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Bioenergetics Approach to Fish Reproductive Potential: Case of Trisopterus Luscus (Teleostei) on the Galician Shelf (NW Iberian Peninsula)

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Bioenergetics Approach to Fish Reproductive Potential: Case of Trisopterus Luscus (Teleostei) on the Galician Shelf (NW Iberian Peninsula) PhD Bioenergetics approach to fish Thesis reproductive potential: case of APRIL Trisopterus luscus (Teleostei) on the 2011 Galician Shelf (NW Iberian Peninsula) UNIVERSIDADE DE VIGO | Alexandre Alonso Fernández Front cover design: original design of Gerardo Fernández Carrera. For its reproduction, permission of the author is required ([email protected]). Back cover picture: original photo of David Villegas Ríos. For its reproduction, permission of the author is required ([email protected]). Bioenergetics approach to fish reproductive potential: case of Trisopterus luscus (Teleostei) on the Galician Shelf (NW Iberian Peninsula) Memoria de Tesis Doctoral para optar al grado de Doctor por la Universidad de Vigo Presentada por: Alexandre Alonso Fernández Universidade de Vigo Departamento de Ecoloxía e Bioloxía Animal Dr. Juan Francisco Saborido Rey, Científico Titular del Instituto de Investigaciones Marinas (Consejo Superior de Investigaciones Científicas) como director de tesis y, Dr. Bernardino González Castro, Profesor Titular en la Universidad de Vigo como ponente, Autorizan la presentación de la memoria adjunta, titulada “Bioenergetics approach to fish reproductive potential: case of Trisopterus luscus (Teleostei) on the Galician Shelf (NW Iberian Peninsula)”, realizada bajo su dirección por D. Alexandre Alonso Fernández, licenciado en Ciencias del Mar, para optar al grado de Doctor por la Universidad de Vigo. Y para que así conste, se expide el presente certificado en Vigo, a 20 de Febrero de 2011. Fdo: Juan Francisco Saborido Rey Fdo: Bernardino González Castro A meus pais, irmá e amigos… … a memoria da miña avoa Juana… …e a María e Lois Miña nai deume os camiños, e meu pai deixoume o mare, non tiñan mais que deixarme nen eu penso mais deixare Celso Emilio Ferreiro “…una de las conclusiones más obvias de El viaje a la felicidad: en el inicio y el final de un trayecto siempre hay una emoción, porque de lo contrario no sería un proyecto.” Eduardo Punset Agradecementos Acknowledgments Non podo máis que agradecer a todos aqueles que me acompañaron neste largo camiño. A todos os meus compañeiros que compartiron interminables horas de traballo. I would like to express my deepest gratitude to all the people at St. Andrew's Biological Station for their hospitality and support during my stay in Canada. Ó meu director de tese pola oportunidade e confianza brindada. Ós meus amigos que sempre estiveron aí cando foi necesario. A toda a miña familia… ós que xa non están e ós que están por vir. A miña irmá coa que sempre podo contar sen nin sequera pedilo. A miña nai que me deu incondicionalmente todo o amor e a comprensión posible. Ó meu pai que me ensinou o que realmente era o mar e guioume na senda do traballo e do esforzo. Pero sobre todo a María e a Lois que co seu infinito amor e apoio fan que todo este sacrificio colla, neste intre, todo o sentido. So espero que todos se sintan orgullosos do traballo feito, do mesmo xeito que eu me sinto orgulloso de contar con todos eles. Moitas grazas e vémonos nos bares… Table of contents AGRADECEMENTOS/ACKNOWLEDGEMENTS TABLE OF CONTENTS SUMMARY 1 1 GENERAL INTRODUCTION 5 1.1. Motivation of the Problem, Hypothesis and Objectives 7 1.1.1 Motivation of the Problem 7 1.1.2 Hypothesis 8 1.1.3 Objectives 8 1.2 Reproductive Potential in Fish Stock Assessment: an Overview 9 1.2.1 Criticism to Spawning Stock Biomass- Recruitment Relationships 10 1.2.2 An Alternative Approach: Stock Reproductive Potential 12 1.2 Study Area: Environmental Constraints 20 1.3 Biological and Ecological Aspects of the Species of Study: Trisopterus luscus (Linnaeus 1758) 21 1.4.1 Taxonomy 23 1.4.2 Habitat 24 1.4.3 Feeding 26 1.4.4 Growth 27 1.4.5 Reproduction and early life history stages 29 2 MATERIAL AND METHODS 31 2.1 Sampling Strategy and Protocol 33 2.2 Histological Assessment of Gonad Development and Sexual Cycle 36 2.2.1 Histological Procedure 36 2.2.2 Follicle Development 37 2.2.3 Maturity Staging and Reproductive Cycle 44 2.2.4 Follicular Atresia 47 2.2.5 Reproduction and Early Life History in Captivity: Experimental Design 48 2.2.6 Statistical Techniques 49 2.3 Egg Production Dynamic, Fecundity Strategy and Spawning Pattern 51 2.3.1 Fecundity Estimation Methods 52 2.3.2 Egg Quality Estimations 55 2.3.3 Statistical Procedure 56 2.4 Proximate Body Composition and Energy Content 60 2.4.1 Biochemical Analysis and Energy Content Estimation 60 2.4.2 Statistical Procedure 62 2.5 Potential Effects of Maternal Factors on Stock Reproductive Potential 64 2.5.1 Maternal Influence on the Variation of the Reproductive Cycle 65 2.5.2 Influence of Nutritional Status on Egg Production 68 2.5.3 Influence of Nutritional Status on Egg Quality 68 2.5.4 Stock Reproductive