low-certainty counterparts. Our results highlight the nonlinear nature of stimuli generalization. We discuss potential mechanisms for our results and provide directions for future research aimed at understanding the role of uncertainty in antipredator decision making. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Predation risk is highly variable in space and time (Lima, 2002; Lima & Bednekoff, 1999; Sih, Ziemba, & Harding, 2000), and the community of potential predators to which prey are exposed at any point in time might change on an hourly, daily, seasonal or yearly basis. In the face of this uncertain environment, some prey have developed fixed or inducible defences, such as armour and defensive spines (Hammill, Rogers, & Beckerman, 2008). Others decrease the predation pressure on certain life stages, by having early or late life-history transitions (Abrams & Rowe, 1996; Benard, 2004; Chivers et al., 2001). For instance, amphibian embryos can hatch early in the presence of egg predators (Warkentin, 1995) but can delay hatching in the presence of larval predators (Sih & Moore, 1993). Many prey species can modulate their exposure to predation risk via behavioural adaptations (Lima & Dill, 1990), trading off the costs and benefits of predator vigilance against foraging or mating. A prerequisite for prey to adaptively respond to predation threats is for them to recognize predators as such. Whether the recognition is based on an innate recognition template (Blumstein,
* Correspondence: M. C. O. Ferrari, Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK S7N 5B4, Canada. E-mail address: [email protected] (M. C. O. Ferrari).
Daniel, Schnell, Ardron, & Evans, 2002) or requires experience (Blumstein, Daniel, & Springett, 2004; Cornell, Marzluff, & Pecoraro, 2012), prey first need to recognize the predator as a threat before they can engage in behavioural, morphological or lifehistory adaptations that will decrease their likelihood of being detected or captured by predators. However, some predator-naïve prey have been shown to respond to predators encountered for the very first time, if they have experience with phylogenetic relatives of that predators. For instance, tammar wallabies, Macropus eugenii, do not innately recognize red foxes, Vulpes vulpes, feral cats, Felis catus, or juvenile goats as a threat. However, once they are taught to recognize the red fox as a threat, they display antipredator response towards feral cats as well, but not to the distantly related goat (Griffin, Evans, & Blumstein, 2001). Based on the similarity between a known predator (fox) and an unknown species (cat), the tammars are making an ‘educated guess’ on the likely threatening nature of the cat. This phenomenon is coined generalization of predator recognition and has since been shown in eutherian mammals (Stankowich & Coss, 2007), reptiles (Webb, Du, Pike, & Shine, 2009), amphibians (Ferrari & Chivers, 2009) and fishes (Ferrari, Gonzalo, Messier, & Chivers, 2007; Mitchell, McCormick, Chivers, & Ferrari, 2013), using either visual or chemical cues of predators. For instance, fathead minnows, Pimephales promelas, taught to recognize the odour of a lake trout, Salvelinus namaycush, as a
http://dx.doi.org/10.1016/j.anbehav.2015.10.026 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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threat, subsequently displayed an antipredator response to the odour of closely related brook trout, Salvelinus fontinalis, and rainbow trout, Oncorhynchus mykiss, but not to the odour of distantly related northern pike, Esox lucius, or suckers, Catostomus commersoni. In contrast, minnows that were not taught to recognize the odour of lake trout as a threat did not respond to any of the odours from the above-mentioned species (Ferrari et al., 2007). In a subsequent study, Ferrari, Messier, and Chivers (2008) showed that the stimulus generalization was dependent on the risk level associated with the learned predator, with prey displaying a broader generalization pattern when they were taught that a predator was a higher threat. Understanding the role of uncertainty has recently come to the forefront of research on antipredator decision making (Chivers, Mathiron, Sloychuk, & Ferrari, 2015; Dall, Giraldeau, Olsson, McNamara, & Stephens, 2005; Munoz & Blumstein, 2012). The term ‘uncertainty’ applies to any situation where the individual may doubt the relationship between the detection of a particular stimulus and the particular response (type, intensity) that must ensue. This uncertainty could come from a time delay since the acquisition of the response (i.e. is this relationship still valid?), a change in context, whether spatial or social (i.e. is the relationship valid in this situation, in this location?) or can simply be a product of the acquisition method itself (i.e. is it the right response to that stimulus?). Uncertainty may lead to a weakening of the response to the stimulus or a switch to a similar, lower-cost response, reflecting the relative costs of displaying a full response in an inappropriate situation. Our work here investigates the effect of certainty on the generalization patterns of prey. Prey species have a number of options to learn to recognize predators. For instance, they can learn from direct encounters with predators, by observing experienced conspecifics displaying fright responses to predator cues (Crane & Ferrari, 2013), or they can rely on publicly available information, such as injured