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University of Southampton UNIVERSITY OF SOUTHAMPTON SCHOOL OF OCEAN AND EARTH SCIENCE Reproduction and larval biology of North Atlantic asteroids related to the invasion of the deep sea Francisco Benitez Villalobos Doctor of Philosophy September 2005 1 Graduate School of the National Oceanography Centre, Southampton This PhD dissertation by: Francisco Benitez Villalobos Has been produced under the supervision of the following persons: Supervisors: Prof. Paul A. Tyler Dr. David S. M. Billett Chair of Advisory Panel: Dr. Martin Sheader 2 DECLARATION This thesis is the result of work completed wholly while registered as a postgraduate in the School of Ocean and Earth Science, University of Southampton. 3 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF SCIENCE SCHOOL OF OCEAN AND EARTH SCIENCE Doctor of Philosophy REPRODUCTION AND LARVAL BIOLOGY OF NORTH ATLANTIC ASTEROIDS RELATED TO THE INVASION OF THE DEEP SEA by Francisco Benitez Villalobos A very important objective of ecological research is to explain the evolution of life histories, more specifically how natural selection modifies reproduction and development in order to generate the patterns that are observed in nature. With few exceptions, the reproductive mechanisms and patterns found in deep-water echinoderms are entirely similar to those found in shallow-water species. The aims of this study were 1) to examine the reproductive biology of the many deep-sea asteroids found on the continental slope to the west of Europe in order to determine if the reproductive adaptations are a function of depth, distribution or are phylogenetically controlled, and 2) to conduct experiments on the effects of pressure and temperature on larval development of Atlantic asteroids, to investigate the physiological potential for deep sea invasion by shallow-water species. Eggs of the shallow-water asteroids Asterias rubens Linnaeus and Marthasterias glacialis (Linnaeus) were fertilized in vitro and incubated through the early embryonic cleavages until the larval stage. They were subjected to different temperature/pressure regimes. Early embryos were able to tolerate pressures up to 150 atm at 15oC and 100 atm at 10oC. Survivorship of A. rubens swimming bipinnaria remained high (> 70%) after incubation at all the pressure/temperature combinations. In M. glacialis the highest survival of swimming larvae was 100% at 1 atm/5, 15 and 20oC and 50 atm/15 and 20oC. Data for the temperature and pressure effects on the later stages of development suggest that all the larval stages are more temperature/pressure tolerant than the early embryos and survivorship becomes greater with larval age. Therefore, the larvae of these two species could survive transport to deeper waters and these species may be capable of sending colonists to the deep sea. In the deep NE Atlantic the habitat has selected for species with specific reproductive traits, which provide them with successful and advantageous life history strategies. This can be clearly observed in the upper bathyal zone between 700 and 1100 m, where the environmental conditions have selected for small species with low fecundity and large eggs, plus habits related directly or indirectly with suspension feeding. These species exhibit reproductive features with trends to the opportunistic strategy and are distinctive of unpredictable environments, although their large egg size probably follows the general trend observed in species from cold waters in order to provide the larvae with energy sufficient for a high survival possibility. Conversely, phylogenetic and evolutionary factors are also important and seem to be decisive at the deepest waters where basically mainly species belonging to the strict deep-sea family Porcellanasteridae are found. All these species possess a mixture of features typical of classical K strategists and equilibrium strategists, which enable them to persist in a relatively stable environment with low energy availability. A comprehensive knowledge of the reproductive processes of the deep-sea fauna is essential in order to evaluate the level of variability caused in the environment principally by human activity and the possible effects on life-history of the species. 4 CONTENTS CHAPTER ONE - GENERAL INTRODUCTION 1.1. The invasion of the deep sea ……………………………………….………..……1 1.2. Larval type and its role in dispersal ………………………………………..……4 1.3. Deep-water formation and species dispersal ………………………….........…..10 CHAPTER TWO - IMPORTANCE OF THE LARVAL STAGE IN THE LIFE HISTORY OF MARINE INVERTEBRATES, SPECIFICALLY ASTEROIDS: A REVIEW 2.1. Introduction ……………………………………………………………………..15 2.2. A revision of the definitions of the early-life history stages …………………19 2.2.1. Embryo ………………………………………………………………………………19 2.2.2. Larva ………………………………………………………………………………19 2.2.3. Juvenile ………………………………………………………………………………21 2.2.4. Metamorphosis ……………………………………………………………………...22 2.2.5. Indirect development ……………………………………………………………..22 2.2.6. Direct development …………………………………………………………..