Effects of Humans on Behaviour of Wildlife Exceed Those of Natural Predators in a Landscape of Fear

Background

Human disturbance can influence wildlife behaviour, which can have implications for wildlife populations. For example, wildlife may be more vigilant near human disturbance, resulting in decreased forage intake and reduced reproductive success. We measured the effects of human activities compared to predator and other environmental factors on the behaviour of elk (Cervus elaphus Linnaeus 1758) in a human-dominated landscape in Alberta, Canada.

Methodology/Principal Findings

We collected year-round behavioural data of elk across a range of human disturbances. We estimated linear mixed models of elk behaviour and found that human factors (land-use type, traffic and distance from roads) and elk herd size accounted for more than 80% of variability in elk vigilance. Elk decreased their feeding time when closer to roads, and road traffic volumes of at least 1 vehicle every 2 hours induced elk to switch into a more vigilant behavioural mode with a subsequent loss in feeding time. Other environmental factors, thought crucial in shaping vigilance behaviour in elk (natural predators, reproductive status of females), were not important. The highest levels of vigilance were recorded on public lands where hunting and motorized recreational activities were cumulative compared to the national park during summer, which had the lowest levels of vigilance.

Conclusions/Significance

In a human-dominated landscape, effects of human disturbance on elk behaviour exceed those of habitat and natural predators. Humans trigger increased vigilance and decreased foraging in elk. However, it is not just the number of people but also the type of human activity that influences elk behaviour (e.g. hiking vs. hunting). Quantifying the actual fitness costs of human disturbance remains a challenge in field studies but should be a primary focus for future researches. Some species are much more likely to be disturbed by humans than by non-human predators: for these species, quantifying human disturbance may be the highest priority for conservation.     

Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics?

Many animals benefit from the presence of conspecifics by reducing their rate of scanning for predators while increasing their time spent foraging. This group size effect could arise from a decreased perception of individual risk (dilution hypothesis) and/or an increased ability to detect predators (detection hypothesis). We compared individual and group vigilance of Rocky Mountain elk, Cervus elaphus, in three regions of Yellowstone National Park, Wyoming, U.S.A. that varied in their encounter frequency with coyote, Canis latrans, grizzly bear, Ursus arctos, and grey wolf,Canis lupus , predators. Adult females without calves increased scanning and decreased foraging with high encounter risk and small herd size. Adult females with calves increased scanning and decreased foraging with high encounter risk, but showed no decrease in scanning with large herd size. Yearlings increased scanning and decreased feeding with small herd size, but not with high encounter risk. Adult males were least vigilant, fed most and were not influenced by encounter risk or herd size. These age-sex class differences led to significant differences in group vigilance depending on the composition of the herd. Herds with a majority of mothers were significantly more vigilant than herds with a majority of adult males. However, these differences in group vigilance had no influence on the individual scanning of females without calves. Thus, the decrease in individual scanning with herd size may depend more on changes in individual risk than on cooperative detection of predators. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Anthropogenic noise reduces avian feeding efficiency and increases vigilance along an urban–rural gradient regardless of species’ tolerances to urbanisation