conspecific cues (Chivers & Smith, 1998; Wisenden & Chivers, 2006). However, personal, social and public information provide different levels of reliability (Campobello & Sealy, 2011), and while they may all lead to learning, not all learning outcomes are equal (Crane & Ferrari, 2015). A number of aquatic species can learn to recognize a novel predator via the pairing of the predator cue (sight, smell or sound) with cues from injured conspecifics (Mathis & Smith, 1993). This learning paradigm is highly efficient, requiring only a single pairing (one conditioning) for the prey to subsequently learn to avoid the predator (Ferrari, Wisenden, & Chivers, 2010). These injured conspecific cues are released in the water column via mechanical damage to the skin, usually following a predation attempt. While the nature of the cues makes them a reliable indicator of risk, the pairing leading to learned information may be subject to errors if the cues are paired with a non-predatorrelated cue, making the relationship between risk and the learned cue potentially questionable. Such uncertainty is detectable not only in the intensity of the learned response just after learning, but in the duration for which the learned information is used in decision making. For instance, woodfrog tadpoles, Lithobates sylvaticus, that were conditioned multiple times to recognize a salamander predator (Ambystoma tigrinum), maintained their antipredator response for longer than those that were conditioned only once, despite the fact that tadpoles from both groups responded to the predator with the same intensity when tested shortly after the lova , Brown, & Chivers, 2012). learning events (Ferrari, Vrte In this experiment, we investigated how increased certainty with regards to a learned predator would affect the ability of prey to generalize their response to novel, closely related predators. We hypothesized that increased certainty with regards to the learned predator, via repeated learning opportunities, would affect the generalization window of prey. However, predictions about the
direction of the change in generalization are complex. On one hand, prey being certain about a known predator could widen their generalization window; that is, prey could respond to a greater diversity of closely related species that would likely share similar hunting tactics or diet. In this case, the change in generalization would indicate that generalization is part of an antipredator strategy aimed to decrease the chance of death upon encountering new predators. On the other hand, prey that are more certain about a known predator could narrow their generalization window and respond only to the known predator, thus indicating that the original wide response pattern may be the result of a lack of discriminability or specificity with regards to the cues used to identify the predator. Finally, it is possible that certainty about the predator does not affect the outcome of generalization. This would indicate that the response to other predators is simply a by-product of a partial match between the known predator and the novel species. METHODS Ethics Statement All work carried out herein was in accordance with the University of Saskatchewan Committee on Animal Care and Supply (protocol 20060014). Experimental Overview All experiments were carried out with wild tadpoles and were performed outdoors under naturally fluctuating light and temperature conditions. Woodfrog tadpoles (Gosner stage 25) (Gosner, 1960) were conditioned, via injured conspecific cues, to recognize the odour of a predatory rainbow trout either once or five times. Tadpoles were then tested for their antipredator response to the odour of rainbow trout (learned predator), brown trout, Salmo trutta (a closely related trout species), and brook trout (a more distantly related trout species) and a distantly related goldfish, Carassius auratus. The response to goldfish controlled simultaneously for the injection disturbance and the introduction of an odour into the test arena. Phylogeny analyses indicate that although both rainbow, brown and brook trout are all heterogeneric species, Salvelinus was the first genus to diverge, followed by Salmo and then Oncorhynchus, leaving Salmo more closely related to Oncorhynchus than Salvelinus (Murata, Takasaki, Saitoh, & Okada, 1993). Stimulus Collection All trout were obtained from the Cold Lake Fish Hatchery (AB, Canada) and fed trout chow, while goldfish were obtained from a local pet store and fed goldfish flakes. All fishes were starved for 48 h prior to odour collection to eliminate the potential effect of diet. Fish odours were collected by placing individual fish in 15 litres of water for 24 h; the cue collection container was equipped with an airstone but no filter. We used a minimum of four fish of each species (rainbow trout, brown trout, brook trout and goldfish) to prepare each odour. The fish were size-matched (total length ~15 cm) to ensure consistency in concentration between species. The fish stimuli were then frozen at 20 C until needed. Tadpoles came from egg clutches collected from a local pond and raised, under natural conditions, until stage 25. Injured tadpoles cues were prepared a few minutes prior to injection, by euthanizing tadpoles with a rapid blow to the head and crushing them with a mortar and pestle. The paste was then diluted to obtain a concentration of three tadpoles per 20 ml of water, and the solution was filtered through glass floss prior to injection.
