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.     

Reduced flocking by birds on islands with relaxed predation

Adaptive hypotheses for the evolution of flocking in birds have usually focused on predation avoidance or foraging enhancement. It still remains unclear to what extent each factor has contributed to the evolution of flocking. If predation avoidance were the sole factor involved, flocking should not be prevalent when predation is relaxed. I examined flocking tendencies along with mean and maximum flock size in species living on islands where predation risk is either absent or negligible and then compared these results with matched counterparts on the mainland. The dataset consisted of 46 pairs of species from 22 different islands across the world. The tendency to flock was retained on islands in most species, but in pairs with dissimilar flocking tendencies, island species were less likely to flock. Mean and maximum flock size were smaller on islands than on the mainland. Potential confounding factors such as population density, nest predation, habitat type, food type and body mass failed to account for the results. The results suggest that predation is a significant factor in the evolution of flocking in birds. Nevertheless, predation and other factors, such as foraging enhancement, probably act together to maintain the trait in most species.     

Changes in the flocking behaviour of wintering English titmice with time,weather and supplementary food

Over the course of one winter, the food supply of birds living in a deciduous woodland in southern England was supplemented and unsupplemented during alternating periods. In the presence of substantial predation pressure from hawks, the sociality of blue tits, Parus caeruleus, and great tits, P. major, showed significant partial correlations with several weather and temporal factors when the woodland was unsupplemented. Such correlations between social behaviour and abiotic factors diminished significantly when the birds had access to extra food. Blue tits and great tits without access to supplemental food flocked significantly more often with other species while foraging than when they were food-supplemented. Long-tailed tits, Aegithalos caudatus, ignored the artificial food and foraged in mixed-species flocks to the same extent in both unsupplemented and food-supplemented periods. Results disprove the hypothesis that mixed-species foraging groups are caused by increased predation protection alone, and they support the hypotheses that mixed-species foraging groups are caused by increased foraging efficiency alone or by a combination of increased foraging efficiency and increased protection from predators.     

Bird mixed‐species flock formation is driven by low temperatures between and within seasons in a Subtropical Andean‐foothill forest

According to both the predation avoidance and foraging efficiency hypotheses, birds within mixed flocks increase their foraging efficiency and/or can spend more time feeding and less time looking out for predators. These hypotheses predict that birds in mixed flocks obtain benefits. Thus, mixed flock formation could serve as a strategy to cope with difficult conditions imposed on birds such as climatic conditions that ultimately result in a change in predation pressure or food resources. We evaluate the hypotheses that forming part of a flock confers benefits to its members and the associated prediction that birds will take advantage of these benefits and flock more often under cold and dry weather conditions between and within seasons to cope with such conditions. We surveyed the presence of mixed flocks, flocking propensity, number of species and individuals in mixed flocks in the Subtropical Yungas foothill of Argentina, to examine seasonality, flocking behavior of birds and their responses to two climatic variables: temperature and humidity. Bird species presented a higher flocking propensity and mixed flocks occurred more frequently during the dry and cold seasons than during the more benign seasons, and lower values of temperature within seasons triggered the flocking behavior. Although effects between seasons were expected, birds also showed a short‐term response to small changes in temperature within seasons. These results strengthen the ideas proposed by the foraging hypothesis. Although benefits derived from flocking have yet to be determined, whatever they are should be understood in the context of seasonal variation in life‐history traits.     

The evolution of communal roosting in birds: origin and secondary losses

Three main benefits are thought to underlie communal roostingin birds: a reduction in thermoregulation demands, a decreasein predation risk, and an increase in foraging efficiency. Iinvestigated interspecific variation in communal roosting tendenciesacross categories of several ecological factors to examine therelevance of each functional hypothesis in the evolutionary transitionto communal roosting and the secondary reversal to solitary roostinghabits. The study phylogenetic tree included 30 families and437 species. Evolutionary transitions to communal roosting occurredmore often on branches with flocking species and with largerspecies but were not associated with diet, territoriality, geographicalarea, or time of day. The association with flocking activitiessuggests that increased foraging efficiency, a factor thoughtto operate through the formation of flocks, may have been akey factor in the origin of avian communal roosting. However,several transitions to communal roosting occurred on brancheswith nonflocking species, indicating that foraging efficiencymay not be the only factor involved in the evolution of communalroosting. Secondary losses of communal roosting habits occurredon several branches, with a concomitant loss of flocking behaviorand a tendency to exhibit territorial behavior and nocturnalforaging. Secondary losses suggest that communal roosting iscostly to perform and maintain and may be lost when an asocialselection regime operates. The large number of exceptions tothe above patterns may force a reevaluation of current functional hypothesesabout communal roosting in birds.     

