CAPTIVE BRED LEMUR BEHAVIOUR AND ENDOCRINOLOGY

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1 CAPTIVE BRED LEMUR BEHAVIOUR AND ENDOCRINOLOGY Ursich Elisa 1, Pier Giovanni Bracchi², Bianco Federico³ Introduction Lemurs are classified as primates (prosimii) and they only exist on the island of Madagascar (two species can also be found on the nearby islands of Comore) and their existence is threatened even there, in fact many species have already completely disappeared. (Tattersall, 1993). Madagascar is situated in the Indian Ocean, between the islands of Mauritius and the Reùnion in the East, the Comore and the Seyshelles in the north and the African Continent in the west, from which it is separated by the Mozambique Channel. The reason why lemurs can be found only in Madagascar is that this island was separated from Africa 180 million years ago, carrying a sample of the African flora and fauna and its subsequent isolation permitted the existence of unique animal and vegetal species that became extinct in the rest of the world. Madagascar in fact is third classified in the world list of countries with higher primate diversity and its 32 species and 50 tassonomical categories are completely endemic. (Tattersall, 1993). Lemurs have a very high morphological variability: the smallest weighs 30 grams and measures 12 cm, the biggest can weigh more than seven kilos. They spend most of the time on trees, they can be diurnal or nocturnal and they usually feed on leaves, fruit and flowers (rarely on small insects). Most lemurs have a long furry tail they use to balance body weight and to communicate and which is not prehensile like higher primates. (Durrell, 1992). Red Ruffed Lemurs (Varecia Variegata Rubra) weigh between three and four kilos (females more than males), their tail measures 60 cm and their body 53 cm. (Stevens, 1993). Their coat is red with a white patch behind the neck, and limbs, tail, belly and face are black. ( To compensate the lack of manual manipulation they use their teeth for grooming: the six incisors of the lower jaw lean slightly forward and are separated from each other, forming a kind of comb. Also the second hind foot toenail is specialised for grooming in fact it is flat. ( org/educate/facts_sheets/r_lemur.htm). 1 Veterinarian, internship in the Equine Clinic Aznalcollar, Sevilla,Spain,elisaursich@hotmail.com ² Department of Animal Production, Vet. Biotechnology and Food Security and Quality Science, Veterinary Science Faculty, Parma University ³ Veterinarian, Doctorate in Domestic Animal Endocrinology. 193

2 Biology Reproductive season: end of dry season (form May to July) in order to give birth at the beginning of the wet season when there is more food (September- October). (Doyle et al., 1979). Gestation lasts days, females reach sexual maturity at the age of two but the first pregnancy occurs when they are three years old. Oestrus cycle lasts 30 days and oestrus lasts 3-6 days. Lemurs are the only case among primates that can have more than one born in the same litter. Red Ruffed Lemurs have three pairs of mammals so their litter size can reach the number of six, but the average is three. Twins are quite common. Age at independence: 135 days. ( Longevity: years in the wild, 19 years in captivity. Habitat and distribution: Red Ruffed Lemurs can be found only in the tropical forests of Masoala Peninsula (Northeast Madagascar). Fig.1: two lemurs playing in the outside part of the enclosure 194

3 Fig.2: sunbathe, groom and and passive rest on branches Behaviour: among all lemurs, Red Ruffed Lemurs are the ones that spend more time on trees. They are crepuscular, being more active at early morning and at late afternoon. A great degree of sociality has been observed among lemurs: Red Ruffed Lemurs live in groups of 2-5 individuals but they can reach the number of 16 depending on the season (in the dry season there is shortage of food, so groups are smaller). Grooming plays a role in strengthening the relationships between individuals. Males are often monogamous, females are dominant, being this the only case of female dominance among primates. ( html). Communication: among the prosimii the sense of smell, of hearing and of seeing have more or less the same importance. But the presence of many skin glands in the Red Ruffed Lemurs (which are used to mark the territory) indicates the great importance of the sense of smell in the communication among lemurs. Also vocalisation is an important strategy in the communication among lemurs: they have a very complex alarm system to warn each other if threatened by a predator. At the Duke Primate Centre there have been identified 12 different kinds of calls (they vary if the predator is on the ground or in the air) that are also used to co-ordinate group activities. (Doyle et al. 1997). Population status: there is very little information about the geographical distribution and even less about the exact number of the population of Red Ruffed Lemurs actually living (since this species is not among the most studied ones) but the most recent estimations talk about individuals. ( Conservation Since man arrived on the Island of Madagascar (less than 2000 years ago) 8 genera and 15 species of lemurs have already become extinct and the actual 195