M. C. O. Ferrari et al. / Animal Behaviour 111 (2016) 207e211
Predator-naïve tadpoles, raised from eggs from six clutches collected from the wild, were maintained in pools filled with conditioned well water (hereafter water) and fed alfalfa pellets. Prior to the start of the experiment, 24 7.4-litre pails (~20 20 cm base) were filled with 4 litres of water and 20 tadpoles, randomly chosen, were placed in each pail. Half the pails were randomly allocated to the ‘1-conditioning group’, while the other half would become the ‘5-conditionings group’. Conditionings took place over 5 days, with one conditioning on day 1, and two conditionings each on day 2 and day 3. Conditionings occurred at random times between 1100 and 1800 hours. Tadpoles from the 5-conditionings group received 20 ml of rainbow trout odour paired 20 ml of injured tadpole cues (three crushed tadpoles/20 ml) at every conditioning. Tadpoles from the 1-conditioning group received 40 ml of water during the first four conditioning events and 20 ml of rainbow trout odour paired with 20 ml of injured tadpole cues during the last conditioning. Each pail received a 100% water change at the end of each day. Food was added to the pails after each water change. Testing The day following the end of the conditioning phase, we randomly selected tadpoles from each pail, placed them individually in 0.5-litre plastic cups (8 cm diameter, 12 cm high) filled with 0.5 litres of water and allowed them to acclimate for 1 h. We observed tadpole behaviour for 4 min to obtain a baseline activity level. We recorded the number of times the tadpoles crossed a medial line on the bottom of the cup: a tadpole was considered to have crossed when its entire body crossed over the line. Following this observation period, we injected 5 ml of rainbow trout, brown trout, brook trout or goldfish odour and observed the behaviour of the tadpole for another 4 min. Tadpoles exhibiting antipredator responses are expected to decrease activity (make fewer line crosses) when compared to their prestimulus baseline. Decreased activity is a common antipredator response in prey species (Lima & Dill, 1990). The order of treatment and pails were randomized and the observer was blind to the treatment while collecting data. We tested a total of 258 tadpoles (N ¼ 27e39/treatment, N ¼ 5e12/ pail). Statistical Analysis We first tested for behavioural bias among treatment groups prior to the introduction of the stimulus. We carried out a threeway nested ANOVA testing the effect of number of conditioning (1 versus 5) and test cue (rainbow trout, brown trout, brook trout or goldfish odour) on the prestimulus data (prestimulus number of line crosses). We added ‘pail’ as a nested factor (type I sum of squares), as tadpoles conditioned in the same pail cannot be considered independent, thus making pail, and not tadpole, the replicative unit. A proportion change in activity from the prestimulus baseline ((post pre)/pre) was computed and used as our response variable in subsequent analyses. We performed a threeway nested ANOVA, once again testing for conditioning and test cues on the response of the tadpoles. Subsequent two-way nested ANOVAs were carried out to investigate significant interaction patterns. All data met parametric assumptions. Data were analysed with SPSS 22 (IBM, Armonk, NY, U.S.A.). RESULTS Tadpoles did not differ in their behavioural baseline prior to stimulus injection (three-way nested ANOVA: conditioning:
F1,20 ¼ 0.1, P ¼ 0.9; cue: F3,231 ¼ 2.0, P ¼ 0.1; conditioning)cue: F3,231 ¼ 1.2, P ¼ 0.3; pail: F22,228 ¼ 1.3, P ¼ 0.2). The behavioural responses of tadpoles were affected by both conditioning regime and test cue (three-way nested ANOVA: conditioning)cue: F3,208 ¼ 6, P ¼ 0.001; Fig. 1). The number of conditionings did not affect the response of tadpoles to the learned rainbow trout (two-way nested ANOVA: conditioning: F1,10 ¼ 0.1, P ¼ 0.81; pail: F22,38 ¼ 1.1, P ¼ 0.44) or to the distantly related goldfish (conditioning: F1,14 ¼ 0.1, P ¼ 0.68; pail: F22,34 ¼ 1.6, P ¼ 0.12). However, the number of conditionings affected the tadpoles' responses to the other trout species in opposite ways. Tadpoles that were conditioned five times to recognize the rainbow trout showed stronger responses to the closely related brown trout than did tadpoles conditioned only once (conditioning: F1,7 ¼ 0.7, P ¼ 0.04; pail: F20,39 ¼ 0.9, P ¼ 0.49). In fact, while tadpoles conditioned once showed a weaker response to the brown trout as compared to the learned rainbow trout (Tukey post hoc test: P ¼ 0.047), tadpoles conditioned five times did not differ in their response to rainbow and brown trout (P ¼ 0.89). Conversely, tadpoles conditioned five times to recognize the rainbow trout displayed weaker responses to the more distantly related brook trout than did tadpoles conditioned only once (conditioning: F1,15 ¼ 6.7, P ¼ 0.02; pail: F21,34 ¼ 1.5, P ¼ 0.10).
DISCUSSION The data presented here provide evidence that the generalization pattern of tadpoles is affected by the information known about the learned predator. While previous studies suggested that the risk level associated with the predator could affect the breadth of the generalization window, our results also indicate that the level of certainty associated with the predator affects this window. When tadpoles were conditioned only once to recognize rainbow trout, they displayed the response pattern predicted from previous studies: their response decreased with increasing phylogenetic
0 Mean proportion change in line crosses
Conditioning
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30
32
32
29
39
38
31
27
–0.2
–0.4
* –0.6
* Rainbow trout Brown trout Brook trout
Goldfish
Figure 1. Mean ±SE proportion change in line crosses of tadpoles that were conditioned to recognize a predatory rainbow trout either one time (open bars) or five times (solid bars), and were subsequently exposed to the odour of a rainbow trout, a closely related brown trout, a less closely related brook trout and a distantly related goldfish. Asterisks indicate differences between conditioning groups at a ¼ 0.05. Numbers above bars indicate sample sizes.
