PSGB Winter Meeting 1999

1^st December 1999

Mating & Social Systems of Old world Monkeys

Venue: Meeting Rooms of the Zoological Society of London, Regent's Park, London NW1 4RY.

The meeting rooms are on opposite side of the Road to the Main Zoo entrance - the map on the London Zoo web page (http://www.weboflife.co.uk) shows how to get there - the meeting rooms are opposite the Bus Stop marked 'London Pride Bus Stop' on this map.

Programme

9:30-9:50 Registration

10:00 Introduction

10:10 Robin Dunbar (University of Liverpool)

The number of males in primate groups

10:30 Caroline Ross & Mairi Macleod (Roehampton Institute London)

Copulatory behaviour in Old World monkeys: a comparative study

10:50 Coffee

11:20 Mairi Macleod (Roehampton Institute London)

Male-female association in samango monkeys

11:40 Anne Carlson and Lynne A. Isbell (University of Wisconsin)

Variation in the mating patterns of patas monkeys.

12:05 PSGB awards

12:25 AGM & lunch

2:30 Joanna Setchell & Alan Dixson (University of Cambridge)

What is the Mating System of the Mandrill?

2:50 Kate Abernethy

The secret life of the Mandrill: new data, new interpretations and a novel social system for Primates

3:10 Dave Hill (University of Sussex)

Female preference, male mobility and troop membership among Japanese macaques - Why stay when you can play away?

3:30 Tea

4:00 Volker Sommer (UCL)

Holy but Selfish, the Socioecology of Indian Langurs

4:20 Ronald Noe (Université Louis-Pasteur & Max-Planck-Institut für Verhaltensphysiologie)

Dispersal patterns of three West-African Colobus species

4:40 Poster session

Registration fees

Non-members £10; Society Members and non-Society Student members £5; Students £3

For more information please contact:

Dr. Caroline Ross or Mairi Macleod
School of Life Sciences
Roehampton Institute London
West Hill
London SW15 3SN
UK.

email: c.ross@roehampton.ac.uk or m.macleod@roehampton.ac.uk.

ABSTRACTS FOR ORAL PRESENTATIONS

The secret life of the Mandrill: new data, new interpretations and a novel social system for primates

Kate Abernethy (1) and Lee J.T. White (2).

(1) Station d'Etudes des Gorilles et Chimpanzés, CIRMF, BP 769, Franceville, Gabon and Dept. of Biological and Molecular Sciences, University of Stirling, Stirling FK9 4LA, Scotland.

(2) Wildlife Conservation Society, Bronx, New York, 10469-1099, U.S.A.

Until recently the Mandrillus species were classified with the baboons, and the scant data available on Mandrill and Drill sociobiology was interpreted using models built on studies of Papio and Theropithecus. During the last 5 years genetic, morphological and ecological studies of mandrills have shown that these classifications and interpretations were largely incorrect. A very different picture of mandrill sociobiology is now emerging, showing a novel social system amongst the rainforest primates. In this paper we present new data on group sizes and compositions for wild mandrill hordes in the Lopé Reserve, Gabon. Mean horde size over the 3-year study was 620 (range 338-845) and hordes remained cohesive throughout the year. Mature males are not resident members of these hordes, but spend most of the year as solitary individuals. Males join the hordes seasonally, in response to the onset of oestrus in females. The number of males in a horde at any given time is unrelated to group size, but best explained by the number of oestrus females present. The implications of this data for models of mandrill evolution in the rainforest habitat are discussed.

Variation in the mating patterns of patas monkeys.

Anne A. Carlson (1) and Lynne A. Isbell (2).

(1) Department of Zoology, University of Wisconsin , Madison, Madison, Wisconsin, USA. E-mail: acarlson@students.wisc.edu.

(2) Department of Anthropology, UCAL, Davis, California, USA.

