Of toads and tolerance: intraspecific variation in host persistence when challenged by disease
| dc.contributor.author | Hardy, Bennett, author | |
| dc.contributor.author | Bailey, Larissa, advisor | |
| dc.contributor.author | Funk, W. Christopher, advisor | |
| dc.contributor.author | Huyvaert, Kathryn P., committee member | |
| dc.contributor.author | Muths, Erin, committee member | |
| dc.contributor.author | Hoke, Kimberly, committee member | |
| dc.date.accessioned | 2023-08-28T10:29:00Z | |
| dc.date.available | 2023-08-28T10:29:00Z | |
| dc.date.issued | 2023 | |
| dc.description.abstract | Infectious diseases are increasingly known to drive population declines and extinctions and ultimately contribute to the loss of global biodiversity. This phenomenon is none more apparent than in the extinctions and extirpations of over 500 amphibian species worldwide due to a disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). This ongoing loss of amphibian diversity is concerning given the important roles amphibians serve for ecosystem function, ecosystem services, and pharmacology, among others. To mitigate these declines, scientists must understand the pathogen, environmental, and host factors that interact to affect disease outcomes. Despite over 25 years of research on amphibian declines and Bd, there is still much we can learn that can crucially inform our conservation actions. For instance, while Bd is undoubtedly a lethal pathogen of severe threat to many amphibians around the world, researchers have observed substantial variation in host responses to Bd infection or presence in the wild and in the laboratory. While many host populations are extirpated by Bd, some persist at lower abundances or rebound completely. Understanding variation in the mechanisms of host population persistence may provide vital hints for how to better conserve vulnerable amphibian populations. This leads me to the central question of my dissertation: "Why do some populations persist with Bd while others do not?". I address this question in three chapters by studying variation in boreal toad (Anaxyrus boreas boreas) responses to Bd at several locations across the toad's range. The boreal toad occurs from coastal southern Alaska down into Colorado. Boreal toads are susceptible to Bd and have experienced dramatic declines and extirpations at the southern edge of its range in New Mexico, Colorado, and southwestern Wyoming, which together are considered the southern Rocky Mountain population. Populations in the northern portion of its range, however, appear to be persisting despite the confirmed presence, and high prevalence, of Bd. Two major hypotheses for the difference in apparent persistence of boreal toad populations with Bd across regions include a) differences in demographic compensation and b) differences in host susceptibility. Therefore, I used observational and experimental studies to investigate these hypotheses to better understand the contexts in which boreal toads persist with Bd. In my first chapter, I leveraged a long-term mark-recapture dataset from multiple populations of boreal toads across a high-elevation gradient in Colorado to test for the existence of compensatory recruitment. Compensatory recruitment is a hypothesized mechanism of host persistence when challenged by disease where hosts increase their baseline recruitment, which compensates for decreased survival attributed to disease, and ultimately stabilizes or slows population declines. Limitations from prior investigations of this phenomenon in other amphibian-Bd systems include the lack of pre-Bd monitoring data, the lack of population replication, and studies that primarily examine low elevation populations. I found a life history trade-off between survival and recruitment across elevations, where high-elevation toads have high survival but low recruitment and vice versa at lower elevations. Once Bd arrived, however, recruitment was reduced across all populations and survival was reduced to zero. Estimates of population abundance and population growth rates were also variable prior to Bd arrival, but dramatically declined after. I did not find evidence for compensatory recruitment in these high elevation boreal toad populations. My findings highlight that demographic responses to disease may be environmentally context-dependent, and that high elevation amphibian populations are particularly vulnerable to the effects of Bd. In Chapter 2, I used a laboratory exposure experiment to identify an appropriate isolate of Bd to use in a future experiment designed to investigate differential susceptibility of boreal toad populations to Bd (Chapter 3). While researchers have known about the potential for laboratory-maintained Bd cultures to lose pathogenicity over time (i.e., pathogen attenuation), most exposure studies use isolates that are available to them, regardless of how long they have been maintained in the laboratory, or are unaware of their chosen isolate's culture history. I exposed wild-caught, captive-reared boreal toads to three different isolates