Antipredator Defenses in Birds and Mammals

by Tim Caro, Sheila Girling

Overview

In nature, the ability to defend against predators is fundamental to an animal's survival. From the giraffes that rely on their spotted coats to blend into the patchy light of their woodland habitats to the South American sea lions that pile themselves in heaps to ward off the killer whales that prey on them in the shallow surf, defense strategies in the animal kingdom are seemingly innumerable.

In Antipredator Defenses in Birds and Mammals, Tim Caro ambitiously synthesizes predator defenses in birds and mammals and integrates all functional and evolutionary perspectives on antipredator defenses that have developed over the last century. Structured chronologically along a hypothetical sequence of predation—Caro evokes a gazelle fawn desperate to survive a cheetah attack to illustrate the continuum of the evolution of antipredator defenses—Antipredator Defenses in Birds and Mammals considers the defenses that prey use to avoid detection by predators; the benefits of living in groups; morphological and behavioral defenses in individuals and groups; and, finally, flight and adaptations of last resort.

Antipredator Defenses in Birds and Mammals will be of interest to both specialists and general readers interested in ecological issues.

Product Details

ISBN-13:	9780226094366
Publisher:	University of Chicago Press
Publication date:	09/01/2005
Series:	Interspecific Interactions
Edition description:	New Edition
Pages:	592
Product dimensions:	6.00(w) x 9.00(h) x 1.30(d)

About the Author

Tim Caro is professor in the Department of Wildlife, Fish, and Conservation Biology at the University of California, Davis. He is also the author of Cheetahs of the Serengeti Plains: Group Living in an Asocial Species, also published by the University of Chicago Press.

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ANTIPREDATOR DEFENSES IN BIRDS AND MAMMALS

By TIM CARO THE UNIVERSITY OF CHICAGO PRESS
Copyright © 2005
The University of Chicago
All right reserved.

ISBN: 978-0-226-09436-6


Chapter One Definitions and Predator Recognition

1.1 Introduction

Because most species are preyed upon by several others, they have been forced to evolve numerous protective responses. As a consequence, the number, subtlety, and complexity of antipredator defenses shown by even one prey individual can be as daunting as they are awe inspiring. Biologists in turn must face the considerable challenge of fathoming how natural selection has shaped mechanisms to avoid premature death at the hands of others. Attempts to understand these antipredator defenses in the animal kingdom have a long history that starts at the end of the nineteenth century, when naturalists working in the tropics described the form and behavior of the new species that they encountered while zoologists in universities and zoological gardens speculated on the function of these traits, particularly animal coloration (Poulton 1890; Beddard 1892; G. H. Thayer 1909). While interest in animal defenses lapsed during the first half of the twentieth century, aside from a scattering of North American work and Cott's (1940) synthesis, it picked up again in the 1950s with the advent of detailed behavioral studies of birds and insects that formed a springboard for modern behavioral ecology, which took off in the 1970s (Bertram 1978a; Harvey and Greenwood 1978). Since then, theoretical advances, especially cost-benefit analyses and models of trade-offs, along with empirical studies in both field and laboratory have grown enormously in number and sophistication to the extent that biologists are in a difficult position of having to synthesize a great deal of information spread over several subdisciplines. Viewed from the outside, it is difficult to be sympathetic to this embarrassment of riches; in truth, biologists simply need to take the time to organize theory and evidence before moving forward. This book makes such an attempt.

This chapter begins by justifying the organizational structure of the text and clarifying terminology. The task of describing defenses quickly becomes burdensome during attempts to understand variation in these defenses across individuals or species. Consequently, antipredator responses to predation threat are often characterized either as a sequence of interactions between predator and prey or else as a list of antipredator defenses organized as stage-specific responses to predation threat. These classificatory schemes each have advantages and drawbacks, but I have adhered to the latter organizational structure in this book (section 1.2). The number of attempts to understand antipredator defenses exhibited by birds and mammals, the taxonomic groups that have been studied the most, has led to a proliferation of terms; it is necessary to elucidate the meanings of some important words, because many are applied in more than one way (section 1.3). After this etymological digression, I proceed to the mechanisms by which prey perceive that they are under threat from predation. The chapter, then, is awkwardly split into two disjunct sections.

