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Gonad Morphology and Sex Change in Sandburrowers

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Gonad Morphology and Sex Change in Sandburrowers UNIVERSITY OF HAWAI'ILIBRARY GONAD MORPHOLOGY AND SEX CHANGE IN SANDBURROWERS (TELEOSTEI: CREEDIIDAE) A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI'I IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN ZOOLOGY MAY 2004 By Ross C. Langston Dissertation Committee: David W. Greenfield, Chairperson Christopher D. Kelley George S. Losey Bruce C. Mundy Timothy C. Tricas Cynthia L. Hunter L¥A\ © Copyright by Ross C. Langston 2004 All Rights Reserved 111 This work is dedicated to my parents, John and Linda Langston. My success in graduate school was due largely to their encouragement, some hard work on my part, and also a good deal of luck. The completion ofmy degree illustrates the axiom: "Even a blind hog gets an acorn some ofthe time." IV ACKNOWLEDGMENTS I would like to thank my advisor David Greenfield for his advice and encouragement throughout my graduate student career. He has taught me a great deal about ichthyology. More importantly, he has taught me to enjoy my research. I would also like to thank my other committee members, George Losey, Chris Kelley, Tim Tricas, Bruce Mundy, and Cindy Hunter for their guidance and review ofthis dissertation. In particular, Bruce Mundy revised numerous drafts ofthis dissertation and greatly improved the accuracy and clarity ofthe final draft. Several individuals and institutions loaned or gave specimens for examination ofgonads: John Lundberg and Mark Sabaj (Philadelphia Academy ofNatural Sciences), John E. Randall and Arnold Suzumoto (Bishop Museum), Chris Paulin and Clive Roberts (National Museum New Zealand), Victor Mthombeni and M.E. Anderson (JLB Smith Institute ofIchthyology), DianneBray (Victoria Museum), Shaun Collin (University ofQueensland), Eugenie Clark and Bev Rodgerson (University ofMaryland), and Dave Catania (California Academy ofNatural Sciences). I am grateful to the following individuals for help with field collections: Erin Baumgartner, Lisa Chau, Jason Collier, Jake Davis, Annmarie Dehn, Tim Fitzgerald, Jennifer Garrison, Adam Jaffe, Ken Longenecker, JeffMahon, Mark Mohlman, Joanna Philippoff, Laura Rodman, Andre Seale, Brett Schumacher, and Dave Strang. I thank Brianna Kiefer, Frank Stanton, Aaron Moriwake, and Virginia Moriwake for their help in feeding and maintaining fishes in captivity. I thank Tina Carvallo, Samuel Haley, Karen Maruska, Steve Spielman for use oftheir facilities and equipment for gonad histology. Photographic assistance was provided by Chris Brown, Jerry Fox, Theresa Lewis, Brian Nedved, Rich Radtke, Steve Robinow, Dave Schafer, and Amber Whittle. Andy Taylor provided help with statistics and study design. I am especially indebted to Kazue Asoh, Kassi Cole, and Tomako Yoshikawa for their expertise in gonad histology as well as their continued guidance and encouragement in the world ofsex changing fishes. In particular, Chris Kelley was a tremendous help with the gonad histology. His instruction in plastic embedding greatly increased the quality ofthe histology in the last chapter ofthis dissertation and (sometimes) reduced my use ofprofanity while at the microtome. This study was funded by a Grant-in-Aid ofresearch from Sigma Xi and the Evolution, Ecology, and Conservation Biology program at the University ofHawaii. Several specimens used in this study were collected during a survey ofthe coral-reef fishes ofFiji, funded by a NSF grant to David Greenfield. During this study, I was supported by teaching and research assistantships from the Zoology Department and Hawaii Institute ofMarine Biology. Specimens collected during this study were obtained under Hawaii DLNR scientific collecting permit SCP 2000-27 and University ofHawaii Animal Care Protocol 98-002. All research was conducted through the University ofHawaii Department ofZoology and Hawaii Institute ofMarine Biology. v ABSTRACT Sex allocation and reproductive ecology ofsandbuITowers (Family Creediidae) were investigated in four studies. The first study examined gonad morphology and size-dimorphism for two creediid species native to Hawaii. Specimens ofCrystallodytes cookei and Limnichthys donaldsoni exhibited multiple signs ofsex change including the presence ofdelimited ovotestes in juveniles and males, presence oftransitional gonads which contained free spermatozoa and vitellogenic oocytes, and presence offemale-active individuals with vestigial testes. Female­ active individuals were significantly larger than male-actives, but did not differ significantly with transitionals. These results indicate that C. cookei and 1. donaldsoni are protandrous hermaphrodites. The second study examined oocyte development, batch fecundity, and seasonal and lunar trends in