Failure of captive-born greater rheas (Rhea americana, Rheidae, Aves) to discriminate between predator and nonpredator models

The capacity to recognize and respond to predators can be lost by captive animals. Habituation to humans caused by the captive environment can be transferred to other stimuli, such as predators, a situation that conservation biologists wish to avoid. Greater rheas are threatened South American birds, for which there are plans for reintroduction programs in Brazil. The goal of this study was to evaluate the behavioral responses of captive-born greater rheas to different models of predators and nonpredators. Seventeen captive-born greater rheas, divided into four groups, from the Belo Horizonte Zoo, Brazil were studied. Three predator and three nonpredator models were presented to the birds and their behavioral responses recorded. Predators versus nonpredator models and the behavior of rheas in three experimental phases (baseline, models, and postmodels) were analyzed. Captive-born greater rheas modified their behaviors in the presence of both predator/nonpredator models, increasing alert and wary behaviors (alert, observing, and pacing behaviors: P?<?0.01), showing some degree of antipredator behavior persistence, but they were unable to discriminate between predator and nonpredator models (all behaviors: P?>?0.05). In conclusion, antipredator training should be implemented to develop the expression of this behavior before reintroductions are attempted.     

Prey Responses to Predator's Sounds: A Review and Empirical Study

Many animals assess their risk of predation by listening to and evaluating predators' vocalizations. We reviewed the literature to draw generalizations about predator discrimination abilities, the retention of these abilities over evolutionary time, and the potential underlying proximate mechanisms responsible for discrimination. Broadly, we found that some prey possess an ability to respond to a predator after having been evolutionarily isolated from a specific predator (i.e., predators are allopatric) and that some prey are predisposed to respond to certain types of predators that they coevolved with but without having ecological experience. However, these types of studies are lacking, and relatively, few studies have examined predator discrimination abilities in ungulates. To begin addressing these knowledge gaps, we performed field experiments on Mule deer (Odocoileus hemionus) in which we investigated the ability of deer to discriminate among familiar predators [coyotes (Canis latrans) and mountain lions (Puma concolor)] and an evolutionary relevant predator with which deer have had no recent exposure [locally extinct wolves (Canis lupus)]. We found that Mule deer respond to and discriminate among predators based on predator vocalizations and have retained an ability to respond to wolves that have been extinct from the study area since the early 20th century. Previous playback studies have shown that responses vary among human‐habituated and non‐habituated populations and differ according to human proximity. Deer greater than 0.5 km from human residences allocated more time to heightened responses both before and after stimulus playback. Our findings may help predict how prey–predator interactions may change as a result of the recovering wolf population with a basis in ecological and evolutionary experience in predator discrimination and desensitization.     

Olfactory Predator Discrimination in Yellow‐Bellied Marmots

The mechanism underlying olfactory predator identification may be relatively experience‐independent, or it may rely on specific experience with predators. A mechanism by which prey might identify novel predators relies on the inevitable creation of sulfurous metabolites that are then excreted in the urine of carnivorous mammals. We tested whether free‐living, yellow‐bellied marmots (Marmota flaviventris) and mid‐sized herbivores that fall prey to a variety of carnivorous mammals could discriminate herbivore (elk—Cervus elephas) urine from predator (red fox—Vulpes vulpes, coyote—Canis latrans, mountain lion—Felis concolor, wolf—Canis lupus) urine, a novel herbivore (moose—Alces alces), and a distilled water control. We further asked how specific this assessment was by testing whether marmots responded differently to predators representing different levels of risk and to familiar vs. unfamiliar predators. We found that marmots responded more to urine from coyotes (a familiar predator on adults), mountain lions (a potentially unfamiliar predator that could kill adults) and wolves (a locally extinct predator that could kill adults) than to elk urine (a non‐predator). Red fox (a predator that poses a risk only to recently emerged marmot pups) urine elicited a less substantial (but not significantly so) response than coyote urine. Marmots can identify predators, even novel ones, using olfactory cues, suggesting that experience with a specific predator is not required to identify potential threats.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

Comparative Patterns of Predation by Cougars and Recolonizing Wolves in Montana's Madison Range

