Fishes Out of Water: Biology and Ecology of Mudskippers (CRC Marine Science)

Mudskippers are amphibious fishes native to the Indo-West Pacific and tropical western Africa. Unlike most fishes, mudskippers emerse to forage, find mates, and defend territories. Adaptations to their morphology, physiology and behavior enable mudskippers to accommodate both aquatic and terrestrial habitats. For these traits, mudskippers have long captured the fascination of scientists, naturalists, and fish hobbyists. Some mudskipper taxa (e.g. __Periophthalmodon__ spp., __Periophthalmus__ spp., __Boleophthalmus__ spp.) are readily observed on mudflats and mangrove forests during the ebb tide. Correspondingly, these conspicuous and widespread taxa are relatively well-studied. The autecology and basic biology for the remaing taxa (e.g. __Apocryptodon__ spp. and __Oxuderces__ spp.) are still poorly understood. **Fishes Out of Water: Biology and Ecology of Mudskippers** is the first comprehensive book to synthesize published scientific information and observation on these fishes. Two dozen subject experts present thorough overviews in fifteen distinct chapters. Contents span mudskipper anatomy, distribution, systematics, physiology, ecology, and conservation. Unique adaptations to terrestriality are discussed within the context of each chapter foci. This authoritative reference equips the reader with the basic foundation to understand mudskipper biology and ecology, while providing a framework in which emerging data are discussed. The book will be of interest to a broad range of students, researchers, and professionals in ichthyology, evolution, ecology, animal behavior, and comparative physiology. Cover 1 Half title page 2 Series page 3 Title page 4 Copyright page 5 Dedication page 6 Contents 12 Foreword 14 Preface 16 Contributors 20 Chapter 1: Taxonomy and Systematics Review 22 1.1 Introduction 23 1.2 Historical Accounts of Oxudercine Gobies 23 1.3 Higher Level Relationships 24 1.4 Sister-Group Relationships 27 1.5 Relationships Among Genera 28 1.6 Species Accounts 29 Apocryptes Valenciennes in Cuvier and Valenciennes 1837 29 Apocryptes Bato (Hamilton 1822) 29 Apocryptodon Bleeker 1874 29 Apocryptodon Madurensis (Bleeker 1849) 31 Apocryptodon Punctatus Tomiyama 1934 31 Apocryptodon Wirzi Koumans 1937 31 Boleophthalmus Valenciennes in Cuvier and Valenciennes 1837 31 Boleophthalmus Birdsongi Murdy 1989 31 Boleophthalmus Boddarti (Pallas 1770) 31 Boleophthalmus Caeruleomaculatus Mcculloch and Waite 1918 34 Boleophthalmus Dussumieri Valenciennes in Cuvier and Valenciennes 1837 34 Boleophthalmus Pectinirostris (Linnaeus 1758) 34 Boleophthalmus Poti Polgar, Jaafar and Konstantinidis 2013 34 Oxuderces Eydoux and Souleyet 1850 34 Oxuderces Dentatus Eydoux and Souleyet 1850 34 Oxuderces Nexipinnis (Cantor 1849) 35 Parapocryptes Bleeker 1874 35 Parapocryptes Rictuosus (Valenciennes in Cuvier and Valenciennes 1837) 35 Parapocryptes Serperaster (Richardson 1846) 36 Periophthalmodon Bleeker 1874 36 Periophthalmodon Freycineti (Quoy and Gaimard 1824) 36 Periophthalmodon Schlosseri (Pallas 1770) 38 Periophthalmodon Septemradiatus (Hamilton 1822) 38 Periophthalmus Bloch and Schneider 1801 38 Periophthalmus Argentilineatus Valenciennes in Cuvier and Valenciennes 1837 38 Periophthalmus Barbarus (Linnaeus 1766) 42 Periophthalmus Chrysospilos Bleeker 1853 44 Periophthalmus Darwini Larson and Takita 2004 45 Periophthalmus Gracilis Eggert 1935 45 Periophthalmus Kalolo Lesson 1831 46 Periophthalmus Magnuspinnatus Lee, Choi, and Ryu 1995 46 Periophthalmus Malaccensis Eggert 1935 46 Periophthalmus Minutus Eggert 1935 46 Periophthalmus