Animal Athletes

How hard do free-living animals work during routine activities such as finding food, or mates, or rearing offspring? Can animals even be described as “athletes”? Do concepts such as “training” and “exercise” apply to free-living animals? These seemingly simple questions are surprisingly poorly resolved, yet as the authors of this excellent book point out the consequences of under-performing are a matter of life and death for animals, unlike for human athletes at the Olympics! The questions addressed in this book, which form the core of Animal Athletes , are especially timely given the rapid pace of recent technological advances (p. 47, 52, 236), which are giving biologists an unprecedented ability to track the behavior of free-living animals 24/7 ( Wilmers et al. 2015 ). However, another reason to read and enjoy this book is simply that it is peppered with very cool examples of animal “performance”, often in comparison to human performance, for example, early on in the Forward (p. v) we are told that rattlesnakes vibrate their tail at 90 Hz for over an hour. Is this an impressive performance? Well, as the authors suggest, try shaking your hand as quickly as you can for an hour to get a sense of what this means! Animal Athletes comprises 12 chapters organized around several main themes: after an initial overview (Chapter 1), Chapters 2–4 discuss the “ecology of performance”, and Chapters 5 and 6 deal with aspects of the “evolution of performance”. The remaining chapters deal with trade-offs and constraints (Chapter 7), sexual selection and performance (Chapter 8), extreme performance (Chapter 9), a population and community perspective (Chapter 9), and human athletes (Chapter 11), before a final conclusion chapter. Throughout, performance is defined very broadly at the whole-organism level (e.g., swimming, jumping, flying, communicating, and feeding), rather than dealing with processes that reflect performance of only parts of the organism (e.g., digestion, metabolism). Nevertheless, the authors take a very integrative approach, exploring behavior, ecology, evolution, morphology, and physiology, arguing that this is essential to “fully comprehend the diversity of animal performance”. One pervading theme throughout book therefore is what level of biological organization causes, or is most important in generating, variation in performance? Here I felt there was an intriguing dichotomy of opinion expressed in different parts of the book: given the hierarchical nature of organisms, to what extent does variation in whole-animal performance depend on lower level traits such as physiology and biochemistry, intermediate traits such as morphology and biomechanics, or emergent traits such as behavior? At one point the authors state that “performance capacities emerge from the whole organism not from individual parts …” (p. 3) and, therefore, that they “will not dwell on the precise mechanism of how performance is produced”. However, soon after we are told “one cannot easily separate the underlying structures that produce performance from the evolution of performance” (p. 10). Admittedly, from my more physiological perspective, I felt that many of the “mechanistic” examples in the book deal with morphological or anatomical variation (limb length, claw or jaw size or shape, etc; as in Chapter 5) and not physiology per se . However, several examples of physiological or biochemical adaptations for performance are given, such as the activity of one specific enzyme, arginine kinase, in burst speed of damselflies (p. 17; see also p. 193), and we are told these biochemical traits “play an especially important role” in organismal performance. A “strong conclusion from [this] book is that one should not ignore the important contribution of mechanistic studies” and, I would argue, at all level of organization, this dictum is true. Overall, therefore, I found that Animal Athletes exposed a dichotomy in current opinion (e.g., see Careau and Garland 2012 ), which represents an area ripe for further research: at what level of organization does selection act most strongly, and is variation in behavior more or less “important” then variation in physiology or biochemistry (p. 35)? Inclusion of the word “athletes” in the book title, and early parallels with human athletes, suggests the idea of individuals operating at, or close to, their maximum performance capacity (obtaining a world record time). Chapter 9 specifically deals with examples of extreme performance, and there are many other examples presented throughout the book (e.g., ballistically-propelled tongues of frogs, long-distance migration). However, a particular strength of Animal Athletes is that it focuses on performance by animals during routine activities in their natural environment, such as finding food or mates (“ecological performance”, Irschick and Garland 2001 ). The authors point out that it might be quite unusual for free-living animals to make “all-out-effort” and to operate at, or close to, their maximum performance capacities, which, in turn, have important implications for morphological or physiological constraints on performance. Rather than expecting animals to perform at 100% of maximum all the time, free-living animals should do “only what they have to do to survive”. Clearly the percentage of maximum capacity that individuals and species use in nature is highly variable, for example, among Anolis lizards some species appear to be “slackers” and some “overachievers” (p. 62–63). The authors highlight the fact that there are limits to the value of extreme performance, perhaps due to trade-offs with other functions (Chapters 2 and 7), and emphasize the need to study performance in the wild (Chapter 3). Any weaknesses in Animal Athletes are minor. Perhaps not surprisingly, given the authors research interests, I found a disproportionate number of examples involved lizard locomotion, though it is true that this has proved to be an excellent study system for the integration of mechanism, performance, and fitness in free-living animals ( Irschick 2003 ; Irschick et al. 2008 ). In addition, several adaptations appear as examples multiple times in different chapters, such as jaw structure of fishes (p. 136, 154, 191, 216) and tongue projection (p. 22, 103–105, 185). These traits are presented as “key innovations that allow animals to explore and occupy new ecological niches” (p. 155–158) and I was left wondering if there aren’t other similar, perhaps less well-known or less studied, examples, or if indeed these represent rare, even unique, innovations perhaps reflecting broader constraints on innovation? Finally, the only chapter I found less than compelling was Chapter 10, which covered genetics, geographic variation, and community ecology. This section considered the role of community structure in molding animal athletics, but I think this reveals a huge opportunity to truly integrate studies of individual variation in performance into population dynamics and community structure. If there are “slackers” and “over-achievers” either among individuals within populations, or among species, within communities, how does this influence ecosystem structure and function—an animal version of “urban planning”?! As bio-tracking devices get ever smaller and cheaper it should soon be possible to study performance interactions among social individuals in space and time ( Vander Wal et al. 2014 ; Strandburg-Peshkin et al. 2015 ), and then (hopefully!) to incorporate analysis of the role of lower-level biochemical, physiological, and morphological mechanism in movement ecology. Animal Athletes is a well-written, readable book that is accessible to non-experts, full of provocative and diverse examples of performance in free-living animals, and should be of interest to anyone working in integrative organismal biology. It would be an excellent text for a graduate course (indeed I plan to use it for my own course in ecological and evolutionary physiology next year). Animal Athletes provides a comprehensive and up-to-date summary of what we currently know about performance in animals (references up to 2015) but what does it suggest for future research? First, I think the idea that free-living animals might not operate even close to their maximum capacity most of the time could be very influential (Chapter 3). How does this idea square with the widely held assumption that certain activities (e.g., raising offspring) involves “hard work” and that individuals that work harder benefit with higher reproductive output? Is efficiency of performance the secret to success, not maximization of performance? Second, as the authors point out most studies of animal performance are still conducted under standardized laboratory conditions (p. 47), often involve extreme (or forced) performance, and might not be very ecologically-relevant. So, further studies of performance in the wild, in the context of fitness are required. Finally, I found Chapter 11 ( Human athletics: a link to non-human animals ) to be one of the most stimulating and intriguing sections of this book. Returning to the opening question, does routine activity in free-living animals equate to “exercise”? Given that some animals have markedly different levels of activity at different life-stages, do animals prepare for periods of more intense activity, and is this equivalent to “training” in humans (see Halsey 2016 )? Combining these lines of thinking with technological advances in bio-tracking (p. 236) is sure to generate fruitful and exciting results from future research.

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