Ecology of Neotropical Arboreal Snakes and Behavior of New World Mollusk-Eating Snakes Julie M
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Old Dominion University ODU Digital Commons Biological Sciences Theses & Dissertations Biological Sciences Winter 2009 Ecology of Neotropical Arboreal Snakes and Behavior of New World Mollusk-Eating Snakes Julie M. Ray Old Dominion University Follow this and additional works at: https://digitalcommons.odu.edu/biology_etds Part of the Behavior and Ethology Commons, and the Environmental Sciences Commons Recommended Citation Ray, Julie M.. "Ecology of Neotropical Arboreal Snakes and Behavior of New World Mollusk-Eating Snakes" (2009). Doctor of Philosophy (PhD), dissertation, Biological Sciences, Old Dominion University, DOI: 10.25777/ysd1-2855 https://digitalcommons.odu.edu/biology_etds/84 This Dissertation is brought to you for free and open access by the Biological Sciences at ODU Digital Commons. It has been accepted for inclusion in Biological Sciences Theses & Dissertations by an authorized administrator of ODU Digital Commons. For more information, please contact [email protected]. ECOLOGY OF NEOTROPICAL ARBOREAL SNAKES AND BEHAVIOR OF NEW WORLD MOLLUSK-EATING SNAKES by Julie M. Ray M.S. May 2004, Northern Illinois University B.S. May 2000, University of Wisconsin - Stevens Point A Dissertation Submitted to the Faculty of Old Dominion University in Partial Fulfillment of the Requirement for the Degree of DOCTOR OF PHILOSOPHY ECOLOGICAL SCIENCES OLD DOMINION UNIVERSITY December 2009 Approved by: Alan H. SavTtzky^Director) Christopher A. Bincklej (Member) ABSTRACT ECOLOGY OF NEOTROPICAL ARBOREAL SNAKES AND BEHAVIOR OF NEW WORLD MOLLUSK-EATING SNAKES Julie M. Ray Old Dominion University, 2009 Director: Dr. Alan H. Savitzky The Neotropics is a biologically diverse region that provides many opportunities for ecological and behavioral studies. I utilized the speciose ophidian fauna of central Panama to explore the general ecology of arboreal snakes, the defensive behaviors of the snake community, and the diet of mollusk-eating snakes. I studied arboreal species to understand interspecific relationships in several morphometric characters and to examine preferences in habitat. There were significant morphometric differences in relative length of jaw, mass, tail length, and size at midbody. The arboreal realm was partitioned among species by distance to ground, distance to water, and diameter of the perch. Correlations were found in some species between body mass or length and distance to the ground and leaf length. Additionally, many arboreal species have been documented to bridge gaps in vegetation, but few studies have investigated this behavior systematically. I tested average bridging ability of five Neotropical arboreal snakes and investigated morphological elements underlying differences in relative cantilevering ability. I found significant interspecific differences in average and maximum distances bridged. Species with the relative heaviest mass had the lowest cantilever ratios. Defensive behaviors, which are employed for protection from predators, also were evaluated. I document interspecific differences in these behaviors at the community