Costs and benefits of group living with disease: a case study of pneumonia in bighorn lambs ( Ovis canadensis )

Abstract

Group living facilitates pathogen transmission among social hosts, yet temporally stable host social organizations can actually limit transmission of some pathogens. When there are few between-subpopulation contacts for the duration of a disease event, transmission becomes localized to subpopulations. The number of per capita infectious contacts approaches the subpopulation size as pathogen infectiousness increases. Here, we illustrate that this is the case during epidemics of highly infectious pneumonia in bighorn lambs ( Ovis canadensis ). We classified individually marked bighorn ewes into disjoint seasonal subpopulations, and decomposed the variance in lamb survival to weaning into components associated with individual ewes, subpopulations, populations and years. During epidemics, lamb survival varied substantially more between ewe-subpopulations than across populations or years, suggesting localized pathogen transmission. This pattern of lamb survival was not observed during years when disease was absent. Additionally, group sizes in ewe-subpopulations were independent of population size, but the number of ewe-subpopulations increased with population size. Consequently, although one might reasonably assume that force of infection for this highly communicable disease scales with population size, in fact, host social behaviour modulates transmission such that disease is frequency-dependent within populations, and some groups remain protected during epidemic events.

Digging for answers: contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal

“…Additionally, social barriers are likely to have contributed to this pattern since colony identity was an important predictor of ectoparasite prevalence, abundance and species richness. Similar effects of group membership have previously been found for closely related social bathyergids (Viljoen et al 2011;Lutermann et al 2013) and other social mammals (Freeland 1979;Leclaire and Faulkner 2014;Manlove et al 2014), supporting the hypothesis that segregation into clusters can reduce parasite transmission rates within a host population (Wilson et al 2003;Rifkin et al 2012;Griffin and Nunn 2012). Further corroborating evidence for significant effects of such social barriers and actual contact rates rather than group size on parasite transmission comes from a several studies in primates (Walsh et al 2009;Griffin and Nunn 2012;Nunn et al 2015;Rimbach et al 2015).…”

“…Although Freeland's observations of group specific endoparasite infracommunities could not be reproduced in a recent study on the same primate population (Chapman et al 2012), several other studies in primates and carnivores have provided theoretical and empirical evidence for a role of intergroup contact rates for endoparasite transmission (Walsh et al 2009;Drewe 2010;Nunn et al 2015;Rimbach et al 2015). Furthermore, a number of recent studies show that group membership is an important determinant of parasite burden suggesting that parasite burden is more similar among group members than between members of different groups in several mammal taxa (Viljoen et al 2011;Lutermann et al 2013;Leclaire and Faulkner 2014;Manlove et al 2014). Consequently, both density-and frequency dependent mechanisms may affect the relationship between parasite burden and sociality, meaning group size alone may be a poor predictor of these mechanisms.…”

“…A comparative study in rodents that explicitly considered the degree of sociality did not find a clear relationship between sociality and endoparasites while it was negative for ectoparasites (Bordes et al 2007). In addition, behavioural mechanisms such as clustering into sub-groups may reduce parasite transmission within larger social groups (Wilson et al 2003;Griffin and Nunn 2012;Manlove et al 2014). The significance of social barriers such as xenophobia and high group integrity to parasite transmission has already been pointed out several decades ago (Freeland 1976;Freeland 1979;Loehle 1995).…”

Brown spider monkeys ( Ateles hybridus ): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics

“…For example, the level of group stability (closed groups versus fluid or open groups) has been shown to affect the relationship between group size and prevalence of intestinal parasites in 11 African bovid species [4]. Similarly, the formation of seasonally stable subpopulations inhibits the spread of pneumonia among bighorn lambs (Oviscanadensis) belonging to different subpopulations [44]. Substructuring into social units (subpopulations or subgroups) probably impacts rates of social behaviour and therefore, potentially, parasite transmission through a population as well [45].…”

Unraveling the disease consequences and mechanisms of modular structure in animal social networks

“…The structural trapping effect (albeit weak) has been observed in a field study of pneumonia transmission in highly subdivided networks of bighorn lambs (SI Appendix, Fig. S13) (21) and others (SI Appendix, Table S2). We also found empirical evidence of structural delay in the spread of mycoplasma in the low-modular network, but highly cohesive subgroups, of house finches described in ref.…”