Group-foraging is not associated with longevity in North American birds

Group-foraging is common in many animal taxa and is thought to offer protection against predators and greater foraging efficiency. Such benefits may have driven evolutionary transitions from solitary to group-foraging. Greater protection against predators and greater access to resources should reduce extrinsic sources of mortality and thus select for higher longevity according to life-history theory. I assessed the association between group-foraging and longevity in a sample of 421 North American birds. Taking into account known correlates of longevity, such as age at first reproduction and body mass, foraging group size was not correlated with maximum longevity, with and without phylogenetic correction. However, longevity increased with body mass in non-passerine birds. The results suggest that the hypothesized changes in predation risk with group size may not correlate with mortality rate in foraging birds.     

Prey size affects the costs and benefits of group predation in nymphs of the predatory stink bug Andrallus spinidens (Heteroptera: Pentatomidae)

Group predation promotes foraging efficiency because it increases the size of prey that can be killed and improves hunting success compared to solitary predation. However, group predation may increase competition among group members during feeding. Earlier studies have focused on the advantages of group predation, but little is known about the costs and benefits of group predation for individual members of the group. Here, we show that the costs and benefits of group predation for individuals of the predatory stink bug Andrallus spinidens vary with prey size in laboratory experiments. We found that when A. spinidens fed on small prey, group predation did not significantly increase foraging efficiency but did increase competition for food among group members. In contrast, when prey was large, group predation promoted foraging efficiency, and competition over food was not detected. Our results suggest that group predation by A. spinidens nymphs is advantageous for individual members because it enables each member to hunt larger prey that could not be hunted alone. However, when group size was large or prey size was small, group predation increased competition among group members.     

Evolving the selfish herd: emergence of distinct aggregating strategies in an individual-based model

From zebra to starlings, herring and even tadpoles, many creatures move in an organized group. The emergent behaviour arises from simple underlying movement rules, but the evolutionary pressure which favours these rules has not been conclusively identified. Various explanations exist for the advantage to the individual of group formation: reduction of predation risk; increased foraging efficiency or reproductive success. Here, we adopt an individual-based model for group formation and subject it to simulated predation and foraging; the haploid individuals evolve via a genetic algorithm based on their relative success under such pressure. Our work suggests that flock or herd formation is likely to be driven by predator avoidance. Individual fitness in the model is strongly dependent on the presence of other phenotypes, such that two distinct types of evolved group can be produced by the same predation or foraging conditions, each stable against individual mutation. We draw analogies with multiple Nash equilibria theory of iterated games to explain and categorize these behaviours. Our model is sufficient to capture the complex behaviour of dynamic collective groups, yet is flexible enough to manifest evolutionary behaviour.     

The starvation–predation risk trade-off, body mass and population status in the Common Starling Sturnus vulgaris

It is theoretically and empirically well established that body mass variation in small birds reflects a trade-off between starvation risk and predation risk. This occurs because carrying increased fat reserves reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, therefore, the theory of mass-dependent predation risk could be used to understand how a bird perceives and responds to the risks in its environment, because its mass will reflect the predictability of foraging opportunities and predation risk. Mass in birds may then provide a relatively straightforward way of assessing the foraging environment of birds and so the potential conservation problems a species faces. This study tests, for the first time for any species, how body mass changes in response to changing starvation risk, changing predation risk and changing population status. Common Starling Sturnus vulgaris mass varies as predicted by starvation–predation risk trade-off theory: mass is lower when foraging conditions are more favourable and when predation risk is increased. The populations that are declining the most strongly have higher mass, which is most likely indicative of a poor foraging environment, leading to lower relative survival. The results suggest that increased mass in Starlings, and possibly in other species, may provide an indication of the poor quality of the foraging environment and/or rapidly declining populations.     

Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest

Forming interspecific associations is one of many strategies adopted by primates in order to avoid predation. In addition to improved predator detection and avoidance, benefits of interspecific associations relate to improved foraging efficiency. In this study we tested these two hypotheses explaining associations between the endangered golden-headed lion tamarin, Leontopithecus chrysomelas and the sympatric Wied's marmoset, Callithrix kuhlii. We estimated predation risk by recording the number of encounters between lion tamarins and potential predators in cabruca agroforest (shaded cacao plantation) and in mosaic forest (a mix of cabruca, primary and secondary forest). To evaluate if the association between the two species was related to foraging benefits we recorded the number of associations between the two species when the lion tamarins were eating and when they were not eating. To test if the association occurred to improve predator detection and avoidance, we evaluated if associations between the species were more frequent in areas with higher predation risk and during the part of the day when predation risk is higher. We also compared the number of associations 3 months before birth events and 3 months after, when the lion tamarins are more susceptible to predation. Predation risk, mainly by raptors, was significantly higher in cabruca than in mosaic forest (0.17 and 0.05 encounters with predators per hour of observation, respectively). Associations were significantly more frequent after birth events and during the part of the day when predation risk was also higher (5-6 am until noon). We did not observe any direct evidence of foraging-related advantages of interspecific associations for the lion tamarins. The tamarins did not associate more when they were foraging. Our findings suggest that lion tamarins are more exposed to predation in cabruca than in mosaic forest and associations between lion tamarins and Wied's marmosets are related to predation avoidance.     

Foraging Patch Selection in Winter: A Balance between Predation Risk and Thermoregulation Benefit

In winter, foraging activity is intended to optimize food search while minimizing both thermoregulation costs and predation risk. Here we quantify the relative importance of thermoregulation and predation in foraging patch selection of woodland birds wintering in a Mediterranean montane forest. Specifically, we account for thermoregulation benefits related to temperature, and predation risk associated with both illumination of the feeding patch and distance to the nearest refuge provided by vegetation. We measured the amount of time that 38 marked individual birds belonging to five small passerine species spent foraging at artificial feeders. Feeders were located in forest patches that vary in distance to protective cover and exposure to sun radiation; temperature and illumination were registered locally by data loggers. Our results support the influence of both thermoregulation benefits and predation costs on feeding patch choice. The influence of distance to refuge (negative relationship) was nearly three times higher than that of temperature (positive relationship) in determining total foraging time spent at a patch. Light intensity had a negligible and no significant effect. This pattern was generalizable among species and individuals within species, and highlights the preponderance of latent predation risk over thermoregulation benefits on foraging decisions of birds wintering in temperate Mediterranean forests.     

Foraging behaviour of Lesser Sheathbills Chionis minor exploiting invertebrates on a sub-Antarctic island

Summary During winter (May through October) many Lesser Sheathbills Chionis minor at Marion Island in the sub-Antarctic were obliged to leave their preferred foraging habitat in penguin colonies to forage for invertebrates on the island's coastal plain. The study describes factors affecting feeding success, time budgets and predation risk of the sheathbills which exploited these small, patchily dispersed prey. The birds appeared to select prey 1 mm in diameter, and ignore smaller, common invertebrates.Sheathbills were highly selective of foraging habitat. During 17 censuses made through the winter, 97% of the 1,504 birdsightings were at only eight of the 19 available vegetation types. Multiple regression analysis revealed that prey density was the most important criterion in habitat preference, followed by plant canopy height and distance of the habitat from the sea. These variables accounted for 78% of the variance of habitat use. Focal-animal observations in a sample of habitats showed that feeding success was correlated with prey density and distance from the sea. Tall vegetation impeded the locomotion and foraging of sheathbills. The sheathbills reduced predation risk from skuas Catharacta lonnbergi and travelling time by foraging near the shore. The spatial distribution of prey within vegetation types was apparently unimportant in habitat selection.During winter 83% of the sheathbills in the study foraged communally and 98% roosted communally. Flocks occurred only on good quality habitat and flocking probably facilitated habitat selection. Feeding success increased initially with increasing flock size but decreased in flocks greater than 15 birds, which was attributed to localized prey deletions. The sheathbills spent 88% of the daytime foraging; and feeding, looking around and walking comprised 99% of foraging time. Feeding time increased with increasing flock size, looking around decreased but walking was unaffected. Aggression was rare, was unaffected by flock size and did not significantly affect feeding. A probability model showed that sheathbills could greatly reduce predation risk by flocking but the benefits would not improve much in flocks greater than eight birds.The habitat selection, time budgets and feeding success of adults, subadults and juveniles were very similar.The exploitation of terrestrial invertebrates by sheathbills was interpreted as an expansion of the population's trophic niche to tap an underexploited resource on a species-poor island.     

