Abstracts from the 8th Congress of the German Primate Society

PLENARY TALKS

Comparative Ape Cognition in Leipzig: The Wolfgang Köhler Primate Research Centre

Josep Call

Historically, one of the pitfalls of comparative psychology has been its narrow focus on a handful of species such as the pigeon, the rat and the rhesus macaque (Beach, 1950). The study of primate cognition, and ape cognition in particular, has fared no better in this regard. Chimpanzees alone account for approximately 70% of the studies on ape cognition, while orangutans, bonobos and gorillas account for only 11%, 10% and 8%, respectively. This knowledge vacuum regarding non-chimpanzee apes has created unfounded perceptions about the cognitive skills of chimpanzees compared to those of other great apes and has limited the scope of the hypotheses regarding the evolution of ape and human cognition. The Wolfgang Köhler Primate Research Centre is our attempt to remedy this situation. This talk will present the facilities, apes and research goals of the centre. Our research agenda can be broadly construed as the investigation of problem solving skills in physical (e.g. tool use) and social (e.g. deception) situations from a comparative and evolutionary perspective. Some examples of current ongoing research projects will highlight the importance of comparative studies in mapping the similarities and differences across ape species including humans.

An Ape Perspective on Human Uniqueness

Svante Pääbo

In defining which traits are unique and those that are shared between contemporary humans and their closest living and extinct evolutionary relatives, we may be able approach some of the genetic traits that define humans as a species. Our laboratory attempts to achieve this using several different approaches, some of which will be discussed here. In order to provide a preliminary insight into the divergence of the human and chimpanzee genomes, we have sequenced over 10,000 random DNA fragments from the chimpanzee. Alignment to corresponding human DNA sequences reveals an average genome-wide sequence difference between the two species of 1.2%. As expected, the X chromosome is the most conserved, while the Y chromosome has diverged the most. Surprisingly, the average amount of sequence difference that has accumulated on the different autosomes differs significantly. To understand better the evolutionary forces that affect human genes, we have sequenced 5,055 expressed sequence tags from the chimpanzee and compared them to their human counterparts. The comparison to intergenic DNA sequences suggests that a substantial proportion of silent sites in protein-coding regions are deleterious and subject to negative selection. Furthermore, an excess of divergence relative to diversity in 5'UTRs suggests that positive selection has affected the 5'UTRs of genes since the divergence of humans and chimpanzees. We study the relative levels of expression of genes in six regions of the brains of humans, chimpanzees and orangutans. About 15% of all genes have changed their level of expression between humans and chimpanzees in at least one region of the brain. The patterns of gene expression changes will be discussed. In collaboration with S. Fisher and A. Monaco at the Wellcome Trust Centre for Human Genetics in Oxford, UK, we have studied the molecular evolution of FOXP2, a gene involved in the development of speech and language. We sequenced the cDNAs that encode the FOXP2 protein in chimpanzee, gorilla, orangutan, rhesus macaque and mouse, and compared them to the human cDNA. In addition, we investigated the intra-specific variation of the FOXP2 gene in humans. The results strongly suggest that FOXP2 has been the target of selection during recent human evolution.

Multi-host Pathogens and the Future of the Wild

Craig Packer

In most tropical countries, rural health service is sparse, while rural veterinary service is practically unknown. Thus the potential for frequent, virulent disease outbreaks will be expected to increase as human populations come into closer contact with wildlife. The risk to humans from wildlife disease is widely recognized (e.g. ebola, anthrax and, possibly, SARS), but less attention has been paid to the risk to wildlife from humans and their domesticated animals. In the Serengeti, for example, wild dogs were decimated by rabies and lions by canine distemper, and both diseases originated from the large populations of unvaccinated domestic dogs living around the National Park. Similar threats clearly endanger small isolated populations of wild primates that, by themselves, could never sustain deadly viruses. In my talk, I will draw parallels between the risks faced by endangered carnivores and primates worldwide, examine the dynamics of infectious disease in complex multi-host systems and describe how we are currently attempting to eradicate three dangerous viruses from the Serengeti through a large-scale vaccination programme in domestic dogs.

Traditions in White-faced Capuchin Monkeys (Cebus capucinus)

Susan Perry

Although it has long been recognized that Japanese macaques and chimpanzees exhibit traditions, it is only recently that social transmission has been generally acknowledged to play an important role in evolutionary biology. Capuchins are ideal candidates for exhibiting social learning because of their intelligence, gregariousness, tolerance of close observation during feeding, proclivity for cooperation in a variety of contexts, reliance on extractive foraging and extreme adaptability. In collaboration with 10 other researchers, I initiated a study encompassing over 20,000 hours of observations on 11 social groups of capuchins at four different study sites. We investigated behavioural variation in the domains of social conventions, food processing techniques and interactions with allospecifics. Capuchins are prone to inventing and transmitting bond-testing behaviours that involve intimate and risky physical contact and often elaborate coordination. There is also considerable within-group and between-site variation in the methods used to process foods, some of which is attributable to social influence. Although capuchins exhibit considerable cross-site uniformity in their response to allospecifics, in most cases it appears that young individuals take cues from adults in shaping their responses to potential predators and prey. Further research is underway to investigate the role of social learning in the development of those traits that have been shown to exhibit extensive behavioural variation within and between sites.

GRASP - the Last Chance for Great Ape Survival (Gorilla gorilla, Gorilla beringei, Pan troglodytes, Pan paniscus, Pongo pygmaeus, Pongo abelii).

Ian Redmond

The dawn of the new millennium does not bode well for our closest relatives in the animal kingdom - the great apes of Africa and Borneo and Sumatra. During the last four decades of the 20th century, scientists gained a greater understanding of apes than ever before. Yet during the same period, most populations of wild great apes declined dramatically. Many experts are now predicting extinction over most of their range during the next 10 to 20 years. Habitat loss, forest fires, logging, hunting for bushmeat, war and the capture of live infants for sale, have all contributed to this decline. Great apes are protected by national law in every country they inhabit, but there is a lack of enforcement capacity in most great ape range-states. Even in supposedly protected areas, poaching, illegal logging and mining all impact on vulnerable ape populations. International law is also failing to protect great apes. All non-human apes are listed on Appendix I of CITES, which bans international trade for primarily commercial purposes, but the high monetary value which some people attach to captive great apes acts as a constant lure to illegal traders and hunters. In addition, the illegal commercial bushmeat trade - a proportion of which involves great ape meat - continues largely unchecked within and between neighbouring countries in Africa. Finally, war, civil unrest and a breakdown in law and order have exacerbated the existing problems in several African countries and Indonesia. There is an urgent need for the development and implementation of a global conservation strategy for all great ape populations, within their dynamic, evolving, natural eco-systems. The GRASP (Great Ape Survival Project) initiative of UNEP and UNESCO is a response to this need. GRASP's strategy is to give cohesion to the existing work of many agencies, organisations and individuals. By means of National Great Ape Survival Plans, drawn up by governments with the collaboration of all stakeholders, it will enable the application of resources to be prioritised more effectively and identify areas that are currently neglected. The prime purpose of GRASP is to co-ordinate efforts to halt the decline in great ape populations and to increase funding to implement the actions necessary to ensure their long-term survival in their natural habitat.

Communication and the Minds of Monkeys

Robert M. Seyfarth, Dorothy L. Cheney

Research on the vocal communication of non-human primates has several goals: to test functional hypotheses about the evolution of animal signals; to examine the role of 'meaning' and information in animal societies; and to collect baseline data that must be part of any theory concerning the evolution of human language. Recent studies have also shown how field playback experiments can be used to test hypotheses not only about vocal communication per se but also about the cognitive mechanisms that underlie social interaction. Two general themes are beginning to emerge. First, despite being part of the same communicative event, signalling and receiving are in many respects fundamentally different. Producing and responding to a vocalization seem to have evolved in response to different evolutionary pressures, exhibit different patterns of development and may involve different cognitive processes. These differences in non-human primate communication recall differences between comprehension and production in human language development. Second, with the possible exception of chimpanzees, non-human primates cannot attribute mental states to others. Their inability to do so constitutes a fundamental difference between non-human primate communication and human language.

Variation in Primate Behaviour and Reproduction: Linking Reproductive Skew and Socioecological Models

Elisabeth H. M. Sterck

Primates show considerable variation in behaviour and reproductive skew, both between species and between the sexes. Variation in female behaviour and reproductive skew can be explained by the costs and benefits of grouping in combination with the distribution of limiting resources. Variation in male grouping patterns has been linked to sexual strategies, yet variation in their behaviour and reproductive success is still not well understood. In addition, callitrichid behaviour does not fit into the socio-ecological model. Here I propose that differences in life history parameters determine this variation. I will link the rate of reproduction and the distribution of resources to intra-group variation in reproductive success and discuss the consequences for social behaviour.

SUBMITTED ABSTRACTS

Olfactory Communication in Mantled Howler Monkeys (Alouatta palliata) - A Field Study

Cornelia Baltisberger, Matthias Laska, Ernesto Rodriguez Luna 

Two social groups of free-ranging mantled howler monkeys living on Agaltepec Island (Province of Veracruz, Mexico) were studied for the occurrence, temporal and individual distribution of olfactory communication. During a total of 250 hours of ad libitum sampling and 250 hours of focal animal sampling we observed nine different types of scent-marking behaviour (two of which have not been described so far for the genus Alouatta), and 12 different types of behavioural reactions to social odours (six of which have not been described so far for Alouatta). Further, we found a) significant differences in the frequency of only three of the 21 olfactory behaviours between males and females (anogenital rubbing: f > m; back rubbing: f > m; anogenital sniffing: m > f), b) that olfactory behaviour directed towards a particular conspecific occurred four times more often in the direction m ® f than vice versa, c) that juvenile animals displayed significantly less olfactory behaviour compared to adults, d) that the frequency of olfactory communication showed typical variations across days and seasons that correlated with general activity patterns and ambient temperature, and e) a complete lack of olfactory behaviour in the context of food choice. Taken together, these findings suggest that olfactory communication in mantled howler monkeys plays an essential role in the context of reproduction and possibly in social coherence.

Great Apes Performance in a Delayed Response Task: The Effect of Movement and Mental Distraction.

Jochen Barth, Josep Call

To date there are no studies that compare the abilities of all four great ape species in the domain of spatial cognition. Therefore we conducted a series of nine spatial tasks to assess individual and species differences among the great apes. On our poster we present a delayed response task. Our subjects were eight chimpanzees, four bonobos, four gorillas and six orangutans, all housed at the Wolfgang Köhler Primate Research Centre in Leipzig. In our study, the experimenter placed food under one of three cups. The subjects had to choose the correct cup after a delay of 60 seconds during which two variables were manipulated: movement and distraction. The subjects were distracted either by a shell game (mental distraction) or by receiving juice (non-mental distraction). Moreover, the apes received these treatments either at the same location where they received the memory task (no movement) or they had to move to another location in the test-unit (movement). Although the apes' performance declined with an increase in the requirements of the task, movement and distraction did not significantly interfere with the subjects' retention of the food location. Moreover, there were no significant differences between the species.

All Great Apes Can Follow Gaze to Distant Locations and Around Barriers

Juliane Bräuer, Josep Call, Michael Tomasello

The ability to follow the gaze of another individual is a social skill with adaptive benefits. This skill may allow individuals to get useful information about food, predators and group-mates. A previous study has shown that chimpanzees can follow gaze both to distant locations and around barriers (Tomasello et al 1999). However, little is known about the gaze-following skills of other great apes. The goal of this study was to investigate these skills. Subjects were 11 chimpanzees (Pan tryglodytes), four bonobos (Pan paniscus), six orangutans (Pongo pygmaeus) and six gorillas (Gorilla gorilla) that were housed in the Wolfgang-Köhler-Primate-Centre in Leipzig. In the first experiment, a human experimenter looked at the ceiling, while in the control condition she looked at the subject. Results show that individuals from all species reliably followed the gaze of humans. In a second experiment, the same subjects were presented with a series of four situations in which the human experimenter looked behind some kind of barrier. The subjects stayed longer in the places from which they could see what the experimenter was looking at than in a control condition (in which the human looked at the ceiling). These results support the idea that great apes can follow gaze both to distant locations and around barriers.

First Evidence for a Gathering Call in a Nocturnal Solitary Ranging Primate

Pia Braune, Sabine Schmidt, Elke Zimmermann

Primates which range alone during the night but sleep in stable sleeping groups during the day are expected to evolve special communication signals to coordinate their reunions. We studied the acoustic behaviour of the golden-brown mouse lemur (Microcebus ravelobensis) from Madagascar to get information on how far vocalisations play a role in reassembling. Nine sleeping groups were observed from September to October 2000 and from August to October 2001 during their dispersal in the evening (51 days) and reunion in the morning (26 days). A spectrographic analysis of the recorded calls revealed prominent differences between the two time periods. Four different call types could be discriminated. "Whistles", "tsaks" and "zips" were uttered rarely, but equally during dispersal and reunion. "Trills", however, showed a distinct difference. They were detected during almost all morning observations (24 of 26) and also in the evening, but only during the mating season. Group members called before they met close to the previous nesting site. Calling resulted in a vocal response (n=1), an approach of another group member (n=5), an aggregation of group members (n=9) or it occurred while the group was moving (n=11). "Trills" were never ignored if group members were present. A discriminant analysis detected group-specific acoustic signatures. Consequently, our results provide the first evidence for a group-specific gathering call enhancing group formation in nocturnal solitary ranging primates.

Noise-dependent Vocal Plasticity in a New World Monkey

Henrik Brumm, Katrin Voß, Ireen Köllmer, Dietmar Todt

This investigation of common marmosets (Callithrix jacchus) is the first to examine noise-dependent mechanisms of vocal plasticity in a New World monkey. Since acoustic communication can be considerably impaired by environmental noise, some animals that use sound to communicate have evolved adaptations to counteract its masking effects. The studied marmosets (n=4) increased the sound level of their spontaneous twitter calls in response to increased levels of white noise broadcast to them. Possibly, such noise-dependent adjustment of vocal amplitude serves to maintain a specific signal-to-noise ratio that is favourable for signal production. Concurrently, it can maintain a given active space for communication. In contrast to some bird species, no subject showed any tendency to increase the number of syllables per call series with increasing noise levels, showing that an increased serial redundancy of vocal signals was not used to communicate under noisy conditions. Finally, we examined a possible noise-dependent prolongation of vocal signals. This approach was guided by the findings of perceptional studies, which suggest an increased detection probability of prolonged signals in noise by temporal summation. We revealed that marmosets indeed increased the duration of their call syllables along with increasing background noise levels. This is the first evidence of such a mechanism of vocal plasticity in an animal communication system. In conclusion, our study demonstrates the capacity for multiple vocal adaptations to temporary situations. Thus, there may be more plasticity in the vocal system of primates than previously thought.