4 predictions claim that many other species could disappear in the next decades if some serious solutions should not be applied. Of the 50 tassonomical categories of lemurs actually living in Madagascar 10 are seriously endangered, 7 are endangered, 19 are threatened and 14 are slightly threatened. Lemurs are facing a very serious threaten: the 2000 red list of the IUCN classifies them as seriously endangered and among them Varecia Variegata Rubra is one of the most threatened in fact it is classified in the Appendix I of CITES list (Convention on the International trade in Endangered Species) and in class A of the 1969 African Convention. ( Main threats There are many factors that threaten lemursʼexistence, but the main ones are three: habitat destruction, hunting for food or for other reasons and live capture. Usually, the most serious threaten is forest destruction, and the same can be said for all primates in general. (Tattersall, 1993). In fact it has been estimated that that 80% of Madagascar forests have been exploited by man for the production of mines, for the animals, to cultivate the land, and for the production of wood, and that proceeding with these rhythms could cause the destruction of all Madagascar forests within ten or twenty years. Aim of the project The aim of my project was to evaluate the behavioural quality of a group of Red Ruffed Lemurs and establish whether the enclosure was appropriate or if more enrichment behaviour was needed. (Kerridge, 1996). To evaluate if the subjects were living in a condition of well being or of sufferance (stress, stereotyped movements) (Mason, 1991) I carried out both a behavioural observation (considering the differences with the in-situ behaviour recorded in literature) and an endocrinological study by measuring the level of cortisol faeces. (Cavigelli, 1999). The aim of this kind of research is to improve the quality of life of captive bred animals by increasing enrichment behaviour devices and by making the animals live in conditions as much similar as possible to their natural environmental conditions. (Ladewig, 2000). Materials and methods The collection of all the data available on the subjects I studied was the first thing I did, then followed one day of pilot study that was necessary to draw the enclosure and decide how to split it up in zones to consider. The aim of the pilot study was also a general observation to pick up the behaviours to consider and the sampling method to use and to evaluate the method and timing of the collection of faeces samples. (Whitten et al., 1998). 196

5 The specimens studied was a family of Red Ruffed Lemurs composed of: dominant male, Bruno, born the dominant female, Tana, born the the dominant male and female gave birth to: two males and one female the one male the After studying and dividing the enclosure into five microhabitats, I selected the most important behaviours that were displayed and I decided which sampling method to use: (Martin et al., 1986). ad libitum sampling one-zero 8.30a.m p.m. 4 minutes intervals total observation time: 80 h. Faeces sampling: group faeces samples were collected daily during the 16 days of observation (it was not possible to identify the provenience of each sample for management reasons), immediately frozen at -20 C and eventually analysed with immuno-enzimatic analysis (EIA kit) to measure the level of cortisol metabolites (11-18 desossicortcosterolo). (Sapolsky, 1982). Discussion The data collected was transformed into graphs to find out a pattern of the different behaviours throughout the day. An important role in the behaviour is played by the enclosure and I carefully studied the way the lemurs used it. (Fig.1-2). It is necessary to deal separately with the dominant male and the rest of the family since the status of the two was very different: most lemurs showed a satisfactory use of the enclosure and a good interest in all the enrichment behaviour strategies carried out during my observation. The behaviour of most lemurs was very good because similar, in most cases, to the behaviour displayed by lemurs in nature, which is a very important aspect in the reintroduction of captive-bred animals in the wild. I identified all the typical behaviours of the species such as grooming, leaping and jumping on branches, vocalising, marking the territory with their skin glands etc. It was also positive to observe the maintenance of their crepuscular nature: as it occurs in nature, lemurs were more active at early morning and late afternoonevening. And it was also very important to verify that lemurs spent most of the time on branches: Red Ruffed Lemurs are arboreal animals and if reintroduced in the wild they would become more vulnerable if spending too much time on the ground. (Cook et al., 2000). But all these considerations are not true for the dominant male Bruno. The 197

