Foraging costs of vigilance in large mammalian herbivores

Vigilance has been assumed to reduce food intake by taking away time from food processing. Such foraging costs of vigilance have been predicted to have profound effects on the structure of communities. Recently, however, it has been argued that mammalian herbivores might be capable of maintaining their rate of food intake despite being vigilant, because of their ability to scan the environment while chewing vegetation. We conducted behavioral observations to evaluate whether vigilance decreases the bite rate of free-ranging female bison ( Bison bison ) in Prince Albert National Park and elk ( Cervus canadensis ) in Yellowstone National Park. Modeling of foraging processes indicated that chewing time exceeded the time that bison and elk spent searching for food, interacting with conspecifics, and scanning. Consequently, bison and elk might have been capable of maintaining their rate of food intake despite vigilance. The maintenance of intake rate would have required bison and elk to match scanning events closely with chewing bouts, but we did not detect a positive correlation between the duration of scanning bouts and the number of consecutive bites taken just before vigilance events. As a result, vigilance was costly, and as it increased, bite rate declined for both herbivore species. Scanning still overlapped partially with food handling. Indeed, we estimated that 31% of feeding time being vigilant decreased bite rate by 20% for bison and 26% for elk, whereas total absence of overlap between chewing and scanning should have reduced bite rate by 31%. While we observed that vigilance induced foraging costs, these costs were less important than traditionally assumed.     

The effects of habitat on the vigilance of shorebirds: Is visibility important?

Previous studies of vigilance have concentrated on situations where the prey species has an unimpaired view of its surroundings. Here the effects of reduced visibility caused by objects adjacent to the prey are studied in two species of shorebird. A reduction in visibility causes an increase in the level of vigilance, indicating an increase in vulnerability despite the greater degree of camouflaging. This increase is due to individuals being less able to see both approaching predators and their neighbours. Turnstones, Arenaria interpres, and purple sandpipers, Calidris maritima, show very similar increases in the level of vigilance with decreasing visibility, but achieve these increases by different means: turnstones lengthen the duration of each vigilant scan, while purple sandpipers scan more often. Increasing scanning rate produces a shortened interval between scans, which reduces the risk of being caught unawares by an approaching predator. However, it may also reduce feeding efficiency, and it is suggested that this might be more serious in turnstones due to greater handling times for food items, so causing them to adopt a different strategy to increase vigilance.     

Sex-Related Differences in the Trade-Off between Foraging and Vigilance in a Granivorous Forager

The relationship between intake rate and food density can provide the foundation for models that predict the spatiotemporal distribution of organisms across a range of resource densities. The functional response, describing the relationship between resource density and intake rate is often interpreted mechanistically as the relationships between times spend searching and handling. While several functional response models incorporate anti-predator vigilance (defined here as an interruption of feeding or some other activity to visually scan the environment, directed mainly towards detecting potential predators), the impacts of environmental factors influencing directly anti-predator vigilance remains unclear. We examined the combined effects of different scenarios of predation risk and food density on time allocation between foraging and anti-predator vigilance in a granivorous species. We experimentally exposed Skylarks to various cover heights and seed densities, and measured individual time budget and pecking and intake rates. Our results indicated that time devoted to different activities varied as a function of both seed density and cover height. Foraging time increased with seed density for all cover heights. Conversely, an increased cover height resulted in a decreased foraging time. Contrary to males, the decreased proportion of time spent foraging did not translate into a foraging disadvantage for females. When vegetation height was higher, females maintained similar pecking and intake rates compared to intermediate levels, while males consistently decreased their energy gain. This difference in anti-predator responses suggests a sexually mediated strategy in the food-safety trade-off: when resource density is high a females would adopt a camouflage strategy while an escape strategy would be adopted by males. In other words, males would leave risky-areas, whereas females would stay when resource density is high. Our results suggest that increased predation risk might generate sexually mediated behavioural responses that functional response models should perhaps better consider in the future.     

