Graduation Year

2016

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

Ruiliang Pu, Ph.D.

Committee Member

Earl McCoy, Ph.D.

Committee Member

Marc Lajeunesse, Ph.D.

Committee Member

Leah Johnson, Ph .D.

Keywords

ecology, disease, amphibians, scale, phenology, climate change

Abstract

Climate change is expected to impact species by altering infectious disease outcomes, modifying community composition, and causing species to shift their phenology, body sizes and range distributions. However, the outcomes of these impacts are often controversial; for example, scientists have debated whether climate change will exacerbate emerging infectious disease and which species are at greatest risk to advance their phenology. There reason for these controversies may be that climate change is impacting diverse processes across a wide range of ecological scales, as the interplay between fine-scale processes and broad-scale dynamics can often cause unpredictable changes to the biosphere. Therefore, it is important to consider how ecological processes change across spatial, temporal and allometric scales in order to understand the impacts of climate change. For example, if community composition controls disease distributions at small spatial scales while abiotic factors do so at large, regional scales, studies conducted at a single spatial scale may misestimate the impacts of climate change on biodiversity. Because small organisms acclimate quickly, they may track their phenology to climatic factors over shorter temporal scales than large organisms. In addition, small organisms have wider thermal breadths, or temperature ranges where performance is relatively strong, than large organisms. This may cause cold-adapted hosts to face performance gaps with parasites at warmer temperatures than those where host or parasite performance peaks, putting them at risk when the climate warms.

I began my dissertation work by examining how spatial scale modulates the observed effects of human modifications to ecological processes. Humans are altering the distribution of species by changing the climate and disrupting biotic interactions and dispersal. A fundamental hypothesis in spatial ecology suggests that these effects are scale-dependent; biotic interactions should shape distributions at local scales while climate should control them at regional scales. Thus, common single-scale analyses might be unable to accurately estimate the impacts of anthropogenic modifications on biodiversity and the environment because they may miss effects at other scales. However, the large-scale datasets and computing power necessary to test scale hypotheses have not been available until recently. I conducted a cross-continental, cross-scale (almost five orders of magnitude) analysis of the influence of biotic, abiotic, and dispersal processes on the distribution of three emerging pathogens: the amphibian chytrid fungus implicated in worldwide amphibian declines, and West Nile virus and the bacterium that causes Lyme disease (Borrelia burgdorferi), which are responsible for ongoing human health crises. For all three pathogens, biotic factors were only significant predictors of distributions at local scales (~102-103 km2), whereas climate factors and a proxy for dispersal limitations were almost always only significant at relatively larger, regional scales (>104 km2). Spatial autocorrelation analyses revealed that biotic factors were relatively more variable at smaller scales whereas climatic factors were more variable at larger scales, consistent with the prediction that factors should be important at the scales they vary the most. Finally, no single scale could detect the importance of all three categories of processes. My results highlight that common, single-scale analyses can misrepresent the true impact of anthropogenic modifications on biodiversity and the environment.

Although it is important to understand how ecological processes affect patterns across scales, a critical step towards understanding the ecological impacts of climate change is to develop cross-scale frameworks that can predict these patterns. Thus, I proceeded to develop a framework to help understand how species are altering their phenology, or the timing of seasonal activities, using data collected across spatial and temporal scales. Phenological shifts are concerning because they can cause species declines by creating asynchronies or “mismatches” in plant–pollinator, plant–herbivore, and host–parasite interactions. Although advancements in the phenology of plants and animals have been widely reported and synthesized, several open knowledge gaps of critical concern have persisted. First, although many phenological studies and syntheses assume climate change as an important driver of phenological shifts, many do so without explicitly testing for any effect of climate, and among those that have, standardized climate data are rarely used. As a consequence, it remains unclear which climatic variables are driving shifts in phenology and whether geographical heterogeneity in these variables across regional scales has impacted their predictive power to detect ecological trends. Second, one of the chief concerns about species shifting the timing of their phenologies is the possibly of ecological mismatches, or asynchrony in the timing of species interactions, especially in mutualisms. I hypothesized that across regional scales, factors driving seasonality would also drive phenological shifts. I also hypothesized that small species might shift their phenology faster than large organisms because they acclimate to new conditions more easily. I addressed these questions by synthesizing 1,011 published time series of animal phenology and historic global climate data using a meta-analytical framework. I found that while temperature drives phenological responses at high latitudes, low-latitude shifts are driven by precipitation. Small body size and ectothermy were associated with strong phenological shifts, suggesting emerging asynchrony between hosts and parasites and predators and prey.

Finally, I looked at how variation across allometric scales might impact host-parasite interactions in the context of changing temperatures. Small organisms have larger performance breadths, or temperature ranges where performance is relatively high, than large organisms, and thus pathogens should typically have broader performance breadths than hosts. Therefore, the performance gap between pathogens and cold- and warm-adapted hosts should occur at relatively warm and cold temperatures, respectively. To test this hypothesis, which I coin the thermal mismatch hypothesis, we quantified the temperature-dependent susceptibility of “cold-“ and “warm-adapted” amphibian species (Atelopus zeteki, Osteopilus septentrionalis, and Anaxyrus terrestris) to the fungal pathogen Batrachochytrium dendrobatidis (Bd) using laboratory experiments and field prevalence estimates from 4,775 host populations. In both the laboratory and field, I found that peak susceptibility for cold- and warm-adapted hosts occurred at relatively warm and cool temperatures, respectively, providing support for the thermal mismatch hypothesis. Finally, I found that the temperature-dependent A. zeteki mortality patterns observed in our experiment accurately predicted historic extinctions of Atelopus spp., suggesting that climate change contributed to the extinctions. My results suggest that as climate change shifts hosts away from their optimal temperatures, the probability of infectious disease outbreaks may increase, but the effect will depend on the host species and the direction of the climate shift. My findings partly explain the tremendous variation in species’ responses to climate change.

Based on the results of my dissertation, I conclude that climate change has diverse effects on ecology across scales. Biotic interactions control disease distributions at small, local spatial scales while abiotic factors do at large scales, suggesting that climate change may impact species distributions differently at different scales. Across temporal scales, differences in acclimation rates could be affecting which species are more likely to shift their phenology. Finally, across allometric scales, differences in thermal breadths between individuals of different body sizes could alter host-parasite interactions by causing hosts to be susceptible to disease even at conditions far from where parasites perform best. Thus, I believe that my dissertation has contributed to what we understand about how scale relates to disease and biodiversity declines in the context of climate change.

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