Modestus Cantor 1842 47 Periophthalmus Novaeguineaensis Eggert 1935 47 Periophthalmus Novemradiatus (Hamilton 1822) 47 Periophthalmus Pusing Jaafar, Polgar, and Zamroni 2016 48 Periophthalmus Spilotus Murdy and Takita 1999 48 Periophthalmus Takita Jaafar and Larson 2008 48 Periophthalmus Variabilis Eggert 1935 48 Periophthalmus Walailakae Darumas and Tantichodok 2002 49 Periophthalmus Waltoni Koumans 1941 49 Periophthalmus Weberi Eggert 1935 49 Pseudapocryptes Bleeker 1874 49 Pseudapocryptes Borneensis (Bleeker 1855) 50 Pseudapocryptes Elongatus (Cuvier 1816) 50 Scartelaos Swainson 1839 50 Scartelaos Cantoris (Day 1871) 51 Scartelaos Gigas Chu and Wu in Chu, Chan, and Chen 1963 52 Scartelaos Histophorus (Valenciennes in Cuvier and Valenciennes 1837) 52 Scartelaos Tenuis (Day 1876) 52 Zappa Murdy 1989 52 Zappa Confluentus (Roberts 1978) 53 Acknowledgments 53 References 53 Chapter 2: The Natural Distribution of Mudskippers 58 2.1 Introduction 58 2.2 Biogeographic Regions of Mangroves and Mudskippers 63 2.3 Distribution of Oxudercine Goby Genera and Species 64 2.3.1 Oxudercine Goby Areas of Endemism 84 2.3.1.1 Tropical Eastern Atlantic Ocean 84 2.3.1.2 Southwestern Indian Ocean 84 2.3.1.3 Arabian Sea 85 2.3.1.4 Bay of Bengal 85 2.3.1.5 South China Sea 85 2.3.1.6 East China Sea 85 2.3.1.7 Banda Sea 86 2.3.1.8 Oceania 86 2.3.2 Distributional Gradients 87 2.4 Summary 87 Acknowledgments 87 References 88 Chapter 3: Early Development of Mudskippers 90 3.1 Introduction 90 3.2 Egg Chamber 92 3.3 Egg Mass 93 3.4 Egg-Capsule Morphology 94 3.5 Embryonic Development 95 3.6 Hatching 97 3.7 Larval Development 98 3.8 Morphology and Age at Settlement 102 3.9 Early Life History of Mudskippers 104 References 107 Chapter 4: Age and Growth 110 4.1 Introduction 111 4.2 Age Determination 111 4.3 Calcareous Structures As Age Characters 112 4.3.1 Sagittal Otolith 112 4.3.2 Second Pectoral-Radial Bone 112 4.3.3 Increment Counting 113 4.3.4 Increment Periodicity 113 4.3.4.1inter- and Intraspecific Difference in Increment Formations: Annual and Biannual 114 4.3.4.2method Using Daily Microincrements 115 4.3.5 Back-Calculation 115 4.4 Length–Frequency Analysis 116 4.5 Growth Curve Function 116 4.5.1 Von Bertalanffy Growth Function 116 4.5.2 Modified VBGF 116 4.5.3 Schnute Growth Function 117 4.6 Age and Growth in Oxudercine Gobies 117 4.6.1 Age and Growth Estimated By VBFG 117 Boleophthalmus Pectinirostris 117 Boleophthalmus Boddarti 118 Periophthalmodon Schlosseri 118 Periophthalmus Argentilineatus 118 Periophthalmus Waltoni 118 Scartelaos Gigas 119 Scartelaos Tenuis 120 4.6.2 Age and Growth Estimated by Modified VBGF 120 Periophthalmus barbarus 120 4.6.3 Age and Growth Estimated by Schnute Growth Function 120 Periophthalmus Argentilineatus 120 4.6.4 Length–weight Relationship Studies 120 Boleophthalmus boddarti 120 Boleophthalmus dussumieri 120 Boleophthalmus pectinirostris 121 Periophthalmodon schlosseri 121 Periophthalmodon septemradiatus 121 Periophthalmus argentilineatus 121 Periophthalmus barbarus 121 Periophthalmus chrysospilos 121 Periophthalmus gracilis 121 Periophthalmus magnuspinnatus 122 Periophthalmus modestus 122 Periophthalmus spilotus 122 Periophthalmus variabilis 122 Periophthalmus waltoni 122 Pseudapocryptes elongatus 122 Scartelaos gigas 122 Scartelaos histophorus 122 Scartelaos tenuis 123 4.6.5 Summary of Growth Characteristics 124 4.7 Future Perspectives 125 Acknowledgments 128 References 128 Chapter 5: Respiratory and Circulatory Adaptations 132 5.1 Introduction 132 5.2 Anatomy 133 5.2.1 Respiratory System 133 5.2.1.1 Gills 133 5.2.1.2 Bucco-Opercular Cavity 137 5.2.1.3 Skin 138 5.2.2 