Host-Pathogen Ecology: Effects of Species Ecology and Environmental Factors on the Intensity and Distribution of Disease Among Illinois Amphibians

Author

Brooke Lee Talley, Southern Illinois University CarbondaleFollow

Date of Award

5-1-2014

Degree Name

Doctor of Philosophy

Department

Zoology

First Advisor

Lips, Karen

Abstract

The worldwide decline of amphibians is due to several interacting factors that vary in their involvement and severity according to species, geography, environment, and individual response (Wake and Vredenburg 2008; Gahl et al. 2011). One of those threats has caused population declines globally (Stuart et al. 2004), Batrachochytrium dendrobatidis (Bd), which is the fungal pathogen that causes chytridiomycosis in amphibians (Berger et al. 1998; Longcore et al. 1999). Bd's effects are not completely known since some areas of the world have been studied (e.g., Panama, Lips et al. 2006; United States Sierra Nevada, Briggs et al. 2010; Australia, Phillott et al. 2013) while other areas have received little or no attention, often because these systems appear stable or because the effect of threats are not known. In the Midwestern United States, widespread anuran population declines occurred historically and are in some cases ongoing (e.g., Vogt 1981, Oldfield and Moriarty 1995, Brodman and Kilmurry 1998, Casper 1998, Hay 1998, Moriarty 1998, Mossman et al. 1998, Varhegyi et al. 1998, Steiner and Lehtinen 2008, Zippel and Tabaka 2008). Large-scale habitat alterations, chemical contaminations, and other threats have likely caused some Midwestern U.S. amphibian declines (Lannoo, 1998), but the role of Bd in historic and current population declines has been limited to small population surveys or incidental discovery of Bd (e.g., Pessier et al. 1999; Beasley et al. 2005; Steiner and Lehtinen 2008). I investigated the current and historic Bd infection levels among amphibians in Illinois and identified species risk factors associated with likelihood of chytridiomycosis-related death. My research questions focused on which biotic and abiotic factors explained Bd prevalence and intensities among current populations, which species risk factors would make them more likely to suffer severe Bd infection, and what the historic Bd status was in Illinois. Working with Illinois amphibians presented the opportunity to answer these research questions because Bd was already known to occur in Illinois (Pessier et al. 1999), there were a variety of anecdotal examples of historic population declines in Illinois (Beasley et al. 2005; Lannoo 1998), and extensive museum holdings were available to document the spatial and temporal pattern of Bd among Illinois populations. In the chytridiomycosis-amphibian disease system, mortality is driven by intensity of infection. Intensity is affected by many factors, including environmental temperatures, amphibian community composition, and fungal traits. However, the relative importance of biotic and abiotic factors on Bd prevalence and intensity in multispecies, natural communities is unknown for any wild populations. In 2008-2009, I conducted one of the first large-scale strategic surveys of both current and historic presence of Bd. I sampled 4,691 Illinois amphibians from current and historic populations to provide a framework of historic Bd infection and current status, and used those results to identify at-risk populations based on natural history and species risk factors. I tested 2,804 amphibians from 12 species for Bd, and determined that Bd was present in all sites, wetlands, and in all species in both years. Statewide prevalence was relatively high (2008 &mu = 34%; 2009 &mu = 55%), as was average individual infection intensity (2008 &mu = 1,773 Z_swab; 2009 &mu = 2,159 Z_swab). Wetland water temperature best explained Bd prevalence, but several biological factors explained intensity. Higher Bd intensities were correlated with species richness and indicated an amplification effect (Ostfeld and Keesing 2012). Hylid treefrogs may be amplifying species because they had the highest infection intensities and their presence was correlated with increased infection in other taxa. Bd can cause declines and extinctions in amphibian populations (Stuart et al. 2004), but other threats may also be involved (Collins and Storfer 2003). In Illinois, amphibian populations may be threatened by a variety of assaults including disease, habitat loss, chemical contaminants, and invasive species (Lannoo 1998). Management for biodiversity typically focuses on identifying and mitigating threats and prioritizing species susceptibility by identifying risk factors. I proposed to study whether species risk factors for Bd also signal general susceptibility to other threats (e.g., Lips et al. 2003; Bielby et al. 2008; Cooper et al. 2008) in Illinois amphibians. I identified nine potential risk factors for each of 21 Illinois species form the literature, and compared association of those traits with disease intensity. I used Bd intensity data from 1,445 Bd-positive amphibians collected 2008-2010. As in Chapter 2, I found that both biological and environmental factors explained disease intensity at the species levels: air temperature during the breeding season was the best predictor of infection intensity with three species biological traits also contributing (i.e., longevity, clutch size, and aquatic index). Conservation status did not explain Bd intensities, likely because conservation status is based upon rarity, population trends, and presence of threats, but which does not always include Bd susceptibility. Since most of the study species were common prior to my disease survey with relatively stable populations with no prior Bd threat, the conservation statuses used in this analysis did not predict Bd risk. Now that I have shown Bd to be widespread and at high intensities in the state, a reassessment of data included in the species status would be timely and might be warranted. I found that Bd was geographically and taxonomically widespread in Illinois, which suggested an established infection status, perhaps longer than the first report from the 1990s (Pessier et al. 1999). Also, this suggests that population declines from chytridiomycosis might have occurred historically. I used museum holdings to determine spatial and temporal distributions of Bd in Illinois amphibians. I tested 1,008 museum specimens from the vertebrate collections at Southern Illinois University, Illinois Natural History Survey, and the University of Illinois Museum of Natural History to determine the oldest date of anuran Bd infection in Illinois. I detected 110 Bd positive specimens (10.7%, CI: 9.0-12.8%) in four species collected during the 1890s-1980s. The earliest Bd record was from a Lithobates sphenocephalus collected in southern Illinois in 1900. I determined that Illinois amphibians have been living endemically with Bd for at least 113 years, extending the date of the oldest U.S. record of Bd infection by 61 years. The long-term presence of Bd, coupled with multiple anecdotal reports of population declines, suggest that Bd may have been involved in historic population declines in Illinois amphibians. I found widespread taxonomic and geographic distribution of Bd among current and historic populations of Illinois amphibians. I found a surprisingly long history of Bd in Illinois that transforms the way we consider impacts on historic species and potential co-evolution of disease in Midwestern U.S. amphibians. My finding is as old as the oldest records from Brazil, Africa, and Asia (Weldon et al. 2004; Goka et al. 2009; Schloegel et al. 2010, 2012), suggesting a more ancient history of Bd and amphibians.