Predator recognition is an important component of antipredator defense mechanisms because many, perhaps most, defenses necessitate prey first recognizing danger, that is, discriminating dangerous situations from harmless ones, and then taking evasive action (McLean and Rhodes 1991). Hence the topic must be dealt with early on. That said, a great many morphological characteristics and behavioral mechanisms used to avoid detection (chapters 2 and 3), as well as some aposematic traits (chapter 7), do not demand that prey recognize predators. Recognition refers to an animal taking note of a threat and can be measured using simple reflexes such as a change in cardiac response (Mueller and Parker 1980), although it is usually recorded as a behavioral change, notably enhanced vigilance, alarm calling, mobbing, or flight. In theory, a threatening stimulus may be classified at different levels of specificity. In decreasing order, these include recognizing a particular predator individual, a hungry individual, a particular species of predator, a class of predator such as a terrestrial or aerial, or simply a threatening situation that need not even involve a predator being present but just a situation in which the likelihood of predation is elevated (McLean and Rhodes 1991). Most analyses focus on prey recognizing a species or category of predator (see chapter 6).

Broadly, the study of predator recognition has centered on three areas of inquiry. The first simply demonstrates that a prey species is able to recognize danger either by observing prey in the wild or using experiments to match the salient features by which prey identify predators (section 1.4). The second area is developmental in nature, that is, understanding the extent to which predator recognition by naïve individuals is innate or learned and the mechanisms by which prey come to recognize dangerous situations accurately (section 1.5). The third and more recent arena of study concerns loss of predator recognition abilities in the absence of interactions with predators over historical or evolutionary time (section 1.6). Loss of ability to recognize predators bears on both ontogeny of recognition during an individual's lifetime and evolution of recognition systems over generations, and is of concern to conservation biologists attempting to understand the consequences of planned predator reintroductions or predator invasions into new or historical ranges (Wolf et al. 1996; Gittleman and Gompper 2001; Pyare and Berger 2003; Jones et al. 2004).

At the end of the chapter, the issue of observational bias in the study of antipredator defenses is broached (section 1.7).

1.2 The predatory sequence

Predation is sometimes portrayed as a series of interactions between two players, the predator and prey, in which the behavior of the predator leads to a defensive response by prey that may then be countered by the predator, and so on. This way of thinking about predation stems from observers collating all the possible products of interactions that they have witnessed, placing them in a logical sequence, and even assigning probabilities to them, as shown in figure 1.1. The advantage of a flow diagram such as this is that it is easy to grasp relatively complex interactions visually. One problem with these charts, however, is that they allow prey only one or a small number of possible responses to a given decision by the predator, thereby limiting the range of antipredator alternatives open to prey at each juncture. Moreover, flow charts can be misleading because they suggest a choreographed game composed of several interactions that are sequentially contingent on each other and thus imply that prolonged interactions are the rule. In nature, the number of interactions are often limited; for example, the predator appears suddenly, the prey sees it and flies off (Cresswell 1996). Furthermore, the prey is always intent on terminating an interaction as soon as possible. This is seen most readily using real data (fig. 1.2), in this case showing that moose (see the appendix for scientific names of vertebrates) are attempting to end the interaction with wolves through flight or intimidation at a number of junctures.

