Predicting the Vulnerability of Great Apes to Disease: The Role of Superspreaders and Their Potential Vaccination

Disease is a major concern for the conservation of great apes, and one that is likely to become increasingly relevant as deforestation and the rise of ecotourism bring humans and apes into ever closer proximity. Consequently, it is imperative that preventative measures are explored to ensure that future epidemics do not wipe out the remaining populations of these animals. In this paper, social network analysis was used to investigate vulnerability to disease in a population of wild orang-utans and a community of wild chimpanzees. Potential ‘superspreaders’ of disease - individuals with disproportionately central positions in the community or population - were identified, and the efficacy of vaccinating these individuals assessed using simulations. Three resident female orang-utans were identified as potential superspreaders, and females and unflanged males were predicted to be more influential in disease spread than flanged males. By contrast, no superspreaders were identified in the chimpanzee network, although males were significantly more central than females. In both species, simulating the vaccination of the most central individuals in the network caused a greater reduction in potential disease pathways than removing random individuals, but this effect was considerably more pronounced for orang-utans. This suggests that targeted vaccinations would have a greater impact on reducing disease spread among orang-utans than chimpanzees. Overall, these results have important implications for orang-utan and chimpanzee conservation and highlight the role that certain individuals may play in the spread of disease and its prevention by vaccination.     

Dispersal Patterns of Orang-utans (<Emphasis Type="BoldItalic">Pongo</Emphasis> spp.) in a Bornean Peat-swamp Forest

Knowledge regarding dispersal patterns in great apes may help in understanding the evolution of dispersal patterns and social grouping in early hominoids, as well as in our own species. However, the social structure and dispersal system of orang-utans (Pongo spp.) remains little understood despite past research. We addressed this question by conducting genetic analyses on a wild orang-utan (Pongo pygmaeus wurmbii) population from the Sabangau peat-swamp in Borneo. We estimated pairwise relatedness among 16 adult individuals using 19 polymorphic microsatellite markers. Mean relatedness among females was significantly higher than in males, irrespective of the relatedness estimator used, following the pattern predicted for male dispersal. Our results support field observations that average dispersal distance for females is less than for males, suggesting that female orang-utans are philopatric, whereas males disperse. This contrasts with previous findings from other sites where anthropogenic influences were present. Based on qualitative mitochondrial DNA analyses, it appears that unflanged adult males show some degree of site fidelity compared to flanged males. Thus, male orang-utans may disperse permanently from their natal range once they are fully flanged. Male-biased dispersal and female philopatry in orang-utans differ from those of extant African apes and are more similar to many Old World monkey species. Hence we hypothesize that this system may represent the ancestral state of early hominoids.     

Breeding orangutans at Perth Zoo: Twenty years of appropriate husbandry

The Perth Zoo orang-utan husbandry strategy, which has been the foundation of 20 years of success in breeding, health, and longevity, is based on respect for the solitary arboreal nature of the species. The orang-utans are housed singly at night and fed only in their night dens. Diets are based on the weight and energy expenditure of the individuals. During the day they are housed singly or in very small groups that correspond in size and structure to wild population units. Adult males and females are only introduced for breeding purposes. Large climbing frames, which permit visual and vocal contact, dominate the day enclosures. A wide variety of manipulable objects are provided daily to enhance activity levels. Since 1968 there have been 21 births, 14 surviving infants, and no post-infancy deaths. All the mature animals are fertile. The major health problems of captive orang-utans and the most common causes of adult mortality have been absent from the colony. The husbandry method used has made it possible to record detailed reproductive data including complete menstrual cycle records for 8 females since 1981, the observation and quantification of cyclic proceptivity for all mature females, the calculation of 19 gestation periods, and the measurement of post-partum amenorrhea and interbirth intervals. Urinary hormone analysis is used regularly to confirm ovulation. A long-term study of the hormones mediating the development of secondary sexual characteristics in males was started in 1988. Captive orang-utans do not have a fertility problem, but the captive population is threatened by the unacceptably high mortality rate in young adults. This appears to be related to inappropriate husbandry methods. The most neglected aspect of orang-utan husbandry is natural social group size and structure.     

Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve,southwest Madagascar (1992-2001)

Gene flow within and between social groups is contingent on behaviourally mediated patterns of mating and dispersal. To understand how these patterns affect the genetic structure of primate populations, long-term data are required. In this study, we analyse 10 years of demographic and genetic data from a wild lemur population (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar. Our goal is to specify how patterns of mating and dispersal determine kinship and genetic diversity among animals in the population. Specifically, we use microsatellite, parentage, and census data to obtain estimates of genetic subdivision (FST), within group homozygosity (FIS), and relatedness (r) within and among social groups in the population. We analyse different classes of individuals (i.e. adults, offspring, males, females) separately in order to discern which classes most strongly influence aspects of population structure. Microsatellite data reveal that, across years, offspring are consistently more heterozygous than expected within social groups (FIS mean = -0.068) while adults show both positive and negative deviations from expected genotypic frequencies within groups (FIS mean = 0.003). Offspring cohorts are more genetically subdivided than adults (FST mean = 0.108 vs. 0.052) and adult females are more genetically subdivided than adult males (FST mean = 0.098 vs. 0.046). As the proportion of females in social groups increases, the proportion of offspring sired by resident males decreases. Offspring are characterized by a heterozygote excess as resident males (vs. nonresident males) sire the majority of offspring within groups. We link these genetic data to patterns of female philopatry, male dispersal, exogamy, and offspring sex-ratio. Overall, these data reveal how mating and dispersal tactics influence the genetic population structure in this species.     

Movement and reproductive behavior of solitary male redtail guenons (Cercopithecus ascanius)

Adult male redtail guenons (Cercopithecus ascanius) live as resident males in heterosexual groups or as nonresident males outside groups. Data are reported here on movement and temporary intrusions by nonresident males in heterosexual groups. These data further elucidate the reproductive strategies of this class of individual. Observations of three radiocollared males provided data on the details of their movement relative to groups. Regular sampling of three heterosexual groups provided data on patterns of nonresident males' intrusions. During peak mating months, nonresident males formed loose affiliations with groups. The males affiliated with one group at a time, with each affiliation lasting several weeks. Nonresident male intrusions in groups were unevenly distributed and were not correlated with the number of potentially fertile females in each group. Estimates of male density indicate that there were about two nonresident males per group, which suggests an adult sex ratio of three females per male within the study area. Nonresident male redtail guenons apparently do not spread their reproductive efforts over several groups at once, but instead each male tends to direct his attention toward the group offering the best opportunity for reproductive payoffs. Factors that determine which groups they attempt to infiltrate may include the characteristics of resident males, female choice, or both, but the number of fertile females probably has no effect. The male low density and female-biased sex ratio among adults should facilitate resident males' attempts to monopolize fertilizations in groups; however, resident males were unable to prevent copulations by nonresident males even when only one nonresident was intruding in a group.     

The social organisation of a population of Sumatran orang-utans

Female orang-utans in a Sumatran swamp forest live in large, but stable, and widely overlapping home ranges. They preferentially associate with some of their female neighbours, possibly relatives, to form socially distinct clusters that also experience reproductive synchrony. Sexually mature males range more widely than females, but among them the dominant adult male has a relatively more limited range. His ranging and that of the subadult males reflect the local abundance of sexually attractive females. The other adult males tend to avoid these concentrations and focus on areas away from the dominant male. Females show philopatric tendencies. Male-biased sex ratios at birth give way to heavily female-biased sex ratios among adults. This suggests a net loss of males as they mature, due either to excess male mortality (e.g. by male mating competition), excess male dispersal from the population or a combination of both. We conclude that the orang-utan social organisation is best described as a loose community, showing neither spatial nor social exclusivity, consisting of one or more female clusters and the adult male they all prefer as mate.     

Interactions between a wild Bornean orang-utan and a Philippine slow loris in a peat-swamp forest

All documented orang-utan–loris interactions have been from Sumatra, where lorises were opportunistically preyed upon by orang-utans. In this paper, we describe two accounts of the Bornean orang-utan (Pongo pygmaeus wurmbii) interacting with the Philippine slow loris (Nycticebus menagensis). The interactions were by two adolescent female orang-utans. No attempts to catch the loris were observed on either occasion. Neither interaction was hostile. During the second observation, which was more detailed, we considered the behaviour to be play rather than aggression or attempted predation. Based upon the lack of interest from the adult females during these rare encounters, we propose that the behaviour represents play or non-aggressive exploration rather than predation.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus): I. Univariate analyses

Based on a homogeneous sample of 212 individuals spanning all postnatal age periods, we examine the ontogeny of cranial sexual dimorphism in Bornean orang-utans (Pongo pygmaeus pygmaeus) by means of univariate statistics. A distinct pattern emerges at the early juvenile stage and continues at all subsequent stages with males tending to exceed females in all cranial dimensions. In conjunction, starting at mid-juvenile stage, there is a strong tendency for an increase in number and strength of significant cranial sex differences, all of them in favor of males. Significant sex differences in the viscerocranium, reflecting stronger prognathism in males, emerge prior to those in the neurocranium. The total ontogenetic pattern of cranial sexual dimorphism in orang-utans is remarkably similar to that of gorillas, except that there is no evidence of a sex difference in timing of the adolescent growth spurt in the orang-utan. As for other catarrhine species (Wood 1976), male variance of cranial dimensions tends to be greater than that of females, thus lending support to Leutenegger & Cheverud's (1982, 1985) model on the evolution of character dimorphism by means of variance dimorphism.     

