Temporal variability, threat sensitivity and conflicting information about the nature of risk: understanding the dynamics of tadpole antipredator behaviour

The importance of temporal variability in predation risk has recently come to the forefront of research examining the behavioural ecology of predator–prey relationships. Temporal variability has been known to drive patterns of behavioural responses associated with foraging, reproduction and territorial defence of prey animals. We investigated whether larval woodfrog, Rana sylvatica, tadpoles learn to adjust the intensity of their antipredator responses to match (1) the temporal patterns of risk they experience throughout the day and (2) the risk level of a predator. We also examined how tadpoles incorporate temporally conflicting information on the risk posed by the predators. Our results indicate that tadpoles show dynamic adjustments in their behaviour, adjusting their response to predators according to the level of threat associated with the predator and the time of day at which the predator represents the most significant threat. Moreover, tadpoles responded to conflicting information by adjusting their response intensity depending on the nature of the change in vulnerability (whether the risk increased or decreased) and the time that the conflicting information was experienced (whether it was recent or old information). We discuss our results within the context of predator predictability in natural systems and game theory approaches to the behavioural response race between predator and prey.

[1]  S. L. Lima,et al.  Behavioral decisions made under the risk of predation: a review and prospectus , 1990 .

[2]  L. Dill,et al.  Fish and game: a game theoretic approach to habitat selection by predators and prey* , 1994 .

[3]  M. C. Ferrari,et al.  Latent inhibition of predator recognition by embryonic amphibians , 2009, Biology Letters.

[4]  W. E. Neill.  Induced vertical migration in copepods as a defence against invertebrate predation , 1990, Nature.

[5]  M. Bowers.  Seed Removal Experiments on Desert Rodents: The Microhabitat by Moonlight Effect , 1988 .

[6]  S. G. Reebs.  Time–Place Learning Based on Food but not on Predation Risk in a Fish, the Inanga (Galaxias maculatus) , 1999 .

[7]  D. J. Hall,et al.  An Experimental Test of the Effects of Predation Risk on Habitat Use in Fish , 1983 .

[8]  A. Portmann,et al.  A test of the risk allocation hypothesis: tadpole responses to temporal change in predation risk , 2002 .

[9]  M. C. Ferrari,et al.  Generalization of learned predator recognition: an experimental test and framework for future studies , 2007, Proceedings of the Royal Society B: Biological Sciences.

[10]  Ziemba,et al.  New insights on how temporal variation in predation risk shapes prey behavior. , 2000, Trends in ecology & evolution.

[11]  Reehan S. Mirza,et al.  Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition , 2006 .

[12]  J. Buskirk,et al.  DOSAGE RESPONSE OF AN INDUCED DEFENSE: HOW SENSITIVE ARE TADPOLES TO PREDATION RISK? , 2002 .

[13]  M. C. Ferrari,et al.  Cultural learning of predator recognition in mixed-species assemblages of frogs: the effect of tutor-to-observer ratio , 2008, Animal Behaviour.

[14]  G. S. Caldwell.  Predation as a selective force on foraging herons effects of plumage color and flocking , 1986 .

[15]  A. Laurila,et al.  Temporal variation in predation risk: stage‐dependency, graded responses and fitness costs in tadpole antipredator defences , 2004 .

[16]  J. Maerz,et al.  Nocturnal shift in the antipredator response to predator-diet cues in laboratory and field trials , 2005 .

[17]  Dietland Müller-Schwarze,et al.  Chemical Signals in Vertebrates 3 , 1983 .

[18]  M. C. Ferrari,et al.  Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs , 2007, Chemoecology.

[19]  M. C. Ferrari,et al.  Larval amphibians learn to match antipredator response intensity to temporal patterns of risk , 2008 .

[20]  J. Holomuzki,et al.  Diel movements of larvae of the tiger salamander, Ambystoma tigrinum nebulosum. , 1983 .

[21]  A. Mathis,et al.  Acquired Recognition of Chemical Stimuli from an Unfamiliar Predator: Associative Learning by Adult Newts, Notophthalmus viridescens , 1998 .

[22]  A. Sih,et al.  Predator and prey space use: dragonflies and tadpoles in an interactive game. , 2007, Ecology.

[23]  Burt P. Kotler,et al.  Foraging games between gerbils and their predators: temporal dynamics of resource depletion and apprehension in gerbils , 2002 .

[24]  R. Relyea.  PREDATORS COME AND PREDATORS GO: THE REVERSIBILITY OF PREDATOR‐INDUCED TRAITS , 2003 .

[25]  M. C. Ferrari,et al.  First Documentation of Cultural Transmission of Predator Recognition by Larval Amphibians , 2007 .

[26]  P. Barbosa,et al.  Ecology of Predator-Prey Interactions , 2005 .

[27]  G. Helfman.  Threat-sensitive predator avoidance in damselfish-trumpetfish interactions , 2004, Behavioral Ecology and Sociobiology.

[28]  Rick A. Relyea,et al.  HOW PREY RESPOND TO COMBINED PREDATORS: A REVIEW AND AN EMPIRICAL TEST , 2003 .

[29]  M. C. Ferrari,et al.  Can prey exhibit threat-sensitive generalization of predator recognition? Extending the Predator Recognition Continuum Hypothesis , 2008, Proceedings of the Royal Society B: Biological Sciences.

[30]  Douglas P. Chivers,et al.  Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? , 2006, Animal Behaviour.

[31]  S. L. Lima,et al.  Temporal Variation in Danger Drives Antipredator Behavior: The Predation Risk Allocation Hypothesis , 1999, The American Naturalist.

[32]  J. Clarke.  Moonlight's influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus) , 1983, Behavioral Ecology and Sociobiology.

[33]  S. L. Lima,et al.  Use of Prey Hotspots by an Avian Predator: Purposeful Unpredictability? , 2006, The American Naturalist.