An alternative method of characterizing the details of predator-prey interactions consists of listing antipredator defenses in a chronological order derived from the predator's behavior and in a way that highlights their effectiveness in counteracting each particular phase of the predator-prey encounter (for example, Pitcher and Parrish 1993; Hileman and Brodie 1994). Phases vary in number and emphasis according to author. Vermeij (1982) separates the recognition or detection phase from the pursuit or escape phase, and again from the subjugation or resistance phase. Edmunds (1974) distinguishes between primary, or indirect, defenses, defined as defenses that operate regardless of whether a predator is in the vicinity, and secondary defenses that operate during an encounter with a predator (table 1.1.a). Endler (1991a) lists antipredator defenses as counterploys to predatory stages that progressively bring the predator closer to its quarry (table 1.1.b). A disadvantage of these sorts of classifications is that they mix evolutionary, ontogenetic, and proximate timescales, whereas flow diagrams usually adhere only to proximate timescales, that is, during the current interaction between predator and prey. Another difficulty is that although some defenses are tailored to a particular phase of encounter with a predator, the same antipredator defenses are sometimes used at more than one stage of predation, notably defenses such as grouping and immobility, although this problem is not insurmountable. The advantage of such a scheme is that it stresses antipredator defenses as alternatives rather than as a sequence of possibilities to which prey can resort only if a previous antipredator ploy has failed.

In this book, I have taken the second approach and constructed a modification of Endler's (1991a; see also Endler 1986) scheme, starting first with morphological (chapter 2) and then behavioral (chapter 3) defenses that prey use to avoid being detected even when predators are not in the vicinity (classic primary defenses). I then examine behavior that prey use to determine whether predators are in the vicinity (chapters 4 and 5) and to warn conspecifics about predation risk (chapter 6); in the main, these behaviors occur whether or not a predator sees the prey. Next I proceed to situations in which the predator has noticed the prey and the prey is trying to avoid being the target of an attack, either when it is alone (chapter 7) or is a member of a group (chapter 8). Then I progress to defenses that the prey uses to fend off attack if it becomes the target, splitting these into morphological (chapter 9) and behavioral defenses, the latter of which is again split into defenses used by individuals (chapter 10) and those employed by individuals in groups (chapter 11). Finally, I examine how animals escape from imminent predatory attack (chapter 12). It is important to note that more than one of these defenses can be used by a prey individual to thwart a predator and that an interaction between prey and predator could start at the beginning, middle, or end of this predatory sequence. Having surveyed these antipredator defenses in this logical sequence, I try to provide a framework for understanding antipredator defenses in animals (chapter 13).

1.3 Definitions

This book is entitled Antipredator Defenses in Birds and Mammals. Defenses refer to suites of behavioral, morphological, and, less commonly, physiological and life history characters that these two taxa use to avoid predation. The word defense carries no connotation of intent on the part of animals, of consciousness or of military stratagem, but it is used to describe the major categories of resistance that prey mount against predators. In a colloquial sense, defense signifies warding off attack and therefore encapsulates some specificity, whereas the words strategies and tactics (that conveniently refer to both morphological and behavioral traits) lack specificity and, to some, imply intent. Moreover, strategies are used in the literature on alternative reproductive phenotypes within the sexes where they denote a genetically based decision rule that results in the allocation of resources to alternative ways of behaving or to morphological characters. These alternative phenotypes are termed tactics (Gross 1996). The special meanings of these terms in reproductive decision making makes them inappropriate to use in an antipredator context, so I have avoided them.

1.3.a Adaptation and evolution The close resemblance between an animal's form and its environment, as between a stick insect and a twig, or between its form and that of another animal, such as the sphingid moth (Leucorampha ornatus) caterpillar and the head of a snake, is so surprising and wondrous that one cannot help but believe that natural selection has been instrumental in making these animals appear cryptic or mimetic to avoid attention of predators; but, from a scientific standpoint, it is troublesome to indulge in "uncritical guessing" about their function (Tinbergen 1963). The function of a character can be investigated in fiveways: (i) by arguing that the trait is sufficiently well designed for a task that it must have been shaped by natural selection to solve a problem faced by an organism; (ii) by demonstrating that interspecific variation in a putative antipredator trait is associated with particular species-related ecological or social factors where it might be particularly useful; (iii) by showing that intraspecific variation in a trait that appears designed to avoid predation is correlated with a component of reproduction or mortality, or better still, with lifetime reproductive success; (iv) by using simple models to predict the optimum solution to a problem based on known constraints and a suitable currency, and then observing whether the animal's behavior matches the prediction quantitatively; and (v) by experimentally eliminating or reducing (or enhancing) the appearance of a morphological or behavioral trait and comparing survivorship or reproduction with a control sample (G. C. Williams 1966). Arguably, these five approaches can be ranked from least to most rigorous in the order given. In addition, the evolution of a trait can be documented by placing its appearance and lossona phylogenetic tree, and by matching these events to the presence of social or ecological variables, evolutionary causation can be inferred (Sillen-Tullberg 1988). Historically, studies of antipredator defenses have principally used argument by design and experimental protocols to investigate function and have very rarely used optimality theory or tried to match defenses to lifetime reproductive success.