Good foragers can also be good at detecting predators

The degree to which foraging and vigilance are mutually exclusive is crucial to understanding the management of the predation and starvation risk trade-off in animals. We tested whether wild-caught captive chaffinches that feed at a higher rate do so at the expense of their speed in responding to a model sparrowhawk flying nearby, and whether consistently good foragers will therefore tend to respond more slowly on average. First, we confirmed that the time taken to respond to the approaching predator depended on the rate of scanning: as head-up rate increased so chaffinches responded more quickly. However, against predictions, as peck rate increased so head-up rate increased and mean length of head-up and head-down periods decreased. Head-up rate was probably dependent on peck rate because almost every time a seed was found, a bird raised its head to handle it. Therefore chaffinches with higher peck rates responded more quickly. Individual chaffinches showed consistent durations of both their head-down and head-up periods and, therefore, individuals that were good foragers were also good detectors of predators. In relation to the broad range of species that have a similar foraging mode to chaffinches, our results have two major implications for predation/starvation risk trade-offs: (i) feeding rate can determine vigilance scanning patterns; and (ii) the best foragers can also be the best at detecting predators. We discuss how our results can be explained in mechanistic terms relating to fundamental differences in how the probabilities of detecting food rather than a predator are affected by time. In addition, our results offer a plausible explanation for the widely observed effect that vigilance continues to decline with group size even when there is no further benefit to reducing vigilance.     

Switching to a feeding method that obstructs vision increases head-up vigilance in dabbling ducks

A major assumption in most models of foraging is that feeding and vigilance are mutually exclusive. A recent experimental study challenged this hypothesis and demonstrated that birds are able to detect predators while pecking seeds on the ground (head-down vigilance). Experimental obstruction of head-down vigilance makes birds increase head-up vigilance (i.e. the classical overt vigilance posture). For many foragers in the wild, visibility varies between habitats and foraging methods. We compared the vigilance of Teal Anas crecca and Shoveler Anas clypeata when foraging with their eyes above the water surface (shallow feeding, only the bill submerged) and when foraging with their eyes underwater (deep feeding, head and neck underwater, or upending), at three wintering sites in western France. Birds of both species spent less time in head-up vigilance during shallow foraging than during deep foraging, with no significant difference between sites, which suggests that they are capable of some vigilance during shallow foraging. During deep foraging, the time spent vigilant increased because the frequency of scans was much higher, while scan length decreased. However, these differences could have resulted from variations in the availability of food at different depths. In an experiment where the food availability was constant, we observed the same pattern, with a higher frequency of scans during deep foraging. This study therefore provides strong support for the idea that vigilance and foraging are not always mutually exclusive and shows that switching between searching methods can cause vigilance time – and, as a consequence, loss of feeding time – to vary. This should be taken into account in future field and experimental studies of the trade-off animals make between vigilance and feeding.     

The effect of habitat complexity on the functional response of a seed-eating passerine

Recent population declines of seed-eating farmland birds have been associated with reduced overwinter survival due to reductions in food supply. An important component of predicting how food shortages will affect animal populations is to measure the functional response, i.e. the relationship between food density and feeding rate, over the range of environmental conditions experienced by foraging animals. Crop stubble fields are an important foraging habitat for many species of seed-eating farmland bird. However, some important questions remain regarding farmland bird foraging behaviour in this habitat, and in particular the effect of stubble on farmland bird functional responses is unknown. We measured the functional responses of a seed-eating passerine, the Chaffinch Fringilla coelebs , consuming seeds placed on the substrate surface in three different treatments: bare soil, low density stubble and high density stubble. Stubble presence significantly reduced feeding rates, but there was no significant difference between the two stubble treatments. Stubble reduced feeding rates by reducing the maximum attack distance, i.e. the distance over which an individual food item is targeted and consumed. The searching speed, handling time per seed, proportion of time spent vigilant, duration of vigilance bouts and duration of head-down search periods were unaffected by the presence of stubble. The frequency of vigilance bouts was higher in the bare soil treatment, but this is likely to be a consequence of the increased feeding rate. We show the influence of a key habitat type on the functional response of a seed-eating passerine, and discuss the consequences of this for farmland bird conservation.     