Life History of Female Free- ranging Hamadryas Baboons (Papio hamadryas)

Valery G. Chalyan, Natela V. Meishvili

The life history of females has been studied in a troop of hamadryas baboons free-ranging in Gumista Reserve, Georgia. The observations were carried out from 1974 to 1992. It was established that are three periods in the life cycle of a female, characterized by different levels of bond stability. A female's early stages of development, as a juvenile, mainly occur in her natal harem. The period from 2 to about 4 years of age may be considered as that of juvenile instability in the life of each female. In this period, the formation of successive, temporary links between the young female and several young males is seen. This period ends with the first pregnancy of the female, which is the sign of the establishment of a long-term relationship between the female and a male, the father of her first infant. During the period from 5 to 16 years of age, the strategy of the females is characterized by a high level of stability and the mean frequency of a female's transfer from one male's harem to another one is 1.5. Females older than 16 sometimes showed a second (senile) period of social bond instability and often changed harems, moving from the one to another.

Managing Conflicts over Play in Baboons (Papio hamadryas)

Fernando Colmenares, Araceli Díaz-Carreras

Conflicts of interest among partners within a relationship often lead to the exchange of aggressive interactions which are then followed by stress-related behaviours and by several post-conflict peaceful and/or aggressive interactions among former opponents and between these and third parties. Most studies of conflict management and resolution in non-human primates have focused on adult individuals. Many interactions among immatures consist of play and a fairly high number of play encounters escalate to serious fighting. Play partners seem to face conflicts of interest mostly arising from disagreements about the type of behaviour used and/or role adopted in the ongoing play interaction, and from their inability to control the play interaction when third parties join in. The present work provides preliminary data on the way immature baboons manage conflicts arising from play interactions that escalate to aggression. The data come from a 152 hour-study of social play interactions among 34 immature members of the Madrid Zoo colony of hamadryas baboons, Papio hamadryas, which were recorded with behaviour sampling. Twenty-five play interactions escalated to serious fighting. We compared the behaviours that former play partners exhibited during a period of five minutes following play episodes without aggression (PPs=140) and with aggression (PCs= 48). We found evidence that play-related conflicts among immatures caused an increase in the levels of post-conflict play, affiliation ("reconciliation"), re-aggression, redirection and stress-related behaviours. Interestingly, this study provides evidence that immatures may use play to manage and resolve their conflicts.

Experimental Evidence for Female Mate Choice in the Grey Mouse Lemur (Microcebus murinus)

Mathias Craul, Elke Zimmermann, Ute Radespiel

Sexual selection predicts mate choice in cases of highly skewed parental investment. In many nocturnal primates, females rear their offspring without any paternal assistance and female mate choice can, therefore, be expected. In order to study this phenomenon under controlled experimental conditions, we developed a two-fold choice experiment for the grey mouse lemur (Microcebus murinus). Mate choice was deduced from time spent in proximity to test males. Trill frequency (advertisement call), age, relatedness and familiarity among test partners were investigated as parameters potentially influencing the choice. Seventeen oestrous females were tested with two out of sixteen males during one-hour observation periods. Twelve females showed a significant preference for one male. In four cases we observed copulations. The preference was significant for males with a higher trill frequency, indicating the possible importance of social dominance for mate choice. The influence of relatedness and familiarity could not be statistically confirmed. However, they were interconnected in the experiments. Corresponding to theoretical predictions, females which did not know the related male from common socialisation (n = 8), chose related and non-related males in equal proportions. In the remaining cases (n = 4), females sometimes chose the related males, but did not copulate (n = 3) or chose the non-related male and copulated (n = 1). The influence of age on female mate choice was not statistically significant. In the cases with copulations, however, there was a female preference for the older male. The results are discussed with respect to their biological significance and theoretical expectations.

Effect of Ophthalmophathy on the Activity Rhythm in Grey Mouse Lemurs (Microcebus murinus)

Robert Dallmann, Esther Lipokatic, Elke Zimmermann, Stephan Steinlechner

In general, grey mouse lemurs (Microcebus murinus) show a robust activity pattern with nocturnal activity and a diurnal resting and sleeping phase (Schilling et al., 2001). The underlying biological clock is located in the suprachiasmatic nuclei (SCN) of the hypothalamus. In order to keep the clock synchronised with the environment, the clock can be reset by external cues. The most important of these so-called Zeitgebers is the daily light/dark cycle. Aging provokes disturbance of this rhythm, resulting in a decrease of amplitude, a fragmentation of activity and a diminished ability to synchronise to a Zeitgeber (Weinert, 2000). Furthermore, ophthalmic disorders, as well as age, can cause a total breakdown of the rhythm or at least a free-running rhythm, which means that the activity pattern is no longer synchronised with the external cues. In this study, we compared eight healthy grey mouse lemurs and three individuals suffering from a glaucoma. In addition, the animals were tested for the effect of ageing on their circadian activity pattern. Two experiments with different light regimes under long day conditions (14 h light/day) were carried out. Subsequently, the animals were transferred to constant darkness in order to investigate their endogenous activity pattern. We found that the healthy individuals easily synchronised to the light/dark cycle, whereas the diseased showed a free-running rhythm. In addition, preliminary data suggest that there are certain differences between the age classes concerning the period length of the free-running rhythm as well as the total amount of activity per day, which confirms the results of Schilling et al. (2001).

The Social System of the World's Smallest Primate, the Pygmy Mouse Lemur (Microcebus berthae)

Melanie Dammhahn, Peter M. Kappeler

The goal of this study was to illuminate aspects of the components of the social system of the pygmy mouse lemur (Microcebus berthae). In the first field study of this newly-described 30g nocturnal lemur, we captured and followed 39 individually marked animals in Kirindy Forest, western Madagascar. Animals were regularly (re)captured, measured and radio-tracked between August and November 2002. The adult sex ratio in this population was male biased (27M; 12F). Males used larger home ranges than females and overlapped the areas of 2-4 females, but also those of up to 9 other males, whereas female ranges overlapped with 6-10 males, but only with 1-2 other females. Males were highly mobile and travelled longer distances than females, presumably because our study encompassed the pre-mating and mating season when males searched widely for mates. All females came into oestrus within 10 days in mid-November. These data define for the first time the exact timing of the mating season of M. berthae. Associated with the mating season, we found fluctuating sexual dimorphism in body mass, with males becoming heavier than females during the mating season; partly because of a 5-fold increase in testes size. Throughout the study, social interactions with conspecifics of both sexes occurred about every 1-2 h during the activity period and inter- and intra-sexual sleeping associations were observed regularly. Based on these preliminary data, M. berthae can be characterized as a solitary forager living in an individualized neighbourhood system with the potential for scramble competition polygyny.
Partly supported by project grants from MECyD (PB98-0773) and from MCyT (BSO2002-00161) to F. Colmenares.

Sensitivity of Population Dynamics to Life History Parameters: an Individual-based Simulation Study for the Fat-tailed Dwarf Lemur (Cheirogaleus medius)

Kathrin H. Dausmann, Barbara Randlkofer, Joanna Fietz, Udo Hommen

Time or feasibility limitations of field studies often prevent researchers making reliable predictions about population dynamics in the face of changing ecological conditions. However, combining field data with computer models can overcome these problems and help to understand how population dynamics develop and which variables are influencing them most. In this study, we designed an individual-based model to analyse how changes in ecological conditions, as found in the case of habitat destruction or the introduction of non-indigenous predators, possibly affect the population dynamics of the fat-tailed dwarf lemur (Cheirogaleus medius). Variables for this model were derived from an extensive long-term field study (1995-2001) on the life history and population dynamics of C. medius in the Kirindy forest, Madagascar. Using the data from the field study (rates of mortality, dispersal, birth and reoccupation of territories) the model predicts a stable population of C. medius, as is indeed found in the field. Changing key parameters of life history, the simulations of this model reveal that C. medius populations are quite sensitive with a distinct threshold towards extinction for some parameters (e. g. reduction of forest size and offspring survival rate, increasing predation pressure), whereas others show no effect in the model (e.g. birth synchrony). This study shows that computer based simulation can be a valuable tool to assess the quality of the collected field data and the resulting assumptions. Furthermore, it can help to predict the development of population dynamics and other biological variables under constant as well as under changing conditions.
The field study on C. medius was financially and logistically supported by DAAD, DFG, and DPZ.

Sex Skin Swellings in Wild West African Chimpanzees (Pan troglodytes verus): A Reliable Indicator of Ovulation?

Tobias Deschner, Michael Heistermann, Keith Hodges, Christophe Boesch

Sexual swellings advertise sexual receptivity in females of a number of Old World monkey species. Several hypotheses that explain the function of this conspicuous trait are based on assumptions about the temporal relation between the period of maximum swelling and ovulation, and remain largely untested. By combining non-invasive urinary progeston analysis with observational data on swelling characteristics, we examined the reliability of sexual swellings as an indicator of the timing of ovulation in free-living chimpanzees of the Taï National Park, Côte d'Ivoire. Our results show a high variability in the length of the maximum swelling period. Furthermore, although ovulation was almost entirely restricted to the second half of the period of maximum tumescence, its timing varied considerably in relation to both the onset and the end of the maximum tumescence phase. The probability of ovulation, however, was not random, but peaked on day 7 after the onset of the maximum swelling phase, and was almost 60% between days 7 and 9. We therefore conclude that, in chimpanzees, perineal swelling indicates the probability of ovulation, but does not provide sufficient information to deduce its exact timing.

Signal Combinations in Hamadryas Baboons (Papio hamadryas hamadryas)

Anja Dube, Michael Tomasello 

Fourteen focal animals of a group of about 35 hamadryas baboons were observed in Leipzig Zoo from April to October 2000. The aim of the study was to investigate their visual and tactile communication. We understand communication as the 'indirect' achievement of a goal via information conveyed by means of signals from the sender to the recipient (without physical power). We were especially interested in intentional signals. Intentionality can be assumed if there are flexible relations between signal and goal as well as special sensitivity by the sender to the social nature of the signals. Flexibility can also be investigated by the number of different ways in which a baboon combined its single signals. The animals used 19 out of the 26 different visual and tactile signals we recorded for combinations (grouped into four categories: eight 'visual signals' (out of 13), five 'visual signals possibly making some noise' (out of six), two 'visual signals often combined with touching' and four 'tactile signals' (out of five). Most common were combinations composed of 'visual signals' and 'visual signals possibly making some noise' as well as pure 'visual' combinations. The occurrence and the frequency of the signals in the different combinations will be demonstrated. Twenty-seven different combinations (25 double and 2 triple) were analysed regarding occurrence and frequency as well as usage by the focal animals. The highest number seen in a focal animal was 12 different combinations (harem leader) and the lowest three (infants). The data were also analysed for age and sex classes.

Molecular Evolution of FOXP2, a Gene Involved in the Development of Speech and Language

Wolfgang Enard, Molly Przeworski, Simon E. Fisher, Cecilia S. L. Lai, Victor Wiebe, Takashi Kitano, Anthony P. Monaco, Svante Pääbo 

Language is an uniquely human trait that probably represents a prerequisite for the development of human culture. It has become clear in recent years that aspects of speech and language development are likely to be influenced by genetic factors. Furthermore, the ability to develop articulate speech relies on capabilities, such as fine motor control of the larynx and mouth, which are absent in chimpanzees and other great apes. Recently, FOXP2, the first gene of relevance to the human ability to develop language, has been described. A point mutation in FOXP2 co-segregates with a disorder in a large family in which half of the members have severe articulation difficulties, accompanied by linguistic and grammatical impairment. In addition, this gene is directly disrupted by a translocation in an unrelated individual who has a similar disorder. Thus, two functional copies of FOXP2 appear to be required for acquisition of normal spoken language. In order to investigate the evolution of FOXP2, we sequenced the cDNAs that encode the FOXP2 protein in chimpanzee, gorilla, orangutan, rhesus macaque and mouse, and compared them to the human cDNA. In addition, we investigated the intra-specific variation of the FOXP2 gene in humans. The results strongly suggest that FOXP2 has been the target of selection during recent human evolution.

Information Content of Sexual Swellings for the Reproductive Status of Females in Free-ranging Long-tailed Macaques (Macaca fascicularis)

Antje Engelhardt, J. Keith Hodges, Carsten Niemitz, Michael Heistermann 

The functional significance of sexual swellings in female primates is controversial and seems to be particularly obscure in female long-tailed macaques, since swelling sizes decline markedly with advancing age. One of the questions that still needs clarification is to what degree swellings advertise reproductive status in this species. Here, we compared individual patterns of swelling sizes, visually scored on a 5-class scale, to faecal oestrogen and progestogen profiles during non-conception cycles (n = 4) as well as conception cycles and ensuing pregnancies (n = 6) in free-ranging female long-tailed macaques. During ovarian cycles, individuals differed considerably in size and duration of maximum swelling (range:5-25 days). Although ovulation almost always occurred during peak swelling, it's timing within this period varied markedly between cycles (range: 2-6 days before detumescence). During early pregnancy, a clear pattern of post-conceptional detumescence could be observed followed by a distinct swelling peak. Peak pregnancy swelling was reached on average 39 days after the onset of conceptional detumescence and was associated with a well-defined period of enhanced sexual activity. Pregnancy swellings remained at peak values for as long as 85 days (average: 45 d). Swelling size showed a significant positive correlation with the faecal oestrogen/progestogen ratio during the cycle and the first third of gestation. These data illustrate that although variation in the size of sexual swellings is related to endocrine status in female long-tailed macaques, this trait is an unreliable cue for the timing of ovulation in this species. On the other hand, peak swellings lasting longer than four weeks are a good indicator of pregnancy.

New Polymorphic Y-Chromosomal Microsatellite Markers for the Chimpanzee, Gorilla, Orangutan and Mandrill as Identified by Cross-Species Amplification

Axel Erler, Mark Stoneking, Manfred Kayser

As a result of international cooperation, more than 170 additional microsatellites for the human Y-chromosome were identified recently (Kayser et al., unpublished data). The evolutionary conservation of DNA sequences allows a successful cross-species amplification of most of these new genetic markers in closely related species of non-human primates. We selected 136 candidate loci for five non-human primate species or subspecies and generated 76 male-specific loci for the central chimpanzee (Pan troglodytes troglodytes), 77 for the western chimpanzee (P. t. verus), 60 for the gorilla (Gorilla gorilla gorilla), 40 for the orangutan (Pongo pygmaeus) and 18 for the mandrill (Mandrillus shinx). Based on 3 to 7 individuals, polymorphism was detected for 49 loci in the central chimpanzee, for 24 loci in the western chimpanzee, for 21 loci in the gorilla, for 12 loci in the orangutan and for 3 loci in the mandrill. Due to allele-length comparisons between humans and non-human primates we predict that an additional 2 loci for the central chimpanzee, 10 for the western chimpanzee, 9 for gorilla, 5 for orangutan and 3 for mandrill will show polymorphism when further individuals are analysed. The evolution of microsatellite DNA and flanking regions was investigated by sequence comparisons. Jukes-Cantor distances between species for 979bp of flanking DNA-sequence show similar values to published data for non-coding regions of the SMCY gene, but 50 to 118 % higher values compared with autosomal regions. Our results provide the primatology DNA community with a large number of polymorphic Y-chromosomal microsatellite markers that should be useful for investigating the diversity of primate paternal lineages and for addressing sociobiological questions such as male relatedness and male vs. female migration patterns.

