Distribution and Environmental Correlates Between Amphibians and the Fungal Pathogen, Batrachochytrium Dendrobatidis
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Distribution and environmental correlates between amphibians and the fungal pathogen, Batrachochytrium dendrobatidis DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Chelsea Anne Korfel Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2012 Dissertation Committee: Thomas Hetherington, Advisor Stanley Gehrt, Thomas Mitchell, David Stetson Copyright by Chelsea Anne Korfel 2012 Abstract Amphibian populations worldwide are vulnerable to a variety of threats, and one serious cause of population declines and extinctions is the pathogenic fungus Batrachochytrium dendrobatidis (Bd). Amphibian species of tropical, montane regions have suffered the greatest impacts of Bd- related declines, extirpations, and extinctions. Bd is also present in temperate regions, but its effects on temperate amphibian species appear to be less severe, although they remain poorly understood. Bd impacts populations, species, and individuals differentially and environmental factors affect host-pathogen relationships. Temperature, specifically, is a major factor impacting the growth and spread of Bd and the ability of amphibians to resist disease. Temperature varies along seasonal, altitudinal, and landscape gradients. Interactions of hosts and the pathogen in tropical and temperate regions along these environmental gradients are explored here. Chapter One: I compiled a thorough review of previous research on the influence of temperature on the interaction between amphibian hosts and the fungal pathogen Bd. The review includes both laboratory and field studies, which explore the effects of microhabitat and regional temperature and the effects of global climate change on amphibian populations. Despite thorough laboratory studies, complete understanding regarding the influence of temperature on the interaction between amphibian hosts and Bd in the natural environment is necessary for understanding dynamics of disease and designing appropriate conservation strategies. Chapter Two: I conducted a survey of Bd prevalence and infection load in amphibian communities in the temperate landscape of central Ohio and engaged other amphibian biologists to create a statewide survey. Bd is widespread throughout Ohio, infecting the ii skin of 19.5% of all amphibians sampled in this study. Prevalence was highest among bullfrogs (59.2%, Lithobates catesbeianus) and the highest infection intensity, 1,946,586 ZE, was in a cricket frog (Acris crepitans). Infection intensities among green frogs (L. clamitans) were relatively high (19,328 ZE) and infection prevalence was moderate (27.3%). No obvious symptoms of infection were observed, even for amphibians with high intensity fungal loads. This survey established that Bd is well-established in a variety of habitats in Ohio and could impact amphibian populations. Chapter Three: I studied Bd prevalence and fungal load intensity with respect to both season and habitat in two common amphibian hosts (green frogs, Lithobates clamitans, and American bullfrogs, L. catesbeianus) in central Ohio, USA. Bd prevalence, the percent of infected animals sampled, was highest among samples collected in spring (89%) and from forested streams (54%). Both were associated with cooler temperatures. Bd infection intensities, the severity of infection per individual, were highest among samples collected in summer (8,240 ± 31,852 ZE) and from emergent streams (72,645 ± 18,092 ZE). Both summer and emergent streams were associated with warm temperatures. These relationships may result from tradeoffs in the effect of temperature on parameters of Bd life history and amphibian behaviors. For example, amphibians congregate in breeding pools in the spring, which could facilitate the spread of disease. However, in summer amphibians in open canopy habitat can bask at temperatures above the lethal temperature for Bd and minimize infections. Despite these factors, amphibians with poor immune function are likely to develop severe infections. Chapter Four: I studied Bd prevalence in marsupial frog (Gastrotheca pseustes) tadpoles in mid to high altitude pools (2500-4200 masl) in Ecuador’s Cajas National Park and the effects of Bd on infected tadpoles. While other field studies have examined the high- temperature climatic threshold for Bd associated with low altitudes, this work investigates a lower critical temperature for Bd prevalence at mid to high elevations. At the upper end of its altitudinal distribution, G. pseustes e eriences tem eratures ithin iii the same ran e as the la orator -determined tem eratures - 0 C) at hich d ro th and development slows. I found widespread but low prevalence of Bd throughout the altitudinal range of our study, and no difference in prevalence between high and mid altitude pools along this gradient. Body condition of infected tadpoles was poor compared to disease-free conspecifics, and there