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Udell, M. A. R., Dorey, N. R., & Wynne, C. D. L. (2008). Wolves outperform dogs in following human social cues. Anim. Behav., 76(6), 1767–1773.
Abstract: Domestic dogs, Canis familiaris, have been shown capable of finding hidden food by following pointing gestures made with different parts of the human body. However, previous studies have reported that hand-reared wolves, C. lupus, fail to locate hidden food in response to similar points in the absence of extensive training. The failure of wolves to perform this task has led to the proposal that the ability to understand others' intentions is a derived character in dogs, not present in the ancestral population (wolves). Here we show that wolves, given the right rearing environment and daily interaction with humans, can use momentary distal human pointing cues to find food without training, whereas dogs tested outdoors and dogs at an animal shelter do not follow the same human points. In line with past studies, pet dogs tested indoors were successful in following these points. We also show that the reported failure of wolves in some past studies may be due to differences in the testing environment. Our findings indicate that domestication is not a prerequisite for human-like social cognition in canids, and show the need for additional research on the role of rearing conditions and environmental factors in the development of higher-level cognitive abilities.
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Patris, B., Perrier, G., Schaal, B., & Coureaud, G. (2008). Early development of filial preferences in the rabbit: implications of nursing- and pheromone-induced odour learning? Anim. Behav., 76(2), 305–314.
Abstract: Newborn rabbits, Oryctolagus cuniculus, discriminate between different categories of adult conspecifics on the basis of their abdominal odour cues. Whether these cues can support the development of filial preferences has not been adequately tested. Using a two-choice paradigm, we assessed the ability of 3-8-day-old pups to orient selectively to the mother versus an unfamiliar female, either spontaneously or after odour conditioning. In experiment 1, nonconditioned pups roamed indifferently over the mother and an unfamiliar female. In experiment 2, pups conditioned to a neutral odorant while nursing or with the mammary pheromone became attracted by the odorant. In experiment 3, pups that had learned the odorant while nursing oriented for longer to any female carrying it, but the unscented mother and a scented unfamiliar female were equally attractive. Finally, in experiment 4, pups that had learned the odorant paired with the mammary pheromone showed a preference for their scented mother, but not systematically for a scented unfamiliar female; furthermore, they were equally attracted by the unscented mother and a scented unfamiliar female. In sum, pups did not spontaneously evince an olfactory preference for the mother when opposed to an unfamiliar female, although they seemed able to detect individual maternal odours. In fact, they appeared to react to both species-specific cues and individual cues that they had learned, and their responses depended on their degree of familiarity with the cues and on the context. The mammary pheromone by itself might act as both a releasing and a reinforcing signal in these early socially oriented behaviours.
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Schwab, C., Bugnyar, T., Schloegl, C., & Kotrschal, K. (2008). Enhanced social learning between siblings in common ravens, Corvus corax. Anim. Behav., 75(2), 501–508.
Abstract: It has been suggested that social dynamics affect social learning but empirical support for this idea is scarce. Here we show that affiliate relationships among kin indeed enhance the performance of common ravens, Corvus corax, in a social learning task. Via daily behavioural protocols we first monitored social dynamics in our group of captive young ravens. Siblings spent significantly more time in close proximity to each other than did nonsiblings. We subsequently tested birds on a stimulus enhancement task in model-observer dyads composed of both siblings and nonsiblings. During demonstration the observer could watch the model manipulating one particular object (target object) in an adjacent room. After removing the model, the observer was confronted with five different objects including the former target object. Observers from sibling dyads handled the target object for significantly longer periods of time as compared with the other four available objects, whereas observers from nonsibling dyads did not show a preference for the target object. Also, siblings matched the model's decision to cache or not to cache objects significantly more often than did nonsiblings. Hence, siblings were likely to attend to both, the behaviour of the model (caching or noncaching) and object-specific details. Our results support the hypothesis that affiliate relations between individuals affect the transmission of information and may lead to directed social learning even when spatial proximity has been experimentally controlled for.
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Lingle, S., Rendall, D., Wilson, W. F., DeYoung, R. W., & Pellis, S. M. (2007). Altruism and recognition in the antipredator defence of deer: 2. Why mule deer help nonoffspring fawns. Anim. Behav., 73(5), 907–916.
