The impact of resource availability on parasite transmission: insights from a natural multi-parasite community

鉴于生境改变和人为变化的速度日益加快，了解野生动物资源可得性与寄生虫感染之间的关系变得越来越重要。这些变化可能会有意无意地改变资源的分布、质量和可用性。然而，了解不同的资源可用性情景（无论是自然的还是人为的）如何影响野生动物的感染水平是一项重大的保护挑战，因为资源在个体和种群尺度上以无数种方式影响宿主。大多数关于资源与传染病之间关系的研究只关注特定方面（例如，食物质量如何影响宿主生理，或食物水平如何影响宿主种群规模）。实际上，资源对疾病风险和负担的影响可能是复杂的，影响到个人和人口两级的各个方面。例如，高质量的资源可以显著改善个人的健康和状况，从而降低对疾病的易感性。然而，聚集的食物斑块会吸引成群的动物，从而增加寄生虫传播的机会。重要的是，对于具有不同传播模式或生命周期的寄生虫，这些影响的相对大小可能不同。考虑到这些不同的影响，理解和预测自然野生动物系统中不同资源可用性情景的影响是极具挑战性的。这一知识差距是理解资源如何影响野生动物保护以及某些疾病如何影响人类和家畜健康的主要障碍。为了帮助理解资源可得性与野生动物疾病之间的关系，我们需要评估(1)不同类型的资源可得性（例如，聚集的还是均匀分布的，高质量的还是低质量的食物），(2)对不同类型寄生虫的影响（例如，直接传播的还是环境传播的，慢性感染的还是急性感染的），以及(3)这些影响是否是由于宿主生理、行为、人口统计或其他寄生虫的变化造成的。据我们所知，没有一项研究在同一项研究中涉及到所有这些方面。然而，我们已经开发了一个理想的自然系统：野生木鼠和它们多样化的寄生虫群落。我们不仅优化了在自然环境中研究这种寄主-寄生虫群落的方法，我们最近还开发了一个实验室群体，其中包括以前的野生木鼠和它们的一些主要天然寄生虫物种，这为使用相同的寄主-寄生虫群落将密集的实验室实验与广泛的实地研究结合起来提供了前所未有的能力。在这里，我们将结合(1)宿主和寄生虫对一系列感染/共感染和资源可用性的反应的实验室研究，以及(2)在野外使用替代资源供应情景的大规模扰动实验，以测量不同形式的资源可用性如何影响广泛的寄生虫类型在其自然宿主中的传播。此外，我们将把这些结果与替代资源情景的一般数学模型结合起来，以更广泛地了解不同资源传播关系如何影响疾病传播。总之，这些方法将使我们能够：(1)评估宿主生理和行为在替代资源可用性情景下是如何变化的，(2)测试我们是否可以对不同寄生虫对不同类型资源的反应做出一般预测，以及(3)深入了解其他野生动物系统如何应对未来资源可用性情景的变化。鉴于人们对人类活动如何影响野生动物的担忧日益增加，该项目非常及时，并将提供急需的实验数据，以及对自然野生动物群落中资源可用性和分布变化如何驱动寄生虫动态的一般见解。

Understanding the relationship between resource availability and parasitic infection in wildlife is of increasing importance given rising rates of habitat modification and anthropogenic change. These changes can alter the distribution, quality and availability of resources, either accidentally or deliberately. However, understanding how different resource availability scenarios, either natural or anthropogenic, affect infection levels in wildlife is a major conservation challenge due the myriad of ways in which resources affect hosts, both at the individual and population scales. Most studies into the relationship between resources and infectious disease focus only on specific aspects (e.g. how food quality affects host physiology, or how food levels affect host population size). In reality the impact of resources on the risk and burden of disease can be complex, affecting various aspects at both the individual and population levels. For example, high quality resources may significantly improve individual health and condition, resulting in reduced susceptibility to disease. However, aggregated food patches that attract groups of animals can lead to increased opportunities for parasite transmission. Importantly, the relative sizes of these effects are likely to differ for parasites with different transmission modes or lifecycles. Given these diverse effects, it can be highly challenging to understand and predict the impact of different resource availability scenarios in natural wildlife systems. This knowledge gap forms a major barrier to understanding how resources affect wildlife conservation and, for some diseases, human and domestic animal health.To help understand the relationship between resource availability and wildlife disease we need to assess (1) different types of resource availability (e.g. aggregated v. evenly distributed, high v. low quality food), (2) the effects on different types of parasites (e.g. direct v. environmentally transmitted, chronic v. acute infections) and (3) whether those effects are due to changes in host physiology, behaviour, demography, or other parasites. To our knowledge, no studies have addressed all these aspects in the same study. However we have developed an ideal natural system: wild wood mice and their diverse parasite community. Not only have we optimised the methods for studying this host-parasite community in its natural setting, we have also recently developed a lab colony of formerly wild wood mice and some of their key natural parasite species, which provides unprecedented ability to combine intensive lab experiments with extensive field studies, using the same host-parasite community.Here we will combine (1) lab studies of host and parasite responses to a range of infections/coinfections and resource availabilities, with (2) large-scale perturbation experiments using alternative resource provisioning scenarios in the wild to measure how different forms of resource availability affect transmission of a broad range of parasite types in their natural host. Furthermore, we will combine these results with general mathematical models of alternative resource scenarios to develop a broad understanding of how different resource-transmission relationships affect disease spread. Together, these approaches will allow us to: (1) assess how host physiology and behaviour change following alternative resource availability scenarios, (2) test whether we can make generalised predictions about how different parasites will respond to different types of resources, and (3) provide insight into how other wildlife systems are likely to respond to changes in resource availability scenarios in the future. Given increasing concerns over how anthropogenic activities impact wildlife, this project is highly timely, and will provide much-needed experimental data, and general insight, into how shifts in resource availability and distribution drive parasite dynamics in natural wildlife communities.