Dropping to Escape: a Review of an Under-Appreciated
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1 Dropping to escape: a review of an under-appreciated 2 antipredator defence 3 4 Rosalind K. Humphreys* and Graeme D. Ruxton 5 6 School of Biology, University of St Andrews, Dyer's Brae House, St Andrews, Fife, KY16 7 9TH, UK 8 9 ABSTRACT 10 Dropping is a common antipredator defence that enables rapid escape from a perceived 11 threat. However, despite its immediate effectiveness in predator–prey encounters (and against 12 other dangers such as a parasitoid or an aggressive conspecific), it remains an under- 13 appreciated defence strategy in the scientific literature. Dropping has been recorded in a wide 14 range of taxa, from primates to lizards, but has been studied most commonly in insects. 15 Insects have been found to utilise dropping in response to both biotic and abiotic stimuli, 16 sometimes dependent on mechanical or chemical cues. Whatever the trigger for dropping, the 17 decision to drop by prey will present a range of inter-related costs and benefits to the 18 individual and so there will be subtle complexities in the trade-offs surrounding this 19 defensive behaviour. In predatory encounters, dropping by prey will also impose varying 20 costs and benefits on the predator – or predators – involved in the system. There may be 21 important trade-offs involved in the decision made by predators regarding whether to pursue 22 prey or not, but the predator perspective on dropping has been less explored at present. 23 Beyond its function as an escape tactic, dropping has also been suggested to be an important 24 precursor to flight in insects and further study could greatly improve understanding of its 25 evolutionary importance. Dropping in insects could also prove of significant practical 26 importance if an improved understanding can be applied to integrated pest-management 27 strategies. Currently the non-consumptive effects of predators on their prey are under- 28 appreciated in biological control and it may be that the dropping behaviour of many pest 29 species could be exploited via management practices to improve crop protection. Overall, this 30 review aims to provide a comprehensive synthesis of the current literature on dropping and to 31 raise awareness of this fascinating and widespread behaviour. It also seeks to offer some 32 novel hypotheses and highlight key avenues for future research. 33 34 Key words: dropping, antipredator defence, predator–prey interaction, behavioural ecology, 35 evolution, biological control, integrated pest-management. 36 37 CONTENTS 38 I. Introduction ............................................................................................................................ 3 39 II. Which taxa exhibit dropping as an antipredator defence and what different forms does 40 dropping take? ............................................................................................................................ 6 41 (1) Release and undirected dropping ..................................................................................... 6 42 (2) Controlled terrestrial descent ........................................................................................... 7 43 (3) Sudden loss of powered flight ......................................................................................... 8 44 (4) Directed aerial descent and gliding ................................................................................. 9 45 (5) Active drift ....................................................................................................................... 9 46 III. What can trigger dropping behaviour? .............................................................................. 11 47 (1) Visual and tactile cues ................................................................................................... 11 48 (2) Auditory cues ................................................................................................................. 12 49 (3) Chemical and parasitism cues ....................................................................................... 12 50 (4) Multiple cues and abiotic factors ................................................................................... 13 51 IV. What are the benefits, costs and trade-offs associated with dropping? ............................. 14 52 (1) Prey perspective ............................................................................................................. 14 53 (a) Benefits ................................................................................................................... 14 54 (b) Costs ....................................................................................................................... 15 55 (c) Cost-reducing mechanisms ..................................................................................... 16 56 (d) Trade-offs surrounding the decision to drop .......................................................... 17 57 (2) Predator perspective ...................................................................................................... 22 58 (a) Benefits ................................................................................................................... 22 59 (b) Costs and trade-offs surrounding the decision to pursue prey ............................... 22 60 V. Non-antipredator functions of dropping ............................................................................. 24 61 VI. What practical applications are there for a better understanding of dropping behaviour? 25 62 VII. Outstanding questions and opportunities for future research ........................................... 28 63 VIII. Conclusions ..................................................................................................................... 30 64 IX. Acknowledgements 65 X. References 66 67 I. INTRODUCTION 68 One of the simplest ways for an organism on a raised substrate or in the air to escape an 69 approaching threat is to drop. Dropping behaviour immediately removes an individual from 70 the perceived hazard – be that a predator or another source of danger (such as a parasitoid or 71 aggressive conspecific) – at least temporarily. Broadly, as an antipredator defence, dropping 72 is a behaviour that could literally mean the difference between life and death for the prey. In 73 the natural world, where organisms are engaged in an ongoing ‘struggle’ to survive and 74 proliferate to pass on their genes to subsequent generations, any evolved adaptations that 75 increase the likelihood of survival and/or breeding opportunities will be of great advantage to 76 an individual or, indeed, a species. Given that antipredator adaptations occur in almost every 77 major taxonomic group and in every biome of the world, Ruxton, Sherratt & Speed (2004, p. 78 2) rightly point out that, “as R. A. Fisher argued, their very presence tells us that predation is 79 a phenomenon of great ecological and evolutionary significance”. Antipredator adaptations 80 can be morphological, chemical, or – as in the case of dropping – behavioural in nature, but 81 all have evolved to reduce the risk of predation and, ultimately, mortality, thereby increasing 82 the fitness of the prey. In many cases, when faced with a predatory threat, a prey species has 83 multiple antipredatory adaptations they could utilise. Some morphological defences, for 84 example camouflage, may be deployed constantly, but where prey have the option to select a 85 behavioural defence in response to an imminent threat they ought to select the behaviour that 86 will best increase their chances of surviving the encounter. 87 We define dropping as a voluntary antipredator defence whereby a prey individual uses 88 gravity, wind or water currents to power escape from imminent threat. Dropping can either be 89 passive, where an individual simply falls away or releases its hold on a substrate, or active, 90 where the individual may jump away from a substrate, sometimes kicking or somersaulting in 91 the process (Brown, 1974); as an example of this variability, Haemig (1997) describes wood 92 ants, Formica aquilonia, both falling and deliberately jumping from trees. Whether passive or 93 active, key to dropping is that the behaviour must result in the individual escaping in a 94 trajectory determined primarily by the external force (gravity or bulk fluid flow) only 95 modified modestly, if at all, by the organism itself. 96 This deceptively simple, but in fact very complex, behaviour is common and widespread as 97 an antipredator defence, but (perhaps due to its lack of required morphological adaptations) it 98 is currently under-studied. As a key antipredator defence, dropping has significant 99 consequences for both prey and predators at both individual and population scales. 100 Undoubtedly, the precise cost–benefit framework surrounding dropping depends on the point 101 of deployment within the predation sequence. Interactions between predators and their prey 102 can be usefully broken down into a sequence of stages comprising: (1) encounter (spatial and 103 temporal proximity), (2) detection, (3) identification, (4) approach, (5) subjugation, and (6) 104 consumption (Caro, 2005; Endler, 1991). In the literature, antipredatory defences employed 105 by prey during stages 1–4 (ahead of subjugation) are referred to as ‘primary defences’, 106 serving to influence the likelihood of the predator physically contacting the prey. So-called 107 ‘secondary defences’ act once subjugation or contact has begun (stages 5 and 6).