• Does positive reinforcement training affect the behaviour and welfare of zoo animals? The case of the ring-tailed lemur (Lemur catta)

      Spiezio, Caterina; Scala, Consuelo; Vaglio, Stefano; Regaiolli, Barbara (Elsevier, 2017-08-05)
      Positive reinforcement training (PRT) is an established tool to facilitate animal husbandry, care and research in modern zoos, with potential positive implications for captive animal welfare. The study explored the role of an isolation PRT training programme on the well-being of ring-tailed lemurs (Lemur catta). Eleven subjects were observed during an isolation training protocol to induce the animals to enter an area (training area) calmly and retrieve rewards separated from group members. Duration of individual and social behaviours were collected over two different periods: the baseline period, before the beginning of the isolation training protocol and the training period, in which the collection of the data started at the end of the isolation training sessions. Additionally, behavioural data within the isolation training sessions (latency to enter the training area and retrieve the reward, display of stress-related behaviours) were recorded. Outside the training sessions, lemurs were out of sight significantly more in the baseline (Mean ± SD: 15.46 ± 5.20) than in the training (Mean ± SD: 4.36 ± 2.89) period. Social behaviour was performed significantly more in the training (Mean ± SD: 31.80 ± 12.34) than in the baseline (Mean ± SD: 12.52 ± 5.14) period; particularly, lemurs were in social contact significantly more in the training (Mean ± SD: 14.09 ± 6.00) than in the baseline period (Mean ± SD: 4.58 ± 2.73). Agonistic behaviours were performed significantly more in the baseline (Mean ± SD: 0.23 ± 0.15) than in the training (Mean ± SD: 0.07 ± 0.07) period. Within the training sessions, all the individuals entered the training area, were isolated from conspecifics, and retrieved the reward in 6 out of 9 sessions. Our findings show that, during the PRT period, lemurs displayed their natural behaviour in their everyday social life with significant increase of their affiliative behaviours and decrease of aggressive behaviours with benefits for their welfare status. Thus, lemurs were able to cope with the use of PRT to isolate each individual from its social group − a situation which, without training, might be very stressful. In conclusion, PRT may play a crucial role for the captive management of ring-tailed lemurs in captive facilities, including zoos.
    • The effects of a zoo environment on free-living, native small mammal species

      Elwell, Emily; Leeson, Christopher; Vaglio, Stefano (Wiley, 2021-03-25)
      One of the main threats to native species conservation is urbanization. It is causing changes to natural habitats and species composition. Urban green spaces have shown to have conservation value for native species by providing safe spaces in urban areas. They typically contain a variety of habitats and plant species which is correlated with greater abundance and diversity of small mammal species. Zoos are a vital resource for animal conservation and, in some instances, could be considered as an urban green space for native species conservation. Their unique environment provides free-living, native species an abundance of resources including food and shelter. This project involved the live trapping of free-living small mammal species (<40 g) between enclosures in Dudley Zoological Gardens to study the effects of the zoo environment. There were no significant differences found between total number of captures and trap proximity to enclosures. There was a significant difference in total captures found between different enclosure trapping areas. Generalized linear mixed models were fitted to the data and there were significant relationships between abundance and both habitat type and enclosure species. Habitats associated with semi-natural woodland had the greatest diversity and total captures of small mammals. Total captures was lower in trapping areas that were associated with predatory species. Similar to research on green spaces, habitat was an important factor determining abundance, but predator enclosures were a factor unique to zoos. This study illustrates the potential of zoos as an urban green space and for the study of small mammals.
    • Effects of hand-rearing on the behaviour of zoo-housed chimpanzees

      Spiezio, Caterina; Vaglio, Stefano; Vandelle, Camille; Sandri, Camillo; Regaiolli, Barbara (Karger, 2021-03-31)
      Early-life experiences may considerably affect the behavioural patterns of adult primates. Particularly, atypical rearing practices might lead to abnormal behaviours and social-sexual deficiencies in captive, adult non-human primates. We conducted behavioural observations of mother-reared (n = 5) and hand-reared (n = 6) adult chimpanzees in a social group at Parco Natura Viva, Italy. We used continuous focal animal sampling to collect behavioural data focusing on individual and social behaviours. We found that all study subjects performed individual and social species-specific behaviours. However, mother-reared chimpanzees performed locomotion and affiliative behaviours significantly more than hand-reared subjects. In addition to these species-typical behaviours, hand-reared chimpanzees showed significantly more abnormal behaviours than mother-reared subjects. Therefore, these findings suggest that hand-rearing could have wide-reaching effects on the behavioural repertoire in adult zoo-housed chimpanzees. Hence, even if sometimes human intervention in rearing may be necessary to ensure the survival of captive infant chimpanzees, our results suggest that zoo-housed chimpanzees might benefit from minimized human-animal interactions and exposure to conspecifics throughout their development. These suggestions should be implemented in regular husbandry practices.
    • Effects of scent enrichment on behavioural and physiological indicators of stress in zoo primates

