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Christian E. W. Steinberg Aquatic Animal Nutrition A Mechanistic Perspective from Individuals to Generations Aquatic Animal Nutrition Christian E. W. Steinberg Aquatic Animal Nutrition A Mechanistic Perspective from Individuals to Generations Christian E. W. Steinberg Department of Biology Humboldt University at Berlin Berlin, Germany ISBN 978-3-319-91766-5 ISBN 978-3-319-91767-2 (eBook) https://doi.org/10.1007/978-3-319-91767-2 Library of Congress Control Number: 2018953153 © Springer Nature Switzerland AG 2018 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface Never attend an expedition to Vietnam that is devoted to the study of freshwater and marine fishes! However, if you do, you run the risk of making good new friends in the commercial and ornamental fish business, sharing some (too many!) Tiger beers and promising to spread new information about the nutrition of fish and other aquatic animals. I took that risk, went to Vietnam, made new friends, and fell in love with South (East) Asia. Several years have passed since then, and experts, as well as laypersons, have had to tolerate and survive several seminars on aquatic animal nutrition, given by me. Now, it is time to keep my promise. A freshwater ecologist by education and a stress ecologist by preference, my primary interest has not been to write a book that discusses higher productivity in the aquaculture industries or reviews recipes for more effective functional aquafeeds to increase survival, reproduction or productivity of farmed animals. Instead, I am more interested in answering the question of how certain dietary ingredients influ- ence the life history traits not only of the consumers but also of their succeeding generations. In evolutionary-ecological terms: How do dietary components impact the Darwinian fitness of populations and thereby influence their long-term persis- tence in the ecosystem? The ecologist in me always noticed gaps in the more prag- matic experimental approaches of raising aquatic animals referenced in this book. To identify the gaps, I had to sometimes crawl ashore, since I felt obliged to borrow information about new developments from terrestrial or laboratory model animal studies. Nevertheless, I hope that my raised forefinger will encourage the develop- ment of new experimental setups for the aquaculture community. The content for the originally planned one-volume book on “Aquatic Animal Nutrition,” however, turned out to be so voluminous that I split it into two volumes. I thank Springer Publishing Company for this courtesy. My sincere appreciation goes particularly to “my Springer ladies” in Dordrecht, namely Alexandrine Cheronet and Judith Terpos, who were always very supportive and never hesitated to answer my questions, even if they were simple. Furthermore, I am thankful to all the photographers and artists who allowed me to use their wonderful images free of charge. Doubtless, they contributed to an attractive appearance of this book. We all agree that good illustrations can often v vi Preface explain complex ideas much better than thousands of words. Nevertheless, also good words count, and I thank Sarah L. Poynton for the excellent word crafting that resulted in the title. Even to a book, space limitation applies. Due to this circumstance, I would like to apologize in advance to all individuals whose research was not cited or whose papers have not been discussed in full but whose work has certainly advanced the understanding of this complex field of research, practice, and education. This book is dedicated to my bright grandkids, Anna S. and Paul N., who like watching colorful and intriguing fishes in a living room tank. Since they started this business at a much younger age than I did, I am certain that one, or both of them, will be inclined to write brilliant books on this fascinating subject. Berlin, Germany Christian E. W. Steinberg Contents 1 Introduction – ‘You Are What You Eat’ .................................................. 1 Appendix ................................................................................................... 6 Technical Note ...................................................................................... 6 References ................................................................................................. 7 2 Diets and Digestive Tracts – ‘Your Food Determines Your Intestine’ .......................................................................................... 9 2.1 Digestive Tract ................................................................................. 9 2.2 Digestion .......................................................................................... 14 2.2.1 Protein Digestion ................................................................. 15 2.2.2 Lipid Digestion .................................................................... 16 2.2.3 Carbohydrate Digestion ....................................................... 16 2.3 Ontogenesis and the Intestine .......................................................... 17 2.3.1 Fishes ................................................................................... 17 2.3.2 Invertebrates ......................................................................... 26 2.4 Herbivory, a Disadvantageous Acquization Strategy? ..................... 34 2.4.1 Fishes ................................................................................... 37 2.4.2 Invertebrates ......................................................................... 40 2.5 Starvation and Gut Morphology ...................................................... 42 2.6 Trophic Positions: An Omnivores’ Dilemma? ................................. 45 2.7 Concluding Remarks ........................................................................ 53 References ................................................................................................. 54 3 The Intestinal Microbiota – ‘Your Eating Feeds a Plethora of Guests’ and ‘This Plethora of Guests Determines Who You Are and How Well You Do’ ....................................................... 61 3.1 Invertebrates ..................................................................................... 67 3.1.1 Hydrozoa .............................................................................. 67 3.1.2 Mollusks ............................................................................... 68 3.1.3 Echinoderms ........................................................................ 72 3.1.4 Crustaceans .......................................................................... 73 vii viii Contents 3.2 Fishes ............................................................................................... 80 3.2.1 Microbiome Ontogenesis ..................................................... 81 3.2.2 Does a Core Microbiome Exist? .......................................... 85 3.2.3 Zebrafish as Witness of Microbiome Development ............. 111 3.2.4 Control Functions by Gut Microbiota .................................. 115 3.3 Concluding Remarks ........................................................................ 128 References ................................................................................................. 