Graduation Year

2018

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Jason Rohr, Ph.D.

Committee Member

Stephen Deban, Ph.D.

Committee Member

Marc Lajeunesse, Ph.D.

Committee Member

Loren Sackett, Ph.D.

Keywords

amphibian decline, amphibians, behavioral ecology, disease, ecology, thermal biology, Batrachochytrium dendrobatidis, ranavirus

Abstract

Amphibians are currently the most threatened vertebra taxa on the planet. Hundreds of species are thought to have gone extinct while thousands more have been listed as threatened or endangered over the past few decades. Habitat loss, invasive species, climate change, and disease are all thought to have partially contributed to these declines. Two pathogens in particular, infectious viruses in the genus Ranavirus (simply referred to as ranavirus) and the fungus Batrachochytrium dendrobatidis (Bd), have been associated with global mass mortality events of amphibians. Virulent pathogens such as these tend to impose strong selective pressures on their hosts driving the evolution of host behaviors that reduce disease.

One example of behavioral disease resistance in ectothermic hosts is behavioral fever, an acute increase in temperature preference in response to pathogen exposure. However, few studies have experimentally examined the effects of host behavior on ranaviral infections. Additionally, both field and laboratory studies testing for behavioral fever in response to Bd exposure have found conflicting results. In the Bd system, these conflicting results could, in part, be caused by some pathogen defenses of host not increasing with temperature. For example, the thermal mismatch hypothesis predicts that host species adapted to cooler temperatures might perform more poorly than the pathogen at warm temperatures, and vice versa, creating a scenario where warm- and cool-adapted hosts most often experience outbreaks at cool and warm temperatures, respectively. Here, I determine if amphibians respond to disease with behavioral fever in the ranaviral and Bd systems and if there are species-level differences in Bd susceptibility predicted by the thermal mismatch hypothesis.

To accomplish these goals, I first needed to detect variation in thermal preferences among individuals and species. However, measuring thermoregulation can often be difficult for many reasons, including cost and confounders like moisture. I designed effective, affordable, and validated methods for measuring the thermal preferences of animals. The thermal gradient apparatus spanned temperatures from 9.29 to 33.94 °C with consistent high humidity across the entirety of the gradient. Additionally, I used simple methods for non-invasively measuring animal and substrate temperatures while avoiding feeding confounders. To validate these methods, I demonstrated that I could detect individual-level consistency and among individual variation in the preferred body temperatures of Anaxyrus terrestris and Osteopilus septentrionalis. I use this design to conduct the experimental work completed in chapters two and three of this dissertation.

Behavior fever is known to influence disease dynamics in some systems, but little work has been done in the ranavirus-amphibian system. Experimental studies, however, have demonstrated that warmer temperatures can mitigate ranaviral infections for some species. I placed A. terrestris in the previously described thermal gradients, recorded their temperature preferences before and after infection, and measured ranaviral loads. I found evidence of behavioral fever during the first 48h after exposure to ranavirus and that individual-level change in temperature preference was negatively correlated with ranavirus intensity. These results suggest that A. terrestris use behavioral fever effectively to resisting ranavirus.

Multiple field studies have documented that individual amphibians within a population that prefer warmer temperatures are less likely to be infected with the fungal pathogen Bd. However, it is unclear whether this phenomenon is driven by behavioral fever or natural variation in thermal preference. To determine if these field patterns were the result of behavioral fever or natural variation, I placed five species of frogs in thermal gradients, recorded temperature preference over time, and measured Bd growth, prevalence, and the survival of infected animals. I found no consistent evidence of behavioral fever to Bd in any of the five tested frog species. Interestingly, individual-level and species-level differences in host temperature preferences affected Bd growth on the host and were predicted by the thermal mismatch hypothesis. For species that preferred warmer temperatures, the preferred temperatures of individuals were negatively correlated with Bd growth on hosts, while the opposite correlation was true for species preferring cooler temperatures. My results suggest that variation in thermal preference, but not behavioral fever, might shape the outcomes of Bd infections for individuals and populations, potentially resulting in selection for individual hosts and host species whose temperature preferences minimize Bd growth and enhance host survival during epidemics.

My evidence for the thermal mismatch in the Bd-amphibian system highlighted the importance of understanding how experimental temperatures might intentionally and unintentionally alter disease outcomes. To better understand how thermal mismatches and other factors impact amphibian host mortality in experiments, I conducted a meta-analysis of 58 laboratory studies on the pathogenic fungus Bd. I found that host mortality was driven by thermal mismatches across experimental studies. Hosts native to cooler environments experienced greater Bd-induced mortality at relatively warm experimental temperatures and hosts native to warmer environments experienced greater mortality at cooler experimental temperatures. I also found evidence that host exposure to novel Bd isolates increased the likelihood of Bd-induced mortality during the first two weeks after exposure. Unsurprisingly, I found that Bd dose positively predicted Bd-induced host mortality and this effect varied across host life stages. My results suggest that thermal mismatches broadly impact Bd-induced mortality in amphibians and that researchers should carefully consider the experimental temperature relative to host thermal tolerance, the novelty of the chosen isolate, and the dose of pathogen when designing host-pathogen experiments.

Quantifying thermal tolerance and regulatory behavior in ectotherms can inform fundamental aspects of organismal physiology, behavior, and ecology that are influential in mediating the effects of both biotic and abiotic stressors. The results of this dissertation highlight the importance of working to disentangle the complicated effects of environmental factors, such as temperature, on disease dynamics, especially as emerging infectious diseases continue to cause declines in biodiversity. Additionally, my results suggest that a nuanced understanding of amphibian thermal biology, which carefully considers the potential for context dependent effects of temperature on disease dynamics, will be crucial for predicting and mitigating disease-mediated amphibian declines.

Download

Share

COinS