Anthropogenic noise can adversely impact urban bird populations by interfering with vocal communication. Less research has addressed if anthropogenic noise masks the adventitious sounds that birds use to aid predator detection, which may lead to increased vigilance and reduced feeding efficiency. We test this hypothesis using a controlled playback experiment along an urban–rural gradient in Sheffield (UK). We also test the related predictions that anthropogenic noise has the greatest impacts on vigilance and feeding efficiency in rural populations, and on species that are more sensitive to urbanisation. We focus on six passerines, in order from most to least urbanised (based on how urbanisation influences population densities): blue tit Cyanistes caeruleus, robin Erithacus rubeculla, great tit Parus major, chaffinch Fringilla coelebs, coal tit Periparus ater and nuthatch Sitta europaea. We used play-back of anthropogenic urban noise and a control treatment at 46 feeding stations located along the urban–rural gradient. We assess impacts on willingness to visit feeders, feeding and vigilance rates. Exposure to anthropogenic noise reduced visit rates to supplementary feeding stations, reduced feeding rates and increased vigilance. Birds at more urban sites exhibit less marked treatment induced reductions in feeding rates, suggesting that urban populations may be partially habituated or adapted to noisy environments. There was no evidence, however, that more urbanised species were less sensitive to the impacts of noise on any response variable. Our results support the adventitious sound masking hypothesis. Urban noise may thus interfere with the ability of birds to detect predators, reducing their willingness to use food rich environments and increase vigilance rates resulting in reduced feeding rates. These adverse impacts may compromise the quality of otherwise suitable foraging habitats in noisy urban areas. They are likely to be widespread as they arise in a range of species including common urban birds.     

Facultative schooling behavior in the spottail shiner (Notropis hudsonius): possible costs and benefits

Synopsis If an individual is less susceptible to predation in a group it should be able to reduce its vigilance for predators and perhaps also its tendency to flee from predators, thereby gaining time and energy for feeding and other activities. These predictions were examined in the field (Veronica Lake, northwestern Ontario) using a facultative schooling species, the spottail shiner (Notropis hudsonius). Schools of various sizes attacked with a fish predator model had a significantly lower reaction distance to the predator than solitary shiners. Solitary shiners must therefore invest more time and energy in defense but may gain a feeding advantage because their visual field does not overlap with conspecific competitors.     

The effects of predation risk on the use of social foraging tactics

The effects of predation on the use of social foraging tactics, such as producing and scrounging, are poorly known in animals. On the one hand, recent theoretical models predict increased use of scrounging with increasing predation risk, when scroungers seeking feeding opportunities also have a higher chance of detecting predators. On the other hand, there may be no relation between tactic use and predation when antipredator vigilance is not compatible with scanning flockmates. We investigated experimentally the effects of predation risk on social foraging tactic use in tree sparrows, Passer montanus. We manipulated predation risk in the field by changing the distance between shelter and a feeder. Birds visited the feeder in smaller flocks, spent less time on it and were somewhat more vigilant far from shelter than close to it. Increased predation risk strongly affected the social foraging tactic used: birds used the scrounger tactic 30% more often far from cover than close to it. Between-flock variability in scrounging frequency was not related to the average vigilance level of the flock members, and within-flock variability in the use of scrounging was negatively related to the vigilance of birds. Our results suggest that in tree sparrows, the increased frequency of scrounging during high predation risk cannot simply be explained by an additional advantage of increasing antipredator vigilance. We propose alternative mechanisms (e.g. increased stochasticity in food supply, and that riskier places are used by individuals with lower reserves) that may explain increased scrounging when animals forage under high predation risk.     

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.     

A simple rule for the costs of vigilance: empirical evidence from a social forager

It is commonly assumed that anti-predator vigilance by foraging animals is costly because it interrupts food searching and handling time, leading to a reduction in feeding rate. When food handling does not require visual attention, however, a forager may handle food while simultaneously searching for the next food item or scanning for predators. We present a simple model of this process, showing that when the length of such compatible handling time Hc is long relative to search time S, specifically Hc/S > 1, it is possible to perform vigilance without a reduction in feeding rate. We test three predictions of this model regarding the relationships between feeding rate, vigilance and the Hc/S ratio, with data collected from a wild population of social foragers (samango monkeys, Cercopithecus mitis erythrarchus). These analyses consistently support our model, including our key prediction: as Hc/S increases, the negative relationship between feeding rate and the proportion of time spent scanning becomes progressively shallower. This pattern is more strongly driven by changes in median scan duration than scan frequency. Our study thus provides a simple rule that describes the extent to which vigilance can be expected to incur a feeding rate cost.     

