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THESIS on CSUMB REPRODUCTIVE STRATEGIES OF THE DOMINANT GASTROPODS OF THE LAU BASIN HYDROTHERMAL VENT SYSTEM: ALVINICONCHA HESSLERI AND IFREMERIA NAUTILEI ______________ A Thesis Presented to the Faculty of the Moss Landing Marine Laboratories and California State University Monterey Bay ______________ In Partial Fulfillment of the Requirements for the Degree Master of Science in Marine Science ______________ by Kyle C. Reynolds Fall 2009 CALIFORNIA STATE UNIVERSITY MONTEREY BAY The Undersigned Faculty Committee Approves the Thesis of Kyle C. Reynolds: REPRODUCTIVE STRATEGIES OF THE DOMINANT GASTROPODS OF THE LAU BASIN HYDROTHERMAL VENT SYSTEM: ALVINICONCHA HESSLERI AND IFREMERIA NAUTILEI ____________________________________________ Nick Welschmeyer, Chair Moss Landing Marine Laboratories ____________________________________________ Michael Graham Moss Landing Marine Laboratories ____________________________________________ Stacy Kim Moss Landing Marine Laboratories ______________________________ Approval Date iii Copyright © 2009 by Kyle C. Reynolds All Rights Reserved iv DEDICATION I wish to dedicate this thesis to Dr. Ellen Strong, who shall forever after be known as my Fairy Gonadmother. EPIGRAPH AND AUTHOR CONTRIBUTIONS The following thesis is comprised of two separate manuscripts, currently in preparation for submission. The first manuscript, which serves as Chapter One, is formatted for submission to the journal Nature. This manuscript reports and puts into context three novel characteristics discovered during the course of this project: 1) a unique embryo transport mechanism, which I discovered and described; 2) a brood pouch within a modified metapodial pedal gland, discovered by Dr. Anders Warén and described by me (taxonomic expertise for this description was provided by Dr. Ellen Young); and 3) a completely new larval form, discovered by me, but the significance and later developmental stages of which were uncovered by Dr. Hiromi Watanabe and Dr. Craig Young, to different degrees. The second manuscript, Chapter Two of this thesis, compares and describes the reproductive structures and strategies of Ifremeria nautilei and Alviniconcha hessleri at both an organismal and cellular level for the journal Deep-Sea Research. The purpose of this manuscript was to fill in gaps left in previous studies with regard to the reproductive anatomies of both species, and to provide evidence of the significance and derivations of the structures described, with reference to their respective phylogenies. This project is a culmination of three long years spent personally transporting these samples to experts in various fields across the country, seeking help in investigating the reproductive aspects of these mysterious animals; the likes of which did not exist in textbooks or scientific literature. As first author on these manuscripts, I had the responsibility of the majority of the specimen collections, lab work, literature review, and writing, although significant contributions were made by all co-authors in their respective areas of expertise. The Japanese team of scientists appearing as co-authors on Chapter 1 began work on Ifremeria nautilei larvae just recently, not knowing that my research had been ongoing for three years prior. Their success with rearing the larvae to the veliger stage was a significant contribution and provided information that I had been unable to obtain. We came to the conclusion as a group that our research was too complementary not to combine and authorship order was agreed upon according to contribution of research. v ABSTRACT Reproductive strategies of the dominant gastropods of the Lau Basin hydrothermal vent system: Alviniconcha hessleri and Ifremeria nautilei by Kyle C. Reynolds Master of Science in Marine Science Moss Landing Marine Laboratories, California State University Monterey Bay, 2009 Reproductive biology and larval development remain elusive processes to researchers for many vent endemic species due to the cost prohibitive nature of sampling in these environments, as well as the difficulties inherent to laboratory culturing of chemosynthetic organisms. Thus, many of these biological processes and strategies have only been inferred from related species living in shallow marine environments, resulting in a paradigm that broadly attributes phylogenetic constraint to any life-history variation found at vents. Alviniconcha hessleri and Ifremeria nautilei comprise the majority of the dominant megafauna found in the Lau Basin hydrothermal vent system. While they share a number of unique anatomical modifications, overlapping distributions, and a recent common ancestry, they employ disparate reproductive strategies. A planktotrophic mode of larval development has been inferred for A. hessleri from its shell morphology, while I. nautilei has been found to protect its young throughout early development in a brood pouch within its foot. Previous studies of these species involved sexually immature specimens, leaving the most pertinent questions unanswered regarding their reproductive biology. In this thesis, I have examined the reproductive anatomy of both species at both organismal and cellular levels. Evidence of iteroparity and a simultaneously periodic reproductive effort was revealed for both species across vent sites. In addition, the following apomorphic characters were discovered in I. nautilei: a novel brood pouch; a unique embryo transport mechanism; and a new larval form, which we have named Warén’s larva. These findings provide some of the first substantial evidence of evolution of developmental traits in a hydrothermal vent organism. vi TABLE OF CONTENTS PAGE DEDICATION .................................................................................................................... iv EPIGRAPH AND AUTHOR CONTRIBUTIONS............................................................... iv ABSTRACT ......................................................................................................................... v LIST OF FIGURES ...........................................................................................................viii ACKNOWLEDGEMENTS ................................................................................................. ix CHAPTER 1 INTERNAL BROODING AND A NOVEL LARVAL FORM IN A DEEP-SEA HYDROTHERMAL VENT GASTROPOD .............................................................. 1 Methods Summary / Methods.............................................................................. 6 References........................................................................................................... 8 Acknowledgements ........................................................................................... 10 Author Information............................................................................................ 11 Figures and Captions ......................................................................................... 11 2 A COMPARATIVE DESCRIPTION OF REPRODUCTIVE STRUCTURES IN IFREMERIA NAUTILEI AND ALVINICONCHA HESSLERI (CAENOGASTROPODA: PROVANNIDAE): HYDROTHERMAL VENT GASTROPODS FROM THE LAU BASIN............................................................. 14 Introduction....................................................................................................... 15 Material and Methods........................................................................................ 17 Expedition and Collection Data ................................................................... 17 Laboratory Protocol and Sample Treatment................................................ 17 Results............................................................................................................... 18 Ifremeria nautilei......................................................................................... 18 Reproductive stage ................................................................................. 18 Foot and brood pouch morphology......................................................... 19 Ontogeny ............................................................................................... 19 Pallial oviduct........................................................................................ 21 vii Alviniconcha hessleri ................................................................................... 21 Reproductive stage ................................................................................. 21 Foot morphology ................................................................................... 22 Ontogeny ............................................................................................... 22 Pallial oviduct........................................................................................ 22 Discussion......................................................................................................... 23 Species Comparisons.................................................................................... 23 Reproductive stage ................................................................................. 23 Foot morphology ................................................................................... 23 Ontogeny ............................................................................................... 23 Pallial oviduct........................................................................................ 24 Brooding in Caenogastropods .....................................................................
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