Meggan E. Craft

Disease transmission in territorial populations: the small-world network of Serengeti lions

Territoriality in animal populations creates spatial structure that is thought to naturally buffer disease invasion. Often, however, territorial populations also include highly mobile, non-residential individuals that potentially serve as disease superspreaders. Using long-term data from the Serengeti Lion Project, we characterize the contact network structure of a territorial wildlife population and address the epidemiological impact of nomadic individuals. As expected, pride contacts are dominated by interactions with neighbouring prides and interspersed by encounters with nomads as they wander throughout the ecosystem. Yet the pride–pride network also includes occasional long-range contacts between prides, making it surprisingly small world and vulnerable to epidemics, even without nomads. While nomads increase both the local and global connectivity of the network, their epidemiological impact is marginal, particularly for diseases with short infectious periods like canine distemper virus. Thus, territoriality in Serengeti lions may be less protective and non-residents less important for disease transmission than previously considered.

Infectious disease transmission and contact networks in wildlife and livestock

The use of social and contact networks to answer basic and applied questions about infectious disease transmission in wildlife and livestock is receiving increased attention. Through social network analysis, we understand that wild animal and livestock populations, including farmed fish and poultry, often have a heterogeneous contact structure owing to social structure or trade networks. Network modelling is a flexible tool used to capture the heterogeneous contacts of a population in order to test hypotheses about the mechanisms of disease transmission, simulate and predict disease spread, and test disease control strategies. This review highlights how to use animal contact data, including social networks, for network modelling, and emphasizes that researchers should have a pathogen of interest in mind before collecting or using contact data. This paper describes the rising popularity of network approaches for understanding transmission dynamics in wild animal and livestock populations; discusses the common mismatch between contact networks as measured in animal behaviour and relevant parasites to match those networks; and highlights knowledge gaps in how to collect and analyse contact data. Opportunities for the future include increased attention to experiments, pathogen genetic markers and novel computational tools.

Distinguishing epidemic waves from disease spillover in a wildlife population

Serengeti lions frequently experience viral outbreaks. In 1994, one-third of Serengeti lions died from canine distemper virus (CDV). Based on the limited epidemiological data available from this period, it has been unclear whether the 1994 outbreak was propagated by lion-to-lion transmission alone or involved multiple introductions from other sympatric carnivore species. More broadly, we do not know whether contacts between lions allow any pathogen with a relatively short infectious period to percolate through the population (i.e. reach epidemic proportions). We built one of the most realistic contact network models for a wildlife population to date, based on detailed behavioural and movement data from a long-term lion study population. The model allowed us to identify previously unrecognized biases in the sparse data from the 1994 outbreak and develop methods for judiciously inferring disease dynamics from typical wildlife samples. Our analysis of the model in light of the 1994 outbreak data strongly suggest that, although lions are sufficiently well connected to sustain epidemics of CDV-like diseases, the 1994 epidemic was fuelled by multiple spillovers from other carnivore species, such as jackals and hyenas.

Network Models: An Underutilized Tool in Wildlife Epidemiology?

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.

Dynamics of a multihost pathogen in a carnivore community

1. We provide the first theoretical analysis of multihost disease dynamics to incorporate social behaviour and contrasting rates of within- and between-group disease transmission. 2. A stochastic susceptible-infected-recovered (SIR) model of disease transmission involving one to three sympatric species was built to mimic the 1994 Serengeti canine distemper virus outbreak, which infected a variety of carnivores with widely ranging social structures. The model successfully mimicked the erratic and discontinuous spatial pattern of lion deaths observed in the Serengeti lions under a reasonable range of parameter values, but only when one to two other species repeatedly transmitted the virus to the lion population. 3. The outputs from our model suggest several principles that will apply to most directly transmitted multihost pathogens: (i) differences in social structure can significantly influence the size, velocity and spatial pattern of a multihost epidemic; and (ii) social structures that permit higher intraspecific neighbour-to-neighbour transmission are the most likely to transmit disease to other species; whereas (iii) species with low neighbour-to-neighbour intraspecific transmission suffer the greatest costs from interspecific transmission.

Dynamics of a morbillivirus at the domestic–wildlife interface: Canine distemper virus in domestic dogs and lions

Significance Morbilliviruses are a growing concern because of their ability to infect multiple species. The spill-over of canine distemper virus (CDV) from domestic dogs has been associated with severe declines in wild carnivores worldwide, and therefore mass dog vaccination has been suggested as a potential control strategy. Focusing on three decades of CDV exposure data in dogs and lions of the Serengeti, we show that cyclic infection dynamics in lions initially driven by dogs became more frequent and asynchronous, suggesting that the wider dog population and other wildlife species drive CDV dynamics. Hence, although widespread dog vaccination reduced the infection in dogs, transmission to lion populations still occurred, warranting further investigation into effective management options of CDV in this species-rich ecosystem. Morbilliviruses cause many diseases of medical and veterinary importance, and although some (e.g., measles and rinderpest) have been controlled successfully, others, such as canine distemper virus (CDV), are a growing concern. A propensity for host-switching has resulted in CDV emergence in new species, including endangered wildlife, posing challenges for controlling disease in multispecies communities. CDV is typically associated with domestic dogs, but little is known about its maintenance and transmission in species-rich areas or about the potential role of domestic dog vaccination as a means of reducing disease threats to wildlife. We address these questions by analyzing a long-term serological dataset of CDV in lions and domestic dogs from Tanzania’s Serengeti ecosystem. Using a Bayesian state–space model, we show that dynamics of CDV have changed considerably over the past three decades. Initially, peaks of CDV infection in dogs preceded those in lions, suggesting that spill-over from dogs was the main driver of infection in wildlife. However, despite dog-to-lion transmission dominating cross-species transmission models, infection peaks in lions became more frequent and asynchronous from those in dogs, suggesting that other wildlife species may play a role in a potentially complex maintenance community. Widespread mass vaccination of domestic dogs reduced the probability of infection in dogs and the size of outbreaks but did not prevent transmission to or peaks of infection in lions. This study demonstrates the complexity of CDV dynamics in natural ecosystems and the value of long-term, large-scale datasets for investigating transmission patterns and evaluating disease control strategies.

