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Induction of Gonadal Growth/Maturation in the Ornamental Fishes Epalzeorhynchos Bicolor and Carassius Auratus and Stereological Validation in C

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Induction of Gonadal Growth/Maturation in the Ornamental Fishes Epalzeorhynchos Bicolor and Carassius Auratus and Stereological Validation in C CICLO MESTRADO EM CIÊNCIAS DO MAR – RECURSOS MARINHOS ESPECIALIZAÇÃO EM AQUACULTURA E PESCAS Induction of Gonadal Growth/Maturation in the Ornamental Fishes Epalzeorhynchos bicolor and Carassius auratus and Stereological Validation in C. auratus of Histological Grading Systems for Assessing the Ovary and Testis Statuses Lia Gomes da Silva Henriques M 2016 Lia Gomes da Silva Henriques Induction of Gonadal Growth/Maturation in the Ornamental Fishes Epalzeorhynchos bicolor and Carassius auratus and Stereological Validation in C. auratus of Histological Grading Systems for Assessing the Ovary and Testis Statuses Dissertação de Candidatura ao grau de Mestre em Ciências do Mar – Recursos Marinhos, Ramo de Aquacultura e Pescas, submetida ao Instituto de Ciências Biomédicas de Abel Salazar da Universi- dade do Porto Orientador – Eduardo Jorge Sousa da Rocha Categoria – Professor Catedrático Afiliação – Instituto de Ciências Biomédicas de Abel Salazar da Universidade do Porto Coorientador – Maria João Tomé Costa da Rocha Categoria – Professor Auxiliar Afiliação – Instituto de Ciências Biomédicas de Abel Salazar da Universidade do Porto “Yesterday is History, Today is a Gift, Tomorrow is Mystery“ Alice Morse Earl Table of Contents List of Figures i List of Abbreviations v Acknowledgements vii Agradecimentos ix Abstract xi Resumo xv 1 - Introduction 01 1.1 – The Ornamental Fish Trade 03 1.2 – Species Studied in the Dissertation 04 1.2.1 – The Goldfish 06 1.2.2 – The Red-tailed Shark 07 1.3 – General Aspects of Fish Reproduction 09 1.4 – Assessing and Quantifying the Maturation of Fish Gonads 14 2 - Objectives 17 2.1 – Induction of Gonadal Growth/Maturation 19 2.2 – Validation of a Histological Grading System 19 3 – Materials and Methods 21 3.1 – Chemicals and Materials 23 3.2 – Fishes and Husbandry 23 3.3 – Induction of Gonadal Maturation 24 3.3.1 – Preliminary Study 25 3.3.2 – Experiment 1 25 3.3.3 – Experiment 2 25 3.3.4 – Experiment 3 26 3.3.5 – Experiment 4 – Trial A 26 3.3.6 – Experiment 4 – Trial B 26 3.3.7 – Experiment 5 26 3.4 – Necropsy and Histology 27 3.5 – Grading the Gonadal Status 29 3.5.1 – Criteria for Staging Ovaries 29 3.5.2 – Criteria for Staging Testis 30 3.6 – Stereological Study 30 3.7 – Statistical Analyses 34 4 – Results 35 4.1 – General Histology of the Gonads 37 4.2 – Biometric Data of Fish Before and After Hormonal Challenge 42 4.2.1 – Goldfish 42 4.2.2 – Red-tailed Shark 43 4.3 – Validation of the Grading System in the Goldfish Gonads 46 5 – Discussion 59 5.1 – Induction of Gonadal Growth/Maturation 61 5.2 – Validation of the Grading Systems in the Goldfish Gonads 64 6 – Conclusions 71 6.1 – Red-tailed Shark 73 6.2 – Goldfish 73 7 – References 75 Appendix 85 A – Histological Processing 87 B – Hematoxylin & Eosin (H&E) Staining 89 C – Experiments Summary 91 List of Figures Number Page Fish phylogenetic tree with emphasis on the Cyprinidae 1 05 family, adapted from Betancur-R et al. (2013). An adult specimen of goldfish (C. auratus) (picture by 2 06 Pedro Fernandes). A specimen of red-tailed shark (E. bicolor) (picture by Ped- 3 08 ro Fernandes). Main steps for the physiological chain of reaction between the reception of external environmental stimuli and the 4 10 gonadal maturation and spawning, as adapted from Harvey and Hoar (1980). Factors that stimulate and inhibit the hypothalamus– 5 hypophysis–gonad axis. Based on Yaron and Levavi-Sivan 11 (2011) and Zohar (1989). Stereological grid used for ovary. The point grid has two 6 lattices of 1:16. At a 100% scale, the distance between 33 points without circles is 1 cm. Stereological grid used for testis. The point grid has three 7 webs of 1:4:16. At a 100% scale, the distance between the 33 unbounded points is 1.5 cm. Microscopy image of goldfish testes in a very late sper- matogenic state. The lobular lumen is expanded and oc- cupied with sperm, in the form of very small cells with 8 roundish nuclei (thin white arrows). The germinal epitheli- 37 um is extremely thin, making the lobule periphery (block green arrows). The connective tissue is very scarce. The H&E staining. Microscopy images of goldfish ovarian follicles, according- ly to their increasing developmental (maturation) stage. (A) Primary; (B) Early cortical alveoli; (C) Early vitellogenic; 9 (D) Mid vitellogenic; (E) Late vitellogenic; (F) Mature; (G) 38 Post-ovulatory; (H) Atresic follicle. The increase in size of growing to mature follicles is obvious from A to F. H&E staining. Undeveloped ovary of a red-tailed shark, from which stand 10 out numerous primary oocytes, mostly in the perinucleo- 39 lar phase. H&E