      Vaglio, Stefano; Kaburu, Stefano; Pearce, Richard; Bryant, Luke; McAuley, Ailie; Lott, Alexandria; Sheppard, Demi; Smith, Sarah; Tompkins, Bethany; Elwell, Emily; et al. (Wiley, 2021-03-04)
      Captive breeding is vital for primate conservation, with modern zoos serving a crucial role in breeding populations of threatened species and educating the general public. However, captive populations can experience welfare issues that may also undermine their reproductive success. In order to enhance the well-being of endangered zoo primates, we conducted a study to assess the effects of a new scent enrichment programme on captive red-ruffed lemurs (Varecia rubra), black howler monkeys (Alouatta caraya), siamangs (Symphalangus syndactylus), Lar gibbons (Hylobates lar) and orangutans (Pongo pygmaeus pygmaeus). We combined behavioural observations and faecal endocrinology analyses to evaluate the effects of a series of essential oils (benzoin, lavender, lemongrass) on five captive troops (N = 19) housed at Dudley Zoo & Castle and Twycross Zoo (UK). We recorded observations of natural species-specific and abnormal stress-related behaviours for 480 hr using instantaneous scan sampling. We collected 189 faecal samples and measured the faecal cortisol concentrations using radioimmunoassay. We found a significant effect of the scent enrichment on behaviours, with red-ruffed lemurs and black howler monkeys reducing their social interactions, as well as red-ruffed lemurs and Lar gibbons decreasing their stress-related behaviours, after they were exposed to the series of essential oils. We also found that red-ruffed lemurs displayed a significant increase in faecal glucocorticoids following the exposure to essential oils. Our contradictory findings suggest that the effects of this series of essential oils may change depending on the species-specific social lives and olfactory repertoires of primates. In conclusion, we cannot recommend using these essential oils widely with zoo primates without additional evaluation.
    • Fecal concentrations of cortisol, testosterone, and progesterone in cotton-top tamarins hosted in different zoological parks: Relationship among physiological data, environmental conditions and behavioral patterns

      Fontani, Sara; Vaglio, Stefano; Beghelli, Valentina; Mattioli, Michela; Bacci, Silvia; Accorsi, Pier Attilio (Taylor and Francis, 2014-05-14)
      The aim of this investigation was to study the welfare of 3 captive groups of cotton-top tamarins housed in different zoological parks. Ethological observations were conducted during 1 year. In addition, fecal samples were collected and the concentrations of glucocorticoids, androgens, and progestogens were measured. Within each group, no significant differences in fecal cortisol concentrations were found between subjects. The fecal concentrations of testosterone and progesterone significantly differed depending on the sexes and ages of the tamarins. A significant association was found among hormone concentrations, exhibit dimensions, and group composition. A highly significant correlation was found between all hormones considered and the space available for each subject. Significant differences in behavioral patterns were observed among groups, including social–individual, affiliative–aggressive, and anogenital–suprapubic scent marking. Correlations between hormone measurements and behaviors were detected. In conclusion, this study confirmed the associations between some behaviors exhibited by these nonhuman primates and both cortisol and testosterone; these data also highlight the role played by progesterone in these behaviors.
    • Female copulation calls vary with male ejaculation in captive olive baboons

      Vaglio, Stefano; Ducroix, Louise; Rodriguez Villanueva, Maria; Consiglio, Rosanna; Kim, Ayong Julia; Neilands, Patrick; Stucky, Kerstin; Lameira, Adriano R (Brill, 2020-08-11)
      Copulation calls are mating-associated vocalizations that are common in primates, with females vocalizing after copulation in several Old World monkeys and apes. Baboon females typically produce copulation calls that correlate with fertile phase. Calls are, thus, regarded as an upshot of cycle physiology and sexually selected calls. Here, we describe three captive troops of olive baboons wherein, against expectation, females suppressed vocalizing during copulations. Vaginal cytology, together with sexual swelling observations, confirmed that females experienced full receptive cycles. Ovulation did not affect vocal probability during sex, while copulation calls were predicted by male ejaculation just as in other Old World primate species. Results cast doubt on the existence of physiological triggers for baboon copulation calls. Social factors may instead play a larger role. Alterations in social structure (as typically observed in the wild) may be implemented strategically as captive enrichment in order to reveal how females in highly social primates change sexual strategies and, therefore, the use of their copulation calls.
    • Gum feeder as environmental enrichment for zoo marmosets and tamarins