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distance between the novel species and the learned predator. However, increasing certainty about this predator affected the generalization in two opposite ways: it widened the generalization window of closely related species, while narrowing the window of more distantly related species. Indeed, tadpoles conditioned five times to recognize the rainbow trout showed a stronger response to the brown trout but a lower response to brook trout compared to tadpoles conditioned only once. Multiple conditionings would give tadpoles opportunities to refine their recognition of the rainbow trout signature, just as multiple training events improve recognition of complex stimuli (Cave, Bost, & Cobb, 1996). As the recognition of the learned stimulus becomes more accurate, one would expect that the related stimuli would become more distinct from the learned one, and hence should not warrant a strong response. This line of thinking would explain why the 5-conditioning tadpoles decreased their response to brook trout. Counterintuitively, tadpoles in the 5conditioning group also increased their response to brown trout, a close relative. The increase in certainty thus appears to work in a two-tier system, where prey increase their generalization to a close relative, while decreasing their response to a more distantly related one. This pattern could be the results of a costebenefit trade-off where prey have to manage uncertainty. Alternatively, the behavioural data might not provide an accurate picture of the threat level perceived by the tadpoles if the response to the learned predator is already maximized. In other words, the asymptotic nature of antipredator response may mask a gradient between the response to rainbow and brown trout. But this may be a moot point if individual survival is based on actual responses. Future work should test whether or not tadpoles with greater certainty (those in the 5conditioning group in our study) perceive the rainbow and brown trout as similar threats through time. We know that high-level threats elicit a stronger and longer response through time, compared to lower-level ones (Ferrari et al., 2012). Being able to generalize from a known threat to unknown species is critical, especially for prey living in highly biodiverse environments. It avoids the necessity of encountering an unknown predator (and surviving the encounter) before avoiding it. Generalization patterns are filled with stimuli and sensory biases (Ghirlanda & Enquist, 2003). Whether or not prey living in temperate versus tropical ecosystems would display different generalization patterns due to the variation in closely related predators in their environment is unknown. Similarly, whether our observed pattern would hold if the stimuli were visual, rather than olfactory, is also unknown. Prey from different taxa may acquire different amounts of information about a predator at each presentation, some learning much faster and others learning much slower than tadpoles (Crane & Ferrari, 2013). How these differences in learning and information acquisition might affect the pattern seen in our experiment is unknown. In any case, generalization of predator recognition probably plays a key role in native prey responding to novel, invasive predators. Predator naïvety is put forward as a main mechanism behind the failure of native prey to respond to invasive predators (Sih et al., 2010). If prey are able to take information from local threats and use them to respond to novel threats, then they might be less susceptible to invasions. Maintaining a wide generalization frame would appear beneficial, as it would protect against a greater variety of predators. Our results highlight that certainty might reduce the width of this frame and strengthen the response to novel threats that are still recognized. Whether this shift in generalization is adaptive or not in the context of invasion is still to be determined. Our work provides insights on how prey animals respond to unknown predators upon their first encounter with them. The first encounter is often considered the most critical predator/prey
encounter. Failure to respond appropriately could result in death, but responding to myriad nonpredators constitutes a waste of time and resources, particularly for young prey animals that are trying to feed and establish territories. For cognitive ecologists trying to understand how predator recognition develops, the next challenge will be to understand how prey incorporate multiple pieces of information during their first few encounters. Failure of the predator to attack the prey could quickly result in labelling the predator as a nonthreat through latent inhibition (Hazlett, 2003; Mitchell, McCormick, Ferrari, & Chivers, 2011). In contrast, several ‘close calls’ could reinforce the importance of the predator as a high risk. The reality of most predator/prey systems is that prey will be exposed to uncertainty with predators that attack intermittently. Sometimes predators are hungry, other times they are not. Sometimes there are alternative prey around, other times there are not. Future work should explore how prey adjust the intensity of their responses based on learning and generalization when given conflicting information (Ferrari & Chivers, 2006).
Acknowledgments for We thank Glen and Jean for access to the field site and Chloe her invaluable support. We thank Janelle Sloychuk and the Cold Lake Fish Hatchery for providing the fish odour. This work was funded by the Natural Sciences and Engineering Research Council of Canada.