Measuring the functional responses of farmland birds: an example for a declining seed-feeding bunting

1. Many farmland bird species have undergone significant declines. It is important to predict the effect of agricultural change on these birds and their response to conservation measures. This requirement could be met by mechanistic models that predict population size from the optimal foraging behaviour and fates of individuals within populations. A key component of these models is the functional response, the relationship between food and competitor density and feeding rate. 2. This paper describes a method for measuring functional responses of farmland birds, and applies this method to a declining farmland bird, the corn bunting Miliaria calandra L. We derive five alternative models to predict the functional responses of farmland birds and parameterize these for corn bunting. We also assess the minimum sample sizes required to predict accurately the functional response. 3. We show that the functional response of corn bunting can be predicted accurately from a few behavioural parameters (searching rate, handling time, vigilance time) that are straightforward to measure in the field. These parameters can be measured more quickly than the alternative of measuring the functional response directly. 4. While corn bunting violated some of the assumptions of Holling's disk equation (model 1 in our study), it still provided the most accurate fit to the observed feeding rates while remaining the most statistically simple model tested. Our other models may be more applicable to other species, or corn bunting feeding in other locations. 5. Although further tests are required, our study shows how functional responses can be predicted, simplifying the development of mechanistic models of farmland bird populations.     

Detecting predators and locating competitors while foraging: an experimental study of a medium-sized herbivore in an African savanna

Vigilance allows individuals to escape from predators, but it also reduces time for other activities which determine fitness, in particular resource acquisition. The principles determining how prey trade time between the detection of predators and food acquisition are not fully understood, particularly in herbivores because of many potential confounding factors (such as group size), and the ability of these animals to be vigilant while handling food. We designed a fertilization experiment to manipulate the quality of resources, and compared awareness (distinguishing apprehensive foraging and vigilance) of wild impalas (Aepyceros melampus) foraging on patches of different grass height and quality in a wilderness area with a full community of predators. While handling food, these animals can allocate time to other functions. The impalas were aware of their environment less often when on good food patches and when the grass was short. The animals spent more time in apprehensive foraging when grass was tall, and no other variable affected apprehensive behavior. The probability of exhibiting a vigilance posture decreased with group size. The interaction between grass height and patch enrichment also affected the time spent in vigilance, suggesting that resource quality was the main driver when visibility is good, and the risk of predation the main driver when the risk is high. We discuss various possible mechanisms underlying the perception of predation risk: foraging strategy, opportunities for scrounging, and inter-individual interference. Overall, this experiment shows that improving patch quality modifies the trade-off between vigilance and foraging in favor of feeding, but vigilance remains ultimately driven by the visibility of predators by foragers within their feeding patches.     

Vigilance and food intake rate in paired and solitary Zenaida Doves Zenaida aurita

We quantified vigilance during feeding in the Zenaida Dove Zenaida aurita, a tropical species with stable pair‐bonds and year‐round territoriality. Both males and females decreased the proportion of time spent vigilant by 30% when feeding with their partner compared with when feeding alone. This reduction was achieved through increasing the length of inter‐scan duration, while scan duration remained constant. No evidence was found for coordination of vigilance between pair members. The equal investment in vigilance by male and female Zenaida Doves might be related to the mutual benefits of long‐term pair‐bonding.     