of Bd that varied in the amount of time maintained in the lab (old vs. new) and the geographic origin of the isolate compared to the host (local vs. novel) to determine the best isolate for use in Chapter 3. I found that boreal toads exposed to the older isolates had higher weekly survival probabilities than those exposed to the new isolate, indicating pathogen attenuation for older isolates. This effect was also mediated by individual body mass, where larger toads had higher survival. My findings indicate that newer, local isolates are likely better choices when exposing amphibian hosts to Bd and that isolate age and host weight can dramatically affect our inferences from exposure studies. In my third chapter, I tested the hypothesis that boreal toads exhibit intraspecific variation in susceptibility to Bd. I expected that the host defense strategies of tolerance and resistance are stronger in boreal toads from Wyoming, and weaker in boreal toads from Colorado, and are primarily responsible for our observations of boreal toad population declines in Colorado, and relative population persistence in Wyoming. Previous studies investigating variation in amphibian host tolerance and resistance to Bd are predominantly focused on species-level comparisons, with fewer focusing on intraspecific variation. Most studies also lack replication among strata of interest (e.g., geography, disease prevalence, host genotypes), and none use a robust methodological framework that can reveal host and pathogen dynamics throughout experimental exposures. Therefore, I conducted a laboratory experimental exposure of boreal toads to Bd, informed by the results of Chapter 2. I included toads from two populations in Colorado and two populations in Wyoming, representing replicates from our strata of interest (i.e., differences in decline severity). Using a multistate modeling approach, I modeled the effects of static covariates (e.g., host population origin, treatment dose of Bd, etc.) and dynamic, individual, time-varying covariates (e.g., weekly individual Bd load, weekly change in individual body mass, etc.) on boreal toad weekly survival and state transition probabilities. State transitions included the weekly probability an individual would clear their infection, or whether a cleared individual would re-gain infection, providing insight into typically hidden infection dynamics. I found that boreal toads from Colorado populations had lower weekly survival probabilities than those from Wyoming when comparing identical Bd loads. This is evidence of increased tolerance to Bd in Wyoming toad populations. As in Chapter 2, individual mass was also important at predicting the effects of Bd on weekly survival probabilities of boreal toads. Boreal toads from Colorado had similar peak Bd loads and cleared Bd at the same probabilities as Wyoming. Colorado boreal toads, however, were on average quicker to reach their peak Bd infection loads and had increased probabilities of re-gaining their infections. These results provide some support for increased resistance among boreal toads in Wyoming compared to those in Colorado. My findings highlight that differential susceptibility to Bd among boreal toads from different regions may play a crucial role in generating the disparity in decline severity across the region. In conclusion, my dissertation provides evidence that intraspecific variation in persistence, when challenged by disease, is an important driver of host-pathogen dynamics. My research has filled vital research gaps for an imperiled amphibian species with the goal of helping wildlife managers make tough conservation decisions about host translocations, reintroductions, and captive breeding. I hope my work aids in the persistence of an iconic Rocky Mountain amphibian for years to come. | |
| dc.format.medium | born digital | |
| dc.format.medium | doctoral dissertations | |
| dc.identifier | Hardy_colostate_0053A_17873.pdf | |
| dc.identifier.uri | https://hdl.handle.net/10217/236924 | |
| dc.language | English | |
| dc.language.iso | eng | |
| dc.publisher | Colorado State University. Libraries | |
| dc.relation.ispartof | 2020- | |
| dc.rights | Copyright and other restrictions may apply. User is responsible for compliance with all applicable laws. For information about copyright law, please see https://libguides.colostate.edu/copyright. | |
| dc.title | Of toads and tolerance: intraspecific variation in host persistence when challenged by disease | |
| dc.type | Text | |
| dcterms.rights.dpla | This Item is protected by copyright and/or related rights (https://rightsstatements.org/vocab/InC/1.0/). You are free to use this Item in any way that is permitted by the copyright and related rights legislation that applies to your use. For other uses you need to obtain permission from the rights-holder(s). | |
| thesis.degree.discipline | Ecology | |
| thesis.degree.grantor | Colorado State University | |
| thesis.degree.level | Doctoral | |
| thesis.degree.name | Doctor of Philosophy (Ph.D.) |
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