Circulatory System 141 5.2.2.1 Heart 141 5.2.2.2 Central Vascular Connection 141 5.2.2.3 Gill Circulation 144 5.2.2.4 Circulation through the Bucco-Opercular Cavity 144 5.2.2.5 Skin Circulation 146 5.3 Physiology 146 5.3.1 Respiratory Gas Exchange 146 5.3.2 Blood Gas Levels 147 5.3.3 Blood Circulation 147 5.3.4 Ecological Interpretation of Data 148 5.4 Future Studies 149 5.4.1 Central Vascular Anatomy of Scartelaos 149 5.4.2 Regulation of Cutaneous Blood Flow 150 5.4.3 Swimming Ecophysiology of Mudskippers 150 5.4.4 Plasticity of Cardiorespiratory System during Ontogenetic Shift to Amphibious Life 151 5.4.5 Cardiorespiratory Anatomy and Physiology of Overwintering Mudskippers 151 Acknowledgments 151 References 152 Chapter 6: Structure and Function of Sensory Organs 158 6.1 Introduction 159 6.2Anatomy of the Eye 159 6.2.1 Gross Morphology 161 6.2.1.1 Cornea and Sclera 161 6.2.1.2 Uveal Layer 161 6.2.1.3 Eye Lens 161 6.2.1.4 Retina 163 6.2.1.5 Conclusion 163 6.3 Anatomy Of Chemosensory Organs 163 6.3.1 Gustatory Organs 163 6.3.1.1 Gross Morphology 164 6.3.1.2 Ultrastructure of Gustatory Receptor Cells 166 6.3.1.3 Ultrastructure of Basal Cells 167 6.3.1.4 Ultrastructure of Supporting Cells 169 6.3.1.5 Ultrastructure of Nerve Plexus 169 6.3.1.6 Conclusions 169 6.3.2 Olfactory Organs 170 6.3.2.1 Gross Morphology 170 6.3.2.2 Ultrastructure of Olfactory Epithelia 174 6.3.2.3 Ultrastructure of Ciliated Olfactory Sensory Neurons 175 6.3.2.4 Ultrastructure of Microvillar Olfactory Sensory Neurons 175 6.3.2.5 Ultrastructure of Crypt Olfactory Sensory Neurons 175 6.3.2.6 Ultrastructure of Ciliated Non-sensory Cells 177 6.3.2.7 Ultrastructure of Supporting Cells 177 6.3.2.8 Ultrastructure of Basal Cells 177 6.3.2.9 Conclusion 178 6.3.3 Solitary Chemosensory Cells 178 6.4 Acoustic Communication 179 6.5 Summary 180 Acknowledgments 181 References 181 Chapter 7: Nitrogen Metabolism and Nitrogenous Waste Excretion 188 7.1 Introduction 188 7.2 Ammonia Production in the Liver 189 7.3 Ammonia Is Toxic 190 7.4 Ammonia Excretion Through Gills 191 7.4.1 Mudskipper Gill Morphologies Affect Branchial Ammonia Excretion 192 7.4.2 Mudskipper Skins Can Facilitate Ammonia Excretion or Uptake 193 7.5 Defense Against Undesirable Accumulation and/or Uptake of Ammonia 194 7.5.1 Mudskippers are Non-Ureogenic and Non-Ureotelic 194 7.5.2 Avoidance of Postprandial Ammonia Toxicity in Periophthalmodon schlosseri 195 7.5.3 Defense Against Endogenous Ammonia Toxicity During Terrestrial Exposure 196 7.5.3.1 Reduction in Proteolysis and/or Amino Acid Catabolism 197 7.5.3.2 Partial Amino Acid Catabolism with the Formation of Alanine 198 7.5.3.3 Active Ammonia Excretion in Connection with H+ Excretion during Emersion 200 7.5.4 Defense against Endogenous and Exogenous Ammonia Toxicity during Exposure to Environmental Ammonia 201 7.5.4.1 Active Ammonia Excretion during Ammonia Exposure 202 7.5.4.2 Lowering of Environmental pH 204 7.5.4.3 Reduction in the Cutaneous NH3 Permeability 204 7.5.4.4 Increased Production of Glutamine 205 7.5.4.5 High Brain Ammonia Tolerance 205 7.6 Summary 206 References 208 Chapter 8: Aquatic and Terrestrial Locomotion 216 8.1 Introduction 216 8.2 Anatomical Modifications of Locomotor Structures 217 8.3 Mudskipper Locomotor Patterns 219 8.3.1 Sustained Aquatic Locomotion 220 8.3.2 Bursting Aquatic Locomotion 221 8.3.3 Sustained Terrestrial Locomotion 222 8.3.4 Bursting Terrestrial Locomotion 224 8.4 Locomotor Strategies for Generating Movement in Aquatic and Terrestrial Environments 225 8.5 Conclusion 227 Acknowledgments 227 References 228 Chapter 9: Review of Reproductive Strategies 230 9.1 Introduction 230 