Group size elicits specific physiological response in herbivores

With increasing group size, individuals commonly spend less time standing head-up (scanning) and more time feeding. In small groups, a higher predation risk is likely to increase stress, which will be reflected by behavioural and endocrine responses. However, without any predator cues, we ask how the predation risk is actually processed by animals as group size decreases. We hypothesize that group size on its own acts as a stressor. We studied undisturbed groups of sheep under controlled pasture conditions, and measured in situ the cortisol and vigilance responses of identified individuals in groups ranging from 2 to 100 sheep. Both vigilance and average cortisol concentration decreased as group size increased. However, the cortisol response varied markedly among individuals in small groups, resulting in a lack of correlation between cortisol and vigilance responses. Further experiments are required to explore the mechanisms that underlie both the decay and the convergence of individual stress in larger groups, and whether these mechanisms promote adaptive anti-predator responses.     

Many eyes or many ewes: vigilance tactics in female bighorn sheep Ovis canadensis vary according to reproductive status

In gregarious animals, there is usually a negative relationship between individual vigilance and group size. This effect of group size is generally explained by increasing probability of predator detection (the many-eyes hypothesis) and by the dilution of risk occurring in larger groups. Few studies have attempted to examine the specific implications of either hypothesis on the expected vigilance pattern of an animal. Here we examine whether reproductive status affects vigilance patterns in bighorn sheep Ovis canadensis ewes. We also test whether the observed vigilance patterns are consistent with predictions from dilution or detection models of vigilance. Although vigilance decreased with increasing group size, vigilance tactics differed between barren and lactating females. Lactating ewes relied solely on predator detection. In contrast, barren ewes benefited from both detection and dilution effects when group size increased and adjusted vigilance effort according to the proportion of lactating ewes in their group. It is generally assumed that gregariousness increases safety. Here we further show that reproductive status influenced how animals reduce predation risk and that some individuals take advantage of the vigilance effort provided by others.     

Fixed vs. Random Temporal Predictability of Predation Risk: An Extension of the Risk Allocation Hypothesis

Predation is a strong selective force acting on prey animals. Predation is by nature highly variable in time; however, this aspect of predation risk has traditionally been overlooked by behavioural ecologists. Lima and Bednekoff proposed the predation risk allocation hypothesis (RAH), predicting how temporal variation in predation risk drives prey antipredator behaviours. This model is based on the concept that prey adaptively allocate their foraging and antipredator efforts across high‐ and low‐risk situations, depending on the duration of high‐ vs. low‐risk situations and the relative risk associated with each of them. An unstudied extension of the RAH is the effect of predictability of predation risk. A predictable risk should lead to prey displaying minimal vigilance behaviours during predictable low‐risk periods and the strongest antipredator behaviours during risky periods. Conversely, an unpredictable predation risk should result in prey displaying constant vigilance behaviour, with suboptimal foraging rates during periods of safety but antipredator behaviours of lower intensity during periods of risk. We tested this extension of the RAH using convict cichlids exposed to high‐risk alarm cues at two frequencies of risk (1× vs. 3×) per day, on either a fixed or random schedule for 5 d. We then tested the fish for a response to high‐risk cues (alarm cues) and to low‐risk cues (disturbance resulting from the introduction of distilled water). Our study supports previous results on the effects of risk frequency and cue intensity on cichlid behaviour. We failed to show an effect of risk predictability on the behavioural responses of cichlids to high‐risk alarm cues, but predictability did influence responses to low‐risk cues. We encourage further studies to test the effect of predictability in other systems.     

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.     

