19-EEID US-UK Collab: Disentangling transport and trophic effects of animal movement on infectious disease

Mobile organisms, such as many species of birds, insects and ungulates, have long fascinated scientists and the general public because of the vast distances over which these animals travel and the large impacts they have on the dynamics of ecosystems they encounter. The high local densities and long-distance movements of mobile organisms provide seemingly ideal conditions for the emergence and spread of disease-causing pathogens, yet the ways in which mobile hosts modify the infection dynamics of less-mobile (i.e. resident) hosts is poorly understood. In this proposal, we take advantage of the widespread occurrence of gastrointestinal nematodes in one of the most intact and largest terrestrial animal migration systems in the world - the Serengeti wildebeest - to advance understanding of the impact of animal movement on parasite dynamics. We hypothesize that mobile hosts can affect parasite dynamics in resident hosts in at least two important ways. First, mobile hosts can shed parasites in locations visited by other hosts, thereby creating areas of high parasite density. Second, mobile hosts can profoundly change the environment in which parasites mature, for example by shortening the height of vegetation both through trampling and foraging, which can directly and indirectly modify the risk of parasite transmission to resident hosts. Because of their large effects on vegetation, mobile herbivores may promote or reduce parasite exposure risk by either i) concentrating parasites on the remaining vegetation, or ii) removing parasites through consumption. Alternatively, mobile hosts may alter the behaviour of other herbivores indirectly through their effects on vegetation, by iii) promoting regrowth of vegetation and thus attracting herbivores, or iv) consuming all of the food and thus displacing them. We aim to determine which of these direct and indirect, positive/negative effects are most important, and their mechanistic underpinnings. We will do so by examining the impacts of highly mobile wildebeest on the parasite abundance in the environment and in four wildlife species: topi, hartebeest, African Cape buffalo, and Grant's gazelle. In wildlife species, we will examine these different mechanisms using a combination of tracking data (GPS collars, camera traps, spatial distribution models) and molecular analyses of parasite infection dynamics in animals. This work will be combined with experiments that manipulate two of the main vegetative mechanisms that alter parasite availability in the environment: density of feces and grazing intensity on grasses. We will use this information to develop a general model of infection dynamics in mobile and resident hosts that will allow insight into the conditions in which infections are most likely to increase or decrease. The same dynamics that occur in resident wildlife hosts are also likely to play out in resident livestock, however in many systems around the world there is a lack of understanding of whether wildlife and livestock even share the same parasites. Thus, a broader impact of our project is to examine the extent to which mobile wildlife change the infection intensity in resident livestock, whether the two groups share the same populations of parasites and whether mobile wildlife benefit livestock by acting as a refugia for parasites that are sensitive to anti-parasite drug treatment (i.e. a natural buffer to anthelmintic resistance). Given that gastrointestinal parasites have an environmental stage to their life cycle, ecology plays a central role in their infection and transmission dynamics, opening the door for a range of exciting future research questions in disease ecology, animal health and wildlife-livestock interactions, as well as training opportunities with local animal health students and authorities.

The long-distance movements and high local densities of mobile animals are often assumed to facilitate the transport of parasites between spatially disparate locations, with some migratory species posing serious disease threats to other species, including humans. However, recent syntheses of the animal movement and infectious disease literature suggest that this idea is based on sparse empirical data. In this proposal, we take advantage of the widespread occurrence of gastrointestinal nematodes (GIN) in a migrating ungulate (wildebeest) to advance our understanding of the impact of mobile hosts on parasite risk and infection. Animal movement can affect parasite dynamics in resident species in at least two important ways. First, mobile hosts can shed GIN in locations visited by other hosts (i.e. transport), thereby creating areas of high GIN density. Second, mobile hosts may modify plant biomass and thereby exert trophic effects that may either directly promote or reduce GIN exposure, or indirectly affect resident host behavior. The question of cross-species transmission of parasites has broad societal relevance in areas where human livelihoods and food supply chains integrate with ecosystems that support many species of animals with varying degrees of mobility. This study combines observational approaches, natural and manipulative experiments, and dynamic statistical modeling to address four main aims: (1) quantify the effect of mobile hosts on the GINs in resident hosts and in the external environment; (2) identify the mechanistic basis by which mobile and resident hosts alter the trophic effects of GIN infections; (3) develop a general model of GIN prevalence that examines the conditions in which movement of mobile hosts directly and indirectly modifies GIN intensity in resident hosts; (4) understand the broader impact that mobile wildlife may have on resident livestock GIN infections