Sociality, age at first reproduction and senescence: comparative analyses of birds

Evolutionary theories of senescence suggest that aging evolves as a consequence of early reproduction imposing later viability costs, or as a consequence of weak selection against mutations that act late in life. In addition, highly social species that live in sites that are protected from extrinsic mortality due to predation should senesce at a slower rate than solitary species. Therefore, species that start reproducing late in life should senesce at a slower rate than species that start reproducing early. In addition, social species should senesce more slowly than solitary species. Here I investigate the rate of senescence using an extensive data set on longevity records under natural field conditions to test predictions about the evolution of senescence among 271 species of birds. Longevity records increased with sampling effort and body mass, but once these confounding variables were controlled statistically, there was a strongly positive relationship between relative longevity and relative adult survival rate. Relative longevity after controlling statistically for sampling effort, body mass and adult survival rate, increased with age at first reproduction, but not with degree of breeding sociality. These findings suggest that the evolution of senescence is related to timing of first reproduction, but that the evolution of breeding sociality has played a negligible role in the evolution of senescence.     

Wintering birds avoid warm sunshine: predation and the costs of foraging in sunlight

Wintering birds can gain significant thermal benefits by foraging in direct sunlight. However, exposure to bright sunlight might make birds easier to detect by predators and may also cause visual glare that can reduce a bird’s ability to monitor the environment. Thus, birds likely experience a trade-off between the thermal benefits and predation-related costs of foraging in direct sunlight. To examine this possible thermoregulation-predation trade-off, we monitored the behavior of mixed-species flocks of wintering emberizid sparrows foraging in alternating strips of sunlight and shade. On average, these sparrows routinely preferred to forage in the shade, despite midday air temperatures as much as 30 °C below their thermoneutral zone. This preference for shade was strongest at relatively high temperatures when the thermal benefits of foraging in sunlight were reduced, suggesting a thermoregulation-predation trade-off. Glare could be reduced if birds faced away from the sun while feeding in direct sunlight, but we found that foraging birds tended to face southward (the direction of the sun). We speculate that other factors, such as the likely direction of predator approach, may explain this southerly orientation, particularly if predators use solar glare to their advantage during an attack. This interpretation is supported by the fact that birds had the weakest southerly orientation on cloudy days. Wintering birds may generally avoid foraging in direct sunlight to minimize their risk of predation. However, given the thermal benefits of sunshine, such birds may benefit from foraging in habitats that provide a mosaic of sunlit and shaded microhabitats.     

Lunar Philia in a Nocturnal Primate

The influence of moonlight on behavior has been well documented for many nocturnal mammals, including rodents, lagomorphs, badgers and bats. These studies have consistently shown that nocturnal mammals respond to bright moonlight by reducing their foraging activity, restricting their movement, and reducing their vocalizations. Lunar phobia among nocturnal mammals is generally believed to be a form of predator avoidance: numerous studies indicate that predation increases during moonlit nights. A study I conducted at Tangkoko Nature Reserve in Sulawesi, Indonesia, demonstrates that spectral tarsiers, (Tarsius spectrum), are not lunar phobic, but are lunar philic; they become more active during full moons. During full moons, spectral tarsiers increased foraging, decreased resting, increased travel (distance traveled per unit time, nightly path length, and home range size), increased the frequency of group travel and decreased the frequency of olfactory communication. I explore several potential hypotheses to account for the lack of lunar phobia and potential increased risk of predation resulting from this unusual behavior. Two hypotheses that may account for the behavior are that: 1) foraging efficiency increases during full moons and outweighs the increased risk of predation, and 2) predation risk is not greater during full moons. Instead, predation risk increases during new moons.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

Mass regulation in response to predation risk can indicate population declines

In theory, survival rates and consequent population status might be predictable from instantaneous behavioural measures of how animals prioritize foraging vs. avoiding predation. We show, for the 30 most common small bird species ringed in the UK, that one quarter respond to higher predation risk as if it is mass-dependent and lose mass. Half respond to predation risk as if it only interrupts their foraging and gain mass thus avoiding consequent increased starvation risk from reduced foraging time. These mass responses to higher predation risk are correlated with population and conservation status both within and between species (and independently of foraging habitat, foraging guild, sociality index and size) over the last 30 years in Britain, with mass loss being associated with declining populations and mass gain with increasing populations. If individuals show an interrupted foraging response to higher predation risk, they are likely to be experiencing a high quality foraging environment that should lead to higher survival. Whereas individuals that show a mass-dependent foraging response are likely to be in lower quality foraging environments, leading to relatively lower survival.     

