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Symbiosis in Fishes: The Biology of Interspecific Partnerships

Symbiosis in Fishes: The Biology of Interspecific Partnerships

Ilan Karplus

ISBN: 978-1-118-75976-9 April 2014 Wiley-Blackwell 464 Pages

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Symbiosis in Fishes provides comprehensive coverage of the biology of partnerships between fishes and invertebrates, ascending the phylogenetic scale, from luminescent bacteria, sponges and coelenterates to molluscs, crustaceans and echinoderms. Both facultative and obligatory partnerships are reviewed with emphasis on the behavioral, ecological and evolutionary aspects of fish symbiosis. Each of the eight chapters of this book focuses on a different group of partners. The structure, physiology and anti-predatory strategies of each group are described to provide the necessary background for the understanding of their partnerships with fishes. The formation of the associations, the degree of partner specificity and its regulation, as well as the benefits and costs for the fishes and their associates, communication between partners and their possible co-evolution are discussed in each chapter.

This is the first attempt to critically review in a single volume all associations of fishes with invertebrates based on the latest studies in these areas, together with studies published many years ago and little cited since then.

Symbiosis in Fishes provides a huge wealth of information that will be of great use and interest to many life scientists including fish biologists, ecologists, ethologists, aquatic scientists, physiologists and evolutionary biologists. It is hoped that the contents of the book will stimulate many to further research, to fill in the gaps in our knowledge in this fascinating and important subject. Libraries in all universities and research establishments where biological sciences are studied and taught should have copies of this exciting book.

Preface x

Introduction 1

1 The Associations between Fishes and Luminescent Bacteria 6

Luminescent Bacteria 6

Symbiotic Luminescent Bacteria in Fish Light Organs 8

Flashlight Fishes 11

Taxonomy and Distribution 11

The Light Organs 13