Abstract: Both white-tailed deer, Odocoileus virginianus, and mule deer, O. hemionus, females defend fawns against coyotes, Canis latrans, but only mule deer defend nonoffspring conspecific and heterospecific fawns. During a predator attack, females may have to decide whether to defend a fawn while having imperfect information on its identity obtained from hearing a few distress calls. Although imperfect recognition can influence altruistic behaviour, few empirical studies have considered this point when testing functional explanations for altruism. We designed a series of playback experiments with fawn distress calls to test alternative hypotheses (by-product of parental care, kin selection, reciprocal altruism) for the mule deer's defence of nonoffspring, specifically allowing for the possibility that females mistake these fawns for their own. White-tailed deer females approached the speaker only when distress calls of white-tailed deer fawns were played and when their own fawn was hidden, suggesting that fawn defence was strictly a matter of parental care in this species. In contrast, mule deer females responded similarly and strongly, regardless of the caller's identity, the female's reproductive state (mother or nonmother) or the presence of their own offspring. The failure of mule deer females to adjust their responses to these conditions suggests that they do not defend nonoffspring because they mistake them for their own fawns. The lack of behavioural discrimination also suggests that kin selection, reciprocal altruism and defence of the offspring's area are unlikely to explain the mule deer's defence of nonoffspring. We identify causal and functional questions that still need to be addressed to understand why mule deer defend fawns so indiscriminately.
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Lingle, S., Rendall, D., & Pellis, S. M. (2007). Altruism and recognition in the antipredator defence of deer: 1. Species and individual variation in fawn distress calls. Anim. Behav., 73(5), 897–905.
Abstract: Mule deer, Odocoileus hemionus, females actively defend fawns against predators, including nonoffspring conspecific fawns and heterospecific white-tailed deer, O. virginianus, fawns. We hypothesized that the defence of nonoffspring fawns was due to a recognition error. During a predator attack, females may have to decide whether to defend a fawn with imperfect information on its identity obtained from hearing only a few distress calls. We examined fawn distress calls to determine whether calls made by the two species and by different individuals within each species were acoustically distinctive. The mean and maximum fundamental frequencies of mule deer fawns were nearly double those of white-tailed deer fawns, with no overlap, enabling us to classify 100% of calls to the correct species using a single trait. A large proportion of calls was also assigned to the correct individual using a multivariate analysis (66% and 70% of mule deer and white-tailed deer fawns, respectively, chance = 6% and 10%); however, there was considerable statistical uncertainty in the probability of correct classification. We observed fawns approach conspecific females in an attempt to nurse; females probed most offspring fawns with their noses before accepting them, and always probed nonoffspring fawns before rejecting them, suggesting that close contact and olfactory information were needed to unequivocally distinguish nonoffspring from offspring fawns. Taken together, these results suggest that acoustic variation alone would probably be sufficient to permit rapid and reliable species discrimination, but it may not be sufficient for mothers to unequivocally distinguish their own fawn from conspecific fawns.
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Scordato, E. S., & Drea, C. M. (2007). Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim. Behav., 73(2), 301–314.
Abstract: The function of olfactory signalling in social species is less well understood than in asocial species. Consequently, we examined olfactory communication in the ringtailed lemur, a socially complex primate that retains a functional vomeronasal organ, has well-developed scent glands and shows a suite of scent-marking behaviour. To assess the information content of different types of scent gland secretions, we decoupled olfactory cues from the visual and behavioural modalities with which scent marking is normally associated. We presented male and female subjects (signal receivers) with a series of choice tests between odours derived from conspecific donors (signal senders) varying by sex, age, social status and reproductive condition. We additionally examined the influence of the receivers' reproductive state and familiarity with the signaller. The reproductive condition, social status and familiarity of senders and receivers affected signal transmission; specifically, male receivers attended most to the odours of conspecifics in breeding condition and to the odours of familiar, dominant animals. By contrast, females varied their responses according to both their own reproductive state and that of the sender. Based on male and female patterns of countermarking, we suggest that scent marking serves a function in intergroup spacing and intrasexual competition for both sexes, as might be expected in a female-dominant species. By contrast, minimal female interest in male odours counters a female mate choice function for scent marking in this species. Nevertheless, scent marks are critical to male-male competition and, therefore, may be subject to sexual selection.
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Hopkins, W. D., Taglialatela, J. P., & Leavens, D. A. (2007). Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim. Behav., 73(2), 281–286.
Abstract: Chimpanzees, Pan troglodytes, produce numerous species-atypical signals when raised in captivity. We examined contextual elements of the use of two of these vocal signals, the `raspberry' and the extended grunt. Our results demonstrate that these vocalizations are not elicited by the presence of food, but instead function as attention-getting signals. These findings reveal a heretofore underappreciated category of animal signals: attention-getting sounds produced in novel environmental circumstances. The invention and use of species-atypical signals, considered in relation to group differences in signalling repertoires in apes in their natural habitats, may index a generative capacity in these hominoid species without obvious corollary in other primate species.
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Christensen, J. W., Zharkikh, T., & Chovaux, E. (2011). Object recognition and generalisation during habituation in horses. Appl. Anim. Behav. Sci., 129(2-4), 83–91.