We studied the mating patterns of 23 female and 11 male patas monkeys during three breeding seasons in Laikipia, Kenya. We observed multi-male mating during the 1995 conceptive season, and single-male mating during 1997 and 1998. Seven different males were associated with the group in 1995, compared with two in 1997 and three in 1998. Intrasexual competition, measured by rates and patterns of wounding, mating harassment and mate-guarding, was always moderate for males; female intrasexual competition, while low at all times, was slightly more intrense during single-male mating. Adult males harassed 19% of all copulations during the multi-male influx, while adult females harassed 15% and 3% of all copulations only during years with single-male mating. When we were able to determine who initiated the copulation, males were significantly more likely to initiate copulations during the multi-male influx compared with single-male breeding seasons. Forced copulation and infanticide were not observed in all three years for which we have data. Our results highlight the dramatically different behaviour patterns observed among species inhabiting similar ecological niches (olive baboons, vervet and patas monkeys). Instead, the mating systems of patas monkeys resemble those of forest guenons, suggesting strong correlations with phylogeny.

Baboons: more social anxiety

Castles, D. L. (1), Aureli, F. (2) and Whiten, A. (3).

(1) Department of Cognitive & Behavioural Science, The University of Tokyo & School of Life Sciences, Roehampton Institute London.

(2) School of Biological & Earth Sciences, Liverpool John Moores University.

(3) School of Psychology, University of St Andrews.

Self-directed behaviour (SDB) can be used as a behavioural indicator of stress and anxiety in non-human primates. It is also a potential index of relationship quality. We have previously demonstrated that when the animal nearest to a female olive baboon, Papio anubis, was a dominant individual, SDB rates (a combined measure of scratching, self-grooming, self-touching, yawning and body-shaking) increased by 40% over those when the nearest neighbour was a subordinate (Castles et al, Animal Behaviour, in press). There was, however, considerable variation among individual females in SDB response according to the identity of the dominant nearest neighbour that could not be completely explained by relative dominance status. Here we develop the link between SDB and relationship quality by exploring associations between SDB rate, friendships and affiliation rate in this population.

The number of males in primate groups.

Robin Dunbar

School of Biological Sciences, Nicholson Building, University of Liverpool, Liverpool L69 3BX, UK. e-mail: rimd@liverpool.ac.uk.

Primate groups differ considerably in the number of males they contain both within species and between species. So far, there has been no general explanation as to what determines the number of males in groups (though they have been a number of suggestions that relate to why species mating systems should differ), and the question has been subject to a great deal of debate. I present a general model that relates the number of males in primate groups to male mate searching decisions: males join groups when they are more likely to gain access to females than if they adopt a roving male strategy. This model explains both inter- and intra-specific variation in the number of males in groups in the Great Ape clade (including humans). An important component of a male's decision here is likely to be the number of co-cycling females (females who are in oestrus on the same day). I will show that the number of co-cycling females is the main determinant of the number of males in a group across a wide range of Anthropoid primates.

Female preference, male mobility and troop membership among Japanese macaques - Why stay when you can play away?

David A. Hill

School of Biological Sciences, University of Sussex, Falmer, Brighton, BN1 9QG. E-mail: D.A.Hill@sussex.ac.uk

Japanese macaques (Macaca fuscata) live in troops consisting of a central core of kin-related females and their offspring, and multiple immigrant adult males. Males are relatively transient members, staying with a troop for only 3 to 4 years on average before leaving to join another. If a male's primary concern was to maintain access to as many oestrous females as possible, then males in troops with relatively many females per male should stay put, but there is little evidence of this happening. In addition to inter-troop transfers, males may also leave their troops temporarily during the mating season to mate with females of other troops (Sprague, 1992). This paper reviews data from various studies of mating behaviour of Japanese macaques in an attempt to explain these patterns of male residence and mobility.

Visitor males are clearly attractive to females, even when they are young and subordinate, and novelty appears to be a major component of sexual attractiveness of males to females. Female preference for novel males may be the proximate mechanism driving male inter-troop mobility. When a male first joins a troop he is a novel mating partner for all resident females. As he becomes more familiar, females may be less eager to mate with him, causing him to seek additional mating opportunities by visiting other troops. When mating within his own troop becomes sufficiently infrequent, the male may decide to change troops. This model fails to explain why all males in the Yakushima population live in troops, and none follows an alternative strategy of living alone and mating solely as a novel visitor. It may be that benefits of group-living for males, other than access to oestrous females, are sufficiently great to outweigh the costs.

Male-female association in samango monkeys

Mairi Macleod

School of Life Sciences, Roehampton Institute London, West Hill, London SW15 3SN.