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Certainty and the cognitive ecology of generalization of predator recognition Maud C. O. Ferrari a, *, Adam L. Crane b, Douglas P. Chivers b a b
Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, Canada Department of Biology, University of Saskatchewan, Saskatoon, Canada
a r t i c l e i n f o Article history: Received 23 June 2015 Initial acceptance 18 August 2015 Final acceptance 17 September 2015 Available online MS. number: A15-00541R Keywords: antipredator behaviour generalized predator recognition predatoreprey interaction risk assessment tadpole uncertainty
Prey exposed to unknown species have the ability to label them as predatory if they are closely related to a predator already known to the prey. This phenomenon is coined generalization of predator recognition. While increasing the threat level of the known predator widens the generalization window (i.e. prey respond to species that are more distantly related), nothing is known about whether or not certainty associated with the identity of the known predator affects the generalization window. Here, we compared the generalization of tadpoles that were conditioned once (low certainty) or five times (high certainty) to recognize the odour of a rainbow trout, Oncorhynchus mykiss, and subsequently tested them for their response to rainbow trout, brown trout, Salmo trutta (closely related), brook trout, Salvelinus fontinalis (more distantly related) or goldfish, Carassius auratus. We found that the window shifted in two opposite ways, with high-certainty tadpoles responding more to brown trout but less to brook trout, when compared to their low-certainty counterparts. Our results highlight the nonlinear nature of stimuli generalization. We discuss potential mechanisms for our results and provide directions for future research aimed at understanding the role of uncertainty in antipredator decision making. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Predation risk is highly variable in space and time (Lima, 2002; Lima & Bednekoff, 1999; Sih, Ziemba, & Harding, 2000), and the community of potential predators to which prey are exposed at any point in time might change on an hourly, daily, seasonal or yearly basis. In the face of this uncertain environment, some prey have developed fixed or inducible defences, such as armour and defensive spines (Hammill, Rogers, & Beckerman, 2008). Others decrease the predation pressure on certain life stages, by having early or late life-history transitions (Abrams & Rowe, 1996; Benard, 2004; Chivers et al., 2001). For instance, amphibian embryos can hatch early in the presence of egg predators (Warkentin, 1995) but can delay hatching in the presence of larval predators (Sih & Moore, 1993). Many prey species can modulate their exposure to predation risk via behavioural adaptations (Lima & Dill, 1990), trading off the costs and benefits of predator vigilance against foraging or mating. A prerequisite for prey to adaptively respond to predation threats is for them to recognize predators as such. Whether the recognition is based on an innate recognition template (Blumstein,
* Correspondence: M. C. O. Ferrari, Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK S7N 5B4, Canada. E-mail address: [email protected] (M. C. O. Ferrari).
Daniel, Schnell, Ardron, & Evans, 2002) or requires experience (Blumstein, Daniel, & Springett, 2004; Cornell, Marzluff, & Pecoraro, 2012), prey first need to recognize the predator as a threat before they can engage in behavioural, morphological or lifehistory adaptations that will decrease their likelihood of being detected or captured by predators. However, some predator-naïve prey have been shown to respond to predators encountered for the very first time, if they have experience with phylogenetic relatives of that predators. For instance, tammar wallabies, Macropus eugenii, do not innately recognize red foxes, Vulpes vulpes, feral cats, Felis catus, or juvenile goats as a threat. However, once they are taught to recognize the red fox as a threat, they display antipredator response towards feral cats as well, but not to the distantly related goat (Griffin, Evans, & Blumstein, 2001). Based on the similarity between a known predator (fox) and an unknown species (cat), the tammars are making an ‘educated guess’ on the likely threatening nature of the cat. This phenomenon is coined generalization of predator recognition and has since been shown in eutherian mammals (Stankowich & Coss, 2007), reptiles (Webb, Du, Pike, & Shine, 2009), amphibians (Ferrari & Chivers, 2009) and fishes (Ferrari, Gonzalo, Messier, & Chivers, 2007; Mitchell, McCormick, Chivers, & Ferrari, 2013), using either visual or chemical cues of predators. For instance, fathead minnows, Pimephales promelas, taught to recognize the odour of a lake trout, Salvelinus namaycush, as a
http://dx.doi.org/10.1016/j.anbehav.2015.10.026 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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threat, subsequently displayed an antipredator response to the odour of closely related brook trout, Salvelinus fontinalis, and rainbow trout, Oncorhynchus mykiss, but not to the odour of distantly related northern pike, Esox lucius, or suckers, Catostomus commersoni. In contrast, minnows that were not taught to recognize the odour of lake trout as a threat did not respond to any of the odours from the above-mentioned species (Ferrari et al., 2007). In a subsequent study, Ferrari, Messier, and Chivers (2008) showed that the stimulus generalization was dependent on the risk level associated with the learned predator, with prey displaying a broader generalization pattern when they were taught that a predator was a higher threat. Understanding the role of uncertainty has recently come to the forefront of research on antipredator decision making (Chivers, Mathiron, Sloychuk, & Ferrari, 2015; Dall, Giraldeau, Olsson, McNamara, & Stephens, 2005; Munoz & Blumstein, 2012). The term ‘uncertainty’ applies to any situation where the individual may doubt the relationship between the detection of a particular stimulus and the particular response (type, intensity) that must ensue. This uncertainty could come from a time delay since the acquisition of the response (i.e. is this relationship still valid?), a