Effect of Group Size on Individual and Collective Vigilance in Greater Rheas

We studied the effect of group size on the proportion of time that greater rheas, Rhea americana, allocated to vigilance and feeding during the non‐breeding season. We tested whether: (1) the proportion of time that one bird allocates to vigilance (individual vigilance) decreases with group size, and (2) the proportion of time that at least one bird of the group is vigilant (collective vigilance) increases with group size. We analyzed video‐recordings of birds that were foraging alone or in groups from two to 12 birds. The proportion of time allocated to individual vigilance decreased and the proportion of time spent feeding increased with group size. In both cases the main significant difference was between birds foraging alone and in groups. Collective vigilance did not vary with group size and it was lower than expected if vigilance bouts were random or sequential. Our results indicate that rheas foraging in large groups would not receive the benefit of an increase in collective vigilance, although they could still benefit from a reduction of predation risk by the dilution effect.     

Incompatibility between antipredatory vigilance and scrounger tactic in nutmeg mannikins, Lonchura punctulata

Most social foragers must search for food while avoiding predators. Group-foraging nutmeg mannikins engaged in a producer-scrounger game search for their own food (play producer) by hopping with the head down and search for others' food discoveries (play scrounger) by hopping with the head up. If the scrounger tactic is compatible with antipredatory vigilance, then an increase in antipredatory vigilance should lead to the detection of more joining opportunities, and hence to more joining by foragers. We tested this prediction as well as the extent to which stationary birds use head up exclusively for antipredatory purposes and hopping birds use head up for foraging purposes only. We observed three flocks of nutmeg mannikins searching for hidden clumps of food in an indoor aviary. We used a 2×2 factorial design in which both the distance to a safe refuge and the food distribution were manipulated. The use of head up by stationary and eating birds increased significantly with increased distance to cover. Distance to cover, however, had no effect on the use of the scrounger tactic or on the level of joining. We found no evidence of compatibility between the scrounger tactic and antipredatory vigilance. Our results provide the first unambiguous evidence for the existence of two distinct and incompatible patterns of vigilance for predators and for conspecifics. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

Common Myna Roosts Are Not Recruitment Centres

We studied communal roosting in the Common Myna (Acridotheres tristis) in the light of the recruitment centre hypothesis and predation at the roost. The number and sizes of flocks departing from and arriving at focal roosts were recorded over a two year period. We also recorded the sizes and behaviour of foraging flocks. We found that flock sizes of birds departing from roosts at sunrise were larger than those at the feeding site, suggesting that there was no recruitment from the roosts. Flocks entering the roosts during sunset were larger on average than those leaving the following sunrise, suggesting no consolidation of flocks in the morning. Flocks entering the roosts at sunset were also larger on average than those that had left that sunrise, although there was no recruitment at the feeding site. There was no effect of group size on the proportion of time spent feeding. Contrary to expectation, single birds showed lower apparent vigilance than birds that foraged in pairs or groups, possibly due to scrounging tactics being used in the presence of feeding companions. Thus, the recruitment centre hypothesis did not hold in our study population of mynas. Predation at dawn and dusk were also not important to communal roosting: predators near the roosts did not result in larger flocks, and resulted in larger durations of arrival/departure contrary to expectation. Since flock sizes were smallest at the feeding site and larger in the evening than in the morning, but did not coincide with predator activity, information transfer unrelated to food (such as breeding opportunities) may possibly give rise to the evening aggregations.     

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).     