If a behavioral or morphological trait can be shown to serve a particular function using one or more of these approaches, it can be termed adaptive in the weak sense of bearers of the trait being more likely to leave more offspring in this and future generations than individuals that do not bear the trait (Clutton-Brock and Harvey 1979). Adaptation in the strong sense demands, in addition to conferring reproductive benefits now, the assumption that it did so in the past, knowing that the trait is heritable and that genetic differences between individuals are responsible for phenotypic differences in the appearance of the trait (Reeve and Sherman 1993). Unfortunately, there are very few examples in any vertebrate where we know that differences in antipredator defenses are determined even in part by genetic differences (Magurran et al. 1995), and no examples in homeotherms. Consequently, I have abstained from using the word adaptation (sensu stricto) in this book to avoid confusion between the two sorts of meaning.

One of the difficulties confronting researchers studying antipredator defenses is that a particular behavior may confer reproductive advantages on its bearer in several different ways, all related to avoiding predation. While the most important one of these mechanisms has, historically, been referred to as the primary function, in most cases it is extremely difficult to discern which are secondary or primary functions. Similarly, if a behavior helps prey escape predation at more than one phase in the predatory sequence, and this is evident in several instances (for example, grouping), then the efficiency with which predators capture prey at a particular phase in the sequence must be less than at other phases of the attack in order to be confident of the behavior's primary function (Vermeij 1982). Unfortunately, there are very few instances in which we have this sort of knowledge.

The book is principally about the evolution of antipredator defenses in the sense that I use a comparative perspective to highlight the diversity and distribution of antipredator defenses across homeothermic taxa. Note that evolution as understood here does not refer to the historical genesis of morphological traits within a clade, owing to the fact that remarkably little work has been done in this area. Modern comparative studies use statistical methods that reconstruct the phylogenetic history of a trait, but this method has been used only sparingly in antipredator studies and simply as a way to check whether shared ancestry could be responsible for the appearance of a trait in extant species (Caro et al. 2004) rather than as an investigative tool to determine when and where it arose over evolutionary time. Note also that evolution as used here does not refer to a change in gene frequencies, because we know so little about the genetics of any antipredator defense in warm-blooded animals despite classic evolutionary studies having been being conducted on invertebrates' defenses, including melanism in peppered moths (Biston betularia), crypsis in banded snails (Cepaea nemoralis), and polymorphisms in hawkmoth caterpillars (Ford 1964; Curio 1970).

(Continues...)

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Table of Contents

Preface, scope, and acknowledgments 

1 Definitions and predator recognition
1.1 Introduction
1.2 The predatory sequence
1.3 Definitions
1.3.a Adaptation and evolution
1.3.b Antipredator terminology
1.4 Ability of prey to recognize predators
1.5 Recognition by young animals
1.5.a Innate recognition
1.5.b Learning to recognize predators
1.6 Relaxed selection
1.7 Observer bias
1.8 Summary 

2 Morphological traits to avoid detection
2.1 Introduction
2.2 Background matching
2.2.a Color resemblance in mammals
2.2.b Color resemblance in birds
2.2.c Color resemblance in birds' eggs
2.2.d Special resemblance in birds' nests
2.2.e Melanism
2.2.f Changes in coloration with changing environments
2.2.g Masquerade
2.3 Concealing shadow
2.4 Disruptive coloration
2.5 Apostatic selection
2.6 Summary 