change in context, whether spatial or social (i.e. is the relationship valid in this situation, in this location?) or can simply be a product of the acquisition method itself (i.e. is it the right response to that stimulus?). Uncertainty may lead to a weakening of the response to the stimulus or a switch to a similar, lower-cost response, reflecting the relative costs of displaying a full response in an inappropriate situation. Our work here investigates the effect of certainty on the generalization patterns of prey. Prey species have a number of options to learn to recognize predators. For instance, they can learn from direct encounters with predators, by observing experienced conspecifics displaying fright responses to predator cues (Crane & Ferrari, 2013), or they can rely on publicly available information, such as injured conspecific cues (Chivers & Smith, 1998; Wisenden & Chivers, 2006). However, personal, social and public information provide different levels of reliability (Campobello & Sealy, 2011), and while they may all lead to learning, not all learning outcomes are equal (Crane & Ferrari, 2015). A number of aquatic species can learn to recognize a novel predator via the pairing of the predator cue (sight, smell or sound) with cues from injured conspecifics (Mathis & Smith, 1993). This learning paradigm is highly efficient, requiring only a single pairing (one conditioning) for the prey to subsequently learn to avoid the predator (Ferrari, Wisenden, & Chivers, 2010). These injured conspecific cues are released in the water column via mechanical damage to the skin, usually following a predation attempt. While the nature of the cues makes them a reliable indicator of risk, the pairing leading to learned information may be subject to errors if the cues are paired with a non-predatorrelated cue, making the relationship between risk and the learned cue potentially questionable. Such uncertainty is detectable not only in the intensity of the learned response just after learning, but in the duration for which the learned information is used in decision making. For instance, woodfrog tadpoles, Lithobates sylvaticus, that were conditioned multiple times to recognize a salamander predator (Ambystoma tigrinum), maintained their antipredator response for longer than those that were conditioned only once, despite the fact that tadpoles from both groups responded to the predator with the same intensity when tested shortly after the lova , Brown, & Chivers, 2012). learning events (Ferrari, Vrte In this experiment, we investigated how increased certainty with regards to a learned predator would affect the ability of prey to generalize their response to novel, closely related predators. We hypothesized that increased certainty with regards to the learned predator, via repeated learning opportunities, would affect the generalization window of prey. However, predictions about the
direction of the change in generalization are complex. On one hand, prey being certain about a known predator could widen their generalization window; that is, prey could respond to a greater diversity of closely related species that would likely share similar hunting tactics or diet. In this case, the change in generalization would indicate that generalization is part of an antipredator strategy aimed to decrease the chance of death upon encountering new predators. On the other hand, prey that are more certain about a known predator could narrow their generalization window and respond only to the known predator, thus indicating that the original wide response pattern may be the result of a lack of discriminability or specificity with regards to the cues used to identify the predator. Finally, it is possible that certainty about the predator does not affect the outcome of generalization. This would indicate that the response to other predators is simply a by-product of a partial match between the known predator and the novel species. METHODS Ethics Statement All work carried out herein was in accordance with the University of Saskatchewan Committee on Animal Care and Supply (protocol 20060014). Experimental Overview All experiments were carried out with wild tadpoles and were performed outdoors under naturally fluctuating light and temperature conditions. Woodfrog tadpoles (Gosner stage 25) (Gosner, 1960) were conditioned, via injured conspecific cues, to recognize the odour of a predatory rainbow trout either once or five times. Tadpoles were then tested for their antipredator response to the odour of rainbow trout (learned predator), brown trout, Salmo trutta (a closely related trout species), and brook trout (a more distantly related trout species) and a distantly related goldfish, Carassius auratus. The response to goldfish controlled simultaneously for the injection disturbance and the introduction of an odour into the test arena. Phylogeny analyses indicate that although both rainbow, brown and brook trout are all heterogeneric species, Salvelinus was the first genus to diverge, followed by Salmo and then Oncorhynchus, leaving Salmo more closely related to Oncorhynchus than Salvelinus (Murata, Takasaki, Saitoh, & Okada, 1993). Stimulus Collection All trout were obtained from the Cold Lake Fish Hatchery (AB, Canada) and fed trout chow, while goldfish were obtained from a local pet store and fed goldfish flakes. All fishes were starved for 48 h prior to odour collection to eliminate the potential effect of diet. Fish odours were collected by placing individual fish in 15 litres of water for 24 h; the cue collection container was equipped with an airstone but no filter. We used a minimum of four fish of each species (rainbow trout, brown trout, brook trout and goldfish) to prepare each odour. The fish were size-matched (total length ~15 cm) to ensure consistency in concentration between species. The fish stimuli were then frozen at 20 C until needed. Tadpoles came from egg clutches collected from a local pond and raised, under natural conditions, until stage 25. Injured tadpoles cues were prepared a few minutes prior to injection, by euthanizing tadpoles with a rapid blow to the head and crushing them with a mortar and pestle. The paste was then diluted to obtain a concentration of three tadpoles per 20 ml of water, and the solution was filtered through glass floss prior to injection.
