Theodore Stankowich

Fear in animals: a meta-analysis and review of risk assessment

The amount of risk animals perceive in a given circumstance (i.e. their degree of ‘fear’) is a difficult motivational state to study. While many studies have used flight initiation distance as a proxy for fearfulness and examined the factors influencing the decision to flee, there is no general understanding of the relative importance of these factors. By identifying factors with large effect sizes, we can determine whether anti-predator strategies reduce fear, and we gain a unique perspective on the coevolution of predator and anti-predator behaviour. Based on an extensive review and formal meta-analysis, we found that predator traits that were associated with greater risk (speed, size, directness of approach), increased prey distance to refuge and experience with predators consistently amplified the perception of risk (in terms of flight initiation distance). While fish tolerated closer approach when in larger schools, other taxa had greater flight initiation distances when in larger groups. The presence of armoured and cryptic morphologies decreased perception of risk, but body temperature in lizards had no robust effect on flight initiation distance. We find that selection generally acts on prey to be sensitive to predator behaviour, as well as on prey to modify their behaviour and morphology.

The re-emergence of felid camouflage with the decay of predator recognition in deer under relaxed selection

When a previously common predator disappears owing to local extinction, the strong source of natural selection on prey to visually recognize that predator becomes relaxed. At present, we do not know the extent to which recognition of a specific predator is generalized to similar looking predators or how a specific predator-recognition cue, such as coat pattern, degrades under prolonged relaxed selection. Using predator models, we show that deer exhibit a more rapid and stronger antipredator response to their current predator, the puma, than to a leopard displaying primitive rosettes similar to a locally extinct predator, an early jaguar. Presentation of a novel tiger with a striped coat engendered an intermediate speed of predator recognition and strength of antipredator behaviour. Responses to the leopard model slightly exceeded responses to a non-threatening deer model, suggesting that thousands of years of relaxed selection have led to the loss of recognition of the spotted coat as a jaguar-recognition cue, and that the spotted coat has regained its ability to camouflage the felid form. Our results shed light on the evolutionary arms race between adoption of camouflage to facilitate hunting and the ability of prey to quickly recognize predators by their formerly camouflaging patterns.

Evolution of weaponry in female bovids

Weaponry is ubiquitous in male ungulates and is driven by intrasexual selection, but the mystery surrounding its sporadic presence in females remains unsolved. Female horns are often smaller and shaped differently to male horns, suggesting a different function; indeed, hypotheses explaining the presence of female horns include competition for food, male mollification and defence against predators. Here we use comparative phylogenetic analyses to show that females are significantly more likely to bear horns in bovids that are conspicuous due to large body size and living in open habitats than inconspicuous species living in closed habitats or that are small. An inability to rely on crypsis or take refuge in deep vegetation has apparently driven the evolution of horns for defence against predators in female bovids, a finding supported by many field observations. Typically, exceptions are small species where females are territorial (e.g. duikers) and use horns in intrasexual contests. Furthermore, we suggest that conspicuousness and territoriality hypotheses may explain other instances of female cranial weaponry (i.e. antlers and ossicones) in other horned ruminants. Our phylogenetic reconstruction indicates that the primary function of horns in females is linked to antipredator defence in most clades, but occasionally to intrasexual competition in others.