was no difference in body condition of infected tadpoles at lower versus higher altitude sites. Despite experiencing temperatures cooler than the ideal range predicted for Bd, the fungus impacts G. pseustes tadpoles at both mid and high altitudes equally. Bd prevalence at mid to high altitudes was comparatively lower than Bd prevalence identified in other studies conducted at low elevations, which may suggest that Bd is of less concern for amphibians with mid to high altitudinal distributions. Chapter Five: Atelopus exiguus is one of the few persisting species of harlequin frogs (genus Atelopus), a genus that has suffered severe declines and extirpations from epizootic Bd in Latin America. I hypothesize that a series of hot and dry years in the early 990’s in s ner ith the arrival of d to the area in the late 980’s ma e res onsi le for the initial population decline. However, the population remains small and all sampled individuals in the current population were not Bd positive despite the detection of Bd in nearby populations of Gastrotheca pseustes. I suggest that this population has adapted to persist with endemic Bd and provides hope for the persistence of global amphibian species. Research in this dissertation provides significant insight into the relationship between amphibians and the fungal pathogen Bd in a variety of environments, and contributes recommendations to inform future efforts in global amphibian conservation. iv Dedication For the frogs, all the people who care about them, and especially the people who taught me to care about them (especially you, Grampa). Frogs do for the night what birds do for the day... they give it a voice. And that voice is a varied and stirring thing that ought to be better known. Archie Carr v Acknowledgments The accumulation of data, variety of perspectives, thoughtful insights, and writing process demonstrated here could not have been completed without the help of many amazing people in my life: some who knew me before I began, others who entered my life because of this work, and others who I’ve met alon the a . Your time, energy, and expertise are appreciated. You have been blessings in my life! M famil has een a constant source of su ort as I’ve follo ed m heart and ursued a somewhat unpredictable route towards a yet unknown career. Mom and Dad, thanks for your encouragement, your patience with my free-spirited ways, your hugs, and for seeing me throu h nearl 25 ears of schoolin . Grann ird, ou’ll never kno ho much our middle-of-the-day phone calls have been my sanity throughout all of this, I love you! Ashle and Lindse , ou’re stuck ith me as a sister, ut I’m so lad ou’re m est friends! Rick, Diane, Tiffan , Parker, Grandmother and Grandadd , I’m so lad ou’re a part of who I call family. Thanks for sharing Brad with me. He’s an amazing field assistant, I’m an unconventional ife, and I appreciate your patience and understanding. With much gratitude, I acknowledge the expertise of my PhD adviser, my committee, and my undergraduate adviser. Tom Hetherington, thank you for letting me pursue my passion, for giving me space to work independently but always being there to guide me, for many hours of planning, thinking, field work, “hmmm….s,” discussin , and editin . My committee members, Dave Stetson, Tom Mitchell, and Stan Gehrt challenged me to vi think critically about my work. I am indebted to them for their varied perspectives and contri utions. Kell , ou’ve su orted me from the da e first met hen I stum led into the UD biology office, you have guided and encouraged me through graduate school, and I hope you continue to do so as I pursue my (or maybe your!) career. For the many friendships and sources of spiritual support that have brought joy to my life. The Branches and the Marianist family, my UD girlfriends, my herp friends, SBS Little Rock, Glene Mynhardt, Dan Fink, Charlie Pizanis, Carrie Petruso, Elizabeth Goussetis, Lauren Kelley. You are the people who have prayed for me and reminded me that there is a reason I’m on this ath and the lon and meanderin journey is all worthwhile. My dream was to work in the tropics, but the work came with many unforeseen challenges that could only be faced with the guidance and support of friends I met along the way. Thank you to Carlos Martinez, David Salazar, Santiago Ron, Luis Coloma, and Elicio Tapia for starting me off and contributing to my research along the way. Thank you to Ernesto Arbelaez and Amanda Vega for being my ground team, for helping me open a bank account, buy a car, slide down a mountain in the car, learn to speak and understand Cuencano, and showing me the beautiful country of Ecuador in spur-of-the- moment adventures, all while literally running a zoo. I appreciate your dedication to conservation and wish you the best with Bioparque Amaru. Thank you to Jose Caceres for being both a friend and my research coordinator for Cajas National Park. Thank you to Giovanni Onore, entomologist, Marianist, and chef extraordinaire! Thank you to my husband.