Investment 68 3 HISTOLOGICAL ASSESSMENT OF GONAD DEVELOPMENT AND SEXUAL CYCLE OF TRISOPTERUS LUSCUS ON GALICIAN SHELF 71 3.1 Available knowledge of Trisopterus luscus reproductive biology 73 3.2 Results 75 3.2.1 Histological Description of Trisopterus luscus Gonads 75 3.2.2 Reproductive Cycle of Female Trisopterus luscus on Galician Shelf 80 3.2.3 Size at Maturation in Trisopterus luscus: Micro- and Macroscopic Classification 84 3.2.4 Prevalence and Intensity of Ovarian Follicular Atresia in Trisopterus luscus 85 3.2.5 Embryonic Development of Trisopterus luscus Under Controlled Conditions 87 3.3 Discussion 94 3.3.1 Concluding Remarks 109 4 EGG PRODUCTION DYNAMIC, FECUNDITY STRATEGY AND SPAWNING PATTERN IN AN ASYNCHRONOUS OVARIAN DEVELOPMENT SPECIES (TRISOPTERUS LUSCUS) 111 4.1 Fecundity as a Key Factor in the Dynamic of Fish Populations 113 4.2 Results 115 4.2.1 Homogeneity of Ovarian Follicle Distribution in Trisopterus luscus 115 4.2.2 Comparison of Fecundity Estimation Methods 116 4.2.3 Fecundity Strategy in a Species with Asynchronous Ovarian Development, Trisopterus luscus 118 4.2.4 Egg Production Pattern under Controlled Conditions in Trisopterus luscus 121 4.2.5 Potential Fecundity Variation: Size, Geographical and Temporal Trends in Trisopterus luscus on the Galician Shelf 123 4.2.6 Batch Fecundity Variation: Size and Temporal Trends in Trisopterus luscus on the Galician Shelf 127 4.2.7 Seasonal Changes of Egg Quality in a Temperate Batch Spawner, Trisopterus luscus 131 4.2.8 Egg Quality Variation of Trisopterus luscus under Controlled Conditions 133 4.3 Discussion 134 4.3.1 Concluding Remarks 153 5 PROXIMATE BODY COMPOSITION AND ENERGY CONTENT IN A MARINE TEMPERATE TELEOST (TRISOPTERUS LUSCUS): DOES REPRODUCTIVE INVESTMENT CONSTRAIN ENERGY ALLOCATION STRATEGY? 155 5.1 Energetic cost of reproduction in fish populations 157 5.2 Results 160 5.2.1 Proximate Composition and Energy Density if Females of Trisopterus luscus 160 5.2.2 Study of Simple Condition Index Suitability in a Marine Temperate Teleost (Trisopterus luscus) 171 5.2.3 Energy Allocation Related to Reproduction in a Marine Temperate Teleost (Trisopterus luscus) 175 5.3 Discussion 178 5.3.1 Concluding Remarks 195 6 POTENTIAL EFFECTS OF MATERNAL FACTORS ON STOCK REPRODUCTIVE POTENTIAL IN A CAPITAL BREEDER (TRISOPTERUS LUSCUS) 197 6.1 Maternal effects as source of variation of reproductive potential 199 6.2 Results 200 6.2.1 Maternal Influence on the Variation of the Reproductive Cycle 201 6.2.2 Influence of Nutritional Status on Egg Production in a Temperate Capital Breeder (Trisopterus luscus) 207 6.2.3 Influence of Nutritional Status on Egg Quality in a Temperate Capital Breeder (Trisopterus luscus) 210 6.2.4 Assessment of Reproductive Output in Trisopterus luscus 215 6.3 Discussion 224 CONCLUSIONS 241 REFERENCES 247 ANEX i RESUMEN i Introducción iii Material y Métodos vi Evaluación histológica del desarrollo gonadal y ciclo sexual de Trisopterus luscus en la plataforma continental de Galicia x Dinámica de producción de huevos, estrategia reproductiva y patrón de puesta en una especie de desarrollo asincrónico (Trisopterus luscus) xv Costes energéticos de la reproducción en Trisopterus lucus xxii Efectos maternales en el potencial reproductive en un “Capital Breeder” (Trisopterus luscus) xxviii Conclusiones xxxix Summary The fish species Trisopterus luscus (Linnaeus 1758), commonly known in English as pouting, is a member of the cod family (Gadidae) and it is of major commercial importance to the artisanal fleet of a number of European countries, primarily France, Portugal and Spain. Since the 1960s and 1970s (with average landings of around 3000 t per annum) a slow but steady decrease in catches has been observed on the Galician shelf, down to landings below 1000 t per annum in recent years. This situation is aggravated by the fact that the information available about this species is generally scarce, especially regarding our knowledge of its reproductive biology. Knowledge of the reproductive biology of a fish species is essential for effective fishery management. There is increasing awareness that the traditional indicators of stock viability are inadequate because the capacity of a population to produce viable eggs and larvae each year is extremely important for stock viability and recovery. Improved estimates of stock reproductive potential should thus lead to improving the current models used in fisheries management. Histological study of gonads of T. luscus was consistent with asynchronous ovarian development. This study shows that pouting on the Galician shelf presents a protracted spawning season, from January to May, with a peak of spawning activity in February, a month when female pouting release a batch almost every day. Length-at-maturation, 150.6 mm, was lower than previously estimated in other studies, and it seems to be in concordance with the established minimum legal size, 200 mm. The development of the pelagic eggs and hatched larvae has been described for the first time ever in this study.
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