Interspecific Communication in Red-fronted Lemurs (Eulemur fuluvs rufus) and Sifakas (Propithecus verreauxi verreauxi)

Claudia Fichtel

Red-fronted lemurs (Eulemur fulvus rufus) and Verreaux's sifakas (Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls to raptors and general alarm calls to carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, despite the fact that the two species rarely interact. In a crossed design, red-fronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons (Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, both lemur species have an understanding of each other's aerial and general alarm calls, indicating that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.

Individual Recognition in Young Barbary Macaques

Julia Fischer

Whereas there is little evidence that non-human primates learn to produce their sounds through imitation, learning does seem to play a role in the usage and comprehension of calls. There are only few studies that have addressed the development of primate infant responses to conspecific vocalizations in the wild. Previous studies on vervet monkey (Cercopithecus aethiops) and chacma baboon (Papio cynocephalus ursinus) infants showed that the appropriate response to, and, hence, the correct classification of alarm and long-distance contact calls emerged at about six months of age. It remained unclear whether the age of six months constitutes a watershed in terms of Old World monkey infants' cognitive development or whether it was due to the types of stimuli used in the experiments. I therefore initiated this study in which I examined the development of Barbary macaque (Macaca sylvanus) infant responses to maternal calls, under the assumption that recognition of the mother is one of the tasks that infants should master as early as possible. I conducted a set of experiments in which I presented infants at different age categories with short bouts of screams recorded from their mothers or another female of the same social group. At 2.5 months, infants responded significantly more strongly to maternal calls than to calls from unrelated females, indicating that they recognized their mothers by voice. At that same age, vervet and baboon infants failed to show any responses to the calls presented to them. Therefore, the development of infant responses apparently depends on the type of call.

"Laughter" in Bonobos?: Preliminary Results of an Acoustic Analysis of Tickling Sounds in a Hand-reared Male

Birgit Förderreuther, Elke Zimmermann

A major unresolved question in the evolution of auditory communication is whether universal principles rule the encoding and decoding of affective states. "Laughter" is an important non-verbal affective visuo-acoustical display regulating social interactions in humans. It is present in deaf and blind infants and shows cross-cultural similarity in form and function (Grammer and Eibl-Eibesfeld 1990; Ruch and Eckman 2001), which implies a pre-human phylogenetic origin. On the basis of similarity in the visual display, van Hooff (1972) homologised human laughter with the chimpanzee's play face, also called the "relaxed open mouth display". As in humans, it is accompanied by a vocalization (Provine 2000). Until now, however, no sophisticated acoustic analysis of this vocalization in any ape taxon has been performed. Within a comparative study of affective acoustic communication in strepsirrhine and anthropoid primates, we investigated if sounds accompany the "relaxed open-mouth display" in a hand-reared infant bonobo from Wuppertal Zoo. We elicited the display by tickling. Our findings showed that the bonobo combined the visual gesture with sounds. The spectrographic analysis of these sounds implied both gross overall similarity with laughing sounds in human infants (as analysed by Schreiner et al. 2003) and prominent differences in the frequency domain. A further comparative analysis on a larger number of individuals and species is in progress to gain more insight into the evolution of emotion in the acoustic communication of primates.

The Influence of Housing Conditions on the Performance of Aberrant Behaviours in Former Laboratory Chimpanzees (Pan troglodytes): Association with Social Interactions?

Cornelia Franz, Sabine Macherhammer, Elfriede Kalcher, Karl Crailsheim, Signe Preuschoft 

Primates in captivity show specific "aberrant" behaviour patterns that are either not observed in the wild or occur in other contexts, frequencies or sequences. If performed repetitively, invariably with no obvious goal or function, such aberrant behaviour is described as stereotypic. We are investigating aberrant behaviours of 10 male former laboratory chimpanzees and one socially experienced male at the Safaripark Gänserndorf, Austria, comparing single-cage housing with group-living in an enclosure during the establishment of an all-male-group. We expected that (a) more space would reduce locomotion stereotypies, and (b) that more social interactions, especially grooming, would diminish aberrant self-directed behaviours. In order to compare the time budgets between the different housing conditions, we analysed five-minute scan samples of each male from video records in single-cages and observations after grouping in the spacious indoor hall. Focal animal records were conducted on grouped individuals to investigate frequencies, durations, sequences and context of aberrant behaviours. Compared to single-caging locomotion, stereotypies decreased once the chimpanzees were housed in groups. Contrary to our expectations, some individuals continued to show typical stereotypies or even developed new ones, potentially copying other group members. Affiliative interactions among group members and tensions within group mainly elicited these stereotypies. This supports the assumption that stereotypies are performed in order to cope with stressful situations or motivational conflicts. We conclude that environmental and social enrichment are important factors for the reduction of aberrant behaviours. Yet, resocialisation can also provide novel opportunities for aberrant behaviours, at least in the short run.

Variability in Feeding Ecology Between Groups of Mountain Gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda

Jessica Ganas, Martha M. Robbins

Examining dietary variability both within and between populations of primates is important in order to address the differences in ecological requirements that arise from varying landscapes. We documented the dietary patterns of one group of mountain gorillas at a high altitude site and two groups at a low altitude site within Bwindi Impenetrable National Park, Uganda and recorded spatial and temporal variability of their foods at each location. There were significant differences in the number of days fruit was eaten, the species eaten, and the number of species consumed of both herbaceous vegetation and fruit between groups at the lowland site and the group at the highland site. We also found differences in species consumed between the two groups at the lowland site. Finally, we recorded higher plant species diversity and greater fruit availability at the lowland site than at the highland site. We attribute variation in diet between the lowland and highland populations to differences in fruit availability and species composition between sites. We suggest differences between the two groups at the lowland site are due to low density and high clumping of fruit species as well as inter-group competition. This study demonstrates the importance of examining dietary requirements of species across their range in order to document what constitutes "good" habitats for them at different locations.

Bachelor Groups of Western Lowland Gorillas (Gorilla gorilla gorilla) at Lokoue Clearing, Odzala National Park, Republic of Congo

Sylvain Gatti, Florence Levréro, Nelly Ménard, Eric Petit, Annie Gautier-Hion

A growing number of studies on western lowland gorillas (G. g. gorilla) allows us to compare social structure among subspecies in the genus Gorilla. Under exceptional conditions, observations conducted on a lowland gorilla population frequenting a small clearing in Odzala National Park have allowed us to identify 31 solitary males and 45 groups (a total of 377 individuals). Of the groups, 37 were reproductive groups containing only one fully adult silverback male with adult females and their offspring and 8 groups contained no reproductively active female. Three of these groups could be considered to be in a transitional state towards reproductive groups (because they contained sub-adult females close to maturity); however, the other five were bachelor groups mainly comprising males and devoid of adult or sub-adult females. Three of the bachelor groups were formed by immature individuals and a solitary silverback joining together. The migrants originated either from disbanded one-male groups after the disappearance of the silverback or from stable reproductive groups. Bachelor or all-male groups are known to occur in eastern lowland gorilla (G. g. graueri) and in mountain gorilla (G. g. beringei) populations; until now, they have not been clearly identified in western lowland gorillas. The origins and relatedness of bachelor group members remain to be investigated, as does their potential role in the social dynamics of gorilla populations. It is interesting to note that their rate of representation in the study population is close to that found in mountain gorillas despite the fact that, contrary to what has been observed in mountain gorillas, no multi-male breeding groups were seen in the study population.

Affect Related Components in Squirrel Monkey Alarm Calls

Kurt Hammerschmidt, Claudia Fichtel 

Primate vocalizations are communicatory signals that express specific information as well as the motivational state of the caller. Following the motivational structural rules (Morton 1979), high-frequency vocalizations should be given in fear associated contexts, whereas, harsh, low-frequency vocalizations should be given in aggression associated contexts. We conducted acoustic analysis and playback experiments of squirrel monkey, Saimiri sciureus, mobbing calls ('yaps') in order to test whether such motivation-associated changes in frequencies of a call are expressed and are meaningful for conspecifics. Acoustic analysis revealed that yaps given in contexts associated with a higher flight motivation are characterized by an increase in frequencies and amplitude. Manipulations in frequency and amplitude of yaps have shown that squirrel monkeys paid more attention to playback experiments with high-frequency calls than to those with low-frequency calls, indicating that the relationship between call structure and the underlying affective state of a caller agreed with the listener's assessment of the calls. To test if calls with harsh, low-frequency components are given in aggression associated contexts, we subsequently conducted playback experiments in which we manipulated only the harsh, low-frequency component of the yap in frequencies and amplitude. Squirrel monkeys showed a longer orienting response to playback calls with both low frequencies and increased amplitude but not to calls with either low frequencies or high amplitude alone. These results indicate that low frequency calls only effect listeners responses when they are combined with a simulated higher effort (higher amplitude) of the sender.

Quantity Based Judgments by Orangutans (Pongo pygmaeus), Gorillas (Gorilla gorilla) and Bonobos (Pan paniscus)

Daniel Hanus, Josep Call, Michael Tomasello

This study investigated the ability of three great ape species to estimate and compare two sets of small quantities (1-6 cereal bits). Subjects were six orangutans (Pongo pygmaeus), five gorillas (Gorilla gorilla) and four bonobos (Pan paniscus). Experiment 1 investigated the ability to choose the larger of two quantities presented in two separate dishes. There were two types of presentation. In the "simultaneous condition" both quantities were concurrently visually available, whereas in the "successive condition" they were presented successively, so that they could not be directly compared. In Experiment 2, the same food quantities were sequentially dropped into two opaque cups, thus none of the quantities was ever viewed in its totality and they could not be directly compared. Orangutans, gorillas and bonobos were capable of selecting the larger of two quantities in Experiment 1 for both conditions. There was also some evidence from Experiment 2 (albeit weaker) that orangutans, gorillas and bonobos may mentally combine the single items in each cup to obtain the larger of two quantities. This study suggests that great apes mentally represent quantities and that they are able to use this information for selecting the larger of two sets of items.

Population Genetics and Biogeography of Mouse Lemurs (Microcebus spp.) and Dwarf Lemurs (Cheirogaleus medius) in Southeast Madagascar

Andreas Hapke, Jörg Ulrich Ganzhorn, Hans Zischler

The region of Fort Dauphin in southeast Madagascar shows a broad variety of different forest ecosystems caused by a strong gradient in annual precipitation and by differences in altitude, soil type and proximity to the seashore. In addition, forests are fragmented to various degrees by natural barriers and human influence. In particular, littoral forests in the region are split up into numerous fragments and are separated from large continuous forests in the nearby mountain ranges by anthropogenic grasslands. Distribution ranges for several species of mouse lemurs (Microcebus spp.) and dwarf lemurs (Cheirogaleus spp.) match and overlap in the region. The study presented here deals with the effects of different kinds of barriers and other ecological factors on the population structure of mouse lemurs and the fat-tailed dwarf lemur (Cheirogaleus medius). A total of 500 individuals of Microcebus griseorufus, Microcebus murinus, Microcebus rufus and Cheirogaleus medius from 22 locations has been sampled and genotyped using a panel of nuclear microsatellite markers and the maternally inherited mitochondrial hypervariable region I. Thus, gender specific dispersal patterns could be taken into account when looking at isolation and migration. The results presented here show effects of fragmentation in littoral forests and a complex pattern of colonisation of now isolated fragments from a large continuous source population in the mountain ranges.
This research was financially supported by the DFG (Ga 342/9-1) (Zi 568/2-2) and the German Primate Centre and complies with the current laws in Madagascar and Germany.

'What Can We Learn About the Evolution of Language by Studying Handedness in Non-human Apes?'

Rebecca M. Harrison, Pia Nystrom

Modern humans show species level right handedness; much research has been focussed on when and why this evolved. This is important because of a perceived connection between handedness and complex behaviours such as tool manufacture and spoken and gestural language. This connection has recently been reinforced by work on mirror neurons in humans. There is only limited evidence from the archaeological record, consequently handedness in extant non-human primates is studied because it is considered to be a means of mapping the evolution of language, cognition and tool use. Despite the extensive body of literature on this subject, the level of handedness in non-human apes remains questionable. Most studies focus on one species, and differing methodologies makes cross comparison across studies difficult. In the present study, handedness was examined in captive groups of bonobos (n=22), chimpanzees (n=7), gorillas (n=21) and orangutans (n=21). Data were recorded over 1000 hours by focal animal observation. The results showed no species level handedness in any apes studied. It can only be surmised that species level handedness in humans evolved after the divergence of the Pan lineage. Mirror neurons are believed to predominate in the left hemisphere of humans. They are also present in macaques but are bilateral. It is possible that this system was commandeered when a need arose for complex behaviours to be located in the same hemisphere for enhanced processing speed. We propose that the manufacture of complex stone tools and the transmission of information regarding their manufacture provided such a requirement.

Assessing Continuity and Stability of Maternal Styles in a Colony of Baboons (Papio hamadryas)

Maite Victoria Hernández-Lloreda, Fernando Colmenares 

Sudden changes across time in the level of performance of a behaviour pattern are often associated with major reorganisations in the processes underlying development. Changes over time in the rankings of individuals on the status of a behaviour pattern are often used to determine stability of individual differences across development. Continuity and stability refer to different developmental processes though, which may or may not be associated with one another. This study explores the relation between continuity and stability of maternal styles by using two different statistical methods of assessing the nature of behavioural changes over time. The assessment of continuity requires a growth modelling approach and the assessment of stability requires approaches that search for patterns of change in rank-orders across time. We use hierarchical linear growth modelling to study continuity/discontinuity and longitudinal cluster analysis to assess stability/instability of individual differences in maternal styles. The behavioural data come from a longitudinal study of the interactions between 23 mothers and their infants, members of the Madrid Zoo colony of hamadryas baboons (Papio hamadryas), collected for 25 consecutive fortnight periods over the infants' first year of life. The findings provide empirical evidence that all kinds of relations between continuity and stability of maternal styles are possible, and illustrate the general but important point that they measure different aspects of behavioural development. The two theoretical constructs and the statistical methods used to assess them provide different but complementary windows to understanding changes across time in maternal style in particular and in behavioural development in general.
Partly supported by project grants from MECyD (PB98-0773) and from MCyT (BSO2002-00161) to F. Colmenares.