Behavioural adjustment in response to increased predation risk: a study in three duck species

Predation directly triggers behavioural decisions designed to increase immediate survival. However, these behavioural modifications can have long term costs. There is therefore a trade-off between antipredator behaviours and other activities. This trade-off is generally considered between vigilance and only one other behaviour, thus neglecting potential compensations. In this study, we considered the effect of an increase in predation risk on the diurnal time-budget of three captive duck species during the wintering period. We artificially increased predation risk by disturbing two groups of 14 mallard and teals at different frequencies, and one group of 14 tufted ducks with a radio-controlled stressor. We recorded foraging, vigilance, preening and sleeping durations the week before, during and after disturbance sessions. Disturbed groups were compared to an undisturbed control group. We showed that in all three species, the increase in predation risk resulted in a decrease in foraging and preening and led to an increase in sleeping. It is worth noting that contrary to common observations, vigilance did not increase. However, ducks are known to be vigilant while sleeping. This complex behavioural adjustment therefore seems to be optimal as it may allow ducks to reduce their predation risk. Our results highlight the fact that it is necessary to encompass the whole individual time-budget when studying behavioural modifications under predation risk. Finally, we propose that studies of behavioural time-budget changes under predation risk should be included in the more general framework of the starvation-predation risk trade-off.     

Applying behavioral-ecological theory to plant defense: light-dependent movement in Mimosa pudica suggests a trade-off between predation risk and energetic reward

Many animal species tolerate different amounts of predation risk based on environmental conditions and the individual's own condition, often accepting greater risk when energetically stressed. We studied the sensitive plant Mimosa pudica to see whether it too accepts greater risk of predation when less light energy is available. This plant displays a defensive behavior of rapidly folding its leaves when stimulated by touch, thereby decreasing visibility to herbivores. Averting herbivory involves a trade-off because leaf closure results in a reduction in light foraging. We manipulated the light environment of individual M. pudica plants and recorded the time it took a plant to reopen its leaves following stimulation as a measure of tolerance of predation risk. As predicted by theory, avoidance behavior was sustained longer under high light conditions than under more light-limited conditions. These findings suggest this species balances the risk and reward of antiherbivore behavior in relation to current environmental conditions and that behavioral-ecological theory is a useful framework for understanding plant responses to predators.     

Titrating the cost of plant toxins against predators: determining the tipping point for foraging herbivores

1. Foraging herbivores must deal with plant characteristics that inhibit feeding and they must avoid being eaten. Principally, toxins limit food intake, while predation risk alters how long animals are prepared to harvest resources. Each of these factors strongly affects how herbivores use food patches, and both constraints can pose immediate proximate costs and long-term consequences to fitness. 2. Using a generalist mammalian herbivore, the common brushtail possum (Trichosurus vulpecula), our aim was to quantitatively compare the influence of plant toxin and predation risk on foraging decisions. 3. We performed a titration experiment by offering animals a choice between non-toxic food at a risky patch paired with food with one of five toxin concentrations at a safe patch. This allowed us to identify the tipping point, where the cost of toxin in the safe food patch was equivalent to the perceived predation risk in the alternative patch. 4. At low toxin concentration, animals ate more from the safe than the risky patch. As toxin concentration increased at the safe patch, intake shifted until animals ate mainly from the risky patch. This shift was associated with behavioural changes: animals spent more time and fed longer at the risky patch, while vigilance increased at both risky and safe patches. 5. Our results demonstrate that the variation in toxin concentration, which occurs intraspecifically among plants, can critically influence the relative cost of predation risk on foraging. We show that herbivores quantify, compare and balance these two different but proximate costs, altering their foraging patterns in the process. This has potential ecological and evolutionary implications for the production of plant defence compounds in relation to spatial variation in predation risk to herbivores.     