Genetic and selective factors in reduction of the hallux in Pongo pygmaeus

Extreme reduction of the hallux is unique to the orang-utan (Pongo pygmaeus) among Primates. Hallucal diminution has advanced so far that 60% of orang-utans lack both distal phalanges and nails. Absence of these structures occurs significantly more often in females than in males. Hypotheses on possible genetic control of the condition have been tested and indicate that either single gene inheritance or polygenic inheritance with variable expressivity is involved. Reduction of pollex and of hallux in Pongo have advanced with selection for a specialized four-digit grasp in hands and feet. Diminution has progressed farther in the great toe than in the thumb due to selection for fine manipulation in the latter digit.     

Happy orang-utans live longer lives

Nonhuman primate ageing resembles its human counterpart. Moreover, ratings of subjective well-being traits in chimpanzees, orang-utans and rhesus macaques are similar to those of humans: they are intercorrelated, heritable, and phenotypically and genetically related to personality. We examined whether, as in humans, orang-utan subjective well-being was related to longer life. The sample included 184 zoo-housed orang-utans followed up for approximately 7 years. Age, sex, species and number of transfers were available for all subjects and 172 subjects were rated on at least one item of a subjective well-being scale. Of the 31 orang-utans that died, 25 died a mean of 3.4 years after being rated. Even in a model that included, and therefore, statistically adjusted for, sex, age, species and transfers, orang-utans rated as being "happier" lived longer. The risk differential between orang-utans that were one standard deviation above and one standard deviation below baseline in subjective well-being was comparable with approximately 11 years in age. This finding suggests that impressions of the subjective well-being of captive great apes are valid indicators of their welfare and longevity.     

Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus)

Philopatry and sex-biased dispersal have a strong influence on population genetic structure, so the study of species dispersal patterns and evolutionary mechanisms shaping them are of great interest. Particularly nongregarious mammalian species present an underexplored field of study: despite their lower levels of sociality compared to group-living species, interactions among individuals do occur, providing opportunities for cryptic kin selection. Among the least gregarious primates are orang-utans (genus: Pongo), in which preferential associations among females have nevertheless been observed, but for which the presence of kin structures was so far unresolved because of the equivocal results of previous genetic studies. To clarify relatedness and dispersal patterns in orang-utans, we examined the largest longitudinal set of individuals with combined genetic, spatial and behavioural data. We found that males had significantly higher mitochondrial DNA (mtDNA) variation and more unique haplotypes, thus underscoring their different maternal ancestries compared to females. Moreover, pedigree reconstruction based on 24 highly polymorphic microsatellite markers and mtDNA haplotypes demonstrated the presence of three matrilineal clusters of generally highly related females with substantially overlapping ranges. In orang-utans and possibly other nongregarious species, comparing average biparental relatedness (r) of males and females to infer sex-biased dispersal is extremely problematic. This is because the opportunistic sampling regime frequently employed in nongregarious species, combined with overlapping space use of distinct matrilineal clusters, leads to a strong downward bias when mtDNA lineage membership is ignored. Thus, in nongregarious species, correct inferences of dispersal can only be achieved by combining several genetic approaches with detailed spatial information.     

On secondary hyperparathyroidism in orang-utans, Pongo satyrus (Linnaeus, 1758)

Orang-utan crania with alterations in bone structure which could be determined morphologically were studied and evaluated. The alterations in bone structure were referred to in the literature up to about 1939 as "rickets"; when vitamin D was given to the animals, the alterations diminished, until they were almost unnoticeable. From about 1941/52, the alterations were diagnosed as "Morbus Paget". Research on orang-utan crania has become possible through comparison of a larger number of single symptoms, occurring in a number of individuals. Out of a larger sample, the study was carried out on 5 individuals, showing these alterations in varying degrees. The individuals also covered various age groups, both sexes and both subspecies of orang-utans. The findings permit a diagnosis of secondary (or tertiary) hyperparathyroidism (= Morbus Engel-von Recklinghausen = fibrous cystic osteitis). The study also showed that orang-utans fall prey to Morbus Engel-von Recklinghausen in a shorter period and suffer more severely than humans. The frequency of orang-utans suffering from this disease, which are kept captive in zoos, is statistically far higher than the occurrence in humans. Orang-utans living under natural conditions do not suffer from the disease at all; according to the study of 500 animals. The authors also believe that there is a psychogenic basis for the occurrence of Morbus Engel-von Recklinghausen in zoo animals; psychological conditions such as apathy, disinterest, etc. are part of the illness, and these symptoms are also shown by animals having no outward signs of fibrous cystic osteitis. The authors believe that improved prophylaxis of orang-utans in zoos would lead to discovery of Morbus Engel-von Recklinghausen in early stages, and allow early therapy to arrest the disease. This is necessary for preservation of the species.     