3 Behavioral mechanisms to avoid detection
3.1 Introduction
3.2 Nest site selection in birds
3.2.a Habitat type
3.2.b Distance from edges
3.2.c Habitat patch size
3.2.d Vegetation around the nest site
3.2.e Nest height
3.2.f Proximity to nests
3.2.g Distribution of nests
3.2.h Proximity to social insects
3.3 Behavior reducing the probability of predators detecting nests
3.4 Refuges
3.4.a Physical structures
3.4.b Habitat shifts in rodents
3.4.c Habitat shifts in ungulates
3.5 Reduced activity
3.5.a Hiding in ungulates
3.6 Changes in foraging under risk of predation
3.6.a When to eat
3.6.b Where to eat
3.6.c What to eat
3.6.d How much to eat
3.6.e Effects of age and reproductive condition on risk-sensitive foraging
3.7 Changes in reproduction under risk of predation
3.8 Summary 

4 Vigilance and group size
4.1 Introduction
4.2 Measures of vigilance
4.3 Benefits of individual vigilance
4.4 Costs of individual vigilance
4.5 Effects of group size on vigilance
4.5.a Increased probability of predator detection
4.5.b Reduced individual vigilance
4.5.c Increased foraging
4.6 Why don't individuals cheat?
4.6.a Predator detection is not collective
4.6.b Vigilant nondetectors are at an advantage
4.6.c Predators select low-vigilance individuals
4.6.d Individuals maintain vigilance so as not to lose group members
4.6.e Multiple attacks are possible
4.7 Vigilance in mixed-species groups
4.8 Summary 

5 Factors affecting vigilance
5.1 Introduction
5.2 Distance from conspecifics and perceived group size
5.3 Position in the group
5.4 Sentinels
5.5 The influence of cover
5.6 Age and parity
5.7 Sex differences and dominance
5.8 Miscellaneous factors
5.9 Predator abundance
5.10 Interspecific differences in vigilance
5.11 Summary 

6 Conspecific warning signals
6.1 Introduction
6.2 Acoustic constraints on alarm calls
6.2.a Localizability
6.2.b Detectability
6.3 Costs of warning signals
6.4 Benefits of warning signals
6.4.a Apparently selfish alarm calls
6.4.b Mutually beneficial alarm calls
6.4.c Altruistic and kin-selected alarm calls
6.5 Alarm calls between species
6.6 Variation in alarm calls
6.6.a Sciurids
6.6.b Birds
6.6.c Primates
6.7 Development of conspecific warning signals
6.7.a Ontogeny of response
6.7.b Ontogeny of alarm calls
6.8 Use of warning signals in deception
6.9 Summary 

7 Signals of unprofitability
7.1 Introduction
7.2 The evolution of aposematism
7.2.a Individual selection
7.2.b Kin selection
7.2.c Synergistic selection
7.3 Mechanisms by which predators select prey
7.3.a Single prey
7.3.b Aggregated prey
7.4 Aposematism in birds
7.4.a Mimicry in birds
7.5 Aposematism in mammals
7.6 Pursuit deterrence
7.6.a Low-cost perception advertisement signals
7.6.b Auditory signals of perception advertisement
7.6.c Inspection as perception advertisement
7.6.d Foot drumming as advertising predator monitoring
7.6.e Stotting as perception and quality advertisement
7.6.f Leaping as quality advertisement
7.6.g Song as quality advertisement
7.6.h Quality advertisement in poikilotherms
7.7 Summary 

8 Antipredator benefits of grouping
8.1 Introduction
8.1.a Definition of groups
8.2 The dilution effect
8.2.a Rates of encounter
8.2.b Reduced risk of capture
8.3 The Trafalgar effect
8.4 The confusion effect
8.4.a Oddity and confusion
8.5 Predator "swamping"
8.5.a Reproductive synchrony
8.6 Miscellaneous mechanisms
8.7 Position in the group
8.7.a Colonially nesting birds
8.7.b Flocks and herds
8.8 Primate groups
8.9 Ecocorrelates of antipredator grouping in homeotherms
8.10 Summary 

