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Title of the Dissertation ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS FOR THE CONSERVATION OF PANAMANIAN GOLDEN FROGS by Corinne L. Richards A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in the University of Michigan 2008 Doctoral Committee: Assistant Professor Laura Lacey Knowles, Co-Chair Professor Ronald A. Nussbaum, Co-Chair Associate Professor Mercedes Pascual Assistant Professor Johannes Foufopoulos Kevin C. Zippel, World Conservation Union Nature's first green is gold Her hardest hue to hold. Her early leaf's a flower; But only so an hour. Then leaf subsides to leaf. So Eden sank to grief, So dawn goes down to day. Nothing gold can stay. - Robert Frost © Corinne L. Richards All rights reserved 2008 To my Mom and Dad, who have always encouraged me following my dreams and to Geoff who is always game for an adventure. ii ACKNOWLEDGMENTS Many people helped bring this research to completion, both physically and intellectually, and I am grateful to them all. First, and foremost, I would like to thank my advisors and co-chairs, Lacey Knowles and Ron Nussbaum for their guidance, feedback, and constructive criticism. I am especially grateful to Lacey for her friendship and the time and effort she has invested in shaping me into an independent scientific investigator. I would also like to thank the remainder of my dissertation committee, Johannes Foufopoulos, Mercedes Pascual, and Kevin Zippel for their help and encouragement throughout. I am grateful to Amanda Zellmer, Tim Connallon, Elen Oneal, Huateng Huang, Bryan Carstens, Heather Adams, and Wendy Grus for their daily help, feedback, friendship and encouragement. Thanks also to Julia Eussen, Norah Daugherty, and Janet Griffin-Bell for their help with all my administrative questions at the University of Michigan. Thanks also to Amanda Zellmer, Lisa Martens, Wendy Luo, Jeff Yeo and Ellen Pederson for their invaluable help in the lab. Thank you to Orelis Arosemana and the rest of the administrative staff at the Smithsonian Tropical Research Institute for their help in obtaining research permits and facilitating my work in Panama. The many sweat- and bug-filled hours of Panamanian field work iii contributed by Tim Connallon, Joni Criswell, Edgardo Griffith, Wendy Grus, Tanya Hawley, Roberto Ibanez, Mark Iwen, Cesar Jaramillo, Nancy Karraker, Santiago Navas, Nick Quiring, Heidi Ross, Tracy Stetzinger, Scott Washkowiak, Lynn Zippel, and Kevin Zippel were not only critical to the success of this research, but to the maintenance of my sanity as well. Thanks guys! Thanks also to Sheila and Dennis for letting us camp on their lawn and to Hennessy Hammocks to making their hammocks insect-proof. Last, but certainly not least, I sincerely thank Geoff Zawacki for his love, constant encouragement, and patience with my frequent trips to Panama. I also thank my family, Tom, Becky, and Leslie Richards, for their support and encouragement of this great educational adventure, even though it often takes me far from home. Without their love and support, none of this would have been possible. A special “no thanks” is extended to the chytrid fungus Batrachochytrium dendrobatidis, which took the lives of many of my close, personal friends, the Panamanian golden frogs. Getting to know them was a truly amazing experience. iv TABLE OF CONTENTS DEDICATION ii ACKNOWLEDGEMENTS iii LIST OF FIGURES vi LIST OF TABLES vii ABSTRACT viii CHAPTER I. INTRODUCTION 1 II. TESTS OF PHENOTYPIC AND GENETIC CONCORDANCE AND THEIR 8 APPLICATION TO THE CONSERVATION OF PANAMANIAN GOLDEN FROGS III. QUANTIFYING THE CONTRIBUTIONS OF ALTERNATIVE LANDSCAPE 48 FACTORS TO GENE FLOW IN PANAMANIAN GOLDEN FROGS IV. PANAMANIAN GOLDEN FROGS COMBAT AN EMERGING FUNGAL 77 EPIDEMIC BY INDUCING A “BEHAVIORAL FEVER” V. CONCLUSION 95 v LIST OF FIGURES Figure 2.1 Map of Panama (lower left) and enlargement (upper right) showing 33 the approximate locations of populations sampled across the extant range of the golden frogs and proposed ESU membership (following Zippel et al. 2006). Figure 2.2 ML tree showing two clades recovered in all phylogenetic analyses. 34 Figure 3.1 Study area and sampled populations. 64 Figure 3.2 Mantel correlation coefficients (r) across landscape gradients and 65 friction ranges. Figure 3.3 Map of the least-cost paths between populations (denoted by red lines) 66 for the landscape friction gradient most strongly correlated with genetic distance (slope100). Figure 4.1 Distribution of A. zeteki body temperatures across sampling periods. 87 Figure 4.2 Average body temperatures of infected frogs are higher than those 88 uninfected for each sampling period. Figure 4.3 Inverse relationship between the log of body condition and body 89 temperature. vi LIST OF TABLES Table 2.1 Component matrix for climate PCA. 35 Table 2.2 Distribution of mtDNA haplotypes and genetic structure among 36 populations (letters correspond to localities on Fig. 2.1). Table 2.3 Analyses of molecular variance (AMOVAs). 