staining. i Undeveloped/early-spermatogenic testis of a red-tailed shark. It displays eosinophilic spermatogonia (the biggest 11 40 cells), nests of darker and smaller spermatocytes (laced), and sperm (arrow) in one lumen. H&E staining. Testis of a red-tailed shark in mid-spermatogenesis. Sper- matocysts at various stages of spermatogenesis are scat- 12 40 tered in the gonad. There are lobules with a significant amount of sperm in the lumen. H&E staining. Body weight and Fulton’s condition factor of the hormo- nally challenged female goldfish. Data given as mean, 13 42 mean ± standard error, and mean ± 0.95 confidence inter- val. Body weight and Fulton’s condition factor of the hormo- 14 nally challenged male goldfish. Data given as mean, mean 42 ± standard error, and mean ± 0.95 confidence interval. Body weight and Fulton’s condition factor of the hormo- nally challenged red-tailed shark in Trial A (see Experi- 15 ment 5 in Methods). Data given as mean, mean ± standard 43 error, and mean ± 0.95 confidence interval. The asterisks (***) signify there is a significant difference (p<0.001). Body weight and Fulton’s condition factor of the hormo- nally challenged red-tailed shark in Trial B (see Experiment 16 5 in Methods). Data given as mean, mean ± standard er- 43 ror, and mean ± 0.95 confidence interval. The asterisks (*) signify there is a significant difference (p<0.05). Body weight of the hormonally challenged red-tailed shark 17 from Trial A and Trial B. Data given as mean ± 0.95 confi- 44 dence interval. Fulton’s condition factor of the hormonally challenged 18 red-tailed shark from Trial A and Trial B. Data given as 44 mean ± 0.95 confidence interval. Initial total length of the hormonally challenged red-tailed 19 shark from Trial A and Trial B. Data given as mean ± 0.95 45 confidence interval. Gonad weight and gonadosomatic index of the hormonal- ly challenged red-tailed shark used in Trial A and Trial B. 20 Data given as mean ± 0.95 confidence interval. The aster- 45 isks signify significant differences between pairs of means (* when p<0.05 and ** when p<0.01). Female goldfish. Distribution of studied fish in view of the 21 46 ovary staging. ii Male goldfish. Distribution of studied fish in view of the 22 46 testis staging. Image from a goldfish ovary in Stage 0 (undeveloped). 23 47 H&E staining. Image from a goldfish ovary in Stage 1 (early vitellogenic). 24 47 H&E staining. Image from a goldfish ovary in Stage 2 (mid vitellogenic). 25 48 H&E staining. Image from a goldfish ovary in Stage 3 (late vitellogenic). 26 48 H&E staining Image from a goldfish ovary in Stage 4 (late vitellogenic). 27 49 H&E staining. Image from a goldfish testis in Stage 0 (undeveloped). 28 49 H&E staining. Image from a goldfish testis in Stage 1 (early spermatogen- 29 ic). The darker basophilic areas correspond to mature sper- 50 matozoa. H&E staining. Image from a goldfish testis in Stage 2 (mid spermatogenic). 30 Most pinkish zones are germinal epithelium and nearby 50 connective tissue. H&E staining. Image from a goldfish testis in Stage 3 (late spermatogenic). 31 51 H&E staining. Image from a goldfish testis in Stage 4 (spent). The gonad 32 as a spongy appearance, being the holes to the lumen of 51 the lobules. H&E staining. Body weight and total length of goldfish females according 33 with the ovary maturation stage. Data given as mean ± 52 0.95 confidence interval. Body weight and total length of goldfish males according 34 with the testis maturation stage. Data given as mean ± 52 0.95 confidence interval. Ovary weight and gonadosomatic index of goldfish females 35 according with the ovary maturation score. Data given as 53 mean ± 0.95 confidence interval. Testis weight and gonadosomatic index of goldfish males 36 according with the testis maturation score. Data given as 53 mean ± 0.95 confidence interval. Relative volumes (VV) of the goldfish ovarian follicle types, 37 according with the maturation score. Data given as mean ± 55 0.95 confidence interval. iii The relative volumes (VV) of the germinal epithelium, sperm, and lobular lumen in male goldfish, according with 38 56 the testis maturation score. Data given as mean ± 0.95 confidence interval. Partition of the goldfish ovary, in each maturation Stage, by the % average relative volumes (V ) of the three analysed 39 V 57 structural compartments. Each histological Stage translates to a particular stereological signature. Partition of the goldfish testis, in each maturation Stage, by the % average relative volumes (V ) of the three analysed 40 V 58 structural compartments. Each histological Stage corres- ponds to a specific stereological signature. iv List of Abbreviations Abbreviation Stands for BSA Bovine serum albumin BW Body Weight Early Vit. Early vitellogenic GnRH Gonadotropin Realizing Hormones GnRHa Gonadotropin Releasing Hormone Analogue GtH Gonadotropin HCG Human chorionic gonadotropin HNO3 Nitric acid Late Vit.
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