Biol. Rev. (2018), 93, pp. 98–114. 98 doi: 10.1111/brv.12334 Biologically meaningful scents: a framework for understanding predator–prey research across disciplines Michael H. Parsons1,2,∗, Raimund Apfelbach3, Peter B. Banks4, Elissa Z. Cameron5, Chris R. Dickman6, Anke S. K. Frank5,7, Menna E. Jones5, Ian S. McGregor8, Stuart McLean9, Dietland M¨uller-Schwarze10, Elisa E. Sparrow11 and Daniel T. Blumstein12 1Department of Biology, Hofstra University, Hempstead, NY 11549, U.S.A. 2Department of Biological Sciences, Fordham University, Bronx, NY 10458, U.S.A. 3Institut f¨ur Neurobiologie, Universit¨at T¨ubingen, T¨ubingen, 72076, Germany 4School of Life and Environmental Sciences, The University of Sydney, Camperdown, 2006, Australia 5School of Biological Sciences, University of Tasmania, Hobart, TAS 7001, Australia 6Desert Ecology Research Group, School of Life and Environmental Sciences, The University of Sydney, Camperdown, 2006, Australia 7Botanisches Institut, AG Linst¨adter, Universit¨at zu K¨oln, D-50674, K¨oln, Germany 8School of Psychology, Brain and Mind Centre, University of Sydney, Camperdown, 2050, Australia 9School of Medicine, University of Tasmania, Hobart, TAS 7001, Australia 10College of Environmental Science and Forestry, State University of New York, Syracuse, NY 13210, U.S.A. 11Department of Environment, Water and Natural Resources, Natural Resources Adelaide and Mt Lofty Ranges, Willunga, 5172, Australia 12Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095-1606, U.S.A. ABSTRACT Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information – scents – in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti-anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory-based risk discrimination. To understand the highly variable literature in this area, we adopt a multi-disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time-limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti-anxiolytic compounds, and help explain the observed variation in post-traumatic-related behaviours (including post-traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans. * Address for correspondence (Tel: +1-914-217-7267; E-mail: [email protected]). Biological Reviews 93 (2018) 98–114 © 2017 Cambridge Philosophical Society Multidisciplinary framework for olfaction studies 99 Key words: anti-anxiolytic scents, appeasement, attractants, conservation, deterrents, ecological informatics, odors, olfaction, PTSD, VNO. CONTENTS I. Introduction .............................................................................................. 99 (1) Objectives ............................................................................................ 100 II. Neurobiological mechanisms underlying prey responses ................................................. 100 (1) Anatomy of olfactory circuits ......................................................................... 101 (2) Accessory structures .................................................................................. 102 (3) Recognition and olfactory learning ................................................................... 102 (4) Conflicting roles of habituation and sensitization ..................................................... 102 III. Chemical information systems ............................................................................ 103 (1) Conspecific communication .......................................................................... 103 (2) Heterospecific information within scents ............................................................. 103 (3) Environmental persistence and decay of scents ....................................................... 104 (4) Consequences of decay: signal intensity, duration and meaning ...................................... 104 IV. Perplexing questions and common conundrums ......................................................... 106 (1) When the same scent can be an attractant and deterrent: predator inspection ....................... 106 (2) When the same scent can be an attractant and deterrent: temporal component ...................... 106 (3) Does size matter? Size-structured mismatches between predator–prey pairs ......................... 107 V. Framework: matched pair example ...................................................................... 107 (1) Catalyst #1: chemistry ................................................................................ 107 (2) Catalyst #2: neuro-mechanism ....................................................................... 107 (3) Catalyst #3: proximity and vulnerability ............................................................. 107 VI. Future directions ......................................................................................... 109 (1) Improved analytical technologies ..................................................................... 109 (a) Standardization of scents ......................................................................... 109 (b) Super scents: creating synthetic analogs and novel scent mixtures ................................ 110 (2) New avenues for scent models transcend disciplines: medical and military ........................... 110 VII. Conclusions .............................................................................................. 110 VIII. Acknowledgements ....................................................................................... 111 IX. References ................................................................................................ 111 I. INTRODUCTION and used their olfactory abilities to help locate resources and keep safe (Eisenberg & Eisenberg, 1981), we should expect Individuals that leave the most descendants may do that olfactory stimuli may have profound effects on many so because they effectively and efficiently trade-off the mammals, including humans. Olfactory–limbic pathways assessment and management of predation risk with other are more direct than other senses (visual, tactile, acous- important activities. Olfactory information often plays a tic), synapsing directly with the amygdala–hippocampal central role in assessment of risk because both predators complex (Otto et al., 1991; Dusek & Eichenbaum, 1998). and prey produce general body odours derived from Odour-evoked memories often are more vivid and arousing skin secretions modified by microbial activity (Davis et al., than auditory (Toffolo, Smeets & Van Den Hout, 2012) or 2013), with contributions from dietary compounds and their visual memories (Herz, 2004). Thus, odours are particularly metabolism (Ferkin et al., 1997), as well as odorants from effective at triggering aversive memories associated with excreta and specific glandular secretions, including steroid stress or trauma (Wiemers, Sauvage & Wolf, 2014). hormones (Zamaratskaia & Squires, 2009). Some of these By studying olfactory-mediated predator–prey interac- chemicals are incidental to general metabolism, while others tions we gain new insights and strategies to create more have evolved to provide signalling functions. Our knowledge effective wildlife lures (Andelt & Woolley, 1996) and wildlife of these potential signals and the trade-offs that individuals deterrents (Schulte, 2016), as well as tools to enrich the lives make in response to them provides a framework with which of captive animals (Wells & Egli, 2004). These insights are we can understand risk management behaviours for a variety not restricted to non-humans. For humans, these insights of organisms. allow us to create novel tools to reinforce emotional states Indeed, olfaction is an ancient, but key modality for (Clark & King, 2008), reduce anxiety (Sheppard & Mills, diverse groups of terrestrial taxa from insects (Persons & 2003), create new models for human pathophysiology Rypstra, 2001) to primates (Willems &