Barbara Regaiolli

Manual lateralization in macaques: handedness, target laterality and task complexity

ABSTRACT Non-human primates represent models to understand the evolution of handedness in humans. Despite several researches have been investigating non-human primates handedness, few studies examined the relationship between target position, hand preference and task complexity. This study aimed at investigating macaque handedness in relation to target laterality and tastiness, as well as task complexity. Seven pig-tailed macaques (Macaca nemestrina) were involved in three different “two alternative choice” tests: one low-level task and two high-level tasks (HLTs). During the first and the third tests macaques could select a preferred food and a non-preferred food, whereas by modifying the design of the second test, macaques were presented with no-difference alternative per trial. Furthermore, a simple-reaching test was administered to assess hand preference in a social context. Macaques showed hand preference at individual level both in simple and complex tasks, but not in the simple-reaching test. Moreover, target position seemed to affect hand preference in retrieving an object in the low-level task, but not in the HLT. Additionally, individual hand preference seemed to be affected from the tastiness of the item to be retrieved. The results suggest that both target laterality and individual motivation might influence hand preference of macaques, especially in simple tasks.

Three actions, two groups: Looking for the origin of primate manual lateralization.

Handedness is the most evident behavioral asymmetry in humans: to study nonhuman primate hand preference could be optimal to investigate the evolutionary origin of handedness in our species, even though behavioral asymmetries are widespread among vertebrates. This study investigated hand preferences in 32 Old World monkeys and 26 great apes during 3 spontaneous actions, assessing the effect of taxonomic group, sex and age on primate handedness. Data about foraging, locomotion, and manipulation were collected and 50 bouts per behavioral category per subject were recorded. A bias toward right-hand use for starting locomotion was reported in both Old World monkeys and great apes. Furthermore, in the great apes, a group-level right-hand preference for manipulation was found. Results suggest an important role of factors such as posture and task complexity in the evolution of primate manual lateralization. The effect of taxonomic group, sex, and age on the hand preference are also discussed. (PsycINFO Database Record

Hand preference on unimanual and bimanual tasks in strepsirrhines: The case of the ring-tailed lemur (Lemur catta)

Assessing manual lateralization in non‐human primates could be an optimal way to understand the adaptive value of this asymmetry in humans. Though many studies have investigated hand preferences in Old and New World monkeys and apes, fewer studies have considered manual lateralization in strepsirrhines, especially in experimental tasks. This study investigated hand preferences for a unimanual and a bimanual task of 17 captive ring‐tailed lemurs (Lemur catta), housed at Parco Natura Viva (VR), Italy. The effect of age on handedness has been also investigated. The lemurs were tested on a unimanual task, in which subjects were restricted to using one hand to retrieve the food inside an apparatus, and on a bimanual task, in which lemurs had to use one hand to keep the apparatus door open while reaching with the other hand to retrieve the food inside it. At the population‐level, our results revealed an asymmetrical hand use distribution, in particular a bias toward a right hand preference for food reaching in both the unimanual and the bimanual tasks. Furthermore, at the individual‐level, the bimanual task seems to elicit a greater hand preference than the unimanual task. Results of this study underline the importance of experimental tasks in determining hand preference in strepsirrhines. Furthermore, as bimanual tasks elicited a stronger degree of lateralization, they appear to be more suited to investigate manual laterality. Finally, findings from this study highlight the presence of a right hand preference in ring‐tailed lemurs, shedding new light on the evolution of human right handedness. Am. J. Primatol. 78:851–860, 2016.

Hand preference on unimanual and bimanual tasks in Barbary macaques (Macaca sylvanus)

The presence of group‐level handedness in non‐human primates remains controversial, as different studies have produced inconsistent results. Bimanual coordinated tasks have been found to elicit more pronounced hand preferences than simple unimanual tasks. The aim of this study was to examine manual lateralization in a group of 15 Barbary macaques during unimanual and bimanual tasks. In the unimanual task, data on simple food reaching in a foraging context were collected. During the bimanual task, macaques had to use one hand to hold a tube‐shaped apparatus while reaching with the other hand to retrieve the food inside it. Data on the hand use to retrieve food were collected. First, no significant group‐level hand preference was found for the unimanual task. However, a significant right hand bias was evident for the bimanual task. At the individual‐level, approximately 47% and 67% of the subjects had a significant hand preference in the unimanual and bimanual task respectively. The strength of the hand preference was greater in the bimanual than in the unimanual task. Findings of this study add Macaca sylvanus to the other species showing a right hand preference for coordinated bimanual tasks. Moreover, our results add to the growing body of evidence that bimanual tasks are more suitable and valid measures to investigate handedness in non‐human primates.

