Diet cues alter the development of predator recognition templates in tadpoles

Abstract

Recognising predators accurately is key to making fine-scale adjustments to behaviour that enhance survival and maximise overall fitness for prey. Prey incorporate information from specific predator features in order to recognise predators and the risk they pose. For olfactory cues, prey can use both predator odour and diet cues to recognise predators. The role of diet cues in predator recognition has only been tested when they provide information about risk and act as an unconditioned stimulus. Thus, it is unclear whether prey use diet cues in the development of more general predator recognition templates. Here, we tested whether diet cues that contain no apparent information about the prey's vulnerability to the predator are used by prey when they learn to recognise predators. We trained predator-naive wood frog tadpoles (Lithobates sylvaticus) to recognise the odour of a novel crayfish (Orconectes virilis) as risky by pairing tadpole alarm cues with the odour of crayfish fed one of two diets: alfalfa pellets or earthworms (Lumbricus sp.). We tested tadpoles from each group for their response to one of the two crayfish diet odour combinations or a water control. Tadpoles displayed antipredator responses to crayfish odour, irrespective of diet. However, their responses were stronger when tadpoles were exposed to crayfish fed the same diet as during training. Such results demonstrate that diet cues play a previously unrecognised but subtle role in predator recognition and suggest that flexibility in prey choice can lead to an advantage for the predator. Significance statementRecognising predators and the threat they pose is critical for prey to adjust their behaviour in response to fluctuations in predation risk. There is therefore a need to understand how prey use different cues to develop effective recognition templates that allow for threat-sensitive adjustments to behaviour. Here, we demonstrate that diet cues of predators contribute to the development of predator recognition templates by prey. These results provide new information about how prey develop recognition templates for predators and that, by incorporating diet cues, they are able to adjust their responses to variable risk posed by different predators within a population. Additionally, we suggest that generalist diets may provide unrecognised benefits to predators when switching between prey types.

Mechanisms underlying the control of responses to predator odours in aquatic prey

“…Many of the studies reviewed here exposed prey to predator odours and diet cues simultaneously, and yet antipredator responses of prey to predator odours can differ when diet cues are present or absent (Mitchell et al, 2015(Mitchell et al, , 2016bRelyea, 2005, 2009;Stabell et al, 2003). While there are a growing number of studies showing innate predator recognition (Dalesman et al, 2006;DeSantis et al, 2013;Langerhans and DeWitt, 2002;Vilhunen and Hirvonen, 2003), many studies have shown that, when diet cues are controlled for, predator-naive prey do not display antipredator responses to predator odours.…”

Tadpoles modulate antipredator responses according to the abundance of vegetation experienced during the embryonic stage

“…These studies reliably showed an absence of a learned response in the control group exposed to water. Given the tadpoles' consistent response to alarm cues and given the fact that the control groups were not necessary for directly assessing the differences between experimental groups in my experiment, I used reduced control groups similar to Mitchell et al (2016). The use of reduced control groups was also useful for reducing the number of animals involved in the study as required by the law of the country in which the experiment took place.…”

Odour recognition learning of multiple predators by amphibian larvae

“…Sample sizes of experiment 2 were as follow: alarm cues + fish/crayfish mixture: 48; control water + fish/crayfish mixture: 36. Several learning studies with this protocol showed not learned response in the control group Chivers et al, 2016;Ferrari et al, 2009a;Lucon-Xiccato et al, 2016;Lucon-Xiccato et al, 2017); thus, we used reduced control groups to minimise the number of wild animals necessary for the study (Mitchell et al, 2016). The tadpoles were exposed to the mixture for 1 h; then, tadpoles were moved into 16 holding pails (approx.…”

“…We moved each individual tadpole to a 0.5-L cup and left them to acclimate for 30 min. The bioassay used to measure antipredator responses is identical to that used in previously published studies on tadpole antipredator responses (Lucon-Xiccato et al, 2016;Lucon-Xiccato et al, 2017;Mitchell et al, 2016). In the predator recognition test, each subject was exposed to a single predator cue.…”

“…If tadpoles conditioned with alarm cues learned to recognize the individual odours in the conditioning mixture, they were expected to show a marked reduction in activity between the initial baseline and the post-injection period. Indeed, a decrease in activity is a common antipredator response in larval amphibians after conditioning with both fish cues (Chivers et al, 2016;Ferrari, Crane, & Chivers, 2016) and crayfish cues (Lucon-Xiccato et al, in preparation;Mitchell et al, 2016). Conversely, tadpoles exposed to water instead of alarm cues in the conditioning phase were expected to not show such activity reduction.…”