6 use of the enclosure was different between him and the rest of the family, which spent a lot of time in the open part of the enclosure, while Bruno isolated himself from the rest of the group sitting in the inside part of the enclosure. He also showed to be highly disturbed by the presence of the public, jumping up against the glass every time a person approached the enclosure, which happened continuously throughout the day. The characteristics of this behaviour respond to the ones described in the compulsive-obsessive behaviour typical of highly stressed and bored captive-bred animals (Mendoza et al., 2000). The results emerged from the faeces analysis show that there are not any significant modifications from the basal cortisol level, which corresponds to a satisfactory behavioural situation for all the subjects of the group except one. (Khan et al., 2002). Conclusion The behaviour of all lemurs except one appeared satisfactory from all the points of view taken in consideration (being similar, for most of the time, to the wild lemurs). The observations I carried out made me draw the conclusion that, since most subjects did not show abnormal behaviours or signs of stress, the enclosure seems well structured and those lemurs have well adapted to it. Most animals responded positively also to the enrichment behaviour strategies that were carried out during my study. (Sapolsky, 1990). But all these conclusions are not valid for the dominant male, Bruno, which often displayed stereotyped movements and often isolated himself from the rest of the group. Also his physical condition was not good (low body condition score, dehydrated fur) but being in a very advanced age (15 years), these problems could be considered as part of the normal ageing process. Medical analysis would be necessary to discover if his bad conditions are caused by physical or other problems, but carrying out medical analysis on a stressed animal would cause an aggravation of his condition, so they are avoided as much as possible in zoos. (Dobson et al., 2000). Anyway, considering the history of the animal and considering that stereotyped behaviours are not likely to be caused by physical pathologies, the most likely hypothesis is that his sufferance has been caused by the recent separation between him and the dominant female because of her post-partum metritis. It should also be considered that these abnormal behaviours were absent before the separation and that Red Ruffed Lemurs are highly sociable animals. Faeces hormonal analysis is a relatively new method that has many advantages compared to the traditional invasive ones (blood sample) but it still has to face many technical obstacles that complicate cortisol level interpretation. This particular study was also limited by the fact that it was not possible to identify the provenance of each faeces sample. Moreover, the lack of this kind of studies on Red Ruffed Lemurs does not permit us to compare the results obtained with normal cortisol level values. (Hau et al., 2001). But for the same reason, the results emerged form my study can be useful not 198

7 only to complete the studies that were planned at Marwell Zoological Park, but also to give consistence to the data bank of this possible new method of animal welfare evaluation with the use of faeces cortisol levels. Use of the enclosure Time percentage spent in different behaviours Key words: lemurs, animal welfare Parole chiave: lemuri, benessere animale Palabras clave: lemures, bienestar animal 199