Abstract: Numerous studies have documented how prey may use antipredator strategies to reduce the risk of predation from a single predator. However, when a recolonizing predator enters an already complex predator—prey system, specific antipredator behaviors may conflict and avoidance of one predator may enhance vulnerability to another. We studied the patterns of prey selection by recolonizing wolves (Canis lupus) and cougars (Puma concolor) in response to prey resource selection in the northern Madison Range, Montana, USA. Elk (Cervus elaphus) were the primary prey for wolves, and mule deer (Odocoileus hemionus) were the primary prey for cougars, but elk made up an increasingly greater proportion of cougar kills annually. Although both predators preyed disproportionately on male elk, wolves were most likely to prey on males in poor physical condition. Although we found that the predators partitioned hunting habitats, structural complexity at wolf kill sites increased over time, whereas complexity of cougar kill sites decreased. We concluded that shifts by prey to structurally complex refugia were attempts by formerly naïve prey to lessen predation risk from wolves; nevertheless, shifting to more structurally complex refugia might have made prey more vulnerable to cougars. After a change in predator exposure, use of refugia may represent a compromise to minimize overall risk. As agencies formulate management strategies relative to wolf recolonization, the potential for interactive predation effects (i.e., facilitation or antagonism) should be considered.     

被捕食动物对捕食者的识别研究及在放归中的应用

对捕食者的认知能力是当前生态学研究的一个热点。一些物种具有对捕食者先天的识别能力,而一些物种必须通过后天学习才能获得对捕食者的认知能力,还有许多动物通过社会学习和文化传播获得对捕食者的识别能力。本文就国外被捕食动物对捕食者的识别的研究进展进行综述,并讨论了该项研究对野外放归工作提供的重要理论意义和应用价值。     

Does habituation to humans influence predator discrimination in Gunther's dik-diks (Madoqua guentheri)?

Animals living around humans may habituate to us, but little is known about the consequences of this habituation. Some wildlife managers assume that habituation to humans makes individuals less likely to respond to natural predators, which is something to be avoided in captive breeding programmes where animals are destined for release. We conducted a playback experiment where we broadcast the sounds of a terrestrial predator and the song from a non-threatening bird to Gunther's dik-diks (Madoqua guentheri), a small ungulate that is vulnerable to many predators, in areas where dik-diks were and were not habituated to humans. Contrary to our expectation, habituated dik-diks discriminated the predator sounds from the birdsong, while unhabituated dik-diks failed to make this discrimination. Our results demonstrate that humans may influence predation hazard assessment, but we should not generally assume that human-habituated animals will be especially vulnerable to predators.     

Assessing differential prey selection patterns between two sympatric large carnivores

Several conceptual models describing patterns of prey selection by predators have been proposed, but such models rarely have been tested empirically, particularly with terrestrial carnivores. We examined patterns of prey selection by sympatric wolves ( Canis lupus ) and cougars ( Puma concolor ) to determine i) if both predators selected disadvantaged prey disproportionately from the prey population, and ii) if the specific nature and intensity of prey selection differed according to disparity in hunting behavior between predator species. We documented prey characteristics and kill site attributes of predator kills during winters 1999–2001 in Idaho, and located 120 wolf-killed and 98 cougar-killed ungulates on our study site. Elk ( Cervus elephus ) were the primary prey for both predators, followed by mule deer ( Odocoileus hemionus ). Both predators preyed disproportionately on elk calves and old individuals; among mule deer, wolves appeared to select for fawns, whereas cougars killed primarily adults. Nutritional status of prey, as determined by percent femur marrow fat, was consistently poorer in wolf-killed prey. We found that wolf kills occurred in habitat that was more reflective of the entire study area than cougar kills, suggesting that the coursing hunting behavior of wolves likely operated on a larger spatial scale than did the ambush hunting strategy of cougars. We concluded that the disparity in prey selection and hunting habitat between predators probably was a function of predator-specific hunting behavior and capture success, where the longer prey chases and lower capture success of wolf packs mandated a stronger selection for disadvantaged prey. For cougars, prey selection seemed to be limited primarily by prey size, which could be a function of the solitary hunting behavior of this species and the risks associated with capturing prime-aged prey.     

Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae)

Some prey can distinguish between chemical cues from predators fed different diets. Here we document the first evidence of diet-based chemical discrimination of predators in a terrestrial arthropod and measure the survival value of behavioural responses to predator chemical cues. We tested activity level and avoidance behaviour of the wolf spider, Pardosa milvina, to faeces and silk associated with the predatory wolf spider, Hogna helluo, fed either P. milvina or crickets (Acheta domesticus). We then measured survival of Pardosa in the presence of Hogna when placed on blank paper or paper previously occupied by Hogna fed either crickets or Pardosa. Filter paper previously occupied by Hogna from each diet treatment or a blank control were simultaneously presented to adult female Pardosa among four treatment pairs (N=15/treatment): (1) blank paper/blank paper, (2) Hogna fed crickets/blank, (3) Hogna fed Pardosa /blank and (4) Hogna fed Pardosa / Hogna fed crickets. Cues from Hogna fed either crickets or Pardosa elicited significantly less activity relative to blank controls. Cues from Hogna fed Pardosa elicited a significantly greater reduction in activity than Hogna fed crickets. When given a choice, Pardosa initially chose the blank substrate significantly more often than either substrate with Hogna cues. Spiders survived longer in the presence of cues from either Hogna diet treatment relative to blank paper, but there was no significant effect of predator diet on survival. Results suggest diet-based predator cues elicit different levels of activity in Pardosa that reduce predation in the presence of Hogna. Copyright 2001 The Association for the Study of Animal Behaviour.     

Surveillance and management of Echinococcus multilocularis in a wildlife park

The fox tapeworm Echinococcus multilocularis is the causative agent of alveolar echinococcosis, a severe zoonotic disease that may be fatal if untreated. A broad spectrum of mammalian species may be accidentally infected even in captivity. In April 2011, liver lesions due to E. multilocularis were observed during the necropsy of a captive-born nutria (Myocastor coypus) in a French wildlife park, leading to initiation of a study to survey the parasite's presence in the park. A comparable environmental contamination with fox's feces infected by E. multilocularis was reported inside (17.8%) and outside (20.6%) the park. E. multilocularis worms were found in the intestines of three of the five roaming foxes shot in the park. Coprological analyses of potential definitive hosts in captivity (fox, lynx, wildcat, genet, wolf, bear and raccoon) revealed infection in one Eurasian wolf. Voles trapped inside the park also had a high prevalence of 5.3%. After diagnosis of alveolar echinococcosis in a Lemur catta during necropsy, four other cases in L. catta were detected by a combination of ultrasound and serology. These animals were treated twice daily with albendazole. The systematic massive metacestode development and numerous protoscoleces in L. catta confirmed their particular sensitivity to E. multilocularis infection. The autochthonous origin of the infection in all the captive animals infected was genetically confirmed by EmsB microsatellite analysis. Preventive measures were implemented to avoid the presence of roaming foxes, contact with potential definitive hosts and contaminated food sources for potential intermediate hosts.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Predator and heterospecific stimuli alter behaviour in cattle

Wild and domestic ungulates modify their behaviour in the presence of olfactory and visual cues of predators but investigations have not exposed a domestic species to a series of cues representing various predators and other ungulate herbivores. We used wolf (Canis lupus), mountain lion (Puma concolor), and mule deer (Odocoileus hemionus) stimuli (olfactory and visual), and a control (no stimuli) to experimentally test for differences in behaviour of cattle (Bos taurus) raised in Arizona. We measured (1) vigilance, (2) foraging rates, (3) giving up density (GUD) of high quality foods and (4) time spent in high quality forage locations in response to location of stimuli treatments. In general, we found a consistent pattern in that wolf and deer treatments caused disparate results in all 4 response variables. Wolf stimuli significantly increased cattle vigilance and decreased cattle foraging rates; conversely, deer stimuli significantly increased cattle foraging rate and increased cattle use of high quality forage areas containing stimuli. Mountain lion stimuli did not significantly impact any of the 4 response variables. Our findings suggest that domestic herbivores react to predatory stimuli, can differentiate between stimuli representing two predatory species, and suggest that cattle may reduce antipredatory behaviour when near heterospecifics.     

Burrow decorations as antipredatory devices

Animal decorations are normally interpreted as signals of quality.In spiders, however, decorations may have different functions,including the attraction of prey to the web or making the spidercryptic to predators. To date, there is scant evidence for thelatter hypothesis. Here we use the burrow-decorating wolf spiderLycosa tarantula to test whether turrets around the burrow serveto prevent burrow invasion and predation from the Occitan scorpionButhus occitanus. We located spiders and scorpions in fieldenclosures and manipulated the presence or absence of decorationsor turrets. We found that the presence of the turret decreasesthe rate of burrow invasion and improves spider survival, possiblybecause the turret makes the burrow cryptic to scorpions. Inaddition, a field survey showed that burrows with larger decorationshad a lower chance of being invaded by scorpions. These resultsprovide evidence that the decoration has an antipredatory functionin nature.     

Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

Prey detect their predators through predator signals and cues and, consequently, respond with anti‐predatory behaviours to inhibit the action of their aggressors. Lepidopterans can intercept signals emitted by predators and may defend themselves through chemical, morphological or behavioural responses. In this study, we investigated the effect of acoustic stimuli of different predators on defensive behaviour of gregarious caterpillars. Our results demonstrated that Hylesia nigricans (Lepidoptera, Saturniidae) caterpillars alter their behaviour (i.e. abruptly raising the head) in response to the acoustic stimulus of the predators (i.e. predation risk signals from birds and wasps). The magnitude of this response depended on predator identity and caterpillar body size. Larger caterpillars responded more strongly to predatory stimuli than smaller caterpillars. However, regardless of the size of the caterpillars, they responded more strongly to the stimuli of wasps. In addition, we identified that H. nigricans caterpillars emit ultrasonic noise after detecting the stimuli of the predators – this noise seems to function as an alert about the risk of predation during the early stages of development (second and fifth instars). The duration of ultrasonic emission (i.e. milliseconds) increases with the number of repetitions of the stimuli (i.e. wing‐beat sounds of the wasps and insectivorous birds). These results provide novel information about predation risk in interactions among caterpillars and their predators, and indicate possible communication among invertebrates mediated by the risk of predation.     

Differential risk effects of wolves on wild versus domestic prey have consequences for conservation

Predators play integral roles in shaping ecosystems through cascading effects to prey and vegetation. Such effects occur when prey species alter their behavior to avoid predators, a phenomenon called the risk effects of predators. Risk effects of wild predators such as wolves are well documented for wild prey, but not for free ranging domestic animals such as cattle despite their importance for ecosystem function and conservation. We compared risk effects of satellite‐collared wolves (n = 16) on habitat selection by global‐positioning‐system‐collared elk (n = 10) and cattle (n = 31). We calculated resource selection functions (RSFs) in periods before, during and after wolf visits in elk home ranges or cattle pastures. The habitat variables tested included: distance to roads and trails, terrain ruggedness, food‐quality and distance to forest. When wolves were present, elk stayed closer to forest cover and selected less for high‐quality‐food habitat. Thus, the risk effects of wolf presence on elk produced a change in the tradeoff between food and cover selection. Cattle responded by avoiding high‐quality‐food habitat and selecting areas closer to roads and trails (where people likely provided security), but these effects manifested only after wolves had left. Artificial selection in cattle may have attenuated natural anti‐predator behaviors. The effects of predators on ecosystems are likely different when mediated through risk effects on domestic compared to wild animals. Furthermore, predator control in response to livestock predation, an important conservation issue, may produce broad ecosystem effects triggered by decrease of an important predator species. Conservation planners should consider these effects where domestic herbivores are dominant species in the ecosystem.     

Reliability and the adaptive utility of discrimination among alarm callers

Unlike individually distinctive contact calls, or calls that aid in the recognition of young by their parents, the function or functions of individually distinctive alarm calls is less obvious. We conducted three experiments to study the importance of caller reliability in explaining individual-discriminative abilities in the alarm calls of yellow-bellied marmots (Marmota flaviventris). In our first two experiments, we found that calls from less reliable individuals and calls from individuals calling from a greater simulated distance were more evocative than calls from reliable individuals or nearby callers. These results are consistent with the hypothesis that marmots assess the reliability of callers to help them decide how much time to allocate to independent vigilance. The third experiment demonstrated that the number of callers influenced responsiveness, probably because situations where more than a single caller calls, are those when there is certain to be a predator present. Taken together, the results from all three experiments demonstrate the importance of reliability in explaining individual discrimination abilities in yellow-bellied marmots. Marmots' assessment of reliability acts by influencing the time allocated to individual assessment and thus the time not allocated to other activities.     

Captive-born collared peccary (<Emphasis Type="Italic">Pecari tajacu</Emphasis>, Tayassuidae) fails to discriminate between predator and non-predator models

Captive animals may lose the ability to recognize their natural predators, making conservation programs more susceptible to failure if such animals are released into the wild. Collared peccaries are American tayassuids that are vulnerable to local extinction in certain areas, and conservation programs are being conducted. Captive-born peccaries are intended for release into the wild in Minas Gerais state, southeastern Brazil. In this study, we tested the ability of two groups of captive-born collared peccaries to recognize their predators and if they were habituated to humans. Recognition tests were performed using models of predators (canids and felids) and non-predators animals, as well as control objects, such as a plastic chair; a human was also presented to the peccaries, and tested as a separate stimulus. Anti-predator defensive responses such as fleeing and threatening displays were not observed in response to predator models. Predator detection behaviors both from visual and olfactory cues were displayed, although they were not specifically targeted at predator models. These results indicate that collared peccaries were unable to recognize model predators. Habituation effects, particularly on anti-predator behaviors, were observed both with a 1-h model presentation and across testing days. Behavioral responses to humans did not differ from those to other models. Thus, if these animals were to be released into the wild, they should undergo anti-predator training sessions to enhance their chances of survival.     