The behaviour and ecology of wild orang-utans (Pongo pygmaeus)

Between June 1968 and November 1971, 21 months of fieldwork were spent studying wild populations of orang-utans in Borneo and Sumatra. Fifteen hundred hours of daylight observation were made on these animals. In contrast to other higher primates, the dispersed distribution of food and the orang-utan's slow mode of travel seem to favour solitary habits. Over, 80 per cent of foraging units seen contined only one independent animal, either alone or with dependent young. Larger groupings were seen when adolescents joined up with other animals or when males and females formed temporary consortships for mating purposes. Comparison between several populations revealed an interesting mechanisms for the natural regulation of animal numbers. Differences between Bornean and Sumatran orang-utans are discussed in relation to the zoogeography of these two islands.     

Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Bottlenose dolphins are one of only a few mammalian taxa where the males are known to cooperate within their social group in order to maintain mating access to single females against other males. Male bonds in bottlenose dolphins have been hypothesized as evolving through kinship and associated inclusive fitness effects. In this study we tested whether individually identified male bottlenose dolphins preferentially associate and form alliances with kin in a small coastal resident population of southeastern Australia using a combination of behavioural data, genetic sexing, sequences of the mitochondrial DNA control region and nuclear microsatellite markers. Males generally associated significantly more often than expected with one to three other males, with whom they jointly herded females for mating. Associations and alliance membership were not associated with either maternal kinship or genetic relatedness. The majority of male pairs within alliances were randomly related, although high relatedness values were found between males of different alliances in the resident population. These findings indicate that mechanisms other than kin selection may be foremost in the development and maintenance of cooperation between male bottlenose dolphins.     

Maternal grouping as a defense against infanticide by males: evidence from field playback experiments on African lions

Female lions roar in order to stay in contact with their pridematesand to defend their territory against other prides. In doingso, however, they risk attracting die attention of potentiallyinfanticidal nonresident males. We used playback experimentsto demonstrate that nonresident males are indeed specificallyattracted to female roars, approaching the roars of female,but not male, conspecifics. However, diere was also evidencediat males adjust their behavior according to the probabilitythat they might execute a successful takeover. Alien male lionswere more reluctant to approach playbacks of three females roaringdian of a single female roaring; single males were more reluctantdian pairs to approach female roars; and old males were morereluctant than younger males to approach female roars. Previousobservational studies have shown diat female lions living ingroups are more successful than singletons at defending theircubs in direct interactions widi potentially infanticidal males.Our results suggest that maternal groups may also, by roaringin chorus, minimize the chances that diese encounters occurat all.     

Linear roadside remnants: Their influence on den‐use,home range and mating system in bobucks (Trichosurus cunninghami)

Abstract Forest clearance results in a marked change in the dispersion of resources such as food and shelter: from a relatively continuous distribution, to patches and strips of remnant habitat set in a more or less inhospitable matrix. Such changes in the patterns of resource dispersion have the potential to strongly influence the dynamics of social and mating systems of resident animal populations. We studied the den‐use patterns, home range characteristics and mating system of a population of bobucks, Trichosurus cunninghami (Marsupialia: Phalangeridae), permanently resident in linear roadside strips of vegetation in north‐eastern Victoria, Australia in order to gain a greater understanding of the impacts of occupying linear roadside habitats on the behavioural ecology of arboreal marsupials. We radio‐tracked 11 adult females and six adult males and collected 2126 diurnal fixes (mean 125/individual) and 1044 nocturnal fixes (mean 61/individual). Males used significantly more den‐trees (mean 16.5 ± 1.5 den‐trees/individual) than females (mean 7.4 ± 0.6 den‐trees/individual) and had home ranges more than twice the size of those of females (male mean 5.1 ± 0.8 ha, female mean 2.1 ± 0.3 ha). On average, each male's home range overlapped with those of three females; there was little intrasexual home range overlap in either sex. Genetic parentage analysis of all young sampled during the study (n = 22) established that only males that overlapped in home range with females had sired those females' young. All but one male in the study sired multiple young in each of the years they were recorded breeding. These behavioural and genetic data indicate that the roadside population was polygynous, in contrast to the socially monogamous bobuck population we studied in a neighbouring forest patch. These differences in behaviour may reflect patterns of resource distribution in the two habitats.     

