Title: The socioecology of parasite infection in wild Bornean orangutans (Pongo pygmaeus wurmbii) in Gunung Palung National Park, West Kalimantan, Indonesia
The socioecological model predicts that food availability and risk of parasite transmission influence sociality in primates. As a semi-solitary ape inhabiting the masting forests of Southeast Asia, orangutans provide a unique opportunity to compare social and non-social periods and highly variable foraging conditions within one population. This study compared two data collection periods when fruit availability differed markedly to determine whether sociality and parasite prevalence decrease as expected during periods of fruit scarcity. Fecal samples were analyzed using direct smear and fecal concentration techniques on-site at Cabang Panti Research Station from 2013-2014 and 2018-2019. From the high fruit period to the low fruit period, sociality decreased from 54% of focal follows containing a social event to 29%, while overall parasite prevalence remained the same at 100%. Interesting differences arose for certain parasite species, however. Enterobius sp. prevalence decreased during the low fruit period for both sexes but even more so for males (50% to 29% for females; 56% to 0 for males). Prevalence of Trichuris sp. increased for females during the low fruit period (5% to 43%) while prevalence among males remained the same. These results lend support to the prediction that social contact influences transmission risk for some parasite species, while other parasites may be more responsive to factors such as changes in reproductive state. These findings suggest that differences in the behavioral strategies of the sexes and the differential energetic demands of life history stages have an influence on parasitic infection patterns. more »« less
O’Connell, Caitlin A.; DiGiorgio, Andrea L.; Ugarte, Alexa D.; Brittain, Rebecca S.; Naumenko, Daniel J.; Utami Atmoko, Sri Suci; Vogel, Erin R.
(, Scientific Reports)
null
(Ed.)
Abstract Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms. Fruit-dependent Bornean orangutans face extreme variation in fruit availability and experience negative energy and protein balance during episodes of fruit scarcity. We evaluate the possibility that orangutans of different sexes and ages catabolize muscle tissue when the availability of fruit is low. We assess variation in muscle mass by examining the relationship between urinary creatinine and specific gravity and use the residuals as a non-invasive measure of estimated lean body mass (ELBM). Despite orangutans having a suite of adaptations to buffer them from fruit scarcity and associated caloric deficits, ELBM was lower during low fruit periods in all age-sex classes. As predicted, adult male orangutans had higher ELBM than adult females and immatures. Contrary to expectation, flanged and unflanged males did not differ significantly in ELBM. These findings highlight the precarity of orangutan health in the face of rapid environmental change and add to a growing body of evidence that orangutans are characterized by unique metabolic traits shaped by their unpredictable forest environment.
Sabbi, Kris H.; Emery Thompson, Melissa; Machanda, Zarin P.; Otali, Emily; Wrangham, Richard W.; Muller, Martin N.
(, Proceedings of the National Academy of Sciences)
null
(Ed.)
Sex differences in physical aggression occur across human cultures and are thought to be influenced by active sex role reinforcement. However, sex differences in aggression also exist in our close evolutionary relatives, chimpanzees, who do not engage in active teaching, but do exhibit long juvenile periods and complex social systems that allow differential experience to shape behavior. Here we ask whether early life exposure to aggression is sexually dimorphic in wild chimpanzees and, if so, whether other aspects of early sociality contribute to this difference. Using 13 y of all-occurrence aggression data collected from the Kanyawara community of chimpanzees (2005 to 2017), we determined that young male chimpanzees were victims of aggression more often than females by between 4 and 5 (i.e., early in juvenility). Combining long-term aggression data with data from a targeted study of social development (2015 to 2017), we found that two potential risk factors for aggression—time spent near adult males and time spent away from mothers—did not differ between young males and females. Instead, the major risk factor for receiving aggression was the amount of aggression that young chimpanzees displayed, which was higher for males than females throughout the juvenile period. In multivariate models, sex did not mediate this relationship, suggesting that other chimpanzees did not target young males specifically, but instead responded to individual behavior that differed by sex. Thus, social experience differed by sex even in the absence of explicit gender socialization, but experiential differences were shaped by early-emerging sex differences in behavior.