Marginal predation methodologies and the importance of predator preferences

Correspondence: T. Stankowich, Psychology Department, Young Hall, One Shields Avenue, University of California, Davis, CA 95616, U.S.A. (email: tstankowich@ucdavis.edu). Biologists have studied group dynamics and attempted to define the benefits of gregariousness across diverse taxa for several decades. The relative costs and benefits of group living (reviewed in Krause & Ruxton 2002) may differ between group members so that each is under selection to maximize its individual fitness in different ways (Rubenstein 1978). For example, individuals on the edge of a group may have higher feeding rates but suffer higher predation risk, whereas those on the inside enjoy lower rates of predation but suffer reduced feeding rates (e.g. colonial spiders: Rayor & Uetz 1990). Many years ago ornithologists studying predation rates in colonialnesting birds reported that predation rates on eggs or fledglings were higher for solitary nests outside of the colony than for those inside the colony, and positions on the periphery of the colony were more susceptible to predation than central positions (e.g. Taylor 1962; Kruuk 1964; Patterson 1965). This phenomenon of differential predation risk within a group (i.e. a greater risk of predation on the periphery relative to the centre) is known as ‘marginal predation’. Similar early studies found the same phenomenon of differential risk in mobile animals (e.g. mammals: Galton 1871; birds: Wynne-Edwards 1962). Following these early studies, several mathematical and geometrical models of the benefits of group formation emerged, the most famous of which is Hamilton’s (1971) theory of the ‘selfish herd’, in which aggregations of animals form purely by selfish behaviour of individuals. Hamilton’s (1971) predictions were echoed and extended by Vine (1971) and since have been refined and formalized by computer models to show how within-group movements of individuals during attacks may minimize their individual predation risk (e.g. Morton et al. 1994; Gueron et al. 1996; Barta et al. 1997; Beecham & Farnsworth 1999; Viscido et al. 2001). While Hamilton’s (1971) ideas have been the inspiration behind most of the theoretical issues at hand, the problem with analysing the empirical validity of these models is that we do not have standardized methodologies for measuring marginal predation and benefits of aggregation.

Fifty years of chasing lizards: new insights advance optimal escape theory

Systematic reviews and meta‐analyses often examine data from diverse taxa to identify general patterns of effect sizes. Meta‐analyses that focus on identifying generalisations in a single taxon are also valuable because species in a taxon are more likely to share similar unique constraints. We conducted a comprehensive phylogenetic meta‐analysis of flight initiation distance in lizards. Flight initiation distance (FID) is a common metric used to quantify risk‐taking and has previously been shown to reflect adaptive decision‐making. The past decade has seen an explosion of studies focused on quantifying FID in lizards, and, because lizards occur in a wide range of habitats, are ecologically diverse, and are typically smaller and differ physiologically from the better studied mammals and birds, they are worthy of detailed examination. We found that variables that reflect the costs or benefits of flight (being engaged in social interactions, having food available) as well as certain predator effects (predator size and approach speed) had large effects on FID in the directions predicted by optimal escape theory. Variables that were associated with morphology (with the exception of crypsis) and physiology had relatively small effects, whereas habitat selection factors typically had moderate to large effect sizes. Lizards, like other taxa, are very sensitive to the costs of flight.

The function of zebra stripes

Despite over a century of interest, the function of zebra stripes has never been examined systematically. Here we match variation in striping of equid species and subspecies to geographic range overlap of environmental variables in multifactor models controlling for phylogeny to simultaneously test the five major explanations for this infamous colouration. For subspecies, there are significant associations between our proxy for tabanid biting fly annoyance and most striping measures (facial and neck stripe number, flank and rump striping, leg stripe intensity and shadow striping), and between belly stripe number and tsetse fly distribution, several of which are replicated at the species level. Conversely, there is no consistent support for camouflage, predator avoidance, heat management or social interaction hypotheses. Susceptibility to ectoparasite attack is discussed in relation to short coat hair, disease transmission and blood loss. A solution to the riddle of zebra stripes, discussed by Wallace and Darwin, is at hand.

A test of the multipredator hypothesis: yellow-bellied marmots respond fearfully to the sight of novel and extinct predators