37 Table 2.4 Identification of ESUs that differ significantly from each other 38 in mean phenotypic variables, based on nonparametric multiple comparisons (Dunnett’s C test). Table 2.5 Results of discriminant function analyses (DFAs) for models 39 containing all four morphological variables (SVL, % black, z-yellow and z-black). Table 2.6 Correlations among genetic, morphological, and environmental 40 variation showing the P- values from the pairwise Mantel tests. Table 3.1 Description of the 15 alternative landscape genetic hypotheses 67 tested. Table 3.2 Mantel test results for 22 alternative distance matrices, ranked by 68 correlation coefficient (r). Table 3.3 Evaluation of alternative landscape isolation hypotheses. 69 Table 3.4 Results of the AMOVA with individuals grouped by drainage 70 basin and population. Table 4.1 Sample sizes, means, and standard errors for body temperature 90 measurements (°C) taken over the five sampling periods. Table 4.2 Sample sizes, means, and standard errors for body temperature 91 measurements (°C) from infected and uninfected frogs during the two epidemic sampling periods. vii ABSTRACT The conservation of endangered species is best achieved by studies that consider both ecological and evolutionary aspects of population viability. Integrative research of this type is especially important for amphibian species as they have been plagued by rapid, global declines and extinctions in recent decades. The aims of this dissertation were to contribute to the conservation of two such declining amphibians, the Panamanian golden frogs, Atelopus varius and A. zeteki, as well as demonstrate the combined utilities of morphological, ecological, and genetic analyses in providing an integrative framework for informing wildlife conservation initiatives. The results of this research engender several important considerations for the conservation of these critically endangered and culturally important amphibians. In my first study, multivariate phenotypic and mitochondrial DNA analyses were used to verify that previously defined management units are supported by concordant patterns of variation among populations as well as to identify phenotypic traits that may be associated with adaptive divergence. The second study examined the contributions of alternative landscape factors to patterns of genetic variation among golden frog populations, highlighting the importance of maintaining the integrity of low slope areas, such as riparian habitat corridors and mountain ridges, for gene flow. The third and final study demonstrated the importance of genetic and phenotypic variability in allowing golden frog populations to adapt to environmental viii change by examining the relationship between thermoregulation behavior and susceptibility to a fungal epidemic. Here I demonstrated that the behavioral fever response mounted by one golden frog population is effective in reducing the odds of infection during a chytridiomycosis epidemic. I concluded by summarizing the implications of this work for the management of Panamanian golden frogs and considering the applicability of these findings to the conservation of other endangered species of Atelopus. ix CHAPTER I INTRODUCTION Conservation biology is truly a multidisciplinary science in that it focuses the knowledge and tools of all biological disciplines, from molecular biology to population biology, on the conservation of biodiversity (Soulé & Wilcox 1980). However, to be effective, there must be a high level of integration among the separate fields as each offers unique insight into the processes affecting viability (Clarke 2000). Decisions based on just one or few lines of inquiry run the risk of overlooking factors critical to effective management, especially when faced with high levels of intraspecific variation. The need for such integrative studies in the conservation of amphibian species is especially poignant as amphibian populations have undergone rapid, global declines and extinctions in recent decades, and many of the most threatened species are also little known (Pounds 2001; Stuart et al. 2004; Wake 1991; Young 2001; Young et al. 2004). Over 30% of all amphibian species are now considered threatened, and as many as 122 species may have become extinct (Stuart et al. 2004). In many cases, this can be attributed to threats amphibians share with other taxa, including habitat destruction and fragmentation, introduction of predators and competitors, pesticides, acid precipitation, increased ultraviolet irradiation,
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