Positive reinforcement training : a tool for care and management of captive vervet monkeys (Chlorocebus aethiops).

In modern zoos, training should be an integral component of the animal care and management. The benefits of training include the opportunity for positive interactions with caretakers. This study was carried out with a group of vervet monkeys (Chlorocebus aethiops) housed at the Garda Zoological Park (Italy). Using focal animal sampling, we observed the behaviour performed by all group members (N = 10) from December 2007 to August 2008. The group took part in a training program to be isolated in a familiar area before the subjects were included in a cognitive study. We collected behavioural data during a pre-training period to assess the social behaviour of the colony and during the training period to investigate the effects of the training program on the behaviour of individuals. Additionally, a second phase of the study was conducted and training sessions with individual monkeys were video-recorded to determine the behaviour of animals during each training session and thus to confirm that they were suitable for participating in the procedure. Our results suggest that the training program enriched the daily routine of these captive primates by increasing affiliative behaviours while decreasing agonistic behaviours. Furthermore, there was behavioural response variability among the individuals under training procedure. However all the individuals were trained to calmly enter in a familiar area and to be isolated from other members of the group. In conclusion, our findings highlight the importance of using the positive reinforcement training to reduce the tension directly associated with potentially stressful procedures by allowing primates to voluntarily participate in these procedures. In addition, the training was found to be an enrichment tool for vervet monkeys.

Asymmetries in mother-infant behaviour in Barbary macaques (Macaca sylvanus)

Asymmetries in the maternal behaviour and anatomy might play an important role in the development of primate manual lateralization. In particular, early life asymmetries in mother’s and infant’s behaviour have been suggested to be associated with the development of the hand preference of the offspring. The aim of this study was to investigate the presence of behavioural asymmetries in different behavioural categories of mother-infant dyads of zoo-living Barbary macaques (Macaca sylvanus). The study subjects were 14 Barbary macaques involved in seven mother-infant dyads housed in Parco Natura Viva, Italy. For the mothers, bouts of hand preference for maternal cradling and infant retrieval were collected. For the infants, we focused on nipple preference and hand preference for clinging on mother ventrum. Moreover, we collected bouts of hand preference for food reaching in both groups. No significant group-level bias was found for any of the behavioural categories in either mothers or infants. However, at the individual level, six out of seven mothers showed a significant cradling bias, three toward the right hand and three toward the left hand. Moreover, all infants showed a significant nipple preference, six toward the mother’s right nipple, one toward the left nipple. Furthermore, a significant correlation was found between the infant nipple preference and their hand preference for food reaching, suggesting that maternal environment rather than behaviour might affect the development of hand preference in Old World monkeys. Our findings seem partially to add to previous literature on perceptual lateralization in different species of non-primate mammals, reporting a lateral bias in mother-infant interactions. Given the incongruences between our study and previous research in great apes and humans, our results seem to suggest possible phylogenetic differences in the lateralization of mothers and infants within the Primates order.

How to be a great dad: parental care in a flock of greater flamingo (Phoenicopterus roseus)

In the last years, studies on captive greater flamingos have increased. Research on zoo animals is important to improve the knowledge on these species and to improve their ex-situ and in-situ conservation. The aim of the present study was to investigate the parental behaviour of a captive colony of greater flamingo hosted at Parco Natura Viva, an Italian zoological garden, to improve the knowledge on this species in zoos. In particular, the present study investigated and compared the parental care of females and males in 35 breeding pairs of greater flamingos. For each pair, we collected durations of parental care behaviour of both females and males, recording their position in relation to the nest (near the nest, on the nest, away from the nest) and individual and social behaviours performed. First, both partners were involved in parental care and displayed species-specific behaviours reported in the wild. The main results were that males spent more time than females on the nest (P = 0.010) and near it (P = 0.0001) and were more aggressive toward other flamingos than females, both when sitting on the nest (P = 0.003) and when near the nest (P = 0.0003). Therefore, male flamingos seem to be more involved in incubation duties and nest protection than females. This kind of research is important not only to expand the knowledge on bird species such as flamingos, but also to improve their husbandry and breeding in controlled environment. Indeed, understanding animal behaviour allows us to gain insights into their individual and social needs, addressing potential animal welfare issues.