Hazardous duty pay and the foraging cost of predation

We review the concepts and research associated with measuring fear and its consequences for foraging. When foraging, animals should and do demand hazardous duty pay. They assess a foraging cost of predation to compensate for the risk of predation or the risk of catastrophic injury. Similarly, in weighing foraging options, animals tradeoff food and safety. The foraging cost of predation can be modelled, and it can be quantitatively and qualitatively measured using risk titrations. Giving‐up densities (GUDs) in depletable food patches and the distribution of foragers across safe and risky feeding opportunities are two frequent experimental tools for titrating food and safety. A growing body of literature shows that: (i) the cost of predation can be big and comprise the forager's largest foraging cost, (ii) seemingly small changes in habitat or microhabitat characteristics can lead to large changes in the cost of predation, and (iii) a forager's cost of predation rises with risk of mortality, the forager's energy state and a decrease in its marginal value of energy. In titrating for the cost of predation, researchers have investigated spatial and temporal variation in risk, scale‐dependent variation in risk, and the role of predation risk in a forager's ecology. A risk titration from a feeding animal often provides a more accurate behavioural indicator of predation risk than direct observations of predator‐inflicted mortality. Titrating for fear responses in foragers has some well‐established applications and holds promise for novel methodologies, concepts and applications. Future directions for expanding conceptual and empirical tools include: what are the consequences of foraging costs arising from interference behaviours and other sources of catastrophic loss? Are there alternative routes by which organisms can respond to tradeoffs of food and safety? What does an animal's landscape of fear look like as a spatially explicit map, and how do various environmental factors affect it? Behavioural titrations will help to illuminate these issues and more.     

Reptile responses to fire and the risk of post-disturbance sampling bias

Altered fire regimes are a driver of biodiversity decline. To plan effective management, we need to know how species are influenced by fire and to develop theory describing fire responses. Animal responses to fire are usually measured using methods that rely on animal activity, but animal activity may vary with time since fire, potentially biasing results. Using a novel approach for detecting bias in the pit-fall trap method, we found that leaf-litter dependent reptiles were more active up to 6 weeks after fire, giving a misleading impression of abundance. This effect was not discovered when modelling detectability with zero-inflated binomial models. Two species without detection bias showed early-successional responses to time since fire, consistent with a habitat-accommodation succession model. However, a habitat specialist did not have the predicted low abundance after fire due to increased post-fire movement and non-linear recovery of a key habitat component. Interactions between fire and other processes therefore must be better understood to predict reptile responses to changing fire-regimes. We conclude that there is substantial bias when trapping reptiles after fire, with species that are otherwise hard to detect appearing to be abundant. Studies that use a survey method based on animal activity such as bird calls or animal movements, likely face a similar risk of bias when comparing recently-disturbed with control sites.     

Negotiation may lead selfish individuals to cooperate: the example of the collective vigilance game

Game-theoretical models have been highly influential in behavioural ecology. However, these models generally assume that animals choose their action before observing the behaviour of their opponents while, in many natural situations, individuals in fact continuously react to the actions of others. A negotiation process then takes place and this may fundamentally influence the individual attitudes and the tendency to cooperate. Here, I use the classical model system of vigilance behaviour to demonstrate the consequences of such behavioural negotiation among selfish individuals, by predicting patterns of vigilance in a pair of animals foraging under threat of predation. I show that the game played by the animals and the resulting vigilance strategies take radically different forms, according to the way predation risk is shared in the pair. In particular, if predators choose their target at random, the prey respond by displaying moderate vigilance and taking turns scanning. By contrast, if the individual that takes flight later in an attack endures a higher risk of being targeted, vigilance increases and there is always at least one sentinel in the pair. Finally, when lagging behind its companion in fleeing from an attacker becomes extremely risky, vigilance decreases again and the animals scan simultaneously.     

Disturbance and predation risk influence vigilance synchrony of black‐necked cranes Grus nigricollis,but not as strongly as expected

Animals monitor surrounding dangers independently or cooperatively (synchronized and coordinated vigilance), with independent and synchronized scanning being prevalent. Coordinated vigilance, including unique sentinel behavior, is rare in nature, since it is time‐consuming and limited in terms of benefits. No evidence showed animals adopt alternative vigilance strategies during antipredation scanning yet. Considering the nonindependent nature of both synchronization and coordination, we assessed whether group members could keep alert synchronously or in a coordinated fashion under different circumstance. We studied how human behavior and species‐specific variables impacted individual and collective vigilance of globally threatened black‐necked cranes (Grus nigricollis) and explored behavior‐based wildlife management. We tested both predation risk (number of juveniles in group) and human disturbance (level and distance) effects on individual and collective antipredation vigilance of black‐necked crane families. Adults spent significantly more time (proportion and duration) on scanning than juveniles, and parents with juveniles behaved more vigilant. Both adults and juveniles increased time allocation and duration on vigilance with observer proximity. Deviation between observed and expected collective vigilance varied with disturbance and predation risk from zero, but not significantly so, indicating that an independent vigilance strategy was adopted by black‐necked crane couples. The birds showed synchronized vigilance in low disturbance areas, with fewer juveniles and far from observers; otherwise, they scanned in coordinated fashion. The collective vigilance, from synchronized to coordinated pattern, varied as a function of observer distance that helped us determine a safe distance of 403.75 m for the most vulnerable family groups with two juveniles. We argue that vigilance could constitute a prime indicator in behavior‐based species conservation, and we suggesting a safe distance of at least 400 m should be considered in future tourist management.     