      Regaiolli, Barbara; Angelosante, Chiara; Marliani, Giovanna; Accorsi, Pier Attilio; Vaglio, Stefano; Spiezio, Caterina (Wiley, 2020-01-15)
      Tamarins and marmosets are small‐bodied social callitrichines. Wild callitrichines feed on exudates, such as sap and gum; particularly, marmosets are mainly gummivores, while tamarins consume gums only occasionally and opportunistically. Zoo marmosets and tamarins are usually provided with gum arabic as an alternative to the exudates normally found in the wild. The aim of this study was to evaluate the effects of a gum feeder on the behavior and well‐being of four zoo‐managed callitrichines. We studied four cotton‐top tamarins (Saguinus oedipus), four red‐handed tamarins (S. midas), two pygmy marmosets (Cebuella pygmaea), and three Geoffroy's marmosets (Callithrix geoffroyi) housed at Parco Natura Viva (Italy). We conducted the study over two different periods, a baseline (control, without the gum feeder) and then a gum feeder (when the gum feeder was provided) period. We used continuous focal animal sampling to collect behavioral data, including durations of social and individual behaviors. We collected 240 min of observations per period per study subject, with a total of 3,120 min for all the subjects in the same period and of 6,240 min in both periods. We analyzed data by using nonparametric statistical tests. First, we found that the gum feeder promoted species‐specific behaviors, such as exploration, and diminished self‐directed behaviors, suggesting an enriching effect on tamarin and marmoset behavior. Moreover, in red‐handed tamarins, the provision of the gum feeder reduced the performance of self‐directed and abnormal behavior, specifically coprophagy. These results confirm that gum feeders are effective foraging enrichment tools for zoo marmosets and tamarins.
    • Histology of the suprapubic and anogenital cutaneous glands in male cotton-top tamarins (Saguinus oedipus)

      Fontani, Sara; Tanteri, Gianfranco; Vaglio, Stefano; Delfino, Giovanni; Moggi-Cecchi, Jacopo (Karger, 2014-03-16)
      In cotton top tamarins (Saguinus oedipus), scent glands have been mostly studied in females from museum collections. This work aims to extend the investigation to male specimens, introducing a novel source of skin samples. Two adult males from zoo populations, one intact and one castrated, were immediately frozen after natural death. Skin samples were later collected at the thawing onset, soaked with cold fixative and processed for light microscopy. Sebaceous units of scent glands showed phasic secretory activity in the intact male and marked fibrosis in the castrated male. It appears, therefore, that light microscopy samples from frozen tissues provide detailed features that can disclose distinctive traits in specimens characterized by different hormonal balances.
    • Olfactory signals and fertility in olive baboons

      Vaglio, Stefano; Minicozzi, Pamela; Kessler, Sharon E; Walker, David; Setchell, Joanna M (Springer Nature, 2021-12-31)
      Female primates signal impending ovulation with a suite of sexual signals. Studies of these signals have focussed on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. We aimed to investigate the information content of female olfactory signals in captive olive baboons (Papio anubis) and relate these to the female fertile period. We studied eight adult females living in four groups at the CNRS Station de Primatologie, Rousset-sur-Arc, France. We used vaginal cytology to detect ovulation. We investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We found a total of 74 volatile compounds, of which we tentatively identified 25, including several ketones, alcohols, aldehydes, terpenes, volatile fatty acids and hydrocarbons that have been identified in odour profiles of other primates. Our results show that vaginal odour intensity differs with sexual cycle stage suggesting that odour might play a role in signalling female baboon fertility. We found differences in vaginal odour between females living in all-female and in mixed sex groups but we could not distinguish the effects of group composition, female age and identity. This study of olfactory signalling improves our understanding of how female primates advertise their sexual receptivity.
    • Pheromone

      Vaglio, Stefano; Bartels-Hardege, Helga; Jorg, Hardege (Springer, 2017)
    • Positive reinforcement training: a tool for care and management of captive vervet monkeys (Chlorocebus aethiops).