Abstract Direct pathogen and parasite transmission is fundamentally driven by a population’s contact network structure and its demographic composition and is further modulated by pathogen life-history traits. Importantly, populations are most often concurrently exposed to a suite of pathogens, which is rarely investigated, because contact networks are typically inferred from spatial proximity only. Here, we use 5 years of detailed observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) that distinguish between four different types of social contact. We investigate how demography (sex and age) affects these different social behaviors. Three of the four social behaviors can be used as a proxy for understanding key routes of direct pathogen transmission (sexual contact, skin contact, and aerosol contact of respiratory vapor above the water surface). We quantify the demography-dependent network connectedness, representing the risk of exposure associated with the three pathogen transmission routes, and quantify coexposure risks and relate them to individual sociability. Our results suggest demography-driven disease risk in bottlenose dolphins, with males at greater risk than females, and transmission route-dependent implications for different age classes. We hypothesize that male alliance formation and the divergent reproductive strategies in males and females drive the demography-dependent connectedness and, hence, exposure risk to pathogens. Our study provides evidence for the risk of coexposure to pathogens transmitted along different transmission routes and that they relate to individual sociability. Hence, our results highlight the importance of a multibehavioral approach for a more complete understanding of the overall pathogen transmission risk in animal populations, as well as the cumulative costs of sociality.
Our lab previously established that repeated exposure to a bitter diet can increase salivary protein (SP) expression, which corresponds to an increase in acceptance of the bitter stimulus. However, this work was exclusively in male rodents, here we examine sex differences. We found that there are no differences in SP expression (experiment 1) or quinine diet acceptance (experiment 2) across stage of estrous cycle. Yet, males and females differ in feeding behaviors, SP expression, and responses to a quinine diet (experiment 3). On a quinine diet, males accepted the diet much faster than females. Males displayed a compensatory increase in meal number as meal size and rate of feeding decreased with initial exposure to a quinine diet, whereas females decreased meal size and rate of feeding with no compensation in meal number. There were sex differences in SP expression at day 14 of quinine exposure but these were gone by day 24. Both sexes increased acceptance of quinine in a brief access taste test after the feeding trial concluded. These data suggest that males and females have different patterns of bitter diet acceptance, but extended exposure to quinine diet still results in altered bitter taste responding and changes in SP profiles in females.
Thompson González, Nicole; Machanda, Zarin; Otali, Emily; Muller, Martin N; Enigk, Drew K; Wrangham, Richard; Emery Thompson, Melissa
(, Evolution, Medicine, and Public Health)
Abstract Background Social isolation is a key risk factor for the onset and progression of age-related disease and mortality in humans. Nevertheless, older people commonly have narrowing social networks, with influences from both cultural factors and the constraints of senescence. We evaluate evolutionarily grounded models by studying social aging in wild chimpanzees, a system where such influences are more easily separated than in humans, and where individuals are long-lived and decline physically with age. Methodology We applied social network analysis to examine age-related changes in social integration in a 7+ year mixed-longitudinal dataset on 38 wild adult chimpanzees (22 females, 16 males). Metrics of social integration included social attractivity and overt effort (directed degree and strength), social roles (betweenness and local transitivity) and embeddedness (eigenvector centrality) in grooming networks. Results Both sexes reduced the strength of direct ties with age (males in-strength, females out-strength). However, males increased embeddedness with age, alongside cliquishness. These changes were independent of age-related changes in social and reproductive status. Both sexes maintained highly repeatable inter-individual differences in integration, particularly in mixed-sex networks. Conclusions and implications As in humans, chimpanzees appear to experience senescence-related declines in social engagement. However, male social embeddedness and overall sex differences were patterned more similarly to humans in non-industrialized versus industrialized societies. Such comparisons suggest common evolutionary roots to ape social aging and that social isolation in older humans may hinge on novel cultural factors of many industrialized societies. Lastly, individual and sex differences are potentially important mediators of successful social aging in chimpanzees, as in humans. Lay summary: Few biological models explain why humans so commonly have narrowing social networks with age, despite the risk factor of social isolation that small networks pose. We use wild chimpanzees as a comparative system to evaluate models grounded in an evolutionary perspective, using social network analysis to examine changes in integration with age. Like humans in industrialized populations, chimpanzees had lower direct engagement with social partners as they aged. However, sex differences in integration and older males’ central positions within the community network were more like patterns of sociality in several non-industrialized human populations. Our results suggest common evolutionary roots to human and chimpanzee social aging, and that the risk of social isolation with age in industrialized populations stems from novel cultural factors.