Variable fledging age according to group size: trade-offs in a cooperatively breeding bird

Group living can provide individuals with several benefits, including cooperative vigilance and lower predation rates. Individuals in larger groups may be less vulnerable to predation due to dilution effects, efficient detection or greater ability to repel predators. Individuals in smaller groups may consequently employ alternative behavioural tactics to compensate for their greater vulnerability to predators. Here, we describe how pied babbler (Turdoides bicolor) fledging age varies with group size and the associated risk of nestling predation. Nestling predation is highest in smaller groups, but there is no effect of group size on fledgling predation. Consequently, small groups fledge young earlier, thereby reducing the risk of predation. However, there is a cost to this behaviour as younger fledglings are less mobile than older fledglings: they move shorter distances and are less likely to successfully reach the communal roost tree. The optimal age to fledge young appears to depend on the trade-off between reduced nestling predation and increased fledgling mobility. We suggest that such trade-offs may be common in species where group size critically affects individual survival and reproductive success.     

Vigilance in Przewalski's gazelle: effects of sex, predation risk and group size

Vigilance in social animals is often aimed at detecting predators. Many social and environmental factors influence vigilance, including sex, predation risk and group size. During the summer of 2007, we studied Przewalski's gazelle Procapra przewalskii , an endemic ungulate to the Qinghai-Tibet Plateau, to test whether and how these three factors affect vigilance. We distinguished groups consisting of males, mothers with lambs and females without lambs making observations on groups in the presence or absence of nearby predators. We assessed the group-size effect on vigilance and how this varied with levels of predation risk and sex. Males and mothers scanned longer and with a higher frequency than females without lambs. Individuals were more vigilant under direct predation threat. Although vigilance generally decreased with group size, the extent of the decrease was independent of predation risk and was not significant in males. The results suggest that mothers are more vigilant suggesting greater vulnerability and that males may have increased their vigilance to compete for higher social ranks. The positive correlation between vigilance and predation risk and the negative correlation between vigilance and group size are consistent with earlier findings, but we failed to find an interaction between group size and predation risk on vigilance perhaps because vigilance levels are low even in small groups, thus making similar vigilant upward adjustments in both small and large groups.     

Predation risk and resource abundance mediate foraging behaviour and intraspecific resource partitioning among consumers in dominance hierarchies

Dominance hierarchies and the resulting unequal resource partitioning among individuals are key mechanisms of population regulation. The strength of dominance hierarchies can be influenced by size‐dependent tradeoffs between foraging and predator avoidance whereby competitively inferior subdominants can access a larger proportion of limiting resources by accepting higher predation risk. Foraging‐predation risk tradeoffs also depend on resource abundance. Yet, few studies have manipulated predation risk and resource abundance simultaneously; consequently, their joint effect on resource partitioning within dominance hierarchies are not well understood. We addressed this gap by measuring behavioural responses of masu salmon Oncorhynchus masou ishikawae to experimental manipulations of predation risk and resource abundance in a natural temperate forest stream. Responses to predation risk depended on body size and social status such that larger fish (often social dominants) exhibited more risk‐averse behaviour (e.g. lower foraging and appearance rates) than smaller subdominants after exposure to a simulated predator. The magnitude of this effect was lower when resources were elevated, indicating that dominant fish accepted a higher predation risk to forage on abundant resources. However, the influence of resource abundance did not extend to the population level, where predation risk altered the distribution of foraging attempts (a proxy for energy intake) from being skewed towards large individuals to being skewed towards small individuals after predator exposure. Our results imply that size‐dependent foraging–predation risk tradeoffs can weaken the strength of dominance hierarchies by allowing competitively inferior subdominants to access resources that would otherwise be monopolized.     