      Spiezio, Caterina; Piva, Federica; Regaiolli, Barbara; Vaglio, Stefano (Universities Federation for Animal Welfare, 2016-01-01)
      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 from December 2007 to August 2008. The group took part in a training programme 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 programme 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 to thus confirm that they were suitable for participating in the procedure. Our results suggest that the training programme 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 the training procedure. However, all the individuals were trained to calmly enter a familiar area and be isolated from other members of the group. In conclusion, our findings highlight the importance of using positive reinforcement training to reduce the tension directly associated with potentially stressful procedures by allowing primates to participate voluntarily in these procedures. In addition, the training was found to be an enrichment tool for vervet monkeys.
    • Sampling and analysis of animal scent signals

      Walker, David; Vaglio, Stefano (MYJoVE Corporation, 2021-02-13)
      We have developed an effective methodology for sampling and analysis of odor signals, by using headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry, to understand how they may be used in animal communication. This technique allows the semi-quantitative analysis of the volatile components of odor secretions by enabling the separation and tentative identification of the components in the sample, followed by the analysis of peak area ratios to look for trends that could signify compounds that may be involved in signaling. The key strengths of this current approach are the range of sample types that can be analyzed; the lack of need for any complex sample preparation or extractions; the ability to separate and analyze the components of a mixture; the identification of the components detected; and the capability to provide semi-quantitative and potentially quantitative information on the components detected. The main limitation to the methodology relates to the samples themselves. Since the components of specific interest are volatile, and these could easily be lost, or their concentrations altered, it is important that the samples are stored and transported appropriately after their collection. This also means that sample storage and transport conditions are relatively costly. This method can be applied to a variety of samples (including urine, feces, hair and scent-gland odor secretions). These odors consist of complex mixtures, occurring in a range of matrices, and thus necessitate the use of techniques to separate the individual components and extract the compounds of biological interest.
    • Sex differences in scent-marking in captive red-ruffed lemurs

      Janda, Ellese D.; Perry, Kate L.; Hankinson, Emma; Walker, David; Vaglio, Stefano (Wiley, 2019-01-21)
      Primate chemical communication remains underappreciated, as primates are considered to rely on other sensory modalities. However, various lines of evidence suggest that olfaction plays an important role in primate societies, including the conspicuous scent-marking behavior of many strepsirrhines and callitrichines. Although lemurs typically show scent-marking, little is known about this behavior in red-ruffed lemurs (Varecia variegata rubra). We combined behavioral observations and semiochemistry analyses to improve our understanding of scent-marking in two captive troops housed at Dudley and Twycross zoos(UK). We collected olfactory behavioral observations by focusing on two family troops (N=7) for 132hr. We investigated the volatile compounds of ano-genital scent-marks using solid-phase microextraction and gas chromatography-mass spectrometry and compared volatile chemical profiles with features of the signaller. Males scent-marked most frequently and predominantly in specific meaningful areas of the enclosure, while within females the occurrence of scent-marking was related to their age. We found behavioral sexual dimorphism, with male predominantly depositing secretions via neck and mandible glands and females via ano-genital glands. We identified a total of 32 volatile components of ano-genital gland secretion, including compounds that have already been found in other mammals as sex pheromones and cues to fitness, in ano-genital scent-marks spontaneously left on filter paper by adult females. Our findings suggest that red-ruffed lemurs might use scent-marking to convey information about sex and female age, with male neck marking behavior playing defensive territorial functions and ano-genital marking related to socio-sexual communication.
    • Sternal Gland Scent-Marking Signals Sex, Age, Rank, and Group Identity in Captive Mandrills.

      Vaglio, Stefano; Minicozzi, Pamela; Romoli, Riccardo; Boscaro, Francesca; Pieraccini, Giuseppe; Moneti, Gloriano; Moggi-Cecchi, Jacopo (Oxford University Press, 2016-02)
      Mandrills are one of the few Old World primates to show scent-marking. We combined ethological and chemical approaches to improve our understanding of this behavior in 3 zoo-managed groups. We observed the olfactory behavior performed by adults and adolescents (N = 39) for 775h. We investigated the volatile components of sternal scent-marks using gas chromatography-mass spectrometry and compared volatile profiles with traits of the signaler. Males marked more than females and within each sex the frequency of scent-marking was related to age and dominance status, but alpha males scent-marked most frequently and particularly in specific areas at the enclosure boundaries. We identified a total of 77 volatile components of sternal gland secretion, including compounds functioning as male sex pheromones in other mammals, in scent-marks spontaneously released on filter paper by 27 male and 18 female mandrills. We confirmed our previous findings that chemical profiles contain information including sex, male age and rank, and we also found that odor may encode information about group membership in mandrills. Our results support the hypotheses that scent-marking signals the status of the dominant male as well as playing territorial functions but also suggest that it is part of sociosexual communication.