Male golden hamsters (<Emphasis Type="Italic">Mesocricetus auratus</Emphasis>) are more reactive than females to a visual predator cue

In most species of small mammals, males are exposed to higher levels of risk than females because they compete for mates, travel greater distances to find and procure mates, and/or defend a territory. This suggests that males and females might have different responses to risky situations, such as the presence of a predator. We tested responses to a visual predator cue (an owl silhouette) in male and female golden hamsters (Mesocricetus auratus). In a laboratory arena, there was no significant sex difference in the latency to enter the burrow or time spent in the burrow immediately after exposure to the owl silhouette. Males, however, were less likely to be active during the 3-min period following the animal’s exposure to the silhouette, indicating that male golden hamsters are more wary after exposure to an aerial predator cue than females. Most studies of responses to predators or predator cues have not considered sex differences, but our results show that males and females may have quite different responses to predator cues. Further work should be done to characterize and quantify sex differences in response to predators or predator cues.     

Optimal predator management for mountain sheep conservation depends on the strength of mesopredator release

Large predators often suppress ungulate population growth, but they may also suppress the abundance of smaller predators that prey on neonatal ungulates. Antagonistic interactions among predators may therefore need to be integrated into predator–prey models to effectively manage ungulate–predator systems. We present a modeling framework that examines the net impact of interacting predators on the population growth rate of shared prey, using interactions among wolves Canis lupus, coyotes Canis latrans and Dall sheep Ovis dalli dalli as a case study. Wolf control is currently employed on approximately 16 million ha in Alaska to increase the abundance of ungulates for human harvest. We hypothesized that the positive effects of wolf control on Dall sheep population growth could be counteracted by increased levels of predation by coyotes. Coyotes and Dall sheep adult females (ewes) and lambs were radiocollared in the Alaska Range from 1999–2005 to estimate fecundity, age‐specific survival rates, and causes of mortality in an area without wolf control. We used stage‐structured population models to simulate the net effect of wolf control on Dall sheep population growth (λ). Our models accounted for stage‐specific predation rates by wolves and coyotes, compensatory mortality, and the potential release of coyote populations due to wolf control. Wolves were the main predators of ewes, coyotes were the main predators of lambs, and wolves were the main source of mortality for coyotes. Population models predicted that wolf control could increase sheep λ by 4% per year in the absence of mesopredator release. However, if wolf control released coyote populations, our models predicted that sheep λ could decrease by up to 3% per year. These results highlight the importance of integrating antagonistic interactions among predators into predator–prey models, because the net effect of predator management on shared prey can depend critically on the strength of mesopredator release.     

Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence

Anti-predator behaviors often entail foraging costs, and thus prey response to predator cues should be adjusted to the level of risk (threat-sensitive foraging). Simultaneously dangerous predators (with high hunting success) should engender the evolution of innate predator recognition and appropriate anti-predator behaviors that are effective even upon the first encounter with the predator. The above leads to the prediction that prey might respond more strongly to cues of dangerous predators that are absent, than to cues of less dangerous predators that are actually present. In an applied context this would predict an immediate and stronger response of ungulates to the return of top predators such as wolves (Canis lupus) in many parts of Europe and North America than to current, less threatening, mesopredators. We investigated the existence of innate threat-sensitive foraging in black-tailed deer. We took advantage of a quasi-experimental situation where deer had not experienced wolf predation for ca. 100 years, and were only potentially exposed to black bears (Ursus americanus). We tested the response of deer to the urine of wolf (dangerous) and black bear (less dangerous). Our results support the hypothesis of innate threat-sensitive foraging with clear increased passive avoidance and olfactory investigation of cues from wolf, and surprisingly none to black bear. Prey which have previously evolved under high risk of predation by wolves may react strongly to the return of wolf cues in their environments thanks to innate responses retained during the period of predator absence, and this could be the source of far stronger non-consumptive effects of the predator guild than currently observed.