Fox Odour Increases Vigilance in European Rabbits: A Study under Semi-Natural Conditions

The recognition of predator odours is a well‐known mechanism in many prey species which may lead to various behavioural and physiological responses. This has been shown for many mammal species under laboratory conditions, but efforts to validate the results in the field often have led to inconclusive results. We investigated the behavioural reactions and the physiological stress response of European rabbits (Oryctolagus cuniculus) to the odour of a mammalian predator (red fox, Vulpes vulpes) under semi‐natural conditions. The study was conducted on a rabbit population living in an outdoor enclosure of 2 ha. We compared the rates of vigilance and exploration, the time allocated to self‐directed behaviours, the home range sizes and the physiological responses of an experimental and a control group. Only animals from the experimental group were confronted with fox faeces. These animals increased their vigilance rate whereas the control animals did not respond. The increase did not differ between adult and subadult individuals. Furthermore, the experimental animals frequently approached the odour of the predator which might indicate an increase in investigative behaviour. Home‐range size, feeding and other self‐directed behaviours did not change in response to fox odour. Moreover, the animals of the experimental and the control group did not differ in serum corticosterone concentrations (measured after adrenocorticotrophic hormone challenge) that we determined in the beginning and in the end of the experiment. We suggest that the observed behavioural responses represent a low‐cost strategy for lowering the individual risk of predation.     

Foraging theory provides a useful framework for livestock predation management

A societal shift toward plant dominant diets and a reduction in livestock rearing could have broad social, environmental and conservation benefits. Livestock husbandry, however, has a wealthy cultural history, strong support and high consumer demand. It is therefore likely to continue as a major land use and conservation issue for predators. From a producer’s perspective, the primary goals of livestock protection are maximising, or at least maintaining, production by minimising losses and mitigating detriment to stock welfare. Lethal removal of predators remains a commonplace solution. Such management measures are questionable as they raise animal welfare and conservation concerns, risk inhibiting ecological processes, are often expensive, and in some circumstances, exacerbate livestock predation problems. Non-lethal alternatives can facilitate co-existence between livestock farmers and predators, ideally reducing the ecological impact of pastoralism and achieving conservation goals. The need for rigorous study of non-lethal approaches has however been recently highlighted. Tools and methods involved in livestock protection, as well as the theoretical basis of how we perceive and manage the problem, require deeper consideration. Non-lethal approaches require knowledgeable implementation and an effective decision making system is a prerequisite for successful practice. Livestock predation and its prevention are fundamentally influenced by the underlying principles of foraging ecology and risk theory. We propose that manipulating elements of Brown’s (1988) quitting harvest rate model provides a useful conceptual framework for reducing livestock predation and encouraging coexistence.     

Spread of false alarms in foraging flocks of house sparrows

In group‐foraging species with no alarm signals, the sudden departure of neighbours can be used to inform the rest of the group about the detection of a threat. However, sudden departures are ambiguous because they can be triggered by factors unrelated to predator detection. We evaluated how animals react to the sudden departure of neighbours in groups of foraging house sparrows (Passer domesticus). We focussed on false alarms that occurred for no apparent reasons to us because predation attempts were not frequent. Three factors can explain how the sudden departure of a neighbour can influence reaction times, namely group size, the distance between neighbours, and predation risk. We predicted reaction times to be longer in larger groups where individual vigilance levels are low, and when group members are further apart and cannot easily monitor each other. In addition, we expected reaction times to be longer when predation risk is lower. Departures that are more temporally clumped are also expected to be less ambiguous and should trigger faster reaction times. Our results show that sparrows reacted faster, not more slowly, to the sudden departures of neighbours in larger groups, and, as predicted, more slowly when neighbours were more distant from each other. Reaction times were longer in one of the two study years in which predation risk was deemed lower. Sparrows reacted more quickly when earlier departures were more temporally clumped. The results thus provided partial support for the predictions, and future work is needed to assess how individuals react to fleeing responses by their neighbours in species with no alarm signals.     