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Predator-naïve tadpoles, raised from eggs from six clutches collected from the wild, were maintained in pools filled with conditioned well water (hereafter water) and fed alfalfa pellets. Prior to the start of the experiment, 24 7.4-litre pails (~20 20 cm base) were filled with 4 litres of water and 20 tadpoles, randomly chosen, were placed in each pail. Half the pails were randomly allocated to the ‘1-conditioning group’, while the other half would become the ‘5-conditionings group’. Conditionings took place over 5 days, with one conditioning on day 1, and two conditionings each on day 2 and day 3. Conditionings occurred at random times between 1100 and 1800 hours. Tadpoles from the 5-conditionings group received 20 ml of rainbow trout odour paired 20 ml of injured tadpole cues (three crushed tadpoles/20 ml) at every conditioning. Tadpoles from the 1-conditioning group received 40 ml of water during the first four conditioning events and 20 ml of rainbow trout odour paired with 20 ml of injured tadpole cues during the last conditioning. Each pail received a 100% water change at the end of each day. Food was added to the pails after each water change. Testing The day following the end of the conditioning phase, we randomly selected tadpoles from each pail, placed them individually in 0.5-litre plastic cups (8 cm diameter, 12 cm high) filled with 0.5 litres of water and allowed them to acclimate for 1 h. We observed tadpole behaviour for 4 min to obtain a baseline activity level. We recorded the number of times the tadpoles crossed a medial line on the bottom of the cup: a tadpole was considered to have crossed when its entire body crossed over the line. Following this observation period, we injected 5 ml of rainbow trout, brown trout, brook trout or goldfish odour and observed the behaviour of the tadpole for another 4 min. Tadpoles exhibiting antipredator responses are expected to decrease activity (make fewer line crosses) when compared to their prestimulus baseline. Decreased activity is a common antipredator response in prey species (Lima & Dill, 1990). The order of treatment and pails were randomized and the observer was blind to the treatment while collecting data. We tested a total of 258 tadpoles (N ¼ 27e39/treatment, N ¼ 5e12/ pail). Statistical Analysis We first tested for behavioural bias among treatment groups prior to the introduction of the stimulus. We carried out a threeway nested ANOVA testing the effect of number of conditioning (1 versus 5) and test cue (rainbow trout, brown trout, brook trout or goldfish odour) on the prestimulus data (prestimulus number of line crosses). We added ‘pail’ as a nested factor (type I sum of squares), as tadpoles conditioned in the same pail cannot be considered independent, thus making pail, and not tadpole, the replicative unit. A proportion change in activity from the prestimulus baseline ((post pre)/pre) was computed and used as our response variable in subsequent analyses. We performed a threeway nested ANOVA, once again testing for conditioning and test cues on the response of the tadpoles. Subsequent two-way nested ANOVAs were carried out to investigate significant interaction patterns. All data met parametric assumptions. Data were analysed with SPSS 22 (IBM, Armonk, NY, U.S.A.). RESULTS Tadpoles did not differ in their behavioural baseline prior to stimulus injection (three-way nested ANOVA: conditioning:
F1,20 ¼ 0.1, P ¼ 0.9; cue: F3,231 ¼ 2.0, P ¼ 0.1; conditioning)cue: F3,231 ¼ 1.2, P ¼ 0.3; pail: F22,228 ¼ 1.3, P ¼ 0.2). The behavioural responses of tadpoles were affected by both conditioning regime and test cue (three-way nested ANOVA: conditioning)cue: F3,208 ¼ 6, P ¼ 0.001; Fig. 1). The number of conditionings did not affect the response of tadpoles to the learned rainbow trout (two-way nested ANOVA: conditioning: F1,10 ¼ 0.1, P ¼ 0.81; pail: F22,38 ¼ 1.1, P ¼ 0.44) or to the distantly related goldfish (conditioning: F1,14 ¼ 0.1, P ¼ 0.68; pail: F22,34 ¼ 1.6, P ¼ 0.12). However, the number of conditionings affected the tadpoles' responses to the other trout species in opposite ways. Tadpoles that were conditioned five times to recognize the rainbow trout showed stronger responses to the closely related brown trout than did tadpoles conditioned only once (conditioning: F1,7 ¼ 0.7, P ¼ 0.04; pail: F20,39 ¼ 0.9, P ¼ 0.49). In fact, while tadpoles conditioned once showed a weaker response to the brown trout as compared to the learned rainbow trout (Tukey post hoc test: P ¼ 0.047), tadpoles conditioned five times did not differ in their response to rainbow and brown trout (P ¼ 0.89). Conversely, tadpoles conditioned five times to recognize the rainbow trout displayed weaker responses to the more distantly related brook trout than did tadpoles conditioned only once (conditioning: F1,15 ¼ 6.7, P ¼ 0.02; pail: F21,34 ¼ 1.5, P ¼ 0.10).