Sleeping Site Use by <Emphasis Type="Italic">Trachypithecus francoisi</Emphasis> at Nonggang Nature Reserve,China

We collected data on sleeping site use of the François’ langur (Trachypithecus francoisi) between August 2003 and July 2004 at Nonggang Nature Reserve, China. We tested hypotheses regarding possible ultimate causes of sleeping site selection in light of our results. Langurs selected the ledges and caves on cliffs as sleeping sites. Of 23 identified sleeping sites, 7 were more frequently used than the others (≥9 times each, accounting for 64% of total observed nights). Langurs used most sleeping sites repeatedly, and reused some of them on consecutive nights; 4 consecutive nights were the longest run. We suggest that langurs choose sleeping sites to make approach and attack difficult by predators, and to increase familiarity so as to improve chances for escape. Langurs’ cryptic behaviors before entering sleeping sites and the rapid movement toward sleeping sites (4 min on average) with an increased level of vigilance may help to decrease the possibility of detection by predators. Access to food appears to have a profound influence on sleeping site selection in François’ langurs, as demonstrated by the langurs’ tendency to select sleeping sites close to their current main feeding sites. The position of sleeping site relative to the last feeding site of the day and the first feeding site of the subsequent morning indicated a strategy closer to that of a multiple central place forager than of a central place forager. Our results do not support the influences of other factors, e.g., avoidance of parasites, seeking comfort, and range or resource defense, on sleeping site selection.     

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.     

Ants visiting extrafloral nectaries and pyrrolizidine alkaloids may shape how a specialist herbivore feeds on its host plants

The presence of extrafloral nectaries (EFNs) attracts predators and parasitoids, and protects the plant against herbivorous insects. By improving plant defences, EFNs reduce the fitness of herbivores. The use of similar host plants with no EFNs or adaptations in response to predators and parasitoids may enhance herbivore fitness. In this context, we studied the feeding habit (on leaves or on unripe seeds inside the pods) of larvae of the specialist moth Utetheisa ornatrix in two Crotalaria host plant species in which EFNs are present (C. micans) or absent (C. paulina). We hypothesized that the moths’ feeding habit was influenced by its natural enemies via their presence on EFNs. In C. micans, we found more larvae feeding inside the pods rather than on the leaves, while in C. paulina, larvae were found in both parts of the plant. There was greater activity of natural enemies in C. micans than in C. paulina. The moth sequesters enough pyrrolizidine alkaloid (PAs) to defend against predators in the leaves and seeds of C. paulina, but only in seeds of C. micans. Therefore, a change in the feeding habit in U. ornatrix larvae is a plastic response that depends on whether EFNs are present or not, or whether PA concentrations are low or high. This change does not affect overall moth performance. However, other factors, such as pod hardness, predation by organisms other than those visiting EFNs or even parasitoids cannot be ruled out as being responsible for the change in feeding habit. To date, both the EFNs and PAs in Crotalaria species are a parsimonious explanation of how larvae of U. ornatrix use different species of Crotalaria for feeding.     

Breeding southern house wrens exhibit a threat-sensitive response when exposed to different predator models

We assessed the ability of southern house wrens (Troglodytes aedon musculus) to recognize and discriminate different birds of prey. We exposed nesting birds to stuffed specimens of two sympatric predator species, the chimango caracara (Milvago chimango, a nest predator) and the roadside hawk (Buteo magnirostris, a predator of adults and nests), and to a dummy of a non-sympatric predator, the double-toothed kite (Harpagus bidentatus, a predator of adults). Nesting wrens avoided going into their nest or took a longer time to resume their parental duties when exposed to the predators than when they were exposed to a control dummy (Chrysomus ruficapillus, a sympatric blackbird). Nest avoidance was higher when birds were exposed to the roadside hawk but no differences were detected when exposed to the chimango caracara or the double-toothed kite. The results indicate that southern house wrens are able to recognize a predator, responding in a graded manner. Our findings support the hypothesis that southern house wrens exhibit a threat-sensitive response during breeding. Also, individuals were able to recognize the unknown predator but failed to correctly assess the threat level represented by it. We propose that correct assessment of threat level by house wrens requires direct experience with the predator, which might mediate in the modulation of the response.     