9.2 Water and Air As Respiratory Media 231 9.3 Marine Hypoxia 233 9.4 Development of Fish Eggs in Air 233 9.5 Mudflats As Spawning Grounds 234 9.6 Changes in Spawning Behavior As Gobies Come Ashore 234 9.6.1 Non-Oxudercine Gobies 236 9.6.1.1 Nesting on the Sea Bottom 236 9.6.1.2 Burrowing 236 9.6.2 Oxudercine Gobies 237 9.6.2.1 Species of Boleophthalmus 237 9.6.2.2 Species of Scartelaos 243 9.6.2.3 Species of Periophthalmodon 243 9.6.2.4 Species of Periophthalmus 243 9.7 Mudskipper Reproduction on the Mudflats 245 9.7.1 Spawning in Burrows 245 9.7.2 Egg Care and Parental Behavior of Mudskippers 246 9.7.3 Evolution of Air Deposition in Mudskippers 249 9.8 Future Studies 250 Acknowledgment 251 References 251 Chapter 10:Review of Reproductive Strategies 258 10.1 Introduction 258 10.2 Feeding Behavior 259 10.2.1 Seasonal Variation 262 10.2.2 Ontogenetic Changes 263 10.2.3 Diel Variation 264 10.2.4 Sex Differences 265 10.3 Relationship Between Diet and Prey Availability 266 10.3.1 Benthic Surveys 266 10.3.2 Community Structure 270 10.3.3 Stable Isotope Studies 270 10.4 Prey Capture and Processing 272 10.4.1 Jaw and Pharyngeal Dentition 272 10.4.1.1 Sensory Detection of Prey 275 10.4.2 Filtering Mechanism 276 10.4.3 Dentition Revisited 277 10.4.4 Alimentary Tract 280 10.4.4.1 Enzymes and Bacterial Flora Distributions 282 10.4.4.2 Juvenile to Adult Transition 284 10.5 Behavior 284 10.6 Recommendations for Future Studies 286 References 287 Chapter 11: Review of Reproductive Strategies 298 11.1 Introduction 298 11.2 Categories And Elements of Behavior 299 11.2.1 Courtship–Agonistic Interplay 304 11.2.1.1 Courtship Displays 304 11.2.1.2 Agonistic Displays 304 11.2.1.3 Common Elements and Changing Behavior 307 11.2.2 Territoriality 307 11.2.2.1 Burrows, Saucers, Turrets, and Other Constructs 308 11.2.2.2 Home Ranges 309 11.3 Factors Affecting Behavior 311 11.3.1 Neuro-Hormonal Control 312 11.3.2 Seasons 313 11.3.3 Daily Cycles 313 11.3.4 Sexual Dimorphism 315 11.4 Recommendations for Future Study 316 References 317 Chapter 12: Emergent Patterns in Spatio-Temporal Ecology 322 12.1 Introduction 322 12.2 Methods 324 12.3 Autecology Of The East African Ps. Argentilineatus: An Annotated Review 324 12.3.1 Burrow and Habitat Distribution 326 12.3.1.1 Burrow Structure and Function 326 12.3.1.2 Territorial and Burrowing Activities 326 12.3.2 Reproduction 329 12.3.3 Settlement and Post-Settlement 330 12.3.4 Diel, Synodic, and Intertidal Movements of Metamorphosed Individuals 330 12.3.5 Daily Activity of Territorial Individuals 334 12.4 Spatio-Temporal Patterns in the Water-To-Land Transition 337 12.4.1 Spatio-Temporal Variation of Eco-Ethological Elements in Ps. cf. sobrinus 337 12.4.2 Burrowing and Feeding Grounds 337 12.4.3 The “Pull” or “Push” Dilemma 339 12.4.4 Predation Risk and Reproduction 340 12.5 Limits, Developments, and Concluding Remarks 341 Appendix A 342 Abbreviations and Definitions 342 Acknowledgments 342 References 342 Chapter 13: Care and Management in Captivity 348 13.1 Introduction 348 13.2 Mudskipper Species in the Aquarium Trade 349 13.3 Mudskippers in Captivity 355 13.3.1 Food and Feeding 355 13.3.2 Diseases and Health Problems 356 13.3.3 Behavior 356 13.3.4 Reproduction 357 13.4 Mudskipper Husbandry 359 13.4.1 Paludarium Design 359 13.4.1.1 Building a Paludarium 363 13.4.2 Ideal Environmental Conditions 363 13.4.2.1 Water Parameters 363 13.4.2.2 Heating 364 13.4.2.3 Lighting 364 13.4.2.4 Filtration 364 13.4.2.5 Aeration 365 13.4.2.6 Tide Simulation 365 13.4.2.7 Other Organisms in the Paludarium 366 13.5 Closing Remarks 367 Acknowledgments 367 References 368 Chapter 14: Taxa and