Using contact networks to explore mechanisms of parasite transmission in wildlife.

A hallmark assumption of traditional approaches to disease modelling is that individuals within a given population mix uniformly and at random. However, this assumption does not always hold true; contact heterogeneity or preferential associations can have a substantial impact on the duration, size, and dynamics of epidemics. Contact heterogeneity has been readily adopted in epidemiological studies of humans, but has been less studied in wildlife. While contact network studies are becoming more common for wildlife, their methodologies, fundamental assumptions, host species, and parasites vary widely. The goal of this article is to review how contact networks have been used to study macro‐ and microparasite transmission in wildlife. The review will: (i) explain why contact heterogeneity is relevant for wildlife populations; (ii) explore theoretical and applied questions that contact networks have been used to answer; (iii) give an overview of unresolved methodological issues; and (iv) suggest improvements and future directions for contact network studies in wildlife.

Dynamics of a morbillivirus at the domestic -wildlife interface

Significance Morbilliviruses are a growing concern because of their ability to infect multiple species. The spill-over of canine distemper virus (CDV) from domestic dogs has been associated with severe declines in wild carnivores worldwide, and therefore mass dog vaccination has been suggested as a potential control strategy. Focusing on three decades of CDV exposure data in dogs and lions of the Serengeti, we show that cyclic infection dynamics in lions initially driven by dogs became more frequent and asynchronous, suggesting that the wider dog population and other wildlife species drive CDV dynamics. Hence, although widespread dog vaccination reduced the infection in dogs, transmission to lion populations still occurred, warranting further investigation into effective management options of CDV in this species-rich ecosystem. Morbilliviruses cause many diseases of medical and veterinary importance, and although some (e.g., measles and rinderpest) have been controlled successfully, others, such as canine distemper virus (CDV), are a growing concern. A propensity for host-switching has resulted in CDV emergence in new species, including endangered wildlife, posing challenges for controlling disease in multispecies communities. CDV is typically associated with domestic dogs, but little is known about its maintenance and transmission in species-rich areas or about the potential role of domestic dog vaccination as a means of reducing disease threats to wildlife. We address these questions by analyzing a long-term serological dataset of CDV in lions and domestic dogs from Tanzania’s Serengeti ecosystem. Using a Bayesian state–space model, we show that dynamics of CDV have changed considerably over the past three decades. Initially, peaks of CDV infection in dogs preceded those in lions, suggesting that spill-over from dogs was the main driver of infection in wildlife. However, despite dog-to-lion transmission dominating cross-species transmission models, infection peaks in lions became more frequent and asynchronous from those in dogs, suggesting that other wildlife species may play a role in a potentially complex maintenance community. Widespread mass vaccination of domestic dogs reduced the probability of infection in dogs and the size of outbreaks but did not prevent transmission to or peaks of infection in lions. This study demonstrates the complexity of CDV dynamics in natural ecosystems and the value of long-term, large-scale datasets for investigating transmission patterns and evaluating disease control strategies.

Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology.

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour–disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour–parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour–parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.

Raccoon contact networks predict seasonal susceptibility to rabies outbreaks and limitations of vaccination

Infectious disease transmission often depends on the contact structure of host populations. Although it is often challenging to capture the contact structure in wild animals, new technology has enabled biologists to obtain detailed temporal information on wildlife social contacts. In this study, we investigated the effects of raccoon contact patterns on rabies spread using network modelling. Raccoons (Procyon lotor) play an important role in the maintenance of rabies in the United States. It is crucial to understand how contact patterns influence the spread of rabies in raccoon populations in order to design effective control measures and to prevent transmission to human populations and other animals. We constructed a dynamic system of contact networks based on empirical data from proximity logging collars on a wild suburban raccoon population and then simulated rabies spread across these networks. Our contact networks incorporated the number and duration of raccoon interactions. We included differences in contacts according to sex and season, and both short-term acquaintances and long-term associations. Raccoons may display different behaviours when infectious, including aggression (furious behaviour) and impaired mobility (dumb behaviour); the network model was used to assess the impact of potential behavioural changes in rabid raccoons. We also tested the effectiveness of different vaccination coverage levels. Our results demonstrate that when rabies enters a suburban raccoon population, the likelihood of a disease outbreak affecting the majority of the population is high. Both the magnitude of rabies outbreaks and the speed of rabies spread depend strongly on the time of year that rabies is introduced into the population. When there is a combination of dumb and furious behaviours in the rabid raccoon population, there are similar outbreak sizes and speed of spread to when there are no behavioural changes due to rabies infection. By incorporating detailed data describing the variation in raccoon contact rates into a network modelling approach, we were able to show that suburban raccoon populations are highly susceptible to rabies outbreaks, that the risk of large outbreaks varies seasonally and that current vaccination target levels may be inadequate to prevent the spread of rabies within these populations. Our findings provide new insights into rabies dynamics in raccoon populations and have important implications for disease control.