In forest guenons, a uni-male troop structure is the norm. However, in some guenon taxa multi-male influxes have been observed to occur during some mating seasons in some troops. This paper examines the factors affecting the occurrence of these influxes during a two year study of three troops of samango monkeys (Cercopithecus mitis erythrarchus) at Cape Vidal, South Africa. The data suggest that the number of males entering troops was not contingent upon the number of females in the groups, nor the number of fertile females, but did appear to be related to the number of proceptive females, particularly where proceptive behaviour was directed at males outside the troop. Such proceptive behaviour was not correlated with fertility, raising the possibility that females may have been sexually soliciting males in order to manipulate male behaviour and male residency in their troops. The question of why females should behave in a way which attracts new males into their troops is discussed. It has previously been postulated that multi-male influxes serve as an infanticide avoidance mechanism in guenons. Data presented here support this hypothesis; male takeovers of troops which occurred without a multi-male influx were followed by infanticidal behaviour, while the takeover occurring during a multi-male influx was not. Observations suggest that one reason for an adult male to remain in a samango troop outside of the mating season, may be to protect infants he has sired from infanticidal attack by other males.

Dispersal patterns of three West-African Colobus species

Ronald Noë

Laboratoire d'Éthologie et Neurobiologie, Université Louis-Pasteur, Strasbourg, France and Max-Planck-Institut für Verhaltensphysiologie, Seewiesen, Germany

The three Colobus species of the Taï National Park in Ivory Coast have radically different social organisations and dispersal patterns. Western black & white colobus (Colobus polykomos) live in harem groups of around 15 individuals, among which one to three adult males. Migration of both sexes occurs, but is probably male biased. The western red colobus (Colobus (Procolobus) badius) live in large groups of 50 &emdash; 75 with many adult males. Females migrate and males are philopatric, although exceptions were observed too. The third species, the olive colobus (Colobus (Procolobus) verus), has a rather fluid social organisation in which small groups of around ten individuals form and dissolve at a regular rate. These characteristics are closely linked not only to the feeding ecology, but especially to the anti-predation defence system of each species. In black & white colobus the group-level alliance of related females defends crucial resources within their large home range against neighbouring groups with which they share extensive areas. The groups have a relatively efficient foraging mode and protect themselves mainly by a cryptic life-style. Female red colobus seem to be attracted to the male alliance that defends the best territory. This territory not only contains food resources, but also a group of diana monkeys. The exclusive access to a diana group is a crucial element in the anti-predation defence of the red colobus. Red colobus frequently mix with diana monkeys in order to profit from their extraordinary skills as sentinels. The olive colobus, finally, heavily depend on the diana monkeys for their defence. Their bodies as well as groups are small, which can either be explained as a price paid for inefficient foraging due to the association with a different species, or as an adaptation that combines well with their extremely cryptic behaviour. Due to the small size of the groups chance demographic events have a large impact, which explains the frequent changes in group composition. We have the impression that males, alone or in alliance, attempt to defend the diana group, a resource important to females, against conspecific males.

Copulatory behaviour in Old World monkeys: a comparative study

Caroline Ross & Mairi Macleod

School of Life Sciences, Roehampton Institute London, West Hill, London SW15 3SN, UK e-mail c.ross@roehampton.ac.uk

Three basic copulatory patterns are observed in male Old World monkeys. The two most commonly reported patterns are a single mounts with brief intromission or multiple brief intromissions. One species (Macaca arctoides) shows the single mounting pattern but may also exhibit a genital lock and has a prolonged intromission. Species with single brief intromissions can be described as having simple copulatory patterns whereas those with multiple intromissions and prolonged intromissions have a more complex copulatory pattern. Assuming that simple mounting patterns are ancestral to the haplorhine primates, complex copulatory patterns have evolved at least four times in the Old World monkeys, within the macaques, baboons, guenons and colobines. In the macaque group there is also evidence that simple mounting patterns have evolved secondarily from complex mating patterns. Shively et al (1982) suggest that, in macaques, species which show multiple mounting have higher levels of male-male competition than species with single mounting patterns. Thus multiple mountings may have evolved as a form of mate defence. An alternative hypothesis suggested here is that complex copulation patterns function as a male display of fitness. If males that are able to show complex copulation patterns are preferred by females, such behaviour could evolve without having other direct benefits to males. In this paper we use comparative analyses to investigate the relationship between copulatory patterns, male competition and female choice in Old World monkeys in particular, and in haplorhine primates generally. Copulatory patterns were classified in a number of ways, single vs. multiple mounting, simple versus complex copulation pattern and intromission time. Male competition was measured by social system (multi-male or uni-male), relative testes size and sexual dimorphism. Despite the predictions of previous studies we could find no correlates between any measure of copulatory behaviour and any measure of social or mating system. If female choice does influence male copulatory patterns we would predict that complex copulatory patterns would be found in species with high levels of female choice. However no clear relationship between female choice and copulatory pattern could be found. Hence it appears that copulatory pattern in primates is not easily explained by social structure or mating system of the species concerned.