Predation on crown-of-thorns starfish larvae by damselfishes

Examining the functional response of predators can provide insight into the role of predation in structuring prey populations and ecological communities. This study explored feeding behaviour and functional responses of planktivorous damselfishes when offered captive reared larvae of crown-of-thorns starfish, Acanthaster sp., with the aim of determining whether these predators could ever play a role in moderating outbreaks of Acanthaster sp. We examined predatory behaviour of 11 species of planktivorous damselfish, testing: (1) the relationship between predator size and predation rate, both within and among fish species; (2) consumption rates on larvae of Acanthaster sp. versus larvae of a common, co-occurring coral reef asteroid Linckia laevigata; (3) maximal feeding rates upon both Acanthaster sp. and L. laevigata; and (4) functional responses of planktivorous fishes to increasing densities of Acanthaster sp. Consumption rates of crown-of-thorns larvae by damselfishes were independent of predator size; however, there was a significant negative relationship between predator size and consumption rate of L. laevigata, when pooling across all predatory species. Some damselfishes, including Acanthochromis polyacanthus and Amblyglyphidodon curacao, consumed larval Acanthaster sp. at a greater rate than for L. laevigata. Most predatory species (all except A. curacao and Pomacentrus amboinensis) exhibited a Type II functional response whereby the increasing feeding rate decelerated with increasing prey density. In addition to revealing that a wide range of planktivorous fishes can prey upon larvae of Acanthaster sp., these data suggest that planktivorous damselfishes may have the capacity to buffer against population fluctuations of Acanthaster sp. Importantly, predators with Type II functional responses often contribute to stability of prey populations, though planktivorous fishes may be swamped by an abnormally high influx of larvae, potentially contributing to the characteristic population fluctuations of Acanthaster sp.     

Fast molecular assay to detect the rate of decay of <Emphasis Type="Italic">Bactrocera oleae</Emphasis> (Diptera: Tephritidae) DNA in <Emphasis Type="Italic">Pterostichus melas</Emphasis> (Coleoptera: Carabidae) gut contents

The molecular analysis of predation through specific DNA amplification has been utilized extensively over the last decade, and has been shown to be fast and effective. However, it is necessary to evaluate the prey detectability half-life if we are to correctly infer the relevance of particular predators to particular pests and to accurately model the effect of biocontrol. We present here the design and analysis of a set of primers to amplify olive fruit fly (Bactrocera oleae) DNA in predator gut contents, allowing fast evaluation of the digestion time. We modified the existing protocol by solubilizing the prey DNA directly from the gut, and we applied this modified protocol to demonstrate that Pterostichus melas, one of the most common carabids in olive groves in Italy, feeds on B. oleae pupae. After feeding carabids with a single pupa, traces of the pest were found to be detectable more than 20 h after ingestion. This method could also be applied to other predators to evaluate trophic interactions of the olive fruit fly. The relevance of generalist predation to the mortality of the pupal stage of B. oleae is of great economic interest since B. oleae causes serious damage during olive production, reducing the commercial value of olive oil and table olives.     

Vigilance does not covary with group size in an island population of silvereyes (Zosterops lateralis)

Numerous studies on different taxonomic groups have found thatvigilance behavior is negatively correlated with group size,as predicted by several theoretical models. This follows thelogical argument that each individual in a larger group canspend less time scanning for predators (and more time feeding),while the group as a whole maintains a high probability of detectingan approaching predator. We investigated the relationship betweenthese variables in the population of silvereyes (Zosterops lateralischlorocephala) on Heron Island, Great Barrier Reef. The studyused procedures of field observation that controlled or measuredother variables with which vigilance is often correlated: fooddensity and quality, temperature, time of day, distance fromcover, habitat obstructions, observer proximity, breeding status,age, sex, and dominance. There was no relationship between scanningbehavior and group size under these conditions. There are severalpossible explanations, related to the silvereyes' biology, forthis lack of covariation. An additional explanation is thatHeron Island is a predator-free environment for this species,and covariation between group size and vigilance is not expectedin the absence of predators.