Correction: Asymmetries in mother-infant behaviour in Barbary macaques (Macaca sylvanus)

[This corrects the article DOI: 10.7717/peerj.4736.].

Investigating individual and social behaviour of the Northern bald ibis (Geronticus eremita): behavioural variety and welfare

The Northern bald ibis (Geronticus eremita) (NBI) is one of the most threatened birds in the world. Intense conservation efforts have been undertaken and several research projects on the species are being done in Morocco and in Europe. Observing animal behaviour has been proved to be an efficient and non-invasive technique to assess the animal welfare, with the performance of a wide array of natural behaviours being one of the mostly used indicators of good mental and physical well-being. The aim of this study was to investigate the behaviour of a flock of 14 zoo-living NBI of different ages. The study focused on the variety of species-specific individual and social behaviours, in the light of reintroduction of the study juveniles in the wild. Per subject, 20 10-min. sessions were done. A continuous focal animal sampling method was used to collect individual and social behaviours. Behavioural data have been compared between adults and juveniles. Moreover, a Behavioural Variety Index (BVI) has been proposed and calculated based on previous literature describing natural ibis behaviours. The BVI might help in the evaluation of the variety of behaviours performed by each individual and the monitoring of the diversity of the behavioural repertoire of zoo animals. Our results showed that the birds performed species-specific behaviours and no abnormal behaviour was reported. Moreover, the BVI highlighted a good behavioural variety as each bird performed approximately 78% of the natural behaviours described in the Northern bald ibis and in close relative species. Our findings seem to suggest the presence of qualitative and quantitative similarities between the behavioural repertoires of the study ibises and those described in wild conspecifics, suggesting a good welfare of the colony. Finally, the BVI proposed in the current study seems to be a useful and practical tool to test behavioural diversity in zoo animals.

Investigating parental care behaviour in same-sex pairing of zoo greater flamingo (Phoenicopterus roseus)

Same-sex pair bonds have been documented in several animal species and they are widespread in birds. However, little is known about the evolutionary origin and the adaptive value of such behaviour. The aim of this study was to investigate the parental behaviour of four zoo female greater flamingos involved in two breeding pairs, housed in a flock at Parco Natura Viva, Italy. Further, the behaviour of the study females was compared with that of male and female flamingos in heterosexual pairs described in a previous published work on this same flock. For each pair, the behaviour of both birds during the incubation period was recorded and twenty 10-minute sessions were run within the incubation period. A continuous focal animal sampling method was used to collect data on location (on the nest or not on the nest) and the parental care behaviour (e.g.: agonistic behaviours toward disturbing conspecifics, egg-care, nest-building, self-comfort behaviour, sleeping) of the two pairs. Data of the current study females were compared with those of females and males involved in heterosexual pairs of this same flock. Results showed that within each pair the egg-layer female stayed away from the nest more than the other female. In addition, the female that did not lay an egg was more involved in agonistic behaviour compared to other females, particularly when in specific locations. In heterosexual pairs, male flamingos were more involved in the incubation and in nest protection. Moreover, no significant differences in the time spent on the nest and away from the nest between the heterosexual male and the non-layer females of same-sex pairs were found. The same findings were reported when comparing heterosexual females and the egg-layer females of the same-sex pairs. Therefore, our findings suggest that in greater flamingos the behaviour of the female–female pairs seems to be equivalent to that of male-female bonds. Such research provides more insight into flamingo social behaviour, and their reproductive cycle, and provides information on why pair bonds may form and how these affect the wider breeding behaviour of the flock.