A review of thanatosis (death feigning) as an anti-predator behaviour

Behavioral Ecology and Sociobiology (2018) 72:22 https://doi.org/10.1007/s00265-017-2436-8 REVIEW A review of thanatosis (death feigning) as an anti-predator behaviour Rosalind K. Humphreys 1 & Graeme D. Ruxton 1 Received: 10 September 2017 / Revised: 18 December 2017 / Accepted: 23 December 2017 # The Author(s) 2018. This article is an open access publication Abstract Thanatosis—also known as death-feigning and, we argue more appropriately, tonic immobility (TI)—is an under-reported but fascinating anti-predator strategy adopted by diverse prey late on in the predation sequence, and frequently following physical contact by the predator. TI is thought to inhibit further attack by predators and reduce the perceived need of the predator to subdue prey further. The behaviour is probably present in more taxa than is currently described, but even within well-studied groups the precise taxonomic distribution is unclear for a number of practical and ethical reasons. Here we synthesise the key studies investigating the form, function, evolutionary and ecological costs and benefits of TI. This review also considers the potential evolutionary influence of certain predator types in the development of the strategy in prey, and the other non-defensive contexts in which TI has been suggested to occur. We believe that there is a need for TI to be better appreciated in the scientific literature and outline potentially profitable avenues for investigation. Future use of technology in the wild should yield useful developments for this field of study. Significance statement Anti-predatory defences are crucial to many aspects of behavioural ecology. Thanatosis (often called death-feigning) has long been an under-appreciated defence, despite being taxonomically and ecologically widespread. We begin by providing muchneeded clarification on both terminology and definition. We demonstrate how apparently disparate observations in the recent literature can be synthesised through placing the behaviour within a cost-benefit framework in comparison to alternative behavioural choices, and how aspects of the ecology differentially affect costs and benefits. Extending this, we provide novel insights into why the evolution of thanatosis can be understood in terms of coevolution between predators and prey. We offer further novel hypotheses, and discuss how these can be tested, focussing on how emerging technologies can be of great use in developing our understanding of thanatosis in free-living animals. Keywords Thanatosis . Tonic immobility . Death feigning . Anti-predatory defence . Trade-offs Introduction Predation is fundamental to the lives of wild animals, influencing key aspects of fitness such as feeding, breeding, and often, ultimately, mortality. In response to the threat of predation, and the fitness costs to an individual associated with such predation, natural selection has resulted in the Communicated by Dhruba Naug * Rosalind K. Humphreys 1 School of Biology, University of St Andrews, Dyer’s Brae House, St Andrews, Fife KY16 9TH, UK evolution of a wide variety of morphological, physiological, chemical and behavioural defensive adaptations in prey species. Very few animals are immune to substantial threat of predation in at least one stage of their ontogeny. As such, the many and sometimes complicated adaptations involved in predator-prey interactions are of great interest to behavioural ecologists. An interaction between a predator and prey individual can often usefully be broken down into a sequence of stages, beginning with the two individuals being in proximity, and leading through detection, identification, reducing separation, contacting, subduing and finally consuming (Endler 1991; Caro 2005). There is a diversity of mechanisms that prey have evolved to avoid attack by predators, some of which require deployment at particular stages in the attack sequence in order to be effective. One interesting and well-known 22 Page 2 of 16 defence that prey can exhibit late in the sequence of a predation event is tonic immobility (hereafter shorted to TI). TI has been discussed in the scientific literature for over a century (e.g. Fabre 1900); but until recently most studies were observational and qualitative (see Edmunds 1974 for an insightful synthesis of these earlier works and Ruxton et al. 2004). As a defensive mechanism, TI can be viewed as a ‘last resort’, occurring not only after the prey has already been detected by the predator but most often following physical contact between the predator and its prey. This makes it quite distinct from immobility used to reduce the risk of predator detection or tracking, since such Bfreezing^ occurs much earlier in the sequence of a predatory attack. That is, we consider stillness that enhances the effectiveness of camouflage or masquerade to be a different process from TI. Further some animals (e.g. pill bugs, armadillos) adopt a curled posture that makes vulnerable body parts inaccessible to predators. We consider this, too, a separate process to TI, which does not rely on making the prey physically less vulnerable to the predator. TI typically occurs when animals are physically restrained, and it involves prey adopting a relatively immobile state that can last—from seconds to hours—even after the physical constraint has been released. In some vertebrates, the behaviour can involve reduced breathing rates, bradycardia, tongue protrusion, and setting the eyes wide open—features very reminiscent of dead individuals of that species. TI is, therefore, also known as death feigning, playing dead, playing possum, animal hypnosis, and thanatosis. By offering the following definition of TI, we hope to clarify the scope of our current study: Tonic Immobility (TI) is the unlearned adoption of a motionless posture by a prey individual triggered by physical contact or very close proximity of – not injury inflicted by – a predator (or other antagonist). The posture does not reduce the sensory ability of the predator to locate or identify the prey, or reduce the physical vulnerability of the prey if the attack is pursued. The state of motor inhibition is maintained for a time even after release by the predator, and when in this state the prey exhibits reduced responsiveness to external stimulation (although monitoring of the environment can still occur). In the absence of mortality or injury during TI, the prey can recover its original physiological state on emerging from TI. Notice that this definition is agnostic as to the function of TI. Although it is generally assumed that TI confers an antipredatory benefit, in causing the predator to break off its attack, we feel this function is not necessary for a clear and effective definition. Indeed, our definition makes no assumption about predatory response to TI. Nor does it make any assumption about the underlying drivers of any predatory response. Our definition is also agnostic as to whether the Beh (...truncated)