The Price of Play: Self-Organized Infant Mortality Cycles in Chimpanzees

Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
PLoS ONE (Impact Factor: 3.23). 02/2008; 3(6):e2440. DOI: 10.1371/journal.pone.0002440
Source: PubMed


Chimpanzees have been used extensively as a model system for laboratory research on infectious diseases. Ironically, we know next to nothing about disease dynamics in wild chimpanzee populations. Here, we analyze long-term demographic and behavioral data from two habituated chimpanzee communities in Taï National Park, Côte d'Ivoire, where previous work has shown respiratory pathogens to be an important source of infant mortality. In this paper we trace the effect of social connectivity on infant mortality dynamics. We focus on social play which, as the primary context of contact between young chimpanzees, may serve as a key venue for pathogen transmission. Infant abundance and mortality rates at Taï cycled regularly and in a way that was not well explained in terms of environmental forcing. Rather, infant mortality cycles appeared to self-organize in response to the ontogeny of social play. Each cycle started when the death of multiple infants in an outbreak synchronized the reproductive cycles of their mothers. A pulse of births predictably arrived about twelve months later, with social connectivity increasing over the following two years as the large birth cohort approached the peak of social play. The high social connectivity at this play peak then appeared to facilitate further outbreaks. Our results provide the first evidence that social play has a strong role in determining chimpanzee disease transmission risk and the first record of chimpanzee disease cycles similar to those seen in human children. They also lend more support to the view that infectious diseases are a major threat to the survival of remaining chimpanzee populations.

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Available from: Peter D Walsh, Mar 20, 2015
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    • "We examined mortality data in nine wild non-human primate taxa across three continents to understand how seasonal variation in rainfall and resource availability may act as selection pressures by influencing mortality. Many factors contribute to primate mortality, including disease (Alexander 1974; Dunbar 1980; Milton 1996; Walsh et al. 2005; Kühl et al. 2008; Williams et al. 2008), predation (Cheney et al. 1981; Cheney and Wrangham 1987; Isbell 1994; Karpanty and Wright 2007; Teelen 2008; Irwin et al. 2009), injury during both interspecific and intraspecific interactions (van Schaik and Janson 2000; Cheney et al. 2006; Williams et al. 2008), and starvation (Dittus 1977, 1980; Dunbar 1980; Hamilton 1985). Resource availability for both primates and their predators, or other environmental variables, such as rainfall and temperature, may influence the importance of these different sources of mortality (Dunbar 1980; Richard 1985). "
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    ABSTRACT: Examining seasonal mortality patterns can yield insights into the drivers of mortality and thus potential selection pressures acting on individuals in different environments. We compiled adult and juvenile mortality data from nine wild non-human primate taxa to investigate the role of seasonality in patterns of mortality and address the following questions: Is mortality highly seasonal across species? Does greater environmental seasonality lead to more seasonal mortality patterns? If mortality is seasonal, is it higher during wet seasons or during periods of food scarcity? and Do folivores show less seasonal mortality than frugivores? We found seasonal mortality patterns in five of nine taxa, and mortality was more often tied to wet seasons than food-scarce periods, a relationship that may be driven by disease. Controlling for phylogeny, we found a positive relationship between the degree of environmental seasonality and mortality, with folivores exhibiting more seasonal mortality than frugivores. These results suggest that mortality patterns are influenced both by diet and degree of environmental seasonality. Applied to a wider array of taxa, analyses of seasonal mortality patterns may aid understanding of life-history evolution and selection pressures acting across a broad spectrum of environments and spatial and temporal scales.
    Evolution 10/2012; 66(10):3252-3266. DOI:10.1111/j.1558-5646.2012.01668.x · 4.61 Impact Factor
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    • "Play is not for free. Despite being performed mostly under favourable conditions (see above), it costs the animals time and energy (Sharpe et al. 2002) and exposes them to injury, predation (Harcourt 1991) and disease transmission (Kuehl et al. 2008). Its actual fitness costs in wild animals have been suggested to vary from negligible (Martin 1984; Caro 1995) to substantial (Harcourt 1991) in different species and situations. "
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    ABSTRACT: Play has long been identified as a potential welfare indicator because it often disappears when animals are under fitness challenge and because it is thought to be accompanied by a pleasurable emotional experience. But animal play is a vexing behavioural phenomenon, characteristically flexible and variable within and between species, with its proximate mechanisms and ultimate functions still not fully understood. Its relationship to animal welfare is therefore complex and merits a focused theoretical investigation. We review evidence on four aspects of the playewelfare relationship: first, that play indicates the absence of fitness threats; second, that play acts as a reward and flags up the presence of opioid-mediated pleasurable emotional experiences; third, that play brings immediate psychological benefits and long-term benefits for fitness and health, and thus improves current and future welfare; and finally, that play is socially contagious and therefore capable of spreading good welfare in groups. On this basis, we argue that play does indeed hold promise as a welfare indicator and also as a tool to improve it; but we also point to difficulties in its study and interpretation and identify some unresolved questions. As a welfare indicator, play may signal both the absence of bad welfare and the presence of good welfare, thus covering a wide range of the welfare spectrum. However, play can also increase in stressful situations, in response to reduced parental care, or as a rebound after a period of deprivation and therefore does not consistently reflect favourable environmental conditions. A better fundamental understanding is needed of the varied ultimate functions and proximate mechanisms of play, and the species-specific play patterns of captive animals, in order to be able to explain exactly what an animal’s play behaviour tells us about its welfare state, and whether and how play might be applied as a tool to improve welfare .
    Animal Behaviour 05/2011; 81(5-5):891-899. DOI:10.1016/j.anbehav.2011.01.007 · 3.14 Impact Factor
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    • "With networks, researchers were able to distinguish spatial patterns of disease spillover from epidemic waves [17]. Temporal changes in contact patterns were also identified as critical for the spread of respiratory diseases in wild chimpanzees [70]. Issues of different spatial scales have been tackled with networks, specifically the relative importance of local versus long range transmission events in driving disease spread [68]. "
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    ABSTRACT: Although the approach of contact network epidemiology has been increasing in popularity for studying transmission of infectious diseases in human populations, it has generally been an underutilized approach for investigating disease outbreaks in wildlife populations. In this paper we explore the differences between the type of data that can be collected on human and wildlife populations, provide an update on recent advances that have been made in wildlife epidemiology by using a network approach, and discuss why networks might have been underutilized and why networks could and should be used more in the future. We conclude with ideas for future directions and a call for field biologists and network modelers to engage in more cross-disciplinary collaboration.
    Interdisciplinary Perspectives on Infectious Diseases 03/2011; 2011(8):676949. DOI:10.1155/2011/676949
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