8 RIASSUNTO: i lemuri sono delle singolari proscimmie che esistono su unʼunica isola al mondo, il Madagascar, ed anche lì la loro esistenza è seriamente minacciata: dallʼarrivo dellʼuomo sullʼisola (meno di 2000 anni fa), 8 generi e 15 specie di lemuri sono già definitivamente scomparsi. (Tattersall, 1993). Lo scopo del mio studio è quello di stabilire, in base ad uno studio sul comportamento di un gruppo di Red Ruffed Lemurs allevati presso il Marwell Zoological Park (e con il supporto del dosaggio ormonale delle feci dei lemuri) se la tecnica di allevamento si adattasse bene alle esigenze di questo animale o se fosse necessario incrementare la qualità di vita dei soggetti. Lo studio ha dimostrato unʼampia variabilità comportamentale ed un soddisfacente utilizzo del recinto per quanto riguarda tutti i componenti del gruppo ad eccezione del maschio dominante, che ha invece dimostrato evidenti segni di stress (comportamenti stereotipati) e di malessere anche fisico (pelliccia arruffata e body condition score non ottimale ). Per risalire alla causa di questo malessere sarebbe necessario effettuare delle indagini di tipo medico, le quali però sono ridotte al minimo negli zoo dato che causerebbero un aggravamento dello stato di stress del soggetto. (Matteri et al., 2000). SUMMARY: lemurs are a very original kind of primate that can be found only on the Island of Madagascar. Their existence is facing a very serious threat, in fact 8 genera and 15 species have already become extinct since the arrival of man on the Island of Madagascar, less that 2000 years ago. (Tattersall, 1993). The aim of this project is to investigate the behaviour of a family of captivebred Red Ruffed Lemurs and to measure the cortisol level of their faeces to evaluate the quality of the husbandry (enclosure, pattern of behaviour, similarity to the in-situ behaviour) and evaluate if the subjects were living in a condition of well-being or if they were facing any sufferance. (Schapiro et al., 1993). The study was carried out at Marwell Zoological Park (England) on a family of six Red Ruffed Lemurs. The enclosure was split up in five microhabitats and the most significant behavioural categories to observe were picked up. I used onezero intervals of four minutes with ad libitum observation from 8.30 a.m. to p.m. reaching a total of 80 hours. The results obtained were satisfactory regarding the behaviour of all the subjects except the dominant male that showed physical sufferance and stereotyped behaviours. (Cooper et al., 2000). Bibliography AA.VV Red Ruffed Lemurs. Sito a cura del Duke Universty Primate Center. AA.VV Red Ruffed Lemurs. Http.// AA.VV Red Ruffed Lemurs. Http.// AA.VV Red Ruffed Lemurs. Http.//wwwsfzoo.org/cgi_bin/animals.py. 200

9 AA.VV Red Ruffed Lemurs. Http.// Cavigelli S.A Behavioural patterns associated with faecal cortisol levels in free ranging female ring-tailed lemurs, lemur catta. Animal Behaviour. 57: Cook C.J., Mellor D.J., Harris P.J., Ingram J.R., Matthews L.R., Handson and hands off measurement of stress. In: the Biology of Animal Stress: Basic Principles and Implcations for Animal Welfare, 2000, Eds: Moberg G.P., Mench J.A. CAB INTERNATIONAL, Oxon, UK, pp Cooper J.J., Mcdonald L., Mills D.S., The effect of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Applied Animal Behaviour Science 69: (1) Dobson H., Smith R.F What is stress and how does it affect reproduction? Animal Reproduction Science 60-61: Doyle G.A. and Martin R.D The study of Prosimian Behaviour. Cap. 2,4,6,7,8,9,10,11,12. Academic press, New York, San Francisco, London. Durrell G Io e i lemuri. Adelphi edizioni, SPA, Milano. Hau J., Andersson E., Carlsson H.E Development and validation of a sensitive ELISA for quantification of secretory IgA in rat saliva and faeces. Laboratory Animals 35 (4): Kerridge F.J. 1996, Behavioural enrichment of ruffed lemurs (varecia variegata) based upon a wild-captive comparison of their behaviour. Doctor of Philosophy thesis. Bolton Institute. Khan M.Z., Altmann J., Isani S.S., Yu J A matter of time: evaluating the storage of fecal samples for steroid analysis. General and Comparative Endocrinology 128 (1): Ladewig J Chronic intermittent stress: a model for the study of long term stressors. The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare, 2000, Eds: Moberg G.P., Mench J.A.CAB. INTERNATIONAL, Oxon, U.K, pp Martin P. and Bateson P Measuring Behaviour. Cambridge University Press. Cambridge. U.K. Mason G.J Stereotypes: a critical review. Animal Behavoiour 41,

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