Temporal variation in site fidelity: scale-dependent effects of forage abundance and predation risk in a non-migratory large herbivore

Large herbivores are typically confronted by considerable spatial and temporal variation in forage abundance and predation risk. Although animals can employ a range of behaviours to balance these limiting factors, scale-dependent movement patterns are expected to be an effective strategy to reduce predation risk and optimise foraging opportunities. We tested this prediction by quantifying site fidelity of global positioning system-collared, non-migratory female elk (Cervus canadensis manitobensis) across multiple nested temporal scales using a long-established elk–wolf (Canis lupus) system in Manitoba, Canada. Using a hierarchical analytical approach, we determined the combined effect of forage abundance and predation risk on variation in site fidelity within four seasons across four nested temporal scales: monthly, biweekly, weekly, daily. Site fidelity of female elk was positively related to forage-rich habitat across all seasons and most temporal scales. At the biweekly, weekly and daily scales, elk became increasingly attached to low forage habitat when risk was high (e.g. when wolves were close or pack sizes were large), which supports the notion that predator-avoidance movements lead to a trade-off between energetic requirements and safety. Unexpectedly, predation risk at the monthly scale increased fidelity, which may indicate that elk use multiple behavioural responses (e.g. movement, vigilance, and aggregation) simultaneously to dilute predation risk, especially at longer temporal scales. Our study clearly shows that forage abundance and predation risk are important scale-dependent determinants of variation in site fidelity of non-migratory female elk and that their combined effect is most apparent at short temporal scales. Insight into the scale-dependent behavioural responses of ungulate populations to limiting factors such as predation risk and forage variability is essential to infer the fitness costs incurred.     

Predation risks suppress lifetime fitness in a wild mammal

Prey often reduce predation risk at the cost of lower resource intake. The cumulative effects of such tradeoffs can alter resource allocation, demography and evolutionary processes. We show how the accumulation of risk effects reduces the growth rate of wild North American porcupines Erethizon dorsatum, and simulate three evolutionary responses related to lifetime reproductive success. Individual porcupines experiencing predation risk from fishers Pekania pennanti grew slower and gave birth to fewer offspring. Simulations show that predation risk alone can lead to population declines, and that a female can replace herself by investing more energy into reproduction or adult survival; females that only invest energy in juvenile survival cannot. We show that the accumulation of predation risk can reduce lifetime reproductive success in natural ecosystems. Estimating the contribution of predation risk, and how evolutionary responses can mediate consequences associated with predation risk, is necessary to understand the evolution of predator–prey systems.     

Impact of increased predation risk on vigilance behaviour in a gregarious waterfowl,the Egyptian goose Alopochen aegyptiaca

Vigilance is amongst the most universal of anti‐predator strategies and commonly declines with increasing group size. We experimentally manipulated predation risk in a system with a known relationship between group size and vigilance levels to explore whether this relationship changes in response to elevated predation risk. We investigated the vigilance levels of Egyptian geese Alopochen aegyptiaca at eight golf courses in the western Cape, South Africa, to assess the perception of and reaction to predation risk. We manipulated predation risk by introducing trained Harris's hawks Parabuteo unicintus where avian predation was otherwise low or absent. The study confirmed the typical reduction in vigilance with group size on control sites, where the risk of predation is low. However, at experimental sites with elevated predation risk, a positive relationship between vigilance and group size was observed. We hypothesize that the mechanism for this relationship might be linked to social information transfer via copying behaviour and manipulation to induce vigilance. Thus, larger groups will have a higher probability of containing individuals with experience of elevated predation risk and their increased vigilance behaviour is copied by naïve individuals. This prediction is based on the intended outcome of introducing avian predation to make the geese feel less safe and to eventually leave the site as a management tool for controlling nuisance geese.