Should prey retain an ability to respond to the sight of their extinct predators? The multipredator hypothesis ( Blumstein 2006 , Ethology, 112, 209–217) assumes that antipredator adaptations evolve together and thus prey may respond to extinct predators as long as they have experience with other predators. We tested this prediction in yellow-bellied marmots, Marmota flaviventris, a species with both extant and extinct predators. Marmots were baited to a predetermined location and then shown one of five life-size photographic stimuli: a medium-size sub-Saharan antelope, the gray duiker, Silvicapra grimmia, as a control stimulus; a red fox, Vulpes vulpes, a low-risk predator; a coyote, Canis latrans, a higher risk predator; a mountain lion, Felis concolor, an extant predator, but one with which our population had no ontogenetic experience; and a wolf, Canis lupus, an extinct predator. Marmots responded differently to each stimulus: they stopped foraging after seeing the duiker, engaged in low vigilance after seeing the fox, seemed to monitor the coyote, fled the wolf, and engaged in high vigilance (and on one occasion alarm-called) in response to the mountain lion. This pattern of responses was consistent with the different risks associated with each species: foxes required monitoring but marmots could generally escape them, coyotes routinely kill adult marmots, solitary hunting mountain lions might be dissuaded from attack once detected, and socially hunting wolves were a very high risk predator, which would be best hidden from. The pattern of responses was not explained simply by stimulus size, stimulus detectability, or stimulus similarity. These results are consistent with the multipredator hypothesis: visual predator discrimination for ontogenetically and evolutionarily novel predators may be maintained in yellow-bellied marmots by extant predation risk.

The functional significance of colouration in cetaceans

Cetaceans show many of the classic mammalian colouration patterns, such as uniform colouration, countershading, and prominent patches of colour, all within one relatively small taxon. We collated all the functional hypotheses for cetacean colouration that have been put forward in the literature and systematically tested them using comparative phylogenetic analyses. We found that countershading is a mechanism by which smaller cetacean species may avoid being seen by their prey. We discovered that prominent markings are associated with group living, fast swimming, and ostentatious behaviour at the surface, suggesting that they function in intraspecific communication. White markings on several parts of the body seem to be involved in the capture of fish, squid, and krill. Therefore, several different selection pressures have shaped the great diversity of skin colouration seen in extant cetaceans, although background matching, disruptive colouration and interspecific communication do not appear to be involved.

ECOLOGICAL DRIVERS OF ANTIPREDATOR DEFENSES IN CARNIVORES

Mammals have evolved several morphological and behavioral adaptations to reduce the risk of predation, but we know little about the ecological factors that favor their evolution. For example, some mammalian carnivores have the ability to spray noxious anal secretions in defense, whereas other species lack such weaponry but may instead rely on collective vigilance characteristic of cohesive social groups. Using extensive natural history data on 181 species in the order Carnivora, we created a new estimate of potential predation risk from mammals and birds of prey and used comparative phylogenetic methods to assess how different sources of predation risk and other ecological variables influence the evolution of either noxious weaponry or sociality in this taxon. We demonstrate that the evolution of enhanced spraying ability is favored by increased predation risk from other mammals and by nocturnality, but the evolution of sociality is favored by increased predation risk from birds of prey and by diurnality, which may allow for enhanced early visual detection. These results suggest that noxious defenses and sociality are alternative antipredator strategies targeting different predator guilds under different lighting conditions.

Armed and dangerous: predicting the presence and function of defensive weaponry in mammals

Mammals possess a wide range of behavioral and morphological adaptations to help detect, assess, deter, and escape from predators, including weaponry that is useful in antipredator defense. While some weapons have evolved in response to natural selection for defense against predators, others may have evolved to serve some other primary function (e.g., intraspecific aggression) but still have defensive uses. In this comprehensive review of extreme morphological weaponry in mammals, I explore specific hypotheses regarding the ecological, morphological, and behavioral correlates of different types of weaponry in order to explain why some taxa have evolved elaborate weapons while others have not. I provide evidence demonstrating that several types of defensive weaponry (e.g., spines, quills, armor, noxious anal secretions) have evolved directly in response to significantly increased potential predation risk. Further, other structures that evolved primarily for intrasexual competition (e.g., cranial weaponry, tusks) or foraging (e.g., enlarged claws) but have additional defensive benefits are more likely to be found in larger species that are able to defend themselves in physical combat. Further comprehensive phylogenetic and comparative studies are needed to confirm the proposed hypotheses regarding selection, ecology, and function.