Habitat Conservation 370 14.1 Introduction 370 14.2 Global Threats to Mangrove Habitat 373 14.2.1 Removal of Mangrove Areas 373 14.2.2 Coastal Pollution 374 14.2.3 Climate Change and Sea-Level Rise 376 14.3 Regional Mangrove Habitat Declines 377 14.3.1 Mangroves of Asia 378 14.3.2 Mangroves of West Africa 378 14.3.3 Mangroves of East Africa and Arabian (Persian) Gulf 380 14.3.4 Mangroves of Australia and Oceania 381 14.4 Recommendations For Mudskipper And Mangrove Conservation 382 References 383 Chapter 15: Challenges and Future Research: An Australian Perspective 390 15.1 Mudskippers In Australia 390 15.2 Mudskipper Studies 391 15.3 Mudskipper Challenges 393 15.4 Conservation Issues 398 15.5 Mudskippers For The Future 400 References 403 Index 406 "Mudskippers are amphibious fishes native to the Indo-West Pacific and tropical western Africa. Unlike most fishes, mudskippers emerse to forage, find mates, and defend territories. Adaptations to their morphology, physiology and behavior enable mudskippers to accommodate both aquatic and terrestrial habitats. For these traits, mudskippers have long captured the fascination of scientists, naturalists, and fish hobbyists. Some mudskipper taxa (e.g. Periophthalmodon spp., Periophthalmus spp., Boleophthalmus spp.) are readily observed on mudflats and mangrove forests during the ebb tide. Correspondingly, these conspicuous and widespread taxa are relatively well-studied. The autecology and basic biology for the remaing taxa (e.g. Apocryptodon spp. and Oxuderces spp.) are still poorly understood. Fishes Out of Water: Biology and Ecology of Mudskippers is the first comprehensive book to synthesize published scientific information and observation on these fishes. Two dozen subject experts present thorough overviews in fifteen distinct chapters. Contents span mudskipper anatomy, distribution, systematics, physiology, ecology, and conservation. Unique adaptations to terrestriality are discussed within the context of each chapter foci. This authoritative reference equips the reader with the basic foundation to understand mudskipper biology and ecology, while providing a framework in which emerging data are discussed. The book will be of interest to a broad range of students, researchers, and professionals in ichthyology, evolution, ecology, animal behavior, and comparative physiology."--Provided by publisher Chapter 1. Taxonomy and systematics review / Edward O. Murdy and Zeehan Jaafar -- chapter 2. The natural distribution of mudskippers / Lynne R. Parenti and Zeehan Jaafar -- chapter 3. Early development of mudskippers / Ken Maeda, Yuko Tsuhako, and Katsunori Tachihara -- chapter 4. Age and growth / Atsushi Nanami -- chapter 5. Respiratory and circulatory adaptations / Atsushi Ishimatsu -- chapter 6. Structure and function of sensory organs / Michał Kuciel, Krystyna Żuwała, Eugenia R. Lauriano, Gianluca Polgar, Stefano Malavasi, and Giacomo Zaccone -- chapter 7. Nitrogen metabolism and nitrogenous waste excretion / Shit F. Chew and Yuen K. Ip -- chapter 8. Aquatic and terrestrial locomotion / Cinnamon Pace -- chapter 9. Review of reproductive strategies / Karen L.M. Martin and Atsushi Ishimatsu -- chapter 10. Feeding behavior: a review / David Clayton -- chapter 11. Territoriality and courtship behavior / David Clayton and Kathy Townsend -- chapter 12. Emergent patterns in spatio-temporal ecology / Gianluca Polgar -- chapter 13. Care and management in captivity / Richard Mleczko and Hans-Georg Rupp -- chapter 14. Taxa and habitat conservation / Beth Polidoro -- chapter 15. Challenges and future research : an Australian perspective / Helen K. Larson.