Do Great Apes Use Iconic Cues to Find Hidden Food?

Esther Herrmann, Alicia Pérez Melis, Michael Tomasello

Two important features of human communication are the iconic and symbolic nature of its signs and the communicative intentions of the sender. The aim of the following three studies was to find out to what extent apes exhibit these features. We investigated whether great apes use an iconic cue to find hidden food in one of two possible hiding places and whether they understand the communicative intentions of a human experimenter. In the first study, the location of a piece of a banana was indicated by placing either a photo or a replica of a banana on top of the correct hiding place. The human's communicative intentions were varied by allowing the ape to see or not see the placement of the icon. In the second study, the subjects were presented with a photo or a replica of a specific fruit that resembled the reward and an arbitrary photo or object as a distractor. In this case, the iconic cue was placed on top of the correct hiding place and the distractor over the empty one. In a third study, the subjects were confronted with either two different fruit photos or replicas while the hidden fruit matched only one of the icons. Subjects could use both iconic cues to find hidden food and were more successful with photos than replicas. However we found no evidence to suggest that apes understood the human's communicative intentions in an object-choice task.

Harem Formation out of Socially Deprived Males and Closely Bonded Females of Papio hamadryas

Christine Hrubesch, Hans Winkler, Signe Preuschoft 

Fourteen female baboons (Papio hamadryas) that were members of one harem were separated from their male to form four new harems. The new harem leaders were socially deprived but had been housed as a compatible group for several years. Only two had experience with a female. We observed the baboons before and after re-grouping. Although hamadryas baboons are described as cross-bonded, not female-bonded, the relationships among these females were unusually close. We assigned each female to one of the four males according to her preferences for that male, as observed in a mate choice experiment, and to her grooming bonds with the other females. We investigated whether a hamadryas harem is formed and kept together by the male's herding behaviour alone or whether female-female bonds can influence a female's tendency to stay within one harem or to change to another. The results indicate that females change harems only when their males fail to herd them or when they get separated. Eight female transfers resulted when one male had to be removed because he excessively herded another harem leader, who consequently lost his females. Two females returned to this male. The other females joined the remaining harems, choosing those in which they had the closest female friends. One additional transfer occurred when a newly introduced male was chosen by an unherded female. We suggest that female choice of male mates and female friends can be expressed when harems dissolve. However, females clearly avoided initiating transfers between groups.

All Males are Equal but Some Are More Equal: Paternity in Polyandrous Moustached Tamarins (Saguinus mystax)

Maren Huck, Petra Löttker, Uta-Regina Böhle, Eckhard W Heymann 

Moustached tamarins are a small Neotropical primate species living in groups of 1-4 adult males and 1-3 adult females. Generally, only one female breeds, mating with more than one male. In order to examine the genetic consequences of this mating pattern, we used 12 microsatellite loci (on average 6,7 alleles per locus) extracted from faecal samples, collected from two major study groups and 6 neighbouring groups. We investigated whether males have equal probabilities of siring offspring and if polyandrous mating can lead to multiple paternity in dizygotic twin litters (total of 30 infants with 9 twin pairs). Although within each group the majority of infants had the same father (both within litters and over consecutive years), in at least one case the father of the oldest offspring was not the sire of the youngest infant, although he was still resident in the group. Furthermore, we found a strong hint for multiple paternity in a supposed twin pair. The results of this first genetic study on wild tamarins suggest that not only the mating system but, indeed, the breeding system of these callitrichids is polyandrous, though normally one male gets primary access to the breeding female. The mechanism by which males try to monopolize access to the breeding female and the overall genetic relationships within groups are the subjects of ongoing studies.

I Know Something You Don't Know - Do Apes Attribute False Beliefs to Conspecifics in a Competitive Object Displacement Task?

Keith Jensen, Josep Call, Michael Tomasello

In past experimental studies, apes have not demonstrated an understanding of false belief, calling into question whether they have a theory of mind. However, one possible problem with the prior studies is that apes have been required to attribute an understanding of beliefs to humans, whereas they may be better at attributing knowledge to conspecifics. In addition, apes - particularly chimpanzees (Pan troglodytes) - might be more finely attuned to competitive tasks than cooperative ones. In this study, for which preliminary results will be presented, an object displacement paradigm is used on the four species of great apes. Conspecific pairs face each other across a table; one (the communicator) sees the hiding of the food, while the other (the observer) does not. However, only the observer can see the location change of the containers under which the food is hidden, and must use incorrect information from the communicator (reaching) as being based on a false belief.

Apes Know When They Are Being Watched

Juliane Kaminski, Josep Call, Michael Tomasello

A number of animal species have evolved the cognitive ability to detect when they are being watched by other individuals either in competitive or communicative situations. Precisely what kinds of information they use to make this determination is unknown. There is particular controversy in the case of the great apes. We show here that apes can determine when they are being watched in a communicative situation. They do this not just on the basis of whether they can see another animal as a whole, or even whether they can see the front of the other animal's body, but rather they are sensitive to the other animal's face in particular, with a minority of individuals even being sensitive to the eyes of others.

Comments on the Hierarchy of Instincts

Adriaan Kortlandt

In the higher vertebrates, instinctive behaviour is, as a rule, organised in and driven by hierarchical systems of goal-steering mechanisms, Mc Dougallian as well as Lorenzian types. Ontogeny and maturation of such systems proceed, as a rule, by isolated development from the bottom level upwards, followed later by ascending integration into the higher level of organisation. In these processes, periods of relatively long and "ganzheitliche" development usually take turns with shorter periods of irregular and "ruptural" behaviour that lead to reorganisations. In phylogeny, sub patterns may break away from their original hierarchy and become independent "derived" patterns that have new forms, new causations and new functions. For instance, so-called "sexual" behaviour in bonobos is predominantly social behaviour. These four issues have been amply documented in studies of birds and mammals, including chimpanzees and humans. Ignoring and/or rejecting these issues with regard to human developmental and medical psychology, for example by "classic" ethnologists, indicates fundamentally anti-Darwinist scientific thinking. For example, human kissing appears to be a derivative of licking a baby for cleaning (common to nearly all mammals) and of orally feeding offspring (common to several carnivores and some human tribes), which has subsequently been partly integrated into sexual and social behaviour.

Which Senses Play a Role in Squirrel Monkey Food Choice?

Stephanie Krause, Matthias Laska

Primates are traditionally considered to be primarily visual animals. However, no study to date has directly addressed the question as to which senses non-human primates actually use for food choice. To test this, we repeatedly presented six squirrel monkeys, Saimiri sciureus, with eight familiar, eight unfamiliar and eight experimentally modified familiar types of food, and analyzed their videotaped behavioural responses. Familiar food items included fruits and vegetables that were part of the animals' daily diet in captivity (e.g. banana, apple, tomato), unfamiliar food items included edibles that the animals had never encountered before (e.g. asparagus, garlic, tuna), and experimentally modified food items included familiar fruits and vegetables that were either dyed with a non-matching food colour (e.g. blue banana) and/or scented with a non-matching food odour (e.g. tomato with citrus aroma). We found that familiar food items were inspected only very briefly and exclusively visually prior to consumption, whereas both unfamiliar and experimentally modified familiar food items were assessed for significantly longer, using olfactory and gustatory senses and both manual and oral tactile information in addition to visual cues. After only one or two presentations, sniffing, licking, touching and probing of unfamiliar or experimentally modified familiar food items decreased markedly, suggesting a quick multimodal learning process as to edibility and attractiveness of potential food. Taken together, these results suggest that olfactory, gustatory and tactile information plays an important role in decision making of squirrel monkeys when presented with unfamiliar, but not with familiar food.

Behavioural Ecology of Olive Baboons (Papio anubis) in a Forest-savannah Mosaic in West Africa

Britta K. Kunz, Karl Eduard Linsenmair

Although baboons have been a favoured subject for behavioural studies of non-human primates, investigations in the wild have been conducted mainly in East and South Africa, and comparatively little is known about the behavioural ecology of western populations. Olive baboons in Comoé National Park (CNP), northern Ivory Coast, live under environmental conditions essentially distinct from those the same species faces in East Africa. These differences should result in prominent behavioural variances. During our field study on olive baboons in CNP, we regularly estimated the population size in an area of about 45 km2, and collected data on group sizes and structure. A small one-male and a larger multi-male group were habituated. When following these groups, their location was mapped and the habitat type was identified. Behaviour was recorded using scan-sampling and diet was identified whenever possible. Generally, group sizes in CNP were smaller than in East Africa. For groups of comparable size, the home ranges of the two habituated groups were also smaller. The home ranges of both groups included savannah, forest islands and gallery forest. Differences in habitat use were evident and varied with season. Contrary to those in East Africa, olive baboons in CNP are highly frugivorous, consuming fruits and seeds of at least 49 plant species out of 23 families. Grass, roots and leaves accounted for only a small part of their diet, and were eaten mainly during periods of fruit scarcity.

Challenging the Dogma of "Microsmatic" Primates - Olfactory Performance in Squirrel Monkeys and Pig-tailed Macaques

Matthias Laska, Alexandra Wieser, Yvonne Simon, Cornelia Rieck, Vera Miethe

Simian primates are typically regarded as visual animals with a poorly developed sense of smell. This view, however, is mainly, if not exclusively, based on an interpretation of neuroanatomical features and not on physiological evidence. Using a conditioning paradigm, we determined olfactory detection thresholds for homologous series of aliphatic esters, alcohols, aldehydes, ketones and carboxylic acids, as well as for some terpenes and volatile steroids in two species of non-human primates, the squirrel monkey (Saimiri sciureus) and the pig-tailed macaque (Macaca nemestrina). The results show both primate species to have a well-developed olfactory sensitivity for aliphatic substances, which in several cases matches or even is markedly better than that of species such as the rat or the dog. In addition, tests of odour discrimination ability for structurally related substances show that with this measure of olfactory performance, non-human primates generally perform as well as non-primate mammals presumed to have a keen sense of smell. These findings lend further support to the growing body of evidence suggesting that between-species comparisons of neuroanatomical features or of the number of functional olfactory receptor genes are poor predictors of olfactory performance. Further, our findings suggest that olfaction may play an important and hitherto underestimated role in the regulation of behaviour in the species tested and that the concept of simian primates as primarily visual and "microsmatic" animals needs to be revised.

Population Dynamics, Gene Distribution and Conservation in Barbary Macaque (Macaca sylvanus) Populations

Marjorie Lathuillière, Brigitte Crouau-Roy, Erik Petit, Wolfgang Scheffrahn, Nelly Ménard 

Our study was conducted on three Barbary macaques, Macaca sylvanus, isolates that included around 2000 to 10000 individuals. Barbary macaques live in multimale-multifemale groups. Males disperse between groups while females are philopatric. Despite this asymmetrical dispersion of the two sexes, the mean degrees of relatedness ("R", calculated from 15 microsatellite markers genotyping), either between adult females or between adult males were near values found between unrelated individuals. Nevertheless, the mean R between adult females was significantly higher than that between adult males in the group that showed the highest increase rate. Fissions of social groups lead to the formation of new independent groups and result in the separation of matrilineages. The observed group fission resulted in a significant increase in the R between adult females, reaching the level of cousins or the level of half-siblings depending on the newly formed group. These values remained identical during the five years following the fission. As a consequence, the within-group R between adults increased after group fission even though the R between males remained low. Group fission enhanced the genetic differentiation between groups within the studied population. Dispersal patterns partly explain the high degree of genetic diversity observed in our Barbary macaque populations (H=0.7), in spite of their reduction and fragmentation. Nevertheless, the reduction of population size led to a decrease in allelic diversity. Fragmentation led to highly differentiated populations (11 to 17%), so that the disappearance of one among the three studied populations would lead to the loss of up to 19% of genetic diversity.

Analyses of Different Viruses in the Wild Chimpanzees (Pan troglodytes verus) in the Taï National Park, Ivory Coast

Fabian Leendertz, Heinz Ellerbrok, Bernhard Ehlers, Eckart Schreier, Sandra Junglen, Christophe Boesch, Georg Pauli 

The last tropical rainforests of the world are suspected to harbour a large variety of different known and unknown viruses. In order to estimate the prevalence of different viruses in the tropical rainforest of West Africa, we screened for various viruses of potential zoonotic relevance in wild chimpanzees living in the Taï National Park, Ivory Coast. The chimpanzees were members of three different groups that have been habituated to the presence of humans and have been studied for more than twenty years. On account of this, results obtained from the virological screening can be interpreted on the basis of detailed information about the social contacts, affinities and the life history of each individual chimpanzee. Here we present our initial results showing the presence of hepatitis B virus, herpes and retroviruses detected in samples from ten chimpanzees that died of unknown causes during the last four years. The sequences we obtained were compared to known human and animal strains and phylogenetic analyses were performed. Since, on the one hand, researchers live in unusual proximity to the chimpanzees and, on the other hand, inhabitants of the area regularly hunt and consume primates, the risk of transmission of different viruses from humans to chimpanzee and vice versa has to be taken into consideration.

Effects of Group Size and Composition on the Sociality of Wild Chimpanzees (Pan troglodytes verus)

Julia Lehmann, Christophe Boesch

The socio-ecological model predicts that the social organisation of primates is influenced by group size and composition, since both advantages and disadvantages of group living are affected by these two variables. Studies assessing these effects are often based on inter-group comparisons, this adds an additional source of variation, namely ecological differences between study sites. In our study on chimpanzee sociality, we assess the effects of group size and composition on social parameters such as fission-fusion organisation, dyadic association and grooming within one community of wild West African chimpanzees (Taï Forest, Côte d'Ivoire). Behavioural data were analysed for a 10-year period during which time community size decreased from 51 to 21 individuals. We found that a decrease in community size led to an increase in association between chimpanzees. Further, the fission-fusion structure was used in a less flexible way as indicated by an increase in party size and duration. Although general gregariousness seemed not to be dependent on community size, the larger proportion of mixed-sex parties in the small community indicated increased cohesiveness between the sexes. In line with other reports, we found that males were generally more gregarious than females, i.e. they spent less time alone, had a higher association index and were found to groom more frequently than expected throughout the study period. However, sex differences in sociality were small in comparison to those reported from East African chimpanzees. Thus, our data demonstrate that under relatively constant ecological conditions group size and composition directly affect chimpanzee social behaviour.