Abstract: The ability of horses to habituate to frightening stimuli greatly increases safety in the horse-human relationship. A recent experiment suggested, however, that habituation to frightening visual stimuli is relatively stimulus-specific in horses and that shape and colour are important factors for object generalisation (Christensen et al., 2008). In a series of experiments, we aimed to further explore the ability of horses (n = 30, 1 and 2-year-old mares) to recognise and generalise between objects during habituation. TEST horses (n = 15) were habituated to a complex object, composed of five simple objects of varying shape and colour, whereas CONTROL horses (n = 15) were habituated to the test arena, but not to the complex object. In the first experiment, we investigated whether TEST horses subsequently reacted less to i) simple objects that were previously part of the complex object (i.e. testing for object recognition) and ii) a novel object (new shape and colour, i.e. testing for object generalisation), compared to CONTROLS. In the second experiment we investigated whether TEST horses reacted to a change in object order and object location. Behavioural reactions to the object, latency to eat, total eating time and heart rate were recorded. Compared to CONTROLS, TEST horses reacted significantly less towards objects, which were previously part of the complex object (e.g. mean heart rate; P = 0.006), indicating object recognition. In contrast to our expectations, TEST horses also reacted significantly less towards the novel object (e.g. mean heart rate; P = 0.018), suggesting that they were capable of object generalisation. We also found that TEST horses showed an increase in exploratory behaviour when objects within the complex object changed order and location (both P < 0.001), whereas there was no increase in heart rate, indicating that the horses were not frightened by the changes. The results demonstrate that it is possible to increase object generalisation in horses by habituating them to a range of colours and shapes simultaneously. This knowledge greatly affects the way in which horses may be trained to react calmly towards frightening objects.
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Gifford, A. K., Cloutier, S., & Newberry, R. C. (2007). Objects as enrichment: Effects of object exposure time and delay interval on object recognition memory of the domestic pig. Appl. Anim. Behav. Sci., 107(3-4), 206–217.
Abstract: A modified spontaneous object recognition test was used to examine object recognition memory in the domestic pig. This test uses preference for a novel object over a previously encountered sample object as indicating recognition of the sample object, and no preference as indicating no recognition. Two factors hypothesized to affect object recognition are duration of exposure to the sample stimulus and delay interval before re-exposure. Both of these factors could be manipulated in a rotational object enrichment program for pigs. Reducing exposure time and increasing the delay interval before re-exposure should decrease object recognition and prolong novelty-induced object exploration. We exposed 5-week-old pigs to different sample objects in their home pens for 10 min and 2 days, respectively. We tested for object recognition memory at various delay intervals after initial exposure by placing littermate pairs in a test pen for 10 min and recording snout contact with a sample object and a completely novel object. At a 1-h delay, half the pairs were tested with the 2-day sample object; the other half received the 10-min sample object. At a 3-h delay, pairs were tested with the opposite sample object. Pairs were also tested with the 2-day sample at a 5-day delay and the 10-min sample at a 6-day delay. We predicted that pigs would show a preference for the novel versus the 2-day sample object at all three delays, but would only prefer the novel object over the 10-min sample object at the 1-h and 3-h delays. Pigs did not show novelty preference in the presence of the 10-min sample object at any delay. Novelty preference in the presence of the 2-day sample object occurred at the 3-h (P < 0.05) and 5-day delays (P < 0.001), but not the 1-h delay. The lack of novelty preference when pigs were tested with the 10-min sample object may have been due to failure to habituate to the sample object. Testing in a different location from the initial sample object exposure and retroactive interference from exposure to the 10-min sample object may have contributed to a temporary lack of novelty preference when pigs were tested with the 2-day sample object at the 1-h delay. The finding that pigs retained a memory for the 2-day sample object for at least 5 days suggests that restricting object exposure to less than 2 days may help to preserve the exploratory value of objects rotated among pens.
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Meehan, C. L., & Mench, J. A. (2007). The challenge of challenge: Can problem solving opportunities enhance animal welfare? Appl. Anim. Behav. Sci., 102(3-4), 246–261.
Abstract: Cognitive mechanisms are an important part of the organization of the behavior systems of animals. In the wild, animals regularly face problems that they must overcome in order to survive and thrive. Solving such problems often requires animals to process, store, retrieve, and act upon information from the environment--in other words, to use their cognitive skills. For example, animals may have to use navigational, tool-making or cooperative social skills in order to procure their food. However, many enrichment programs for captive animals do not include the integration of these types of cognitive challenges. Thus, foraging enrichments typically are designed to facilitate the physical expression of feeding behaviors such as food-searching and food consumption, but not to facilitate complex problem solving behaviors related to food acquisition. Challenging animals by presenting them with problems is almost certainly a source of frustration and stress. However, we suggest here that this is an important, and even necessary, feature of an enrichment program, as long as animals also possess the skills and resources to effectively solve the problems with which they are presented. We discuss this with reference to theories about the emotional consequences of coping with challenge, the association between lack of challenge and the development of abnormal behavior, and the benefits of stress (arousal) in facilitating learning and memory of relevant skills. Much remains to be done to provide empirical support for these theories. However, they do point the way to a practical approach to improving animal welfare--to design enrichments to facilitate the cognitive mechanisms which underlie the performance of complex behaviors that cannot be performed due to the restrictions inherent to the captive environment.
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