level. With knowledge gained from the ophidian community in Panama, I further documented on the defensive behaviors of other New World mollusk-eating snakes. Finally, I studied the diet of selected mollusk-eating snakes. I evaluated fecal samples of Dipsas and Sibon and found that their diet is broader than mollusks alone. In fact, a majority of Dipsas in central Panama were feeding on oligochaetes. Some species of Sibon were feeding on mollusks, whereas others fed primarily on amphibian eggs and oligochaetes. The discovery of a broader diet in these taxa may have conservation implications as populations of amphibians and terrestrial mollusks decline worldwide. The expansion of our knowledge of the natural history, ecology, and behavior of Neotropical snakes has provided information that will be important for future studies of community- and ecosystem-level interactions and for the conservation of the biota of central Panama. iv This dissertation is dedicated to Pablo Santana, Alexander Santana, and Aurelio Gonzalez and to my parents, John and Joanne Ray. V ACKNOWLEDGMENTS As with many projects of this magnitude, especially those performed in extreme locations including lands where the language and culture are foreign, many persons deserve acknowledgement. First, thank you to my committee and the people who helped me get to Panama: Alan Savitzky, Frank Day, Christopher Binckley, Roberto "Figa" Brenes, Karen Lips, Chad Montgomery, and Matt Whiles. Thank you to the part-time field help: Santana Arcia, Sarah Becker, Elicia Cano, Clint and Tammy Otto, Sandra Galeano, Scott Goetz, Edgardo Griffith, Andrew Hein, Melissa Miller, Heidi Ross, Amanda Rugenski, and Doug Woodhams. Thank you to the park staff: Jose Perez (director of the park), Natalio Vargas, Jose Carmen, and Andres Gonzalez. A very special thanks to Aurelio Gonzalez, Alexander Santana, and Pablo Santana for extensive help in the field. Thank you for assistance with collections, analyses, or logistics to Mike Lane, Andy Mahon, Heidi Mahon, Greg Pauly, Richard B. King, Jace Robinson, Bud Rodi, and Jeremy Weisz. Thank you to all funding sources: American Society of Ichthyologists and Herpetologists, Chicago Herpetological Society, National Science Fund, North Carolina Herpetological Society, Sigma Xi, Society for the Study of Amphibians and Reptiles, Sophie Danforth Conservation Fund, and Wisconsin Division for Vocational Rehabilitation. Thank you to the Smithsonian Tropical Research Institute and ANAM, the Panamanian Environmental Authority, for logistical support while in Panama. Finally, to Lucy, mi chico, and Brett for making me believe. VI TABLE OF CONTENTS Page LIST OF TABLES ix LIST OF FIGURES xii Chapter I: GENERAL INTRODUCTION 1 INTRODUCTION 1 STUDY SITES 1 PARQUE NACIONAL GENERAL DE DIVISION OMAR TORRIJOS HERRERA, COCLE PROVINCE, REPUBLIC OF PANAMA 2 ALTOS DEL MARIA, PANAMA PROVINCE, REPUBLIC OF PANAMA 4 CENTRAL VALLEY, CALIFORNIA 4 LAKE ERIE ISLANDS, OTTAWA AND ERIE COUNTIES, OHIO 5 POTAWATOMI WOODS FOREST PRESERVE AND KISHWAUKEE RIVER STATE FISH AND WILDLIFE AREA, KIRKLAND, ILLINOIS 6 BEAVER ISLAND, MICHIGAN 6 STUDY ORGANISMS 6 NEOTROPICAL SNAKE COMMUNITIES 6 NEOTROPICAL ARBOREAL SNAKES 7 MOLLUSK-EATING SNAKES 8 TROPICAL