Social Communication in Captive Siamangs (Symphalangus syndactylus): Use of Gestures and Facial Expressions

Katja Liebal, Michael Tomasello

The majority of work on primate communication has concerned vocalizations. In contrast, gestures and facial expressions have been studied in very few primate species, mostly in macaques and chimpanzees, while almost nothing is known about the use of these signals in smaller apes (Hylobatidae). In the present study, the focus was on intentional signals used by captive siamangs, Symphalangus syndactylus. The goal was  to describe the signal repertoire (tactile and visual gestures, actions, facial expressions),  to focus on differences related to group, age and sex and (3) to investigate the use of signals in terms of flexibility (social context, recipient's behaviour, signal combination). Fourteen individuals of four family groups were observed in two different zoos for 140 hrs. Thirty-one different signals - 12 tactile gestures, 8 visual gestures, 7 actions and 4 facial expressions - were observed. In general, tactile gestures and facial expressions were most frequently used. Group differences concerning the number of signals were caused by social factors or housing conditions. The range of signals increased up to the age of six, but declined in adults. The proportions of signal categories performed also varied depending on age. Differences in the repertoire of males and females were most obvious in the sexual context. The majority of signals was used flexibly in three or more social contexts and almost one-third of signals occurred in combination with other signals. Siamangs also adjusted their signals appropriately for the recipient, using visual signals most often when the recipient was already looking. These observations are discussed in the context of siamang ecology, social structure and cognition.

Use of Gesture Sequences in Chimpanzees

Katja Liebal, Josep Call, Michael Tomasello

The gestural communication of a group of 19 captive chimpanzees was observed, with particular attention to gesture combinations (sequences). The goal of the study was  to describe the inventory of gesture sequences with regard to the number and modalities of gestures combined and  to investigate whether chimpanzees accommodate the gesture modality to the attention state of the recipient or even manipulate the recipient's state of attention by using particular gestures serving as attention-getters. The majority of combinations occurred in the context of play and were sequences of two or three gestures, which were most often repetitions of the same gesture. Other sequences combined gestures either within modality (visual, auditory, tactile) or across modalities. All combinations were used for functions that could also have been indicated with single gestures. Although chimpanzees used visually based gestures mostly when the recipient was already attending and tactile gestures regardless of the other's attentional state, they almost never used an attention-getter as the first gesture in a sequence - in order to secure attention - followed by a visual gesture. Instead of manipulating the recipient's state of attention, other strategies were used to ensure they were in the visual range of the recipient before performing visual gestures. Moreover, although the recipient frequently did not respond to the first gesture, the sender continued repeating the same gesture. Therefore, chimpanzee gesture sequences do not seem to represent a strategy to increase the flexibility of the chimpanzee gestural repertoire, but rather seem to emerge as a result of the recipient's lack of responsiveness.

No Signs of Post-Partum Oestrus in Wild Female Moustached Tamarins (Saguinus mystax)

Petra Löttker, Maren Huck, Michael Heistermann, J. Keith Hodges, Eckhard W. Heymann 

In callitrichid primates the occurrence of a post-partum oestrus may result in a new pregnancy while a female is still lactating. Since callitrichids give birth to heavy and rapidly developing twins, the energetic burden of these simultaneous reproductive activities has been invoked as a major explanation for the evolution of alloparental care. However, almost all pertinent information about callitrichid reproductive biology comes from studies in captivity, where reproductive strategies may be strongly modified. In order to investigate female reproductive strategies and the underlying proximate mechanisms (behaviour, hormones), we conducted a 12-month study on two groups of wild moustached tamarins (Saguinus mystax). Animals were followed 8-10 h per day and faecal samples were collected as often as possible. To assess ovarian activity, the concentrations of immunoreactive pregnanediol-glucuronide and total oestrogens were determined by enzyme-immunoassay. In each of the two study groups a single female gave birth to twin offspring. After parturition both females showed an extended period of ovarian inactivity, and ovarian cyclicity began only two to three months after parturition. Conception occurred in the second or third cycle. Thus, our study did not provide evidence for the occurence of a post-partum oestrus. This is in line with the observation of only one birth per female per year in our study population and in other moustached tamarin populations. We conclude that a) findings from captivity should only carefully be transferred to the situation in the wild, and b) additional explanations have to be invoked for the evolution of alloparental care in callitrichid primates.

Time-Matched Grooming by Female White-faced Capuchins and Bonnet Macaques

Joseph H. Manson, C. David Navarrete, Joan B. Silk, Susan Perry

The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout ('time-matching'). Models of allogrooming based on biological markets theory predict an inverse relationship between grooming partners' dominance rank distance and how closely they match each others' grooming contributions within each bout. These predictions have been confirmed in female chacma baboons, Papio cynocephalus ursinus. We tested them using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Most grooming bouts were not reciprocated at all in either species. However,  the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and  when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, though significant. These results indicate that although some form of time-matching may be a general characteristic of grooming in female-bonded primate species, time-matching accounts for relatively little of the variation in the distribution of grooming within bouts.

Kinematics of the Grasping Tail in Spider Monkeys: Implications for its Movement Control

Franziska Martin, Carsten Niemitz

The prehensile tail of spider monkeys serves as a third extremity in brachiation. Based on its anatomy, this highly flexible unpaired grasping organ has virtually unlimited degrees of freedom, which challenge movement planning and coordination. We try to understand the movement control by identifying the basic principles of the tail kinematics. Using three synchronized video cameras, we recorded four adult female A. geoffroyi brachiating along a rope in Frankfurt Zoo. Applying Peak5 Motion Analysis System for kinematic analysis, spatial positions and velocities of the tail tip (td), the proximal end of the prehensile pad (tp), and the base of the tail (ts) of each 40 off- and on-phases were analysed. The spatial marker positions showed that the tail is divided into a distal (td - tp) and a proximal functional segment (tp - ts). At the very beginning of the tail moving forward, tp formed a bending point, which initiated and guided the movement. Tp showed less excursions from the calculated straightest path towards the next tail-hold than td. The proximal segment remained close to the sagittal plane, whereas the distal segment frequently changed its orientation. The maximum velocity of tp appeared earlier than that of td, indicating a leading function of the tp. Our data suggest that the position of the tp in space and time is the important controlled variable. We discuss, how this might serve as a strategy in order to reduce the immense redundancy and thus to simplify motor control.

Interactions with Third Individuals and Post-conflict Reconciliation in Anubis Baboons (Papio anubis)

Natela V. Meishivili, Valery G. Chalyan, M.L.Butavskaya 

The characteristics of post-conflict bonding of participants in a conflict with a third animal were investigated in a captive group of anubis baboons (Papio anubis) in the Russian Primate Centre between 1999- 2001. In total, we observed post-conflict behaviour 364 times. Focal observations of aggressors and victims were made during the 5 minute post-conflict period and on the following day. The average reconciliation index (Veenema et al. 1994) was 27.3 for the group, 24.2 for males and 28.2 for females. The mean index of bonding of conflict participants to the third individual was -2.6 for the group, -11.6 for males and -0.4 for females. Some sex differences were found. The males mainly bonded with the third individual when it was a female. For female victims, the most preferable partners were males. As a whole, both males and females chose partners on the basis of the quality of their relationship with the third individual and also on the basis of its rank, but partners were not selected by their kinship.

Evaluation of Sex Skin Swelling Patterns in Female Barbary Macaques (Macaca sylvanus) During the Breeding Season

Ulrike Möhle, V. Reinberg, John Dittami, J. Keith Hodges 

The significance of prominent anogenital swellings (AS) in the strictly seasonally breeding Barbary macaques, Macaca sylvanus, is poorly understood. Since reliable data on AS characteristics in normally cycling females are not available, the aim of the present study was to establish a quantitative method for assessing AS in a free-ranging population of Barbary macaques in Gibraltar. Single frames were extracted from digital video sequences taken from the back and flank of 12 focal females and used to obtain accurate measurements of 4 parameters: width, height and depth of the circumanal region and width of the labia. Direct measurements of the callosities served as a reference measure. All parameters were significantly correlated; the product of AS width and height was used for the subsequent analysis. Females displayed clear seasonal fluctuations in AS size with an increase of 233% (median) from baseline to maximum levels. All individuals showed a total of 2 or 3 swelling cycles, including one post-conception cycle in those that became pregnant (n=10). Since in ovulatory cycles swelling size increased continuously without an obvious plateau, the maximum swelling period was defined as ³ 80% of the maximum AS value recorded. In all cases, ovulation, determined retrospectively by faecal progestin rise, occurred within this period. Conspicuous post-conception swellings were recorded in all pregnant females; the maximum swelling period occurred approximately 26 days after ovulation, with values reaching 79% (median) of those preceding conception. Studies are currently underway to characterise AS expression in relation to age, social and reproductive status and to examine its effects on social interactions and mating behaviour.

Ecological Pressures Driving Tool Use in Capuchin Monkeys

Antonio C. de A. Moura

Why do capuchin monkeys (Cebus spp.) in captivity use tools so frequently and their wild counterparts rarely show any tool-use? Some authors consider the frequent tool use in captive animals as a way to escape boredom. Some attribute the lack of tool use in wild monkeys to their lesser intelligence as compared to the great apes, which exhibit habitual use of tools in the wild. However, what was lacking were studies on capuchin monkey groups living in harsh environments, where the use of feeding tools could have direct implications for survival. I studied a group of C. apella libidinosus in the caatinga dry forest of NE Brazil over one year. In this area droughts are frequent, there is an extended dry season and annual rainfall is usually below 800mm. I recorded a total of 134 tool use events. This population of capuchin monkeys used tools regularly for probing and for cracking seeds and other materials. The most frequent and remarkable tool was a stone used to help dig up tubers/roots. The strong reliance on tool use for acquiring food resources is the key strategy allowing this population to survive in the harsh conditions of the caatinga. Interestingly, baboons live in areas that are harsher and rely heavily on underground plant organs for their staple food. Yet, use of feeding tools by baboons living in harsh environment has not been observed. Probably, this discrepancy can be related to differential selective pressures driving brain evolution in capuchin monkeys and Old World monkeys.
Supported by the Brazilian Research Council,: CNPq (student scholarship)

Mental Representation and Planning in the Tool Using Behaviour of Gorillas (Gorilla gorilla) and Orangutans (Pongo pygmaeus)

Nicholas J. Mulcahy, Josep Call, Robin I Dunbar

Two basic elements of problem solving involving tool use in primates are the use of mental representation to encode tool features and the ability to chain (i.e., plan in advance) discrete behaviours to achieve the goal. In this study, we investigated these two basic elements in the tool use of orangutans and gorillas. We used the stick and out-of-reach reward paradigm in which a subject had to use a tool to retrieve a reward on a platform. First, we addressed the mental representation issue by looking at whether subjects can encode the requirements that a tool should meet in terms of its length to be effective. We manipulated whether subjects were able to select tools of an appropriate length to reach the reward (that in some cases was not simultaneously visible) and whether subjects would refuse to use tools that were too short. Second, we studied the issue of mental planning by looking at whether subjects were able to choose the correct sequence of tools to reach the reward. In particular, whether they used a tool to retrieve another tool and whether, upon getting a tool, they could decide whether they needed a longer tool or they could directly reach the reward with the tool in their possession. The results showed that that subjects were able to encode and mentally compare tool length. Moreover, they also used tools in a sequence to get other tools that were appropriate to get the reward. These results show that both orangutans and gorillas can encode tool features such as length and can use tools in sequence to obtain a reward.

Agonistic Behaviours and Coalitions in an All-male Group of Western Lowland Gorillas (Gorilla g. gorilla) at Loro Park, Tenerife (Spain)

Marianne Nitsch, Carsten Niemitz

In captivity, western lowland gorillas (Gorilla g. gorilla) are frequently housed in one-male groups with several females and offspring. As a result of encouraging breeding, zoos nowadays face a "surplus" of males, mainly housed alone. Studies on wild mountain gorillas (Gorilla g. beringei) revealed that males may eventually join all-male groups. Thus, various zoos in Europe and North America started to house all-male groups of lowland gorillas. For the long-term successful management of such groups, it is important to understand the dynamics of the social behaviours (affiliative, agonistic behaviours) within these groups. So far, little has been published on the importance of coalitions in captive all-male groups. Here we present data focusing on the rate of agonistic behaviours and whether coalitions between individuals existed in an all-male group at Loro Park, Tenerife (N=6; 6-26 years). All occurrence sampling of all social behaviours and ad libitum sampling of agonistic interactions were carried out. The occurrences of agonistic behaviours ranged for all subjects from 0.6 to 8.2 events per hour, with the highest rates exhibited by two of the older blackbacks and the lowest rates by the silverback and the juveniles. The silverback received the majority of agonistic support from one of the blackbacks, thus avoiding serious, subsequent fights. Coalitions were seen mainly between the silverback and one of the blackbacks and among juveniles. Establishing coalitions and mutual support for individual group members showed that all-male groups apply similar mechanisms to coexist in captivity as has been observed among wild gorillas.

Cooperative Problem-solving Behaviour in Chimpanzees (Pan troglodytes)

Alicia Pérez Melis, Brian Hare, Michael Tomasello

The few studies that have investigated the cooperative problem-solving abilities of chimpanzees (e.g. Crawford 1937, 1941, Povinelli and O'Neill 1993, Chalmeau 1994, Chalmeau and Gallo 1996) have shown that their cooperative behaviour in an experimental set-up was far from spontaneous. Even in those experiments in which the task itself was an intuitive one, like pulling a rope attached to a baited box, human assistance was necessary to coordinate the subjects' actions on the box or several sessions were necessary before the animals learned to coordinate their behaviour with that of their partner. A possible explanation for these findings is that those tasks did not offer enough motivational incentives for cooperation to appear. In this study our main goal was to find a paradigm in which chimpanzees cooperated spontaneously, reliably and without training. Therefore, we tried to increase their social and non-social motivation to cooperate in an intuitive pulling-task. We increased the social motivation by using tolerant dyads as partners and making them compete against other dyads, thus adding a competitive incentive to the task. We increased the non-social motivation by using highly sharable food, so that both partners may profit from their efforts. Our hypothesis was that the social-competitive context would increase their tolerance level and motivation to work together in order to defeat the common enemy. We report first results of this project still in progress.

Simple Discrimination in the Great Apes

Dana Pfefferle, Josep Call

In the first half of the last century many studies were devoted to investigating the learning abilities of animals. Most work in this area was aimed at studying complex discrimination, such as learning set formation or cross-modal recognition. Comparatively little effort was devoted to the study of basic discrimination problems such as shape, colour and size discrimination. This lack of research is particularly notable in regard to species differences in these basic skills. In this study we investigated six orangutans, four bonobos, five gorillas and eight chimpanzees, housed at the Wolfgang Köhler Primate Centre in Leipzig Zoo. Each subject received a problem involving colour discrimination (blue vs. red), size discrimination (9 cm vs. 12 cm) and shape discrimination (house vs. tree). Problem presentation and the correct stimulus were counterbalanced across subjects. We found overall significant differences between species. Chimpanzees and bonobos got the highest scores while orangutans got the lowest. The gorillas' scores fell in between those of Pan and Pongo. Moreover, species differed in their ability to solve problems across different dimensions. For instance, chimpanzees performed significantly better in colour than in shape discrimination, while orangutans performed equally.