Reference: Shiveley, C; Clarke, S; King, N, Schapiro, S & Mitchell, G (1982) Patterns of sexual behaviour in male macaques. Am J. Primatol. 2 373-384.

Holy but Selfish: The Socio-ecology of Indian Langur Monkeys.

Volker Sommer

Department of Anthropology, University College London, Gower Street, London WC1E 6BT, UK.

The social organisation of langur monkeys (Presbytis entellus) varies across the Indian subcontinent. Adult males at some sites monopolise females whereas multi-male-multi-female troops develop elsewhere and all-male-bands are not found.

At Jodhpur / Rajasthan, about 1800 langurs live in a strictly harem-structured population. Local people provision the monkeys whom they consider sacred. A long-term study, pioneered by S. M. Mohnot and now in its fourth decade, revealed mechanisms which foster harem structures. (a) Provisioning reduces harem holders' foraging time and improves their physical fitness. Bands are rarely provisioned since they move over vast areas, often encountering food and water scarcity. (b) The large band ranges are also associated with high mortality because of accidents and predation. Thus, cohorts of (half-) brothers emigrating from natal troops thin out quickly. This limits cooperation within bands, especially possibilities for brothers to jointly oust harem holders. (c) Provisioning allows year-round breeding. Consequently, females are spatially clumped but fertility is temporally dispersed. Harem holders can thus effectively guard the one or two troop females which ovulate on any given day. In addition, furtive matings are made difficult by the open arid environment. (f) High paternity certainty results in frequent infanticide by immigrant males. Females could synchronise cycles which would bring about multi-male troops and reduce infant-killing. However, cycles are desynchronised, probably because food competition from co-resident males would lengthen birth intervals.

Multi-male organisation in other populations is predicted to be associated with (a) pronounced seasonal peaks of food availability which lead to seasonal reproduction and thus temporal clumping of fertile females; (b) reduced male mortality which lowers competition amongst interrelated rivals.

Abstracts for poster presentations

Female social relationships in hamadryas baboons (Papio hamadryas hamadryas).

Deleu, R.(1); Leinfelder, I.0; Zinner, D.(2) & Nelissen M.(1)

(1) University of Antwerp (RUCA), Behavioural Biology, Groenenborgerlaan 181, B-2020 Antwerpen, Belgium

(2) German Primate Center (DPZ), Ethology and Ecology, Kellnerweg 4, D-37077 Gottingen, Germany

Different models have been developed to explain the evolution of female social relationships in non-human primates. According to the ecological model, predation risk forces females of most diurnal primates to live in groups and the type of competition for food (and safety) within and between groups determines female social relationships. Recently, an evaluation of this model revealed two other factors (habitat saturation and infanticide avoidance) that can explain some features of female social relationships, leading to a socioecological model. Hamadryas baboons live in multilevel societies of which the One-Male Unit is the smallest stable entity. Field studies on these baboons have focused on male-male and male-female social relationships because females are the dispersing sex. As a consequence data on female social relationships in hamadryas baboons are scarce. In this presentation, literature from field and captive studies is reviewed on what is known about female social relationships for this species. In addition, a preliminary attempt is made to evaluate the socioecological model for hamadryas baboons.

The reproductive physiology of the black-handed spider monkey (Ateles geoffroyi).

Leonor Hernández-López and Ricardo Mondragón-Ceballos.

Instituto Mexicano de Psiquiatría, Departamento de Etología, México, D.F., México.