O’Connell, Caitlin A., Robinson, Natalie, Karimah, Ishma Fatiha, Susanto, Tri Wahyu, Foitova, Ivona, and Knott, Cheryl D. The socioecology of parasite infection in wild Bornean orangutans (Pongo pygmaeus wurmbii) in Gunung Palung National Park, West Kalimantan, Indonesia. Retrieved from https://par.nsf.gov/biblio/10186253. American journal of physical anthropology 171.Supplement 69
O’Connell, Caitlin A., Robinson, Natalie, Karimah, Ishma Fatiha, Susanto, Tri Wahyu, Foitova, Ivona, & Knott, Cheryl D. The socioecology of parasite infection in wild Bornean orangutans (Pongo pygmaeus wurmbii) in Gunung Palung National Park, West Kalimantan, Indonesia. American journal of physical anthropology, 171 (Supplement 69). Retrieved from https://par.nsf.gov/biblio/10186253.
O’Connell, Caitlin A., Robinson, Natalie, Karimah, Ishma Fatiha, Susanto, Tri Wahyu, Foitova, Ivona, and Knott, Cheryl D.
"The socioecology of parasite infection in wild Bornean orangutans (Pongo pygmaeus wurmbii) in Gunung Palung National Park, West Kalimantan, Indonesia". American journal of physical anthropology 171 (Supplement 69). Country unknown/Code not available. https://par.nsf.gov/biblio/10186253.
@article{osti_10186253,
place = {Country unknown/Code not available},
title = {The socioecology of parasite infection in wild Bornean orangutans (Pongo pygmaeus wurmbii) in Gunung Palung National Park, West Kalimantan, Indonesia},
url = {https://par.nsf.gov/biblio/10186253},
abstractNote = {The socioecological model predicts that food availability and risk of parasite transmission influence sociality in primates. As a semi-solitary ape inhabiting the masting forests of Southeast Asia, orangutans provide a unique opportunity to compare social and non-social periods and highly variable foraging conditions within one population. This study compared two data collection periods when fruit availability differed markedly to determine whether sociality and parasite prevalence decrease as expected during periods of fruit scarcity. Fecal samples were analyzed using direct smear and fecal concentration techniques on-site at Cabang Panti Research Station from 2013-2014 and 2018-2019. From the high fruit period to the low fruit period, sociality decreased from 54% of focal follows containing a social event to 29%, while overall parasite prevalence remained the same at 100%. Interesting differences arose for certain parasite species, however. Enterobius sp. prevalence decreased during the low fruit period for both sexes but even more so for males (50% to 29% for females; 56% to 0 for males). Prevalence of Trichuris sp. increased for females during the low fruit period (5% to 43%) while prevalence among males remained the same. These results lend support to the prediction that social contact influences transmission risk for some parasite species, while other parasites may be more responsive to factors such as changes in reproductive state. These findings suggest that differences in the behavioral strategies of the sexes and the differential energetic demands of life history stages have an influence on parasitic infection patterns.},
journal = {American journal of physical anthropology},
volume = {171},
number = {Supplement 69},
author = {O’Connell, Caitlin A. and Robinson, Natalie and Karimah, Ishma Fatiha and Susanto, Tri Wahyu and Foitova, Ivona and Knott, Cheryl D.},
}
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