Sounds and Size - Identification of Variables that Reflect Body Size in Hamadryas Baboons

Dana Pfefferle, Julia Fischer

The acoustic structure of animal sounds may be influenced by a number of factors, such as the context or the motivational state of the caller. Due to the mechanisms of sound production, however, all sounds invariably transmit information about physical properties of the caller. In mammals, sound is produced by airflow generated in the lungs that drives oscillations of the vocal tract folds located in the larynx. The source signal then passes the vocal tract, which acts as a bandpass-filter allowing a narrow range of frequencies to pass ('formants'). Whereas the fundamental frequency is determined by the length and tension of the vocal folds, theory predicts that the location and spacing of the formants ('formant dispersion') is related to vocal tract length. Recent studies suggested that formant dispersion, but not fundamental frequency, serves as a reliable predictor of body size and weight. To test this assumption, we examined grunts recorded from captive hamadryas baboons (Papio hamadryas) in the German Primate Centre, Göttingen. We used linear predictive coding to extract the formants, and a spectrogram-based analysis to measure the fundamental frequency and a range of other variables related to the amplitude distribution in the spectrum. Our results show that - across and within age and sex classes - the fundamental frequency is more closely related to most physical measurements (including vocal tract length) than formant dispersion. Our findings indicate that depending on the call type, the fundamental frequency can serve as a reliable indicator of physical characteristics of the caller.

Choice Experiments Show Multi-sensorial Prey Detection in Grey Mouse Lemurs (Microcebus murinus) in the Laboratory

Marcus Piep, Björn M. Siemers, Ute Radespiel, Sabine Schmidt, Elke Zimmermann

Grey mouse lemurs (Microcebus murinus) feed mainly on fruit and arthropod prey. It has not been investigated, however, how the mouse lemurs find their prey. We therefore investigated the sensory basis of prey detection in six captive-born mouse lemurs at the Hannover colony. We aimed at pinpointing the sensory cues involved in the detection of arthropods. We used choice experiments to separate visual, olfactory and auditory information and to quantify their respective roles in prey detection. The lemurs were offered two similar dishes, one of which contained a mealworm. We covered the dishes with black plastic lids to exclude visual cues. Transparent lids were used as controls. To eliminate auditory cues, we presented freshly killed mealworms (with living mealworms rustling on a plastic sheet as the control condition). To exclude olfactory information, we sealed the mealworms in small air-tight plastic bags (non-sealed mealworms as controls). By combining these treatments, we offered the animals either one or two types of sensory information per task. The experiments were conducted in a sound attenuated chamber under dim red light. We scored the behavioral response of the mouse lemurs as removing the lid of the container with (correct) or without (wrong) mealworms or as inspection without decision to remove any of the lids (prey specific information not sufficient). Our results clearly show that the mouse lemurs used all three types of sensory information for prey detection. When only a single sensory modality was presented, the animals performed best with visual in comparison with auditory or olfactory information. Performance was increased when two types of sensory cues were available. We conclude that prey detection in these captive mouse lemurs is multi-sensorial with visual cues being of prevailing importance.

Sociosexual Behaviour Among Former Laboratory Chimpanzees (Pan troglodytes) During Resocialisation: A Comparison Between Hormone Implanted and Non-treated Females

Katharin Pieta, Signe Preuschoft 

Among apes, evidence for the communication role of sex ("communication sex", Wrangham 1993) comes mainly from bonobos. The three main contexts for this sociosexual behaviour are the development of social relationships, prevention of aggression in the face of potential conflict and reconciliation following aggression. Yet, sociosexual behaviour seems to occur also in chimpanzees and appears to be more common in captive than in wild chimpanzees. If communication sex does indeed function as conflict management it should be independent of the female's sexual cycle. We investigate the role of sexual interactions among former laboratory female chimpanzees (Pan troglodytes) that are currently being resocialized. Seven females are implanted with the contraceptive Implanon (active ingredient: etonogestrel), five others are not treated hormonally. All females are or will be grouped with at least one male. The males of the hormonally untreated females are vasectomized. We record all interactions involving contact with another chimpanzee's genitals and their context. Two hypotheses are tested: 1) In both groups, female-female as well as female-male sexual interactions become less frequent over the course of the resocialisation, since relationships consolidate. 2) In both groups of females, sexual signals do not become less frequent, however, they may change contexts, becoming less associated with relaxed socialising and more with social tension. Preliminary results show no significant difference in sociosexual behaviour among the implanted and non-implanted females. They also show that, throughout the development of the relationship, homosexual interactions among females remain associated with greeting after separation.

Hornbills Can Distinguish Between Primate Alarm Calls

Hugo J. Rainey, Klaus Zuberbühler, Peter J.B. Slater 

Some mammals discriminate between and respond appropriately to the alarm calls of other mammal and bird species. However, the ability of birds to distinguish between mammal alarm calls has not been investigated. Diana monkeys, Cercopithecus diana, produce different alarm calls to two predators: crowned eagles, Stephanoaetus coronatus, and leopards, Panthera pardus. Yellow-casqued hornbills, Ceratogymna elata, are vulnerable to predation by crowned eagles but are not preyed on by leopards and might therefore be expected to respond to the Diana monkey eagle call but not the leopard alarm call. We compared responses of hornbills to playback of eagle shrieks, leopard growls, Diana monkey eagle alarm calls and Diana monkey leopard alarm calls and found that they discriminate appropriately between the two predator vocalisations as well as between the two alarm calls of the Diana monkey, an ability previously undescribed for any bird species.

Diverging Annual Rhythms of Closely Related Nocturnal Primates: a Comparison of Golden Brown and Brown Mouse Lemurs

Blanchard Randrianambinina, Daniel Rakotondravony, Ute Radespiel, Elke Zimmermann 

Contrasting patterns of seasonal changes in the environment should be related to divergences in annual rhythms of small mammals in nature. We tested this hypothesis for the first time in small free-living nocturnal primates by comparing annual variations in activity, body mass and reproduction of the golden brown mouse lemur (Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar with those of its sister species, the brown mouse lemur (M. rufus), in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions, but with different seasonal constraints concerning ambient temperatures and potential food supply. We used data from radiotelemetry, focal observation and mark-recapture studies of two individually known populations. The golden brown mouse lemurs were active throughout the whole year irrespective of changing environmental conditions, whereas some brown mouse lemurs showed prolonged seasonal torpor related to body mass during short photoperiods and low ambient temperatures. Body mass and tail thickness (adipose tissue reserve) did not show differences between short and long photoperiods in M. ravelobensis, but differed significantly in M. rufus, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species exhibit seasonal reproduction with a photoperiodic control in males, but a more complex and species-specific pattern in females. Females of the golden brown mouse lemur cycled for at least four successive months, whereas in brown mouse lemurs this occurred in only one month, implying species-specificity in the control of reproduction. Our findings revealed the flexibility in reaction norms of closely related species within the same genus.
Supported by DAAD, DFG and VW.

Co-sleeping in Solitary Ranging Pairs: an Unusual Pattern of Sociality in the Nocturnal Milne-Edwards' Sportive Lemur (Lepilemur edwardsi) of North-western Madagascar

Solofonirina Rasoloharijaona, Berthe Rakotosamimanana, Blanchard Radrinamabinina, Elke Zimmermann 

Safe sleeping sites may be a limited resource crucial for survival. In order to investigate their potential significance for social organization in nocturnal primates, we investigated the spatial distribution of daily sleeping sites, their characteristics, their usage and sleeping group composition and dynamics in the nocturnal Milne-Edwards' sportive lemur during a six month field study in the dry deciduous forest of north-western Madagascar. Sexes did not differ either in body size or mass. Sleeping sites were almost exclusively used by adult male-female pairs. Individuals showed a high sleeping site fidelity limited to 2-3 different sleeping sites in close vicinity during the whole study period. Most females showed a higher fidelity to one distinct sleeping site than did their male partner. Sleeping groups consisted of one adult male and one adult female and remained stable in composition over the whole study period. Exclusive pair-specific usage of sleeping sites suggests sleeping site related territoriality of male-female pairs, perhaps influenced by inter- and intra-sexual resource competition. Our results give the first insights into the distribution patterns and social organization of this species. They imply dispersed monogamy, with sleeping sites as a potentially restricted and defendable resource.
Supported by DAAD and VW.

Feeding Regimes of Two Sympatric Mouse Lemurs in North-western Madagascar (Microcebus murinus and M. ravelobensis): No Clear Evidence for Niche Separation

Wiebke Reimann, Ute Radespiel, Elke Zimmermann

Ecological theory predicts that, in evolutionary time-scales, inter-specific competition leads to niche partitioning in resource utilisation to enable stable coexistence of sympatric species. To investigate this ecological hypothesis for nocturnal sympatric sibling species, we studied the feeding ecology of the grey (M. murinus) and the golden brown (M. ravelobensis) mouse lemur in the dry deciduous forest of Ampijoroa, northwestern Madagascar. Data were collected over a period of three months during the dry season, when food availability was expected to be low. Direct focal observations of 10 radio-collared females (6 M. murinus, 4 M. ravelobensis) during the whole night, feeding experiments and analyses of faecal samples were performed. The diet of both species was omnivorous and fairly similar in composition containing gums, secretions of homopteran larvae, fruits, nectar, small insects, spiders and vertebrates. No difference was found between the species in the time spent feeding on different items. Both species fed primarily on gum and insect secretions. Minor divergences occurred with regard to plant species used as food resource. While M. ravelobensis used a broad range of species, M. murinus seemed to be limited to only a few. Whether this inter-specific difference between the two sympatric species limits food competition and allows stable coexistence over time or if it is sign of an ongoing inter-specific competition which, in the long run, may lead to a population decline of one species, will be examined in the ongoing long-term project at Ampijoroa.

The Long Calls of Wild Male Orangutans : A Phylogenetic Approach

Marina Davila Ross, Thomas Geissmann, Elke Zimmermann

Although several genetic, molecular, and morphological studies have been carried out to clarify orangutan systematics, ongoing taxonomic controversies still exist. This project illustrates a new approach to orangutan phylogeny with a focus on their long calls. As shown by numerous studies, analyses of the species-specific loud calls of primates can help one to understand phylogenetic influences and to reconstruct taxonomy. Orangutan males produce long calls to regulate inter-male spacing and to attract mates. In this project, 64 variables (qualitative: n = 4; numerical: n = 26; metrical: n = 34) of 75 long calls from ten populations of wild orangutans (Borneo: n = 5; North Sumatra: n = 5) were analyzed. All of the four possibe geographically isolated Bornean groups were, thereby, represented. The results of the analyses neither support nor reject island bifurcation. Monophyletic groups were found for northwest Borneo (72-73%), east Borneo (73-85%) and Ketambe in Sumatra (74-78%). Although there are some inconsistencies that may be explained by further investigations of long calls, long call analysis is an appropriate way to study orangutan phylogeny. As proposed by the Orangutan Action Plan, this study indicates that, for conservation management purposes, the orangutans from geographically isolated areas should be dealt with separately. However, additional phylogeographic studies are needed so as to be certain of avoiding hybridization of orangutan taxa.

Personality as a Predictor for Stress Susceptibility and Stress Coping Mechanisms in Former Laboratory Chimpanzees (Pan troglodytes)

Michaela Reimers, Franz Schwarzenberger,Signe Preuschoft 

Twenty-five former laboratory chimpanzees (Pan troglodytes), maintained in groups, pairs or alone, were rated on non-social personality traits using four different test situations. Faecal samples were collected to extract the steroid hormones cortisol and testosterone. Levels of cortisol and testosterone are used as physiological measures of well-being. The chimpanzees were between 18 and 29 years old and have similar biographies. They have spent between 10 and 25 years under conditions of social and environmental deprivation and are now on their way to a social life in a zoo. We are quantitatively assessing the stress encountered by different individuals throughout this process of resocialisation and rehabilitation. While still in the old facility, the chimpanzees were presented with three novel objects (a toy, a coloured banana and a box). After relocation to the new primate house at Safaripark Gänserndorf, the chimpanzees were observed while they entered the new spacious and enriched indoor facilities for the first time. An individual's reaction to those situations reflects personality traits such as fearfulness, timidity, boldness and curiosity. We analysed latency to tackle the novel situation, total duration of exploration, method of investigation and vocalisation (fear, pleasure, excitement). Personality differences assessed in this way are used as predictors for the difference between baseline (laboratory) and relocation steroid levels. The stress levels of different individuals correlate with their personalities, their social skills and their success in developing relationships with conspecifics and vary depending on active or passive methods to deal with stressors.

A Study of the Facial Expressions in Pig-tailed Macaques (Macaca nemestrina)

Marco M. Rigamonti

Facial expressions in non-human primates are of great interest when studying communication, emotion, cognitive functions, lateralized behaviours and social relations. Complex methodological problems, however, must be faced if one tries to measure this behaviour finely. For this research we constructed an apparatus expressly designed to study facial expressions in pig-tailed macaques (Macaca nemestrina). We trained 20 subjects to climb into the apparatus in which rewards could be administered. Moreover pictures or movies could be presented on a computer monitor. A video camera was placed frontally at a short distance from the subject. A lighting system was built to light the face of the monkey uniformly. A second video camera was placed over the top to monitor the position of the subject with respect to the apparatus. Using this technique we recorded digital movies that were analysed frame by frame. Results were obtained for dynamic motor patterns of facial expressions and asymmetry of the face. Every element of the face (e.g.: eyebrows, lips, ears) was identified and analysed separately in several facial expressions. The role of each component varied in different situations and in different facial expressions. In addition, we obtained individual patterns of asymmetry in the face at rest.

Conflict Management Strategies of Aggressors in a Colony of Baboons (Papio hamadryas): Post-conflict Affiliation and Aggression and Time-sharing

Maite T. Romero-Benavente, Fernando Colmenares

Ethologists hold that behaviours that are associated in time (i.e., time-shared) are likely to share causal factors and that behaviours that are controlled by incompatible behavioural systems will tend not to co-occur. The objective of this study was twofold. First, we examined the rate at which aggressors engage in several post-conflict affiliative and aggressive interactions. Second, we explored the extent to which the various affiliative and aggressive behaviours exhibited by aggressors were time-shared. The data came from a study of conflict management and resolution carried out in a large, multi-harem colony of hamadryas baboons, Papio hamadryas, where aggressors were sampled for ten minutes following a conflict (PC samples) and then during a matched control observation (MC samples). Focal individuals were all adults and included 12 males and 23 females. We analysed the PC data from 653 agonistic conflicts in order to determine the frequency and level of time-sharing of three affiliative patterns, reconciliation (RC), consolation (CS) and triadic affiliation (TA), and two aggressive patterns, re-aggression (RA) and redirection (RD). Affiliation alone occurred much more often than aggression alone (69.8% vs 6.41%) and both time-shared in 23.7% of PCs. Within categories, TA alone occurred more often than CS alone and RC alone (58.1% vs 21.5% vs 20.3%), and RD alone was far more common than RA alone (79.5% vs 20.5%). The level of time-sharing between behaviours was higher within the affiliation category than across the two categories. The study of time-sharing between post-conflict behaviours across dyads, groups and species can throw new light on the nature and function of the strategies of conflict management and resolution.
Partly supported by a Studentship from the Universidad Complutense de Madrid to M. T. Romero-Benavente and project grants from MECyD (PB98-0773) and from MCyT (BSO2002-00161) to F. Colmenares.

