1. Ecological immunology and disease ecology are two relatively young disciplines that apply ecological approaches and principles to traditionally non-ecological fields. In both cases, an ecological ...perspective has allowed new insights to emerge by focusing attention on variation over space and time, and by emphasizing the role of the environment in shaping individual responses and the outcome of host-pathogen interactions. Here we review the growing conceptual interface between these two rapidly evolving fields. 2. Areas of synergy between ecological immunology and disease ecology aim to translate variation in within-host processes (e.g. immunity) into between-host dynamics (e.g. parasite transmission). Emerging areas of synergy include potential immune mechanisms that underlie host heterogeneity in disease susceptibility, teasing apart the effects of environmental factors such as seasonality and climate on host susceptibility and pathogen dynamics, and predicting the outcome of co-infection by functionally distinct groups of parasites that elicit different immune responses. 3. In some cases, practical limitations have constrained the merging of ideas in ecological immunology and disease ecology. We discuss several logistical challenges, including dissecting the relative roles of host exposure and susceptibility, establishing links between measures of immunity and pathogen resistance in wild populations, and incorporating relevant immune variation into prevailing disease ecology modeling frameworks. 4. Future work at the interface of these two fields should advance understanding of life-history theory, host-pathogen dynamics, and physiological ecology, and will also contribute to targeted approaches for wildlife health and zoonotic disease prevention.
Recent progress in the field of wildlife disease ecology demonstrates that infectious disease plays a crucial role in the lives of wild animals. Parasites and pathogens should be especially important ...for social animals in which high contact among individuals increases the potential for disease spread. As one of the best studied mammalian groups, primates offer a unique opportunity to examine how complex behaviours (including social organization) influence the risk of acquiring infectious diseases, and the defences used by animals to avoid infection. This book explores the correlates of disease risk in primates, including not only social and mating behaviour but also diet, habitat use, life history, geography and phylogeny. The authors examine how a core set of host and parasite traits influence patterns of parasitism at three levels of biological organization: among individuals, among populations, and across species. A major goal is to synthesize, for the first time, four disparate areas of research: primate behavioural ecology, parasite biology, wildlife epidemiology, and the behavioural and immune defences employed by animals to counter infectious disease. Throughout, the authors provide an overview of the remarkable diversity of infectious agents found in wild primate populations. Additional chapters consider how knowledge of infectious diseases in wild primates can inform efforts focused on primate conservation and human health. More generally, this book identifies infectious disease as an important frontier in our understanding of primate behaviour and ecology. It highlights future challenges for testing the links between host and parasite traits, including hypotheses for the effects of disease on primate social and mating systems.
Animal Migration and Infectious Disease Risk Altizer, Sonia; Bartel, Rebecca; Han, Barbara A
Science (American Association for the Advancement of Science),
01/2011, Volume:
331, Issue:
6015
Journal Article
Peer reviewed
Animal migrations are often spectacular, and migratory species harbor zoonotic pathogens of importance to humans. Animal migrations are expected to enhance the global spread of pathogens and ...facilitate cross-species transmission. This does happen, but new research has also shown that migration allows hosts to escape from infected habitats, reduces disease levels when infected animals do not migrate successfully, and may lead to the evolution of less-virulent pathogens. Migratory demands can also reduce immune function, with consequences for host susceptibility and mortality. Studies of pathogen dynamics in migratory species and how these will respond to global change are urgently needed to predict future disease risks for wildlife and humans alike.
Urbanisation and agriculture cause declines for many wildlife, but some species benefit from novel resources, especially food, provided in human‐dominated habitats. Resulting shifts in wildlife ...ecology can alter infectious disease dynamics and create opportunities for cross‐species transmission, yet predicting host–pathogen responses to resource provisioning is challenging. Factors enhancing transmission, such as increased aggregation, could be offset by better host immunity due to improved nutrition. Here, we conduct a review and meta‐analysis to show that food provisioning results in highly heterogeneous infection outcomes that depend on pathogen type and anthropogenic food source. We also find empirical support for behavioural and immune mechanisms through which human‐provided resources alter host exposure and tolerance to pathogens. A review of recent theoretical models of resource provisioning and infection dynamics shows that changes in host contact rates and immunity produce strong non‐linear responses in pathogen invasion and prevalence. By integrating results of our meta‐analysis back into a theoretical framework, we find provisioning amplifies pathogen invasion under increased host aggregation and tolerance, but reduces transmission if provisioned food decreases dietary exposure to parasites. These results carry implications for wildlife disease management and highlight areas for future work, such as how resource shifts might affect virulence evolution.
Urbanization is intensifying worldwide, with two-thirds of the human population expected to reside in cities within 30 years. The role of cities in human infectious disease is well established, but ...less is known about how urban landscapes influence wildlife–pathogen interactions. Here, we draw on recent advances in wildlife epidemiology to consider how environmental changes linked with urbanization can alter the biology of hosts, pathogens and vectors. Although urbanization reduces the abundance of many wildlife parasites, transmission can, in some cases, increase among urban-adapted hosts, with effects on rarer wildlife or those living beyond city limits. Continued rapid urbanization, together with risks posed by multi-host pathogens for humans and vulnerable wildlife populations, emphasize the need for future research on wildlife diseases in urban landscapes.
Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic ...drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.
Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between ...infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition–infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition–infection relationships in wildlife systems. We then perform a meta‐analysis of 553 condition–infection relationships from 187 peer‐reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition–infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host–parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.
Seasonal variations in temperature, rainfall and resource availability are ubiquitous and can exert strong pressures on population dynamics. Infectious diseases provide some of the best-studied ...examples of the role of seasonality in shaping population fluctuations. In this paper, we review examples from human and wildlife disease systems to illustrate the challenges inherent in understanding the mechanisms and impacts of seasonal environmental drivers. Empirical evidence points to several biologically distinct mechanisms by which seasonality can impact host-pathogen interactions, including seasonal changes in host social behaviour and contact rates, variation in encounters with infective stages in the environment, annual pulses of host births and deaths and changes in host immune defences. Mathematical models and field observations show that the strength and mechanisms of seasonality can alter the spread and persistence of infectious diseases, and that population-level responses can range from simple annual cycles to more complex multiyear fluctuations. From an applied perspective, understanding the timing and causes of seasonality offers important insights into how parasite-host systems operate, how and when parasite control measures should be applied, and how disease risks will respond to anthropogenic climate change and altered patterns of seasonality. Finally, by focusing on well-studied examples of infectious diseases, we hope to highlight general insights that are relevant to other ecological interactions.
Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies (
Danaus plexippus
) and a ...protozoan parasite (
Ophryocystis elektroscirrha
) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long-distance migration weeds out infected animals (i.e., migratory culling). We combined field-sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within-breeding-season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.
The monarch butterfly (Danaus plexippus) population in North America has sharply declined over the last two decades. Despite rising concern over the monarch butterfly's status, no comprehensive study ...of the factors driving this decline has been conducted. Using partial least-squares regressions and time-series analysis, we investigated climatic and habitat-related factors influencing monarch population size from 1993 to 2014. Potential threats included climatic factors, habitat loss (milkweed and overwinter forest), disease and agricultural insecticide use (neonicotinoids). While climatic factors, principally breeding season temperature, were important determinants of annual variation in abundance, our results indicated strong negative relationships between population size and habitat loss variables, principally glyphosate use, but also weaker negative effects from the loss of overwinter forest and breeding season use of neonicotinoids. Further declines in population size because of glyphosate application are not expected. Thus, if remaining threats to habitat are mitigated we expect climate-induced stochastic variation of the eastern migratory population of monarch butterfly around a relatively stationary population size.
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