DISCUSSION The data presented here provide evidence that the generalization pattern of tadpoles is affected by the information known about the learned predator. While previous studies suggested that the risk level associated with the predator could affect the breadth of the generalization window, our results also indicate that the level of certainty associated with the predator affects this window. When tadpoles were conditioned only once to recognize rainbow trout, they displayed the response pattern predicted from previous studies: their response decreased with increasing phylogenetic
0 Mean proportion change in line crosses
Conditioning
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30
32
32
29
39
38
31
27
–0.2
–0.4
* –0.6
* Rainbow trout Brown trout Brook trout
Goldfish
Figure 1. Mean ±SE proportion change in line crosses of tadpoles that were conditioned to recognize a predatory rainbow trout either one time (open bars) or five times (solid bars), and were subsequently exposed to the odour of a rainbow trout, a closely related brown trout, a less closely related brook trout and a distantly related goldfish. Asterisks indicate differences between conditioning groups at a ¼ 0.05. Numbers above bars indicate sample sizes.
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distance between the novel species and the learned predator. However, increasing certainty about this predator affected the generalization in two opposite ways: it widened the generalization window of closely related species, while narrowing the window of more distantly related species. Indeed, tadpoles conditioned five times to recognize the rainbow trout showed a stronger response to the brown trout but a lower response to brook trout compared to tadpoles conditioned only once. Multiple conditionings would give tadpoles opportunities to refine their recognition of the rainbow trout signature, just as multiple training events improve recognition of complex stimuli (Cave, Bost, & Cobb, 1996). As the recognition of the learned stimulus becomes more accurate, one would expect that the related stimuli would become more distinct from the learned one, and hence should not warrant a strong response. This line of thinking would explain why the 5-conditioning tadpoles decreased their response to brook trout. Counterintuitively, tadpoles in the 5conditioning group also increased their response to brown trout, a close relative. The increase in certainty thus appears to work in a two-tier system, where prey increase their generalization to a close relative, while decreasing their response to a more distantly related one. This pattern could be the results of a costebenefit trade-off where prey have to manage uncertainty. Alternatively, the behavioural data might not provide an accurate picture of the threat level perceived by the tadpoles if the response to the learned predator is already maximized. In other words, the asymptotic nature of antipredator response may mask a gradient between the response to rainbow and brown trout. But this may be a moot point if individual survival is based on actual responses. Future work should test whether or not tadpoles with greater certainty (those in the 5conditioning group in our study) perceive the rainbow and brown trout as similar threats through time. We know that high-level threats elicit a stronger and longer response through time, compared to lower-level ones (Ferrari et al., 2012). Being able to generalize from a known threat to unknown species is critical, especially for prey living in highly biodiverse environments. It avoids the necessity of encountering an unknown predator (and surviving the encounter) before avoiding it. Generalization patterns are filled with stimuli and sensory biases (Ghirlanda & Enquist, 2003). Whether or not prey living in temperate versus tropical ecosystems would display different generalization patterns due to the variation in closely related predators in their environment is unknown. Similarly, whether our observed pattern would hold if the stimuli were visual, rather than olfactory, is also unknown. Prey from different taxa may acquire different amounts of information about a predator at each presentation, some learning much faster and others learning much slower than tadpoles (Crane & Ferrari, 2013). How these differences in learning and information acquisition might affect the pattern seen in our experiment is unknown. In any case, generalization of predator recognition probably plays a key role in native prey responding to novel, invasive predators. Predator naïvety is put forward as a main mechanism behind the failure of native prey to respond to invasive predators (Sih et al., 2010). If prey are able to take information from local threats and use them to respond to novel threats, then they might be less susceptible to invasions. Maintaining a wide generalization frame would appear beneficial, as it would protect against a greater variety of predators. Our results highlight that certainty might reduce the width of this frame and strengthen the response to novel threats that are still recognized. Whether this shift in generalization is adaptive or not in the context of invasion is still to be determined. Our work provides insights on how prey animals respond to unknown predators upon their first encounter with them. The first encounter is often considered the most critical predator/prey
encounter. Failure to respond appropriately could result in death, but responding to myriad nonpredators constitutes a waste of time and resources, particularly for young prey animals that are trying to feed and establish territories. For cognitive ecologists trying to understand how predator recognition develops, the next challenge will be to understand how prey incorporate multiple pieces of information during their first few encounters. Failure of the predator to attack the prey could quickly result in labelling the predator as a nonthreat through latent inhibition (Hazlett, 2003; Mitchell, McCormick, Ferrari, & Chivers, 2011). In contrast, several ‘close calls’ could reinforce the importance of the predator as a high risk. The reality of most predator/prey systems is that prey will be exposed to uncertainty with predators that attack intermittently. Sometimes predators are hungry, other times they are not. Sometimes there are alternative prey around, other times there are not. Future work should explore how prey adjust the intensity of their responses based on learning and generalization when given conflicting information (Ferrari & Chivers, 2006).
Acknowledgments for We thank Glen and Jean for access to the field site and Chloe her invaluable support. We thank Janelle Sloychuk and the Cold Lake Fish Hatchery for providing the fish odour. This work was funded by the Natural Sciences and Engineering Research Council of Canada.
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