Acoustical Analysis of the Cries in Chimpanzees (Pan troglodytes) and Humans (Homo sapiens)

Hartmut Rothgänger

Chimpanzees and humans have a rich repertoire of sounds which are used as bioacoustical signals during interaction of adults and children. In spite of very close relationship between chimpanzees and humans, there are just a few comparative acoustical researches on crying of both species. The aim of this study was to compare the voluminous material on human infant and adult cries with the cries of adult and young chimpanzees. We recorded 136 cries of seven adults and 29 cries of three infant chimpanzees in Berlin Zoo (Germany) and in Burgers´ Zoo (Netherlands). Human cries were collected from 25 infants (88 hunger cries, 93 pain cries) born without complications in the Clinics of Humboldt-University Berlin. Later, 306 cries of 17 mothers in labour were analysed. The acoustical analysis of chimpanzee cries revealed a mean fundamental frequency of 1.235 Hz with a mean length of 435 ms in adults and 1.512 Hz and 276 ms in infants. Human cries have a mean fundamental frequency of 472 Hz with a mean length of 583 ms in adults (female) and 463 Hz with 1.049 ms in new-borns. Both the human and chimpanzee cries are characterised as typical cries of mammals, with a high number of harmonics, rising-falling melodies and varied fundamental frequencies. On the other hand, both species exhibit typical characteristics. Although they have similar body weights, the pitch of their calls are very different. In this context, phylogenetic relationships between chimpanzees and humans will be discussed.

Comparison of the Acoustical Patterns of the Beg Sounds in the Infant and Adult Chimpanzees (Pan troglodytes)

Hartmut Rothgänger

Beg sounds were defined by Marler and Tenaza (1977) and by Goodall (1986) as whimpering or hoo-whimpering in the context of the begging that occurs in both infant and adult chimpanzees. Infants exhibit this sounds as a part of the mother-child behaviour in the time of the breaking up of the close connection with their mother. Whereas adults beg loudly to get food. Beg sounds are a series of sounds, their character becoming progressively either louder and higher or softer and lower, but there is little known about the temporal structure and the course of the fundamental frequency of the beg sound series in infants and adults. The aim of this study was to compare the beg sounds of infant and adult chimpanzees, using high resolution fundamental frequency analysis to gain insight in this topic (Lüdge and Gips 1989, Lüdge and Rothgänger 1990, Rothgänger 1999). The sounds of chimpanzees were recorded at Burgers´ Zoo, Arnhem. During the study, a sample of 170 cries of seven adults aged from 11 to 40 years and 220 cries of eight infants aged from zero to ten years was taken and analysed. Cries of both age groups consisted of short calls with a high modulated melody and constant pauses between series. The mean series contains 6.5 calls in the adults and 9 calls in the infants. Consequently the beg sounds of the different ages are similar in the temporal structure and the course of fundamental frequency, although they differ in their behavioural context.

Cytogenetic Arguments in Favour of the Specific Status of Propithecus tattersalli

Yves Rumpler, Nicole Andriaholinirina, Clément Rabarivola (3)

The taxonomic status of Propithecus tattersalli remains controversial, as on the basis of recent molecular data some authors propose that P. tattersalli should be considered as a subspecies of P. verreauxi. A previous cytogenetic study, performed with G-banding, was unable to supply decisive arguments to classify P. tattersalli as a species apart and to locate it on the chromosomal evolutionary tree of the Indriidae. A new cytogenetic study was done on skin biopsies, taken from 2 females during fieldwork conducted by a multidisciplinary team*. The data obtained show clearly that the R-banded karyotype of P. tattersalli differs from those of the other two Propithecus species, P. verreauxi and P. diadema, by 6 and 14 chromosomal rearrangements, respectively. The monobrachial homology between many large metacentric chromosomes allows one to predict the occurrence of meiotic chains involving at least 5 and 7 chromosomes, respectively, in hypothetical heterozygotes between P. tattersalli and the other two species. These meiotic configurations lead to sterility of the males, thus erecting an inter-specific barrier.
*The field-team was composed of the Galatée Team (Marc Cremades, Xavier Petter, Aude Mesnil, Yannick Clerquin) and C.R.

Do Sumatran Orangutans (Pongo abelii) and Yellow-cheeked Crested Gibbons (Nomascus gabriellae) Know What is Where?

Marina Scheumann, Josep Call

In natural habitats, animals have to solve many problems to find enough food. The food sources of orangutans and gibbons are distributed over a large area and available at different times during the year. so it would be advantageous for these apes to know which food type is where. We tested the spatial memory skills of a group of six captive Sumatran orangutans, Pongo abelii, and a yellow-cheeked crested gibbon, Nomascus gabriellae, at the Wolfgang-Köhler Primate Centre. In the first experiment, we hid kiwi pieces in ten different locations in the outdoor enclosure (1900m²) and placed 10 kiwi pieces in full view of the apes in an additional location. The gibbon and four of six orangutans approached the food locations significantly more often in the test condition than in the control condition in which no food was hidden. In the second experiment, we hid two types of food in different locations so that the animals had to remember which food type was where. The food type, which was hidden, was also presented on a visible location. There were three conditions. In the banana condition, bananas were hidden in 10 different trees. In the grape condition, grapes were hidden in 10 different bamboo shrubs. In the control condition, oranges were only left in the visible location to rule out the possibility that finding food may trigger searching food locations. All apes approached the banana locations more often in the banana than in the other two conditions. Three orangutans approached the grape locations more often in the grape than in the other two conditions. The results suggest that orangutans and gibbons can remember what is hidden where.

Sociability in Former Laboratory Chimpanzees (Pan troglodytes): Personality and Predictors of Successful Resocialisation

Elke Schüttler, Carsten Niemitz, Signe Preuschoft 

Lack of predictability makes introductions of unfamiliar chimpanzees risky, especially if the chimpanzees are socially inexperienced. The goal of this study was to improve predictability by identifying personality traits in chimpanzees and by using a stepwise introduction procedure. At Home of Primates Europe we staged dyadic introductions among eleven male chimpanzees, in which we gradually increased their chances to interact. We recorded social interactions in three situations: finger-tipping through double wire mesh (31 dyads), meeting at a gap in the interconnecting door (98 dyads), and first unrestricted encounters in the same cage (64 dyads). Behaviours were categorised into six social categories (van Hooff 1973): friendly, open-minded, little informative, cautious, unfriendly and non-social. To assess an individual's consistency across different partners and different situations we compared the rate of behaviours in each category. Moreover, caretakers completed questionnaires describing each chimpanzee's social behaviour towards themselves, prior to resocialisation. These we compared with the chimpanzee-chimpanzee interactions to assess how general and temporally stable the trait "sociability" is. We also compared dyads across the different situations to see whether interactions during the first, highly restricted encounter were predictive of the speed of relationship formation and the quality of the developing relationship. We found that prolonged visual contact may bore or frustrate chimpanzees if they cannot flexibly move on to more contact. Therefore, finger-tipping was of limited value to predict later encounters. However, individuals who were reluctant to interact during finger-tipping were still reluctant in the door gap situation and remained uncommunicative even when grouped with others.

Taxonomic Relationships in Lemuridae (Primates): a Morphological Approach Based on the Shape Quantification of the Skull in Superior View using Elliptical Fourier Analysis

M. Schmittbuhl, Herimalala Raveloson, J.M. Le Minor, Yves Rumpler

Lemur taxonomy continues to be widely debated as indicated by the abundance of systematic studies dedicated to Lemuridae. For the investigation of taxonomic relationships from morphological data, lemur skulls were particularly studied mostly using conventional linear measurements. From an osteological sample consisting of 166 lemur skulls (Eulemur: n=79; Hapalemur: n=36; Lemur: n=18; and Varecia: n=33), the shape of the outline of each skull in superior view was quantified using Elliptical Fourier analysis, and then compared by multivariate statistical approaches. An individual characterization of the cranial shape was obtained with great precision by using this approach. Differentiation between the four genera studied was obtained from the discriminant analysis of the Elliptical descriptors. The first discriminant plane contributed to separate significantly Hapalemur from the group Eulemur-Lemur-Varecia; the second discriminant plane allowed the differentiation between Eulemur and Lemur. The morphological differences between the genera studied were principally explained by the elongation of the whole skull (1st Fourier ellipse), the transversal development of the neurocranium (3rd Fourier ellipse) and the postorbital constriction (6th Fourier ellipse). Within Lemuridae, the morphological quantitative data of the present study suggest the relative homogeneity of the group Eulemur-Lemur-Varecia and, on the other hand, the individualisation of Hapalemur. This seems not to reflect genetic affinities so much, rather the functional specializations of Hapalemur, related to its particular dietary habits based on bamboo feeding.

Sensory Ecology of Prey Detection in Free-living Grey Mouse Lemurs (Microcebus murinus)

Björn M. Siemers, Marcus Piep, Jean-Baptiste Ramanamanjato, Jörg U. Ganzhorn 

On their nocturnal foraging excursions, grey mouse lemurs (Microcebus murinus) roam through the Malagasy forests in search of fruit and arthropod prey. Whereas fruiting trees might have a selective advantage by advertising the presence of ripe fruit to potential seed dispersers, arthropods will be inclined to conceal their whereabouts from potential predators. The foraging lemur is left with the problem of detecting and localizing its food in its three-dimensional, nocturnal forest environment. We investigated which type of sensory cues wild mouse lemurs use to find fruit and arthropods, respectively. In addition, we wanted to identify the cues used to classify food and to tell prey from potentially harmful animals such as snakes and scorpions. In south-eastern Madagascar we set up a series of behavioural experiments with freshly captured, experimentally naïve mouse lemurs. The animals' behaviour was video-taped under IR-illumination. To investigate the importance of auditory information, we recorded various rustling sounds of prey insects as well a snakes and scorpions and played them back to the mouse lemurs. We presented purely visual information to the lemurs by offering them plastic insects, scorpions and a plastic snake. Finally, we used choice experiments to investigate the role of olfactory cues. The lemurs were offered simultaneously two dishes covered with black plastic lids. One of the dishes contained a piece of banana or a dead insect, while the other was empty. In our experiments and behavioural observations we found that olfactory information is sufficient for the lemurs for finding fruit. Insect rustling sounds as acoustic cues are likewise sufficient to elicit prey capture behaviour. However, the animals responded only once or twice to acoustic prey dummies before they habituated to the playbacks. Visual prey dummies (plastic insects) were ignored by most of the mouse lemurs, as were plastic scorpions. The plastic snake, however, was attentively inspected from a distance for about 20 min, before some of the animals dared to touch it.

The Nigerian Chimpanzee (Pan troglodytes vellerosus) at Gashaka: Two years of Habituation Efforts

Volker Sommer, Andrew Fowler, Jeremiah Adanu 

Cross-population comparisons of chimpanzees can shed light on the pathways of hominid evolution. So far, no eco-ethological data exist for the recently recognized fourth subspecies Pan troglodytes vellerosus. We report from the first two years of a new long-term study from what is perhaps their last remaining stronghold: Gashaka-Gumti National Park, Nigeria. The mosaic habitat (woodland, lowland and gallery forest) receives 1826 mm rain per year, with 4-5 months being completely dry. Primates at Gashaka are not hunted and the chimpanzees are therefore relatively tolerant of human observers. We focused on the Gashaka-Kwano community, investing 3000 h of patrols. A total of 95 sightings were achieved which lasted for an average of 27 min (range 1-190 min). Party size averaged 3.7 animals (range 1-17) but was, similar to encounter length, susceptible to a wide range of methodological, social and ecological factors. The Kwano community comprises an estimated 35 members that occupy a home range of 26 km2. The area represents the West African equivalent of a chimpanzee site very similar to the forest-woodland-habitat in which early humans might have evolved.

Inter- and Intra-individual Variability in Duration of Sexual Swellings in Female Hamadryas Baboons

Daniel Stahl, Dietmar Zinner 

Characteristics of sexual swellings of female Old World monkeys and apes, such as size and colour, are believed to play an important role in female mating strategies. It was hypothesized that swellings indicate females' reproductive quality and that females use sexual swellings in intra-sexual competition for matings with certain "high quality" males. Alternatively, swellings were regarded as tools in the sexual conflict, e.g. females use sexual swellings to increase their degree of freedom during mate choice, to bias paternity to certain males and/or to confuse paternity, to reduce the risk of infanticide. Size is the most obvious character of a swelling and its relationships to female quality and male mate choice was recently investigated, but the results did not provide clear support for either hypothesis. Beside the geometrical dimensions of a swelling, its temporal dimension, i.e. duration, can be of importance. Females that are able to produce longer swellings may have an advantage in female-female competition or during the process of mate choice. We therefore analysed the relationship of swelling duration to individual and social factors, describing, for instance, the competitive regime and females' reproductive success. Records of swelling and the reproductive history of 19 hamadryas baboon females of the DPZ colony over 18 years constitute the database. In a General Linear Model approach including all adult females, we identified female individuality and number of swelling post partum as the most important factors explaining variability of swelling duration. Furthermore, swelling duration is longer in adult females compared to adolescent and senescent females. Factors related to female-female competition, such as sex ratio in one-male units of the whole colony or the number of synchronously swollen females, seem to have no impact on swelling duration.

Piagetian Conservation of Discrete and Continuous Quantities in Bonobos (Pan paniscus), Chimpanzees (Pan troglodytes) and Orangutans (Pongo pygmaeus)

Chikako Suda, Josep Call

Piagetian conservation refers to an ability to understand that objects' physical properties remain constant even when the objects change their appearance. This ability is considered to be a precursor for the formation of logical thinking in children. Previous studies revealed that conservation across different properties emerges at different points in human development. Children acquire the conservation of numbers prior to that of liquid quantities. It is hypothesized that discreteness in quantities (as in number conservation) helps subjects to understand the invariance of quantities (as in liquid conservation). In our study, bonobos, chimpanzees and orangutans received liquid and number conservation tasks. The appearance of edible rewards (either juice or cereals) was modified by changing the shape of the containers. Our results showed that all ape species were more likely to make a correct conservation judgment of discrete quantities than of continuous quantities, which is analogous to the results with human children.