Despite how much is known about Atelines ecology, their behaviour and physiology has seldom been studied. The present work describes some of the basic female and male reproductive physiology features of the black-handed spider monkey. Concerning females, both vaginal cytology and endocrine (estradiol and progesterone) profiles show that this species has a menstrual cycle of around 24 days in average. The four distinctive phase of the menstrual cycle (menses, follicular, periovulatory and luteal) were identified by vaginal swaps. Endocrine profiles showed two estradiol peaks, one occurring at the mid-cycle (periovulatory) and the other one at the mid-luteal phase. Progesterone values increased following the periovulatory estradiol peak, kept high throughout the remaining periovulatory phase and the first two-thirds of the luteal, decreasing sharply during the late luteal phase. Males' ejaculation parameters were determined from electro-ejaculates. The mean ejaculate volume was 1.9 ml, being larger than in most non-human primates, consisting of a solid and a liquid phase. Mean number of spermatozoids per ml was around 52 millions. These figure being lower than those reported for even smaller primates. Whether this is an artefact due to the procedure or might be related to the mating system of the black-handed spider monkey needs to be elucidated. Concerning the semen viability obtained by this procedure, it yielded satisfactory results. As much as 80% of the spermatozoids were recovered live, 58% of them showing linear motility. Finally, abnormal spermatozoids were no more that 30%, a value that has been consistently reported in other primate species. Although primarily descriptive, these results might be of interest to researchers working in physiology, socioecology or assisted reproduction.

The effects of contraceptive implantation and a reduction in number on the behaviour of a captive troop of Hamadryas baboons

Neil Jordan

Paignton Zoo Environmental Park, Totnes Road, Paignton, Devon, TQ4 7EU School of Biological Sciences, The University of Manchester, Oxford Road, Manchester

In January 1999, due to rapid population growth and overcrowding of their enclosure, the baboon troop at Paignton Zoo was reduced in overall number from 82 to 62 and all adult females were implanted with a contraceptive. The effects of this management procedure on the baboons' behaviour has been evaluated. There has been a significant decrease in displacement behaviours performed by adults of both sexes suggesting that the reduction in numbers has reduced social stress levels in the troop. Time budgets have also been altered significantly, the percentage of time that the baboons are engaged in grooming activities having decreased. Time spent immobile has increased, possibly due to the direct hormonal effects of the contraceptive combined with seasonally affected sunbathing behaviour. Agonistic and sexual interactions however have not been affected significantly. Although five babies have been born since January, knowledge of the gestation period suggests that only one was conceived post-implantation. This suggests that the implants have been effective. Further observations are continuing to evaluate the longer term consequences for troop social behaviour of a reduced birth rate and more females coming into oestrus more often.

Reconciliation occurs faster between kin than between non-kin in stumptail macaques.

Ricardo Mondragón-Ceballos and Alejandra Bautista.

Instituto Mexicano de Psiquiatría, Departamento de Etología, México, D.F., México. 

It has been repeatedly reported in a number of Cercopithecine species that reconciliation between kin is significantly higher than between non-kin. Being (hypothetically) kin relationships inherently secure, it was thought that they do not require high rates of explicit resolution of conflicts. Nonetheless, data do not support the above statement, but in fact contradict it. Although this conciliatory tendency is correlated with other factors such as dominance style or relationship value, to date no satisfying proximal or ultimate explanation has been given. Simultaneously, it has been found that post-conflict anxiety is higher when the relationships are praised (by the animals) as more valuable; and, on the other hand, it is long-known that high levels of anxiety are elicited whenever kin relationships are put in jeopardy (such as mother-infant separation). Thus, in order to test if anxiety mediates conciliatory tendencies between kin, we assessed if reconciliation occurred more readily between kin (i.e., mothers and offspring, siblings) than between non-kin in a captive group of stumptail macaques. The rationale behind this idea was that proneness to reconcile would be related to levels of post-conflict anxiety: as more anxiety was elicited reconciliation would occur more quickly. Our results show that reconciliation latency between kin is shorter than between non-kin, and seemingly (as assessed by rates of post-conflict scratching and self-grooming) between kin conflicts elicit much more anxiety. Thus, reconciliation is not only more frequent among kin, but also occurs faster. Yet, the inherently secure relationship between relatives could account for this last finding close kin being more confident of one another, and so being less fearful of approaching each other soon after conflict ended.