…22 2.3. Types of larvae recognized in scientific literature ………………………………...…23 2.4. Larvae as a mechanism for dispersal ……………………………………………24 2.4.1. Classification of larvae regarding dispersal potential ………………………..…24 2.5. Larval types of asteroids ……………………………………………………………..26 2.5.1. The bipinnaria …………………………………………………………………...…26 2.5.2. The brachiolaria ……………………………………………………………………...27 2.5.3. The yolky brachiolaria: a derived larval form …………………………….……..27 2.5.4. The barrel-shaped larva: a derived larval form …………………………….……..29 2.6. Patterns of development in asteroids ……………………………………………29 2.7. Larval cloning in asteroids ………………………………………………….…33 CHAPTER THREE - TEMPERATURE AND PRESSURE TOLERANCES OF EMBRYOS AND LARVAE OF THE ATLANTIC SEASTARS Asterias rubens AND 5 Marthasterias glacialis (ECHINODERMATA: ASTEROIDEA) POTENTIAL FOR DEEP-SEA INVASION FROM THE NORTH ATLANTIC. 3.1. Introduction ………………………………………………………………..…….35 3.1.1. Chapter objectives ……………………………………………………..………41 3.2. Material and methods ……………………………………………………………..41 3.2.1. Field sampling and spawning …………………………………………………….41 3.2.2. Temperature/pressure effects on fertilized eggs …………………………………...42 3.2.3. Temperature/pressure effects on larvae ……………………………………………45 3.3. Results ………………………………………………………………………………46 3.3.1. Temperature/pressure effects on fertilized eggs …………………………….…..…46 3.3.2. Temperature/pressure effects on swimming bippinaria at 24 h …………….……54 3.4. Discussion ………………………………………………………………………………55 3.5. Recommendations………………………………………………………………………60 CHAPTER FOUR – REPRODUCTIVE FEATURES OF ASTEROIDS IN THE PORCUPINE SEABIGHT AND PORCUPINE ABYSSAL PLAIN, N.E. ATLANTIC AND THEIR RELATION TO DEPTH DISTRIBUTION OF THE SPECIES 4.1. Introduction ……………………………………………………………………...62 4.1.1 Fecundity and egg size ……………………………………………………………..63 4.1.2. Body size ………………………………………………………………………………68 4.2. Material and methods …………………………………………………………..…69 4.2.1. Collection of data ……………………………………………………………………...69 4.2.2. Histology ………………………………………………………………………………72 4.2.3. Image analysis and estimation of fecundity …………………………….……..72 4.2.4. Statistical analysis ………………………………………………………..……75 4.3. Results ………………………………………………………………………………76 4.4. Discussions …………………………………………………………………...…82 4.4.1. Body size, fecundity and egg size ……………………………………………….……82 4.4.2. Depth allocation of the species and possible causes ……………………..……86 CHAPTER FIVE – SYNTHESIS AND CONCLUSIONS 5.1- Factors controlling the bathymetric distribution of species and their effects on early life-history stages of echinoderms …………………………………………………….94 6 5.2- Effect of hydrodynamic mechanisms on larval dispersal …………………………..95 5.3- Larval physiological tolerances of shallow-water asteroids ……………….…97 5.4.- Reproductive strategies of the different deep-sea asteroid species in the North-East Atlantic Ocean ……………………………………………………………………...99 5.5- Final remarks …………………………………………………………………….101 REFERENCES References ……………………………………………………………………………104 7 Acknowledgments I know everybody says “this work would not have been possible without the help of a number of people, to whom I am deeply grateful”, and I would not like to repeat the same phrase but it is immensely true, so there it is. I would like to thank my two supervisors Prof. Paul A. Tyler and Dr. David Billett, for their constant supervision, patience, and friendship along the process of doing a PhD at the National Oceanography Centre, Southampton. Thanks also to my examiners Dr. Andrew C. Campbell and Dr. Antony C. Jensen because their suggestions and important corrections made this work richer and more interesting and now I feel very pleased with it. Many thanks to Dr. Modesto Seara Vazquez and Biol. Mario E. Fuente Carrasco (Universidad del Mar, Mexico), Dr. Francisco Solis Marin and Dr. Alfredo Laguarda Figueras (ICMyL UNAM, Mexico) because they believed in me since I was and undergraduate student and gave me all their support when I decided to come to study a PhD, and throughout my time in England. I wish also thank everyone in the DEEPSEAS Benthic Biology Group. To be part of the group has been a pleasure and a great experience. Special thanks to Dr. Jon Copley, Dr. Alan Hughes and Dr Bryan Bett for their advice on the statistical analysis in the fourth chapter of this thesis. Many thanks to our research group for their help and support: Liz, Rhian, Kerry, Ben, Ian, Francisco S., Eva. Special thanks to my officemates: Laura, Hannah, Abi, Lizzie and the last but no the least Emily, because they made my time at the office a joyful one and I am proud that I shared my office with the most
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