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The Ecology of Developmental Timing in a Neotropical Turtle

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The Ecology of Developmental Timing in a Neotropical Turtle THE ECOLOGY OF DEVELOPMENTAL TIMING IN A NEOTROPICAL TURTLE, KINOSTERNON LEUCOSTOMUM A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Brian D. Horne August 2007 © 2007 Brian D. Horne All Rights Reserved This dissertation titled THE ECOLOGY OF DEVELOPMENTAL TIMING IN A NEOTROPICAL TURTLE, KINOSTERNON LEUCOSTOMUM by BRIAN D. HORNE has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Willem M. Roosenburg Associate Professor of Biological Sciences Benjamin M. Ogles Dean, College of Arts and Sciences Abstract HORNE, BRIAN D., Ph.D., August 2007, Biological Sciences THE ECOLOGY OF DEVELOPMENTAL TIMING IN A NEOTROPICAL TURTLE, KINOSTERNON LEUCOSTOMUM (136 pp.) Director of Dissertation: Willem M. Roosenburg I studied how the expression, timing, and duration of embryonic diapause (ED), morphogenesis, and embryonic aestivation (EA) relate to variation in environmental conditions experienced by turtle embryos. ED and EA are putative mechanisms that increase embryonic survivorship. ED arrests development before main morphogenesis and is induced before the onset of adverse environmental conditions. EA prolongs incubation by depressing the metabolism of the embryo after completion of morphogenesis. I tested two hypotheses with regard to the environmental conditions that stimulate ED and EA based on climatic patterns. My first hypothesis suggested a single suitable developmental period (SDT; periods when soil moisture and temperature of nesting substrate are within the physiological tolerances of developing embryos) during the dry seasons, and my second hypothesis predicted two SDTs at the transition from the rainy and dry seasons. Incubation experiments using white-lipped mud turtle, Kinosternon leucostomum, embryos confirmed that temperature is an important factor in determining the duration of both ED and morphogenesis, and that morphogenesis occurs during the dry season SDT. Female size generally correlates positively with egg and offspring size. However, when embryos experience prolonged incubation periods, females may alter their reproductive investment strategies to offset potential additional embryonic energy expenditures. When accounting for female size, larger clutches had eggs with greater mass than smaller clutches; and egg size increased with female size. Thus in K. leucostomum the typical relationship between egg size and clutch size as it pertains to division of maternal resources per propagule is weakened by the embryo’s ability to arrest development during extended incubation periods. Nearly 50% of all turtle taxa are undocumented as to the expression of ED. I used categorical data modeling to create probabilities for predicting ED expression. Results indicate that greater than one-half of the undocumented species have a high probability of expressing ED. Conservation projects that alter incubation conditions of eggs may alter life history patterns and create unforeseen implications for population viability. Thus, it is critical for biologists performing ex-situ chelonian conservation projects with species which posses prolonged incubation periods to understand the role of ED and EA has in chelonian developmental ecology. Approved: Willem M. Roosenburg Associate Professor, Biological Sciences Dedication For my parents, Dick and Rama, who gave me my first pet snake when I was four, and my siblings, Mike and Jen, who have always been my best friends. Acknowledgments I have a great many people to thank for their assistance in completing my dissertation, without their help, I would not been able to accomplish this project. Willem Roosenburg, my dissertation advisor was gracious in his willingness to indorse my endeavors and he did not shy away from supporting my decisions to conduct fieldwork in Mexico. I am thankful for his insights into chelonian reproductive ecology, but more importantly, I am thankful that he believed in my abilities as a scientist when others doubted. My departmental committee members Geoff Buckley, Kelly Johnson, Don Miles, and Matt White provided guidance during the early phases of designing my dissertation proposal and willingly gave of their time during the both my proposal defense and comprehensive exams. Steve Reilly was also instrumental in helping formulate the model of facultative developmental timing. The Department of Biological Sciences provided funding for me to attend national and international meetings, as well as to participate in an Organization of Tropical Studies graduate course. The late Mike Ewert guided me throughout the design of this project. I truly wish he could have seen the results; I know he