Predation avoidance and foraging efficiency contribute to mixed-species shoaling by tropical and temperate fishes

The formation of mixed-species social groups, whereby heterospecifics form and maintain either transient or stable groups with each other, can confer substantial fitness benefits to individuals. Such benefits may arise via multiple mechanisms associated with both predation avoidance and foraging efficiency. In fishes, mixed-species shoaling reportedly occurs where displaced tropical species (known as “vagrants”) interact with resident temperate species, although little is known about the nature and frequency of such interactions. To investigate this phenomenon, we used displaced tropical Indo-pacific Sergeant Abudefduf vaigiensis settling in temperate south-eastern Australia as a model system. Underwater visual surveys revealed shoal composition and size differed significantly between open-water and reef habitats, with shoals in open habitats being larger and more speciose. Shoals containing A. vaigiensis were mainly mixed-species, and larger and more speciose in open habitats than nearer to reef. Since both foraging efficiency (via access to plankton) and predation threat likely increase with increasing distance from reef habitat, we suggest that mixed-species shoaling mitigates predation risk whilst allowing increased foraging opportunities for A. vaigiensis in open areas. These findings provide support for the importance of mixed-species shoaling to the persistence of tropical reef fishes in temperate regions.     

Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation

A growing body of work suggests that breeding birds have a significant capacity to assess and respond, over ecological time, to changes in the risk of predation to both themselves and their eggs or nestlings. This review investigates the nature of this flexibility in the face of predation from both behavioural and reproductive perspectives, and also explores several directions for future research. Most available work addresses different aspects of nest predation. A substantial change in breeding location is perhaps the best documented response to nest predation, but such changes are not always observed and not necessarily the best strategy. Changes in nesting microhabitat (to more concealed locations) following predation are known to occur. Surprisingly little work addresses the proactive avoidance of areas with many nest predators, but such avoidance is probably widespread. Individual birds could conceivably adopt anti‐predator strategies based on the nest predators actually present in an area, but such effects have yet to be demonstrated. In fact, the ways in which birds assess the risk of nest predation is unclear. Nest defence in birds has historically received much attention, but little is known about how it interacts with other aspects of decision‐making by parents. Other studies concentrate on predation risk to adults. Some findings suggest that risk to adults themselves influences territory location, especially relative to raptor nests. An almost completely unexplored area concerns the sorts of social protection from predators that might exist during the breeding season. Flocking typical of the non‐breeding season appears unusual while breeding, but a mated pair may sometimes act as a “flock of two”. Opportunistic heterospecific sociality may exist, with heterospecific protector species associations more prevalent than currently appreciated. The dynamics of singing during the breeding season may also respond to variation in predation risk, but empirical research on this subject is limited. Furthermore, a few theoretical and empirical studies suggest that changes in predation risk also influence the behaviour of lekking males. The major influence of predators on avian life histories is undoubtedly expressed at a broad phylogenetic scale, but several studies hint at much flexibility on an ecological time scale. Some species may forgo breeding completely if the risk of nest predation is too high, and a few studies document smaller clutch sizes in response to an increase in nest predation. Recent evidence suggests that a female may produce smaller eggs rather than smaller clutches following an increase in nest predation risk. Such an increase may also influence decisions about intraspecific brood parasitism. There are no clear examples of changes in clutch/egg size with changes in risk experienced by adults, but parental responses to predators have clear consequences for offspring fitness. Changes in risk to adults may also influence body mass changes across the breeding season, although research here is sparse. The topics highlighted herein are all in need more empirical attention, and more experimental field work whenever feasible.     

Non-random foraging in certain bird pests of field crops

Two systems of bird-crop interactions were studied to explain the between- and the within-field variation in the foraging pattern of bird pests in agro-ecosystems. Weaverbirds and munias select rice fields with greater vegetation complexity and not based on the resource status. Within a selected area the concentration of feeding birds was greater close to vegetation cover and decreased non-linearly with increase in distance. Certain structural features and earhead characters of rice plants predisposed particular varieties for intense grain predation by birds. In the parakeet-sunflower system the extent of damage among plants within a field was closely linked to the foraging pattern of parakeets. The extent of achene predation by parakeets was influenced by certain structural features of sunflower plants and not the resource load of each plant. Selective feeding on sunflower plants was governed by the predator vigilance pattern; parakeets prefer to feed on plants that offered better field of vision. The results suggest that the observed pattern of foraging by bird pests in agro-ecosystems is non-random and is dependent on factors favouring predator avoidance behaviour and not on resource maximization.