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Because parasites (including marcoparasites e.g., worms, and microparasites e.g., bacteria and viruses) can strongly impact host populations, their relationships with hosts have been extensively studied in the past several decades. Despite a depth of knowledge in ecology and evolution of infectious diseases, one critical aspect often overlooked is the role of animal behavior in shaping host-parasite relationships. Behavior acts as an intermediary between environmental and within-host factors, such as physiology, immunological responses, and infection status, and has profound feedback effects that influence these factors. Driven by this perspective, my research aims to investigate the importance of behavioral variability in mediating host-parasite dynamics, considering variation in both biotic and abiotic environmental influences. I have approached this topic by examining multiple wild host-parasite systems, integrating empirical fieldwork and theoretical modeling to build a comprehensive understanding of the parasite-behavior-environment relationships.

Behavior-mediated effects of environmental context

Behavioral responses to environmental changes can be a key determinant of disease dynamics in natural populations. Abiotic factors such as temperature and rainfall, as well as biotic factors like population density and interspecific interactions, create complex environmental contexts that influence disease transmission. Hosts respond to these variations by altering their behaviors e.g., daily activity and movement patterns. These behavioral shifts can, in turn, affect the spread and persistence of parasites.

In my research on environmental transmission, I have focused on diseases where the parasites use environmental reservoirs to facilitate transmission. A prime example is anthrax, caused by Bacillus anthracis, which persists in soil and is transmitted to herbivores when they ingest contaminated vegetation or soil. While environmental factors such as rainfall and temperature have been shown to correlate with anthrax outbreaks, the direct role of host behavior in intermediating these outbreaks remains underexplored.

My work on anthrax transmission dynamics in plains zebra (Equus quagga) and other herbivores in Etosha National Park (Namibia) and Kruger National Park (South Africa) provides insights into this parasite-behavior-environment relationship. I hypothesized that while environmental fluctuations are distal causes of transmission, the proximate driver is the behavioral response of herbivores to these changes. Specifically, I tested whether alterations in movement patterns, driven by environmental factors, intermediate anthrax transmission. I approached this hypothesis by (1) examining temporal correlations between herbivore anthrax mortality and environmental variables, such as rainfall and vegetation dynamics, with different time lags, (2) evaluating habitat selection and range size in relation to anthrax risks, using GPS telemetry data to track herbivore movements, and (3) simulating transmission dynamics under varying movement strategies to explore how environmental and behavioral factors interact with transmission.

The results revealed that rainfall and vegetation changes—key drivers of herbivore behavior—are closely linked to anthrax transmission. I identified specific time lags (one month for rainfall and two weeks for vegetation dynamics) that best explain the correlation between environmental fluctuations and anthrax mortality. These time lags correspond to a mechanism whereby herbivore behavioral responses to changes in vegetation—triggered by rainfall—lead to increased anthrax exposure. Moreover, my research revealed that herbivore habitat selection and range size in response to resource availability affect their anthrax risks. Additionally, my simulations showed that an interaction between range size and range shifting strategies drives the likelihood of animals to encounter anthrax spores, linking movement behavior to transmission risk. In summary, while environmental transmission is clearly influenced by weather conditions, my research suggests that host behavior is a critical proximate factor driving disease dynamics. These findings challenge the traditional view that environmental factors alone dictate disease outbreaks of environmentally-transmitted parasites, and highlight the need for a behaviorally-informed understanding of disease ecology.

Behavior-mediated effects on individual fitness

Parasitic infections typically reduce host fitness by impacting key physiological processes, such as immune function, body condition, and survival. However, the relationship between infection and fitness is not always straightforward, as animal behavior can modify these outcomes. For example, social behaviors that increase the risk of infection can also confer survival advantages, creating a nuanced interaction between behavior, infection, and fitness.

In my research on Mycoplasma ovipneumoniae infection in bighorn sheep (Ovis canadensis) in Montana, USA, I examined how social behavior influences survival during disease outbreaks. Mycoplasma infection, which causes severe pneumonia, has resulted in high mortality rates (>80%) in some Rocky Mountain bighorn sheep populations. While social connectivity is often considered a risk factor for transmission, I found that individuals with higher social connectivity had higher survival during outbreaks. This counterintuitive result suggests that social behavior provides survival benefits, possibly through enhanced access to resources or social support during illness, even when it increases exposure to pathogens. These findings challenge the simplistic view that sociality always increases fitness costs in the context of infectious disease.​

I am also investigating the effects of parasitism on sexual selection, focusing on coccidial infection in wild turkeys (Meleagris gallopavo) in Florida, USA. Coccidial infection correlates with male physical traits that are associated with female sexual preference, which plays a key role in mate attraction and selection. By comparing the courtship and mating behaviors of males with varying infection burdens, my research aims to determine whether parasitism influences male turkey reproductive behavior, to evaluate the indirect fitness cost caused by parasitism in addition to direct consumptive effects.

Miscellaneous behavior-related effects of parasitism

In addition to behaviorally mediated effects on disease transmission and on host fitness, parasite-behaviorrelationships can have be more complex with feedbacks or extended to another trophic levels. Parasites can alter their hosts' behavior, while behavioral changes also affect likelihood of parasite infection. For example, some parasites manipulate host behavior to enhance transmission, while others cause sickness behaviors (e.g., lethargy and anorexia) that reduce the host’s energy expenditure and decrese futher infection. These behavioral changes are not fixed and can vary depending on environmental conditions.​

In my research, I have examined how infections influence host behavior and how these behavioral changes, in turn, affect ecological interactions. One example is my current work on wild turkeys, where I investigate behavioral differences between infection status across multiple populations living in different environmental contexts. I focus on viral and protozoan infection, and compared variation in behavioral differences. My findings showed that the magnitude of behavioral differences varied significantly between populations, with one population maintaining consistent activity levels regardless of infection status, while the other exhibited increased activity of infected individuals. These positive association between activity and infection in this population can be due to energy demands induced by the infection, or due to high acitivity lead to high risk of infection. The difference between two populations indicate that behavioral variation can differs with the environment, and it can become more pronounced due to trade-offs and variation in environmental contexts.

I have also explored the ecological consequences of parasite-induced behavioral changes in a community by investigating trophic cascades. In particular, I studied how anorexia induced by helminth infections affects herbivore feeding behavior and, subsequently, plant biomass dynamics. In systems where herbivores such as Grant’s gazelle (Nanger granti) in Mpala Research Centre (Kenya) are infected with strongyle nematodes, reduced feeding rates i.e., anorexia, can lead to increased plant biomass. In addition, variation in individual feeding responses increases the plant biomass than homogeneity in feeding responses. This parasite-induced trophic cascade demonstrates that parasitism can regulate communities or ecosystems not only through direct effects on hosts but also through indirect effects on other trophic levels. This study further emphasizes the complexity of host-parasite-environment relationships.

Overall, my research explores how animal behavior influences host-parasite relationships across various behaviors (e.g., foraging, social, movement, and reproductive), disease transmission modes (direct and environmental), levels of pathogenicity (chronic/mild to acute/lethal), host taxa (mammals and birds), and ecological scales (individual, population, and community). My work underscores the critical role of animal behavior in shaping these interactions and highlights the complex dynamics between hosts, parasites, and the environment, and further highlights that more studies are needed to investigate these relationships.

*Images generated by OpenAI's DALL-E through ChatGPT

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Yen-Hua Huang, Ph.D., D.V.M

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