reproductive effort for females ofC. cookei and 1. donaldsoni collected from Hawaiian waters. Four stages ofoocytes were present. Batch fecundity ranged between 25-162 and 32-143 oocytes for C. cookei and 1. donaldsoni respectively and was positively correlated with body­ length. Both species spawned throughout the year, but C. cookei exhibited a significant reduction in reproductive effort during September and October. Spawning ofC. cookei was also correlated with the lunar cycle. Reproductive effort was elevated around the new- and quarter moon phases, and was depressed around the full moon. The third study examined the effects ofsex-ratio on sex change in artificially constructed social groups ofC. cookei. Males were maintained in social groups with and without females for 30 days. Gonads ofthree individuals showed evidence ofprotandrous sex change; however, the proportion ofgroups in which sex change occurred did not differ significantly between groups in VI which females were present or removed. In contrast, the ratio oftestis-to-ovary was significantly lower in males ofthe female-removal groups. Together, these results indicate that males allocate a greater proportion ofgonad volume to ovarian tissue in the absence offemales, but they do not become functional as females over a period of30 days. Future experiments should maintain experimental groups for longer time periods in order to determine ifmales with ovary-biased gonads eventually assume female function. The fourth study examined the distribution ofthe delimited ovotestis morphology in the family Creediidae and its sister groups. Delimited ovotestes were present in specimens of Chalixodytes tauensi$ Crystallodytes pauciradiatus, Limnichthys nitidus, and 1. fasciatus and were not present in Apodocreedia vanderhorsti, Creedia haswelli, 1. rendahli, 1. polyactis, and Tewara cranwellae. Representative species from sister group taxa Percophidae and Trichonotidae also lacked delimited ovotestes. When transposed onto phylogenetic relationships proposed for the family and its sister groups, these results suggest that delimited ovotestis morphology and protandrous sex change evolved within the family Creediidae, but are not shared by all derived species. Vll TABLE OF CONTENTS Acknowledgments v Abstract vi Table ofContents viii List ofTables x List ofFigures xi CHAPTER I. General Introduction :.. 1 Overview 1 Organization 6 CHAPTER II. Histological evidence ofsequential hermaphroditism in two Hawaiian sandburrowers, Crystallodytes cookei and Limnichthys donaldsoni 7 Introduction 7 Materials and Methods 8 Results 10 Discussion 26 CHAPTER III. Spawning dynamics ofHawaiian sandburrowers, Crystallodytes cookei and Limnichthys donaldsoni 31 Introduction 31 Materials and Methods 33 Results 35 Discussion 59 Vlll CHAPTER IV. Effects offemale removal on gonad allocation and sex change in the Hawaiian sandburrower, Crystallodytes cookei 66 Introduction : 66 Materials and Methods 70 Results 73 Discussion 80 CHAPTER V. Patterns ofgonad morphology and sex allocation in creediid fishes 87 Introduction 87 Materials and Methods 89 Results 92 Discussion '" 116 CHAPTER VI. Dissertation summary and conclusions .124 LITERATURE CITED 128 IX LIST OF TABLES 1.1 Taxonomic status and geographical distribution ofcreediid species .4 2.1 Size class and gonad classification for individuals of C. cookei ll 2.2 Size class and gonad classification for individuals of1. donaldsoni .l2 2.3 Proportion oftesticular tissue in gonad cross-section for DOT gonads .l2 3.1 Oocyte diameters in ovaries of C. cookei and 1. donaldsoni... 39 3.2 Cosine regression models for seasonal and lunar trends in GIS data .43 3.3 Relationships between SL (in mm) and various life history parameters for C. cookei and L. donaldsoni 56 4.1 Size structure ofindividuals of C. cookei in experimental groups 75 4.2 Sex change times in some sequential hermaphrodite species 83 5.1 Gonad classification by size for creediid species with unisexual gonads 97 5.2 Gonad classification by size-class for specimens ofCreedia haswelli 98 5.3 Gonad classification by size for creediid species with delimited ovotestes 100 5.4 Gonad classification by size for percophid species l 06 5.5 Gonad classification by size class for specimens ofT elegans 112 5.6 Summary ofgonad morphology, size- and sexual dimorphism for the families Creediidae Percophidae and Trichonotidae 113 x LIST OF FIGURES Figure 2.1 Gonad morphology and development in C. cookei.. 14 2.2 Gonad morphology and development in 1. donaldsoni 15 2.3 Cellular structure oftesticular tissue in 1. donaldsoni and C cookei 16 2.4 Anterior to posterior gonadal sections from a transitional 1. donaldsoni 17 2.5 Size frequency distribution ofreproductive classes of C. cookei 24 2.6 Size frequency distribution ofreproductive classes of1. donaldsoni
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