How group size affects vigilance dynamics and time allocation patterns: the key role of imitation and tempo

In the context of social foraging, predator detection has been the subject of numerous studies, which acknowledge the adaptive response of the individual to the trade-off between feeding and vigilance. Typically, animals gain energy by increasing their feeding time and decreasing their vigilance effort with increasing group size, without increasing their risk of predation ('group size effect'). Research on the biological utility of vigilance has prevailed over considerations of the mechanistic rules that link individual decisions to group behavior. With sheep as a model species, we identified how the behaviors of conspecifics affect the individual decisions to switch activity. We highlight a simple mechanism whereby the group size effect on collective vigilance dynamics is shaped by two key features: the magnitude of social amplification and intrinsic differences between foraging and scanning bout durations. Our results highlight a positive correlation between the duration of scanning and foraging bouts at the level of the group. This finding reveals the existence of groups with high and low rates of transition between activities, suggesting individual variations in the transition rate, or 'tempo'. We present a mathematical model based on behavioral rules derived from experiments. Our theoretical predictions show that the system is robust in respect to variations in the propensity to imitate scanning and foraging, yet flexible in respect to differences in the duration of activity bouts. The model shows how individual decisions contribute to collective behavior patterns and how the group, in turn, facilitates individual-level adaptive responses.     

Coots Fulica atra reduce their vigilance under increased competition

Birds frequently interrupt feeding to scan their surrounding environment. Usually an inverse correlation between scan rate and flock size exists. The 'many-eyes' hypothesis suggests that more eyes are able to detect a predator earlier. Due to the 'dilution-effect' animals in larger groups experience 'safety in numbers', while the 'scramble competition' hypothesis suggests that individuals reduce their vigilance in larger groups since they compete for a limited amount of scarce resources. Here, I induced competition in natural coot populations. Coots preferred feeding on grass and were occasionally fed by passers-by at the study sites. However, this resource was scarce and coots experienced additional food as a very limited resource. I sampled coots prior and after an experimental treatment with an additional food supply. Correlations between vigilance rate (number of scans during 1 min of foraging), nearest neighbor distance and flock size existed before the experimental treatment but afterwards the correlation between vigilance and nearest neighbor distance faded. I found a significantly lower vigilance rate and nearest neighbor distance after inducing competition. This study provided experimental evidence for the 'scramble competition' hypothesis namely that individuals in groups lowered their vigilance when faced with competition for a limited amount of food resources given similar flock sizes.     

How foraging allometries and resource dynamics could explain Bergmann's rule and the body‐size diet relationship in mammals

Two dramatic large scale patterns characterize body size in mammalian herbivores. One is Bergmann's rule that notes that mammals tend to increase in body size at higher latitudes. The other is the inverse relationship between herbivore body size and diet quality. Here, we present a model that may explain both. We start by noting that searching for and handling resources are fundamental activities for feeding mammals. We note that if with body size, encounter probability increases less favorably and handling time more favorably than metabolic costs, then body size represents a tradeoff between search efficiency (favors smaller body size) and handling efficiency (favors larger). If so, then optimal body size increases with both temperature and the conspicuousness of the food, but decreases with food quality. For this to happen there must be food limitation where the herbivores influence food standing crop. Lower energetic foraging costs (lower latitude, lower seasonality and/or higher temperatures) or higher food quality result in lower standing crops of food. A lower standing crop of food favors searching efficiency and, hence, smaller body sizes. Factors that increase the standing crop of food favor handling efficiency and larger body sizes. Simply maximizing net profit from foraging or foraging efficiency that are often assumed to help explain Bergmann's rule do not predict either Bergmann's rule nor the inverse relationship between food quality and body size. With the inclusion of consumer–resource dynamics, fitness maximization predicts both. Testing the model's predictions invites empirical research into the allometries of foraging parameters relating to search and handling.     

Does the thermal environment influence vigilance behavior in dark-eyed juncos (Junco hyemalis)? An approach using standard operative temperature