Effective Population Size Dynamics and the Demographic Collapse of Bornean Orang-Utans

Bornean orang-utans experienced a major demographic decline and local extirpations during the Pleistocene and Holocene due to climate change, the arrival of modern humans, of farmers and recent commercially-driven habitat loss and fragmentation. The recent loss of habitat and its dramatic fragmentation has affected the patterns of genetic variability and differentiation among the remaining populations and increased the extinction risk of the most isolated ones. However, the contribution of recent demographic events to such genetic patterns is still not fully clear. Indeed, it can be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric demographic events. Here, we investigated the genetic structure and population size dynamics of orang-utans from different sites. Altogether 126 individuals were analyzed and a full-likelihood Bayesian approach was applied. All sites exhibited clear signals of population decline. Population structure is known to generate spurious bottleneck signals and we found that it does indeed contribute to the signals observed. However, population structure alone does not easily explain the observed patterns. The dating of the population decline varied across sites but was always within the 200–2000 years period. This suggests that in some sites at least, orang-utan populations were affected by demographic events that started before the recent anthropogenic effects that occurred in Borneo. These results do not mean that the recent forest exploitation did not leave its genetic mark on orang-utans but suggests that the genetic pool of orang-utans is also impacted by more ancient events. While we cannot identify the main cause for this decline, our results suggests that the decline may be related to the arrival of the first farmers or climatic events, and that more theoretical work is needed to understand how multiple demographic events impact the genome of species and how we can assess their relative contributions.     

Male bimaturism and reproductive success in Sumatran orang-utans

Although orang-utans live solitary lives most of the time, theyhave a complex social structure and are characterized by extremesexual dimorphism. However, whereas some adult male orang-utansdevelop full secondary sexual characteristics, such as cheekflanges, others may stay in an "arrested" unflanged conditionfor up to 20 years after reaching sexual maturity. The resultis a marked bimaturism among adult males. Flanged males allowfemales to overlap with their home range and often toleratethe presence of unflanged males. However, wherever possibleflanged males actively prevent unflanged males from copulatingwith females. Two competing hypotheses, previously untested,have been advanced to explain male reproductive behavior andbimaturism in orang-utans: (1) the "range-guardian" hypothesis,which asserts that the flanged males are postreproductive anddefend a range in which they tolerate sexually active, unflangedmale relatives; and (2) the "female choice" hypothesis, whichasserts that flanged males tolerate unflanged males in their range because they rely on female preference to favor flangedmales. We investigated these hypotheses and a third hypothesisthat the two male morphs represent co-existing alternativemale reproductive strategies ("sitting, calling, and waiting"for flanged males versus "going, searching, and finding" forunflanged males). Fecal samples were collected from a well-studiedpopulation in Indonesia, and eight human microsatellites wereanalyzed for 30 individuals that have been behaviorally monitoredfor up to 27 years. By carrying out paternity analysis on 11offspring born over 15 years, we found that unflanged malesfathered about half (6) of the offspring. Relatedness betweensuccessful unflanged males and resident dominant males wassignificantly lower than 0.5, and for some unflanged/flangedmale pairs, relatedness values were negative, indicating thatunflanged males are not offspring of the flanged males.     

Cyclic proceptivity in a captive female orang-utan (Pongo Pygmaeus Abelii)

An adult male—female pair of orang-utans was observed for a 3-month period, commencing with the introduction of the animals to each other. After approximately 2 weeks, the female began to show proceptive behaviors towards the male. Two other proceptive periods were observed, occuring from 26 to 30 days apart, and lasting for 4–6 days. These female-initiated periods of sexual activity began with increased locomotor activity, solitary play, proximity to the male, following the male, and social grooming. The peak periods of proceptive behaviour included hand—genital contact, mouth—genital contact, rolling the male onto his back, both dorso-ventral and ventro-ventral mounting, and pelvic thrusting. Although hormonal levels could not be assessed in this study, it is believed that these peaks coincided with ovulation. In previous reports, the presence of proceptive behaviors was perhaps over-shadowed by highly aggressive sexual behavior on the part of male orang-utans. The visibility of proceptivity in this study is attributed to the large cage which allowed the female to escape the male's advances, enabled distance between the animals when they preferred it, and continuous exposure of the orangs to each other. This female orang-utan behavior was compared to the female sexual behaviours of the other great ape species — the chimpanzee and the gorilla.