would have enjoyed them. My great friend, the late Abigail Sorenson, shared my enthusiasm for tropical turtles and assisted in the field; I wish she too could have seen the results of this project. Special thanks must be given to my collaborators in Mexico: Ottho Aquino, Gustavo Aguirre León, Erasmo Cazares Hernández, Miguel de la Torre Loranca, Veronica Espejel González, Nora Lopez, Marco Antonio Lopez Luna, Basillio Sanchez, and Eladio Velasco; without their assistance I would never have been able to make the cultural conversion necessary to accomplish my field research. Rosamond Coates, Gonzalo Perez, and Martin Ricker, were instrumental in providing a base for my field research. I am indebted to Dick Vogt for his invitation to work at his previous field sites and his assistance in getting me started in Mexico. His extensive knowledge of the region’s turtles laid the groundwork for my research. Peter Pritchard and Tim Walsh of the Chelonian Institute and Jamie Pena of the Glady’s Porter Zoo are owed a debt of gratitude for facilitating the importation of my samples from Mexico. Additionally, John Iverson shared unpublished reproductive data on Geoemydids. My fellow graduate students both current and past provided immeasurable assistance throughout my time at OU; I will remember them fondly. My lab mates: Phil Allman, Dawn Ford, Tomek Radizo, and Laura Stadler were truly great sounding boards during the development of this project and with its analysis. I thank them for being some of my toughest critics. I must thank Noah Anderson and Tom Lorenz for their numerous discussions on turtle nesting ecology; and many thanks are due to Jonathan Willis for endearing me to the nuisances of survivorship analyses. My oldest friend, Bob Stone, encouraged my appreciation of life beyond academia. My brother, Mike, and my sister, Jen, have always been ready to lend an ear, offer a hand, or give word of encouragement; for this, I am humbly grateful. My parents Dick and Rama not only encouraged me to chase my dreams but also generously provided the extra financial resources that made this project a possible. Words cannot express my true gratitude towards my family; they have and always will be the principal factor of my success. No one could ask for greater family support. 9 Table of Contents Page Abstract ……………………………………………………………………………….4 Acknowledgements …………………………………………………………….……..7 List of Tables …………………………………………………………………………10 List of Figures ………………………………………………………………………...11 Chapter 1: An Evolutionary Context for Embryonic Diapause …………...……...…13 Chapter 2: Embryonic Diapause in Turtles: Its Geographic Distribution Defined…..18 Chapter 3: Strategies for Seasonal Synchronization of Morphogenesis and Increasing Embryonic Survivorship: Modeling Developmental Timing in a Neotropical Turtle………………………………………………………………………………….33 Chapter 4: The Effect of Female Size on Egg/Clutch Size and Hatching Success in a Turtle (Kinosternon leucostomum) with Embryonic Diapause ………………………62 Literature Cited ………………………………………………………………………76 Appendix A. ED Categorical Modeling Database…………………..………………..100 Appendix B. Calculated Probabilities of Expressing ED …………………………….110 Appendix C. Calculated Probabilities of Not Expressing ED ………………………..112 Appendix D. Tables…………………………………………………………………...113 Appendix E. Figures…………………….………………………………………….….118 10 List of Tables Table Page 3.1: Summary of Constant Temperature Equivalents (CTE) based on timing of oviposition and timing of developmental event. ……………………..……………113 3.2: Percent mortality by stage per month ………………………………………….114 4.1: Gravid female body size, clutch size and hatchlings per clutch………..............115 4.2: Morphological differences (averaged by clutch) between population egg parameters and eggs that produce hatchlings………………………………………...116 4.3: Relationship between hatching success and egg parameters……………………117 11 List of Figures Figure Page 2.1: Geographic distribution of the ED trait…………………………………………..118 2.2. Phylogenetic tree of extant turtle families with incidences of embryonic diapause evolution rooted with the extinct turtle Proganochelys; modified from Schafer et al., 1997……………………………………………………………………………………119 2.3: Frequency of ED expression of turtles within the two broad geographic bands…120 2.4: Frequency of ED expression amongst turtles whose distribution is outside the two broad geographic bands………………………………………………………………..121 2.5: Kinosternon phylogeny modified from Iverson, 1991…………………………….122 3.1: Latitudinal changes in seasonal precipitation duration and timing, modified from Savage, 2004…………………………………………………………………………...123 3.2: Ontogenetic model for facultative developmental timing…………………………124 3.3: Soil temperature profile from the semi-natural incubation experiment……………126 3.4: Relationships
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