128 4 Dietary Restriction, Starvation, Compensatory Growth – ‘Short-Term Fasting Does Not Kill You: It Can Make You Stronger’ ...................................................................... 137 4.1 Indicators of Starvation .................................................................... 143 4.2 Starvation Tolerance and Starvation Impact .................................... 148 4.2.1 Cnidarians ............................................................................ 162 4.2.2 Rotifers ................................................................................. 163 4.2.3 Mollusks ............................................................................... 166 4.2.4 Echinoderms ........................................................................ 168 4.2.5 Crustaceans .......................................................................... 170 4.2.6 Fishes ................................................................................... 192 4.2.7 Summary of Starvation Effects ............................................ 198 4.2.8 Starvation: Point-of-no-Return ............................................ 199 4.3 Compensatory Growth ..................................................................... 201 4.3.1 Invertebrates ......................................................................... 206 4.3.2 Fishes ................................................................................... 214 4.4 Compensatory Growth in Populations ............................................. 228 4.5 Regulation of Compensatory Growth .............................................. 230 4.5.1 Appetite-Regulating Hormones ........................................... 233 4.5.2 Neuropeptides ...................................................................... 236 4.5.3 Transcription of Growth Regulators .................................... 243 4.6 Concluding remarks ......................................................................... 252 References ................................................................................................. 255 5 Chrononutrition – ‘The Clock Makes Good Food’ ............................... 289 5.1 How Does a Biological Clock Work? .............................................. 293 5.1.1 Fishes ................................................................................... 294 5.1.2 Invertebrates ......................................................................... 302 5.2 Food and Circadian Gene Transcription .......................................... 308 5.2.1 Major Nutrients .................................................................... 308 5.2.2 Xenobiotic or Antinutritional Compounds........................... 315 5.3 Concluding Remarks ........................................................................ 323 References ................................................................................................. 325 Contents ix 6 Transgenerational Effects – ‘Your Offspring Will Become What You Eat’ ........................................................................................... 333 6.1 Parental Effects ................................................................................ 335 6.1.1 Maternal Effects ................................................................... 344 6.1.2 Paternal Effects .................................................................... 373 6.2 What Is Epigenetics? ........................................................................ 378 6.2.1 Time Scales of Epigenetic Inheritance ................................. 380 6.2.2 Epigenetic Mechanisms ....................................................... 381 6.3 Concluding Remarks ........................................................................ 414 References ................................................................................................. 416 7 Trophic Diversification and Speciation – ‘Your Eating Fuels Evolution’ ....................................................................................... 431 7.1 Individual Specialization.................................................................. 437 7.2 Underlying Mechanisms of Speciation ............................................ 438 7.3 Trophic Speciation ........................................................................... 441 7.3.1 Ancient Lakes ...................................................................... 441 7.3.2 Rivers ................................................................................... 451 7.3.3 Coral Reefs ........................................................................... 452 7.4 Convergent Evolution ...................................................................... 454 7.5 Rapid Speciating Taxa ..................................................................... 458 7.5.1 Pumpkinseed Sunfish ........................................................... 458 7.5.2 Cyprinodon .......................................................................... 459 7.5.3 Terapontidae (Grunters) ....................................................... 460 7.5.4 Three-Spined Stickleback .................................................... 460 7.5.5 Arctic Charr ......................................................................... 462 7.6 Time Span of Trophic Speciation .................................................... 465 References ................................................................................................. 467 Abbreviations and Glossary AAs amino acids abcb4 gene encoding multidrug resistance protein 3, a membrane- bound transporter abcg2 gene encoding ATP-binding cassette subfamily G member 2, a membrane-bound tranporter Acrophase time at which the peak of a rhythm occurs AgRPs agouti-related proteins: neuropeptides produced in the brain with an appetite-stimulating potential; activated by the hormone ghrelin, inhibited by the hormone leptin AHR anti-hydroxyl radical AhR aryl-hydrocarbon receptor, Ah receptor: a ligand-activated transcription factor involved in the regulation of biological responses to planar aromatic (aryl) hydrocarbons, includ- ing xenobiotic compounds ahr2 gene encoding the aryl-hydrocarbon receptor 2 found in zebrafish AL ad libitum = “at one’s pleasure” Alternative splicing a regulated process during gene expression that results in a single gene coding for multiple proteins ambra1a, ambra1b autophagy-regulating genes AMPK AMP-activated protein kinase: 5’adenosine monophosphate-a ctivated protein kinase, an enzyme cen- tral in cellular energy homeostasis anadromous fish migrate from the sea up into freshwater to spawn; examples are salmon and striped bass anorexigen appetite-suppressing drug or food constituent apaf-1 encodes apoptotic protease-activating factor 1, a pro- aptotic protein arα, arβ encode androgen receptor α and β ASA anti-superoxide anion xi

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This book is a unique cross fertilization of aquatic ecology and aquaculture. It shows how diets structure the digestive tract and its microbiota and, in turn, the microbiota influences life history traits of its host, including behavior. Short-term starvation can have beneficial effects on individu
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