One might expect that increased thermal stress would cause wintering birds to forage faster in order to meet the increased metabolic demand. Faster foraging should, in turn, lead to a reduction in vigilance, since feeding and vigilance are mutually antagonistic activities. We examined these intuitive behavioral expectations using newly developed standard operative temperature sensors designed specifically to characterize the thermal effect of the microclimate environment (rain excluded) on wintering dark-eyed juncos (Junco hyemalis). These sensors allowed us to distinguish the behavioral effects of thermal stress from non-thermal effects associated with micrometeorological conditions (e.g. wind noise). Our analysis indicated that neither thermal nor non-thermal aspects of the physical environment influenced the proportion of time spent vigilant by juncos. However, the rate of food ingestion (measured as pecking rate) exhibited a negative correlation with thermal stress per se. This unexpected result may reflect the effect of thermal stress on feeding posture, peripheral muscle cooling, or both. The effect of thermal stress on pecking rate was nevertheless minor in comparison to the effect of flock size, which exerted by far the largest effect on both vigilance and pecking rate. Our overall results suggest that birds experiencing thermal stress will not necessarily lower their vigilance, but rather increase feeding bout length to compensate for the greater metabolic demand. This interpretation is consistent with theoretical models of vigilance in a non-time-limited environment, and may help explain the contradictory results to date on the effect of thermal stress on vigilance.     

The effects of mixed-species flocking on the vigilance of shorebirds: Who do they trust?

The benefit of reduction in individual anti-predatory vigilance with increasing group size has previously been demonstrated only within single species. Here the effect of mixed species flocking on vigilance is investigated in two species of wading bird wintering on rocky shores. Both turnstones, Arenaria interpres, and purple sandpipers, Calidris maritima, ‘share’ vigilance with conspecifics, but also with some other waders; the extent of sharing appears to depend on the relative size of, and habitat overlap with, the other species. Vigilance is not shared with much larger species, nor with those rarely found in the same areas. There is no sharing of vigilance between neighbouring birds unable to see each other. Variation in vigilance level results from an alteration in both rate of scanning and duration of single scans; these two variables are adjusted independently over the range of densities experienced. This is due to constraints on a high scanning rate (which may reduce feeding efficiency) and a short scan duration (which cannot be lower than the minimum required to take in the necessary information).     

Dilution games: use of protective cover can cause a reduction in vigilance for prey in groups

Antipredatory vigilance usually decreases in groups. The generallyaccepted "collective detection" explanation implies that becausethere are more eyes to scan the surroundings for predators,individuals in a group can lower their personal investment invigilance without increasing their predation risk. The roleof other factors, such as numerical risk dilution caused bythe mere presence of companions, has been neglected. In a model,we explore a dilution game when foragers in groups have accessto protective cover. We show that foragers can take advantageof risk dilution and that this leads to changes in vigilancewith group size without the need to invoke collective detection.We identify a cost to maintaining high levels of vigilance asless vigilant foragers gather food faster and so depart thegroup sooner (to reach cover) leaving more vulnerable stragglersbehind. In groups, there is a scramble to reach safe sites thatcan induce a reduction in vigilance levels. Such a mechanismoperates less forcefully in large groups because individualsin these groups are less vulnerable to the departure of an individual.We also demonstrate that individuals should adopt lower levelsof vigilance, to reach safe sites sooner, when predator evasionis compromised or when the rate of food intake is high. Themodel provides new insights into the mechanisms underlying changesin vigilance with group size in animals.     

Vigilance and scanning patterns in birds

We present a new approach to the analysis of scanning patterns in feeding birds. We estimate the probability of a bird detecting a predator from the frequency distribution of inter-scan intervals and the proportion of time spent scanning. This method avoids, several unrealistic assumptions implied in earlier analyses of vigilance data, and can accommodate predators attacking randomly or using prey behaviour to time an attack. The practical application of this approach is illustrated using data for feeding and vigilance in the ostrich (Struthio camelus). The analysis is discussed with reference to the hunting tactics of predators and Pulliam's (1973) model of feeding and vigilance in birds.     