9 Morphological and physiological defenses
9.1 Introduction
9.2 Body size
9.2.a Body size and locomotor performance
9.3 Forms of locomotion
9.4 Spines and quills
9.5 Dermal plates and thickened skin
9.6 Weapons used for feeding
9.7 Sexually selected weaponry
9.8 Malodor and unpalatability
9.9 Venom resistance
9.10 Life history characteristics
9.11 Summary 

10 Nest defense
10.1 Introduction
10.2 Scope of nest defense activities
10.2.a The study of nest defense
10.3 Distraction displays
10.4 Costs of nest defense
10.5 Benefits of nest defense
10.5.a Driving predators away
10.5.b Silencing offspring
10.6 Effects of predation risk on nest defense
10.7 Parent's renesting potential
10.7.a Renesting potential within breeding seasons
10.7.b Renesting potential over lifetimes
10.8 Parental sex
10.9 Parental interactions
10.10 Offspring age
10.10.a Past and future parental investment
10.10.b Changes in offspring vulnerability
10.10.c Revisitation hypothesis
10.11 Offspring number
10.12 Offspring condition
10.12.a Harm-to-offspring hypothesis
10.13 Parental defense in mammals
10.14 Summary 

11 Mobbing and group defense
11.1 Introduction
11.2 Definition of mobbing
11.3 Variation in mobbing behavior
11.4 Costs of mobbing
11.5 Benefits of mobbing
11.5.a Direct benefits: lethal counterattack
11.5.b Direct benefits: the move-on hypothesis
11.5.c Direct benefits: perception advertisement
11.5.d Direct benefits: selfish-herd effect and confusion effect
11.5.e Direct benefits: attract the mightier
11.5.f Indirect benefits: alerting others
11.5.g Indirect benefits: silencing offspring
11.5.h Benefits unclear: cultural transmission
11.5.i Other hypotheses
11.6 Mobbing and group size
11.7 Mobbing and mixed-species associations in birds
11.8 Group defense in mammals
11.8.a Snake-directed behavior in sciurids
11.8.b Protective behavior in ungulates
11.8.c Group attacks in primates
11.9 Summary

Editorial Reviews

"A reviewer describes the book as 'a wonderful encyclopedic treatment of defenses against predators in mammals and birds,' but this description is incorrect insofar as it fails to mention that the book is also a great synthesis and magnificently organized. . . . A valuable information bank for any zoologist."

Journal of Mammal Evolution - Simone Teelen

"In-depth reviews of nearly every aspect of prey defenses make this essential reading for researchers and students embarking on studies of prey or predator behavior. The writing is clear and any reader is bound to encounter novel and intriguing material along the way. . . . An important contribution that will help integrate and bolster theoretically and empirically driven work in this field."

Ecology - Susan Lingle

"Antipredator Defenses in Birds and Mammals is a comprehensive review of what we know empirically of how animals avoid predation.... [It is] full of fascinating natural history stories that make it an easy and enjoyable read."

Ibis - Will Cresswell

This is a field that Caro has devoted much of his career to, and his comfort with the literature shows through. . . .Antipredator Defenses is a major contribution to the field and will be consulted for a long time to come. . . .Caro’s book is a comprehensive survey of the field, with well articulated arguments and balanced views. I recommend it unreservedly.”

Trends in Ecology and Evolution - Thomas N. Sherratt

"The work is technically clean and is graced with lovely and topical sketches at the head of each chapter. The treatment is quite nonmathematical and where equations are presented, they are explained quite clearly. . . . This is an important book. . . . Excellent for graduate-level seminars."

Auk

"This book is clearly and intelligently written. . . . It could be read with profit by active researchers in predation . . . by those with a more general interest in mammals and birds who are looking for a readable, reliable, and comprehensive reference in tihs area; and by undergraduates in courses related to ecology and animal behavior. . . . I can think of no better recommenation than the considerable number of my colleagues who have bought their own copy after having found themselves reluctant to ask me yet again to lend them mine!"

Bioscience - Graeme D. Ruxton

"An encyclopedic survey that is sure to be a much consulted classic."

Northeastern Naturalist