Ranging and Roaming in Red Colobus Monkeys at Ngogo, Kibale National Park, Uganda

Simone Teelen

Red colobus monkeys (Procolobus badius) are the preferred prey species of chimpanzees wherever they co-occur. This is the case at Ngogo, Kibale National Park, where the intensity of chimpanzee predation is unusually high. Stanford (1995) has suggested that red colobus monkeys try to avoid chimpanzee predation by avoiding areas of high hunting pressure, and that peripheries or overlap areas between chimpanzee communities are refuges from predation because inter-group aggression between neighbouring chimpanzee communities makes these areas dangerous for chimpanzees, so they hunt less in them than in range centres. However, given the high intensity of predation at Ngogo compared to other chimpanzee study sites, peripheral areas may not function as refuges there. In this talk, I will discuss how chimpanzee predation influences the ranging behaviour of red colobus monkeys at Ngogo. In particular, I will compare red colobus day journey length, travel speed and group spread in overlap areas vs. non-overlap areas and in areas of high hunting pressure vs. areas of low hunting pressure. I will also discuss the influence of group size, inter-group conflicts, local primate density and diet on red colobus home range size and sub-grouping behaviour.

Do Great Apes Benefit from a Demonstrator in a Simple Social Learning Task?

Claudio Tennie, Josep Call, Michael Tomasello

In social learning, observers have potential access to several kinds of information. If, for example, observers see demonstrators cracking nuts, they could learn about: 1) performed actions (imitation): 2) resulting effects in the environment (emulation). We wanted to explore whether great apes that observed a demonstration (actions and results) would have advantages over apes that observed results only. Recent studies have suggested that marmosets and great apes do use action information (Bugnyar and Huber 1997; Whiten et al 1996), however these studies may have been confounded by mixing action and result information. In our study we separated the two types of information. We used a baited box as a manipulandum. In order to cancel out mere stimulus enhancement the box had a door installed that could be opened by either pushing or by pulling it. One group of apes saw conspecifics open this box, so that they received information on actions and results. Another group saw the box open "by itself", so that they had access to results information only. In neither condition, and for no ape species, could clear effects of demonstration be shown, so that our original question could not be answered. However, our findings highlight the importance of task-difficulty as a factor in social learning experiments because our task might have been too easy for the apes.

Insidious Numts - a Case Study of Great Apes

Olaf Thalmann, Juliane Hebler, Hendrik Poinar, Svante Pääbo and Linda Vigilant

In the last decades, the application of genetic analyses to infer the evolutionary history of primates has become of fundamental importance. In particular, the analysis of sequence variation in mitochondrial DNA (mtDNA) has allowed scientists to describe the phylogeny and phylogeography of many species. A disadvantage associated with the use of mtDNA is the danger of inadvertent amplification and analysis of Numts - nuclear insertions of mtDNA. In this study we directly examined whether published mtDNA control region (HV1) sequences from great apes are likely to represent authentic mtDNA or Numts. Sequences of HV1 segments of authentic mtDNA were obtained following a procedure designed to prohibit any amplification of Numts. Using the same sampled individuals and more commonly used methodology, Numt sequences similar to authentic mtDNA sequences were obtained from chimpanzees and gorillas, but not from humans, bonobos or orangutans. Our results imply that more rigorous methods than previously assumed are needed to ensure that only authentic mtDNA sequences are determined, and furthermore that accurate analysis of gorillas poses a considerable challenge.

Vocalisations Produced by Barbary Macaques that Monitor Triadic Encounters: Do Individuals Comment on What They See ?

Dietmar Todt, Henrik Brumm, Silke Kipper and Cord Riechelmann

A major portion of a primate's daily activity is filled by vigilance behaviours that, to a great extent, serve to collect socially relevant information. It has been hypothesized that individuals engaged in monitoring other group mates should concentrate predominantly on both detailed extraction and optimal processing of such information, and thus remain rather still and quiet. We have investigated this issue in two groups of Barbary macaques (Macaca sylvanus) living semi-free in an outdoor enclosure at Rocamadour (France). Remarkably enough, our study did not confirm the hypothesis, but, instead, we documented for the first time vocal displays that should be categorized as 'vocal comments'. This classification is justifiable because of the following properties: First, the vocalisations were mainly uttered by adults that monitored close-contact encounters among group mates, typically involving either an infant or a yearling. Second, there was evidence that the 'comments' were not addressed to the interacting individuals but to other adult group mates lingering in close proximity to the commentator. Finally, the structure of the signals co-varied with the agonistic quality of the monitored encounters. Our findings suggest that such comments signal an observer's social and perceptional competence as well as his or her reliable vigilance and may, at the same time, also stimulate the monitoring behaviour of other adults.

A Comparative Study of the Picture-making Activity of Three Ape Species: Pan troglodytes, Gorilla gorilla and Pongo pygmaeus

Marina Vancatova

The process of making scribbles is very similar in both apes and children up to the age of three. Chimpanzees, orangutans and gorillas modify tools and use these tools for different techniques of painting. Preliminary analysis of the pictures drawn by the apes illustrated that they react to different graphical symbols, the placing of these symbols on the paper, their orientation, character, form and combination with other symbols. Many graphic elements and combinations of elements are produced by the apes in their pictures. The size, form and orientation of the paper during the drawing activity also influence the results. Apes select part of the paper for their picture, either its centre, periphery or corners. The pictures drawn by the apes clearly illustrate features of elementary composition: balance of format, orientation of elements and their reciprocal harmony, and contrast with nearest neighbours in colour, size or character. Our results can be used to interpret how prehistoric human populations may have made their pictures.

A Puzzle Box Task Requiring Single and/or Double Actions by the Great Apes (Pan troglodytes, Pan paniscus, Gorilla gorilla gorilla and Pongo pygmaeus abelii)

Iris van der Eerden, Josep Call 

The history of ape cognition started with problem-solving tasks and was mainly focused on individual learning. Great apes are very skilful at manipulating objects in order to obtain food rewards. These manipulative skills can be observed in their natural food processing behaviour. However, less is known about the causal understanding underlying these manipulative abilities. The goal of this study was to investigate the level of causality understanding in a puzzle box task. We tested twelve chimpanzees, four bonobos, eight orangutans and six gorillas, housed at the Wolfgang Köhler Primate Research Centre, in Leipzig Zoo. A specially designed puzzle box, equipped with two levers, allowed the experimenter to present the subjects with different levels of manipulative complexity that increase in difficulty. The simple levels of complexity consisted of manipulating one of the two levers; in the more complex levels the manipulation of both levers was required either consecutively or simultaneously. Individuals of each species were divided into two groups, counterbalanced for age and sex. One group was offered an opaque version of the box and the other group a transparent version, so that the effects of their actions on the mechanism were visible. If subjects have some understanding of causality regarding the effect of their actions on the results, we would expect to see different response patterns between the transparent and the opaque group. We also expect to find species specific differences in the handling of the apparatus. The study is still in progress and we will report our preliminary data.

Dispersal and Relatedness in Wild Chimpanzees (Pan troglodytes)

Linda Vigilant, Dieter Lukas, Uta-Dorothee Immel, Vernon Reynolds and Christophe Boesch

Chimpanzee society has been described as male-bonded; that is, fundamentally characterized by kinship ties and cooperative behaviour among the community males. Such features have been taken as a reflection of high relatedness levels among males resulting from the pattern, unusual for mammals, of female rather than male dispersal. We genotyped the members of four habituated chimpanzee communities (3 western, 1 eastern) and estimated average relatedness among the adult males of each community. Our results indicated that average relatedness among adult males was rarely significantly higher than that among adult females of the same community. Similarly, average relatedness of males living within the same community was rarely higher than average relatedness of males compared between communities. We conducted simulations in order to understand the basis of these results, and found that low average relatedness among chimpanzee males is actually to be expected under a range of realistic demographic and reproductive skew situations. These results imply that relatedness, a prerequisite for kin-selected behaviour, is not generally high among chimpanzee males and therefore alternative explanations for cooperative male behaviour that focus on direct benefits to individuals deserve attention.

Inhibition in Great Apes: Performance on a Detour-reaching Task

Petra Vlamings, Jochen Barth, Josep Call

Until now there have been no studies that compare inhibitory control between the four great ape species. To investigate inhibitory control a new detour-reaching task was developed. In this detour-reaching task, subjects were presented with an opaque box with two transparent doors. Food was placed behind one of the doors. If the subject tried to reach for the food directly, the door pushed the food away. Subjects were able to retrieve the food only when they reached for it indirectly, through the other door. In this study four bonobos, 10 chimpanzees, six gorillas and seven orangutans were tested. Results showed that only the orangutans were able to solve the task. Within two sessions (10 trials each) all orangutans were reaching through the door behind which no food was placed. The bonobos, chimpanzees and gorillas on the other hand persevered with reaching for the food directly, thus loosing it in every trial. One possible explanation for these results is that orangutans, unlike the other apes, face less food competition and this may have translated into being less impulsive. Orangutans, in contrast to the other species of great apes, may have a better impulse or inhibitory control.

Use of Blood-sucking Bugs (Reduviidae, Heteroptera): A Minimally Invasive Method to Obtain Blood from Vertebrates for Endocrinological and Haematological Studies

Christian C. Voigt, Ruth Thomsen

To capture animals and to collect blood during anaesthesia is often difficult or even dangerous for the animals concerned. In the case of small mammals or birds, which have small vessel sizes, it may even be impossible to access blood without inducing vessel damage and haematomas. Recently, non-invasive techniques to measure steroid metabolites have become available in some vertebrate species, but due to considerable species differences in steroid metabolism one cannot predict which faecal metabolites may predominate and which antibody might work well in any one species. Our previous studies on some small sized mammals showed that bugs (Dipetalogaster maxima) from the subtropics can be used to obtain blood from veins that are difficult or even impossible for human experimenters to access. Here we summarize our current knowledge about this novel, minimally invasive method. To see whether there were differences between the blood collected from domestic rabbits (Oryctolagus cuniculus) with bugs compared to that collected using a conventional method, we undetook two experiments. In the first, for endocrinological studies, we compared concentrations of three steroid hormones (hydrocortisol, progesterone and testosterone). In the second, for veterinary studies, we compared haematological parameters. Overall, we could not find a significant difference in steroid hormone concentrations or haematological parameters between the two methods. Thus, we conclude that the use of tropical bugs presents a gentle and minimally invasive method to obtain blood at least for endocrinological and veterinary studies. Collecting blood by using bugs probably has great potential for use on many primate species.

Reproductive Skew in Male Rhesus Macaques: Causes and Consequences

Anja Widdig, Fred B. Bercovitch, Wolf Jürgen Streich, Peter Nürnberg, Michael Krawczak

When access to mates is monopolised by a small subset of individuals, the resulting conditions may be conducive to reproductive skew. Paternity studies in primates have revealed that reproduction is restricted to a limited number of males each year, but no in-depth analysis of primate reproductive skew has been published as yet. We measured the reproductive output in a group of male rhesus macaques, Macaca mulatta, from Cayo Santiago over six consecutive birth seasons in order to assess the magnitude of reproductive skew and to investigate its potential causes and consequences.

Olfactory Sensitivity for Androstenone in Three Species of Non-human Primates

Alexandra Wieser, Matthias Laska,Laura Teresa Hernandez Salazar

Social communication by means of odour signals is widespread among mammals. In pigs, for example, the C19-steroid 5-a-androst-16-en-3-one is secreted by the boar and induces the mating stance in the sow. In humans, the same substance has been shown to be a major compound of body odour and is presumed to affect human behaviour. Using a conditioning paradigm, we determined olfactory detection thresholds for androstenone in four pig-tailed macaques (Macaca nemestrina), four squirrel monkeys (Saimiri sciureus) and three spider monkeys (Ateles geoffroyi). We found that all three species of non-human primates were able to detect androstenone at concentrations lower than those reported in pigs and humans. Additional tests, using a habituation-dishabituation paradigm, showed that none of the ten animals tested per species was anosmic to this odorant. These results suggest that androstenone may be involved in olfactory communication in the non-human primate species tested and that the specific anosmia for this odorant found in ~30% of human subjects may be due to the reduced number of functional olfactory receptor genes in humans compared to non-human primates.

Linear Dominance Hierarchy Due to Contest Competition Among Female Chimpanzees (Pan troglodytes verus).

Roman M. Wittig, Christophe Boesch

The study of social relationships among female chimpanzees (Pan troglodytes) has been regularly neglected, since chimpanzees are usually referred to as male-bonded. This is largely due to the fact that dominance relationships have commonly been found to be ambiguous among female chimpanzees and linear hierarchies have not yet been detected. Following the idea of the socio-ecological model, a linear hierarchy among female chimpanzees is expected when they face contest competition over food. Indeed, at one study site more dominant females had a higher reproductive success. This is expected if high- ranking females can obtain access to the best foods, enabling them to invest more energy in reproduction. We investigated food competition and relationships among 11 adult female chimpanzees in the Taï National Park, Côte d'Ivoire (West Africa). Females faced contest competition over food. The contest competition increased when either the food was monopolisable or the number of competitors increased. We detected a formal linear hierarchy among the females based on greeting vocalisations, emitted by the subordinate towards the dominant female. Winning contests over food, but not the age of the chimpanzees, was related to dominance rank. Comparison among five different study sites revealed differences in the dominance relationships of female chimpanzees. It seems possible that these differences are affected by type of food competition and predation risk as well as observation time. However the comparison also supported the idea that Taï chimpanzees are bisexually-bonded.

A mtDNA Phylogeny of Papio

Dietmar Zinner, Andreas Hapke, Christian Roos, Hans Zischler

The phylogenetic relationships among members of the Old World monkey genus Papio are not clear and the taxonomic status of the various morphotypes is controversial. Five to nine morphologically distinct populations are recognized. Hybrid zones are confirmed for two population contact zones, but they are expected for almost all contact zones. We therefore inferred the phylogenetic relationships within the genus Papio from nucleotide sequences of the mitochondrial cytochrome b-gene (645 bp) and the hypervariable region I of the mitochondrial control region (340 bp) with special interest in the hamadryas-anubis relationships. We included samples from 11 regions in Africa and Arabia. DNA was extracted mainly from faecal samples and in a few cases from tissue of museum specimens. Maximum likelihood and maximum parsimony reconstructions revealed that phylogenetic relationships among Papio morphotypes are primarily explained by geography and only secondarily by morphological similarity. Eastern olive baboons (Ethiopia and Tanzania) form a clade with hamadryas baboons, while their western "conspecifics" (olive baboons from Nigeria, Ivory Coast) form a clade with Guinea baboons. This points to secondary reproductive contact of olive baboons with their western and eastern sister taxa. Implications of the results on the taxonomic status of Papio morphotypes and on species concepts will be discussed.