Experimental Predictions of The Functional Response of A Freshwater Fish

The functional response is the relationship between the feeding rate of an animal and its food density. It is reliant on two basic parameters; the volume searched for prey per unit time (searching rate) and the time taken to consume each prey item (handling time). As fish functional responses can be difficult to determine directly, it may be more feasible to measure their underlying behavioural parameters in controlled conditions and use these to predict the functional response. Here, we tested how accurately a Type II functional response model predicted the observed functional response of roach Rutilus rutilus, a visually foraging fish, and compared it with Type I functional response. Foraging experiments were performed by exposing fish in tank aquaria to a range of food densities, with their response captured using a two‐camera videography system. This system was validated and was able to accurately measure fish behaviour in the aquaria, and enabled estimates of fish reaction distance, swimming speed (from which searching rate was calculated) and handling time to be measured. The parameterised Type II functional response model accurately predicted the observed functional response and was superior to the Type I model. These outputs suggest it will be possible to accurately measure behavioural parameters in other animal species and use these to predict the functional response in situations where it cannot be observed directly.     

Sexual,Seasonal and Group Size Differences in the Allocation of Time between Vigilance and Feeding in the Greater Rhea,Rhea americana

We studied the effect of sex and group size on the proportion of time a greater rhea, Rhea americana, allocates to vigilance and feeding during the breeding and the non-breeding seasons. We analysed 175 records of focal animals that were feeding alone or in groups of 2 to 26 birds. In both seasons, males spent more time in vigilance and less time in feeding than females. Both sexes spent more time in vigilance and less time in feeding during the breeding season. Sexual and seasonal differences in vigilance were the result of different mechanisms. Males had shorter feeding bouts than females but there were no sexual differences in the length of the vigilance bouts. On the contrary, seasonal differences were the result of males and females having longer vigilance bouts during the breeding season but there were no seasonal differences in the length of the feeding bouts. During the non-breeding season, individual vigilance was higher in rheas foraging alone than in groups. In this case, solitary birds had longer vigilance and shorter feeding bouts than birds foraging in groups. We discuss the possible effect of intragroup competition and food availability on the allocation of time between feeding and vigilance in this species.     

Foraging strategy and predator avoidance behaviour: an intraspecific approach

Relationships between predator avoidance behaviour (scanning and flocking) and foraging were studied in Calidris alpina, to test predictions regarding the effect of foraging techniques on such behaviours. The scanning hypothesis predicts that individuals with a tactile hunting technique and individuals with a visual hunting technique (both continuous searchers) do not differ in any variable related to scanning behaviour. The flocking hypothesis predicts that visually hunting individuals witl tend to form smaller flocks than tactile-foraging individuals. The two continuous feeding strategies did not differ among individuals in vigilance rate, nor in vigilance time or mean scan duration. However, with respect to flocking behaviour, visual foragers differed from tactile foragers in foraging flock size. The relationships between flocking behaviour and foraging strategy are discussed. The pattern found at the intraspecific level are the same as those found at interspecific level.     

Seeing a Ghost? Vigilance and Its Drivers in a Predator‐free World

Vigilance is a key to the early detection of predators, but may be costly if it impairs foraging efficiency. Hence, we would expect vigilance to be suppressed and/or counter‐selected in predator‐free environments, although this might depend on the environmental drivers influencing perceived predation risk. We studied vigilance in two populations of Sitka black‐tailed deer (Odocoileus hemionus sitkensis) on Haida Gwaii (Canada) which have not been exposed to predators since they colonized the study islands approx. 60 yr ago. In this context, anti‐predator behavior should not have any obvious current benefit. Moreover, its maintenance should be particularly costly in our study populations because these deer have depleted their food resources and, thus, anti‐predator behaviors should interfere with time spent searching for scarce resources. We used bait stations equipped with camera traps to assess vigilance under standardized feeding conditions. We expected to observe lower vigilance levels than those observed elsewhere in locations with predators. We investigated how vigilance varied in relation to the amount of bait, the level of visibility, and between day and night. During the day, deer spent, on average, 14% of their time in overt vigilance during foraging bouts, a level similar to, although in the lower range of, values reported at sites where predators are present. Levels of vigilance were lower at night, and decreased with increasing visibility, but not during the day. Deer were less vigilant when bait availability was high, but only when visibility was also high. We discuss why the maintenance of vigilance is here best explained by the ghosts of predators past, and how, at the temporal scale of a few generations, the ecological factors driving vigilance levels might override the absence of significant risk from large predators.