STUDY SPECIES 9 TEMPERATE STUDY SPECIES 12 GENERAL METHODS 13 METHODS FOR TROPICAL RESEARCH 13 METHODS FOR TEMPERATE RESEARCH 15 II: MORPHOMETRICS AND NICHE PARTITIONING OF A NEOTROPICAL ARBOREAL SNAKE ASSEMBLAGE 16 INTRODUCTION 16 MATERIALS AND METHODS 18 MORPHOMETRIC DATA COLLECTION 18 ENVIRONMENTAL DATA COLLECTION 19 GENERAL CHARACTERISTICS OF THE SNAKE ASSEMBLAGE 20 STATISTIC - MORPHOMETRIC ANALYSES 20 STATISTICS - ENVIRONMENTAL ANALYSES 22 vii RESULTS 23 GENERAL CHARACTERISTICS OF THE SNAKE ASSEMBLAGE 23 MORPHOMETRIC ANALYSES 23 ENVIRONMENTAL ANALYSES 29 DISCUSSION 38 III: BRIDGING THE GAB: INTERSPECIFIC DIFFERENCES IN CANTILEVERING ABILITY IN A NEOTROPICAL ARBOREAL SNAKE ASSEMBLAGE 44 INTRODUCTION 44 MATERIALS AND METHODS 45 STUDY SITE AND SPECIES 45 EXPERIMENTAL DESIGN 46 FIELD OBSERVATIONS 47 STATISTICS 48 RESULTS 48 DISCUSSION 53 IV: DEFENSIVE BEHAVIORS OF A NEOTROPICAL SNAKE COMMUNITY 56 INTRODUCTION 56 MATERIALS AND METHODS 60 STUDY SITES 60 STUDY SPECIES 61 BEHAVIORAL TRIALS AND ANALYSES 61 QUANTITATIVE ANALYSIS OF DEFENSIVE BEHAVIORS 61 PHYLOGENETIC BASIS OF BEHAVIORS 63 ANALYSIS OF SCARS 64 POTENTIAL OPHIDIAN PREDATORS 64 RESULTS 65 BEHAVIORAL DIVERSITY 65 QUANTITATIVE DATA 65 PHYLOGENETIC BASIS OF BEHAVIORS 71 ANALYSIS OF SCARS 78 POTENTIAL PREDATORS OF SNAKES 81 DISCUSSION 83 V: DEFENSIVE BEHAVIORS OF NEW WORLD MOLLUSK-EATING SNAKES 88 INTRODUCTION 88 STORERIA 88 CONTIA TENUIS 89 D1PSAS 90 SIBON. 91 viii NINIA 92 TOMODON 92 SIBYNOMORPHUS 93 MATERIALS AND METHODS 93 STUDY SPECIES AND SITES 93 DOCUMENTATION OF DEFENSIVE BEHAVIORS 93 PHYLOGENETIC BASIS OF BEHAVIORS 95 RESULTS 96 DEFENSIVE BEHAVIORS 96 CONTIA TENUIS 97 QUANTITATIVE ANALYSES OF CONTIA TENUIS 97 STORERIA OCCIPITOMACULATA 99 STORERIA DEKAYI 100 DIPSAS CATESBYI. 100 DIPSAS SP 100 DIPSAS NICHOLSI 101 SIBON ARGUS 102 SIBON LONGIFRENIS 102 SIBON NEBULATUS 103 SIBON ANNULATUS 104 NINIA SP 104 NINIA CELATA 104 NINIA MACULATA 104 PHYLOGENETIC BASIS OF BEHAVIORS 104 DISCUSSION 105 VI: DIET OF THE NEOTROPICAL SNAKE GENERA DIPSAS AND SIBON 116 INTRODUCTION 116 OPHIDIAN ADAPTATIONS FOR THE CONSUMPTION OF MOLLUSKS 117 REVIEW OF DIPSAS AND SIBON DIET 119 MATERIALS AND METHODS 121 STATISTICS 123 RESULTS 123 DISCUSSION 131 CONSERVATION IMPLICATIONS IN RELATION TO DIET 134 RELATIONSHIPS WITHIN DIPSADINAE 135 FUTURE DIRECTIONS 136 VII: GENERAL CONCLUSIONS 137 REFERENCES 139 VITA 154 IX LIST OF TABLES Table Page 1.1. Study transects in Parque Nacional G. D. Omar Torrijos Herrera (PNGDOTH) 2 1.2. Study transects in Altos del Maria 5 1.3. Species documented in Parque Nacional G. D. Omar Torrijos Herrera (PNGDOTH) and in Altos del Maria (ADM) ! 10 1.4. Data collected for snakes captured in Parque Nacional G. D. Omar Torrijos Herrera, 2006 - 2007 14 2.1. Relative abundance and general natural history information for arboreal snakes captured in 2006-2007 PNGDOTH 24 2.2. Results of the ANCOVA testing for intraspecific differences in mass (corrected for SVL) for arboreal snakes in PNGDOTH 28 2.3. Results of a Student-Newman-Kuels post-hoc analysis for interspecific differences in size at midbody (log-transformed) among arboreal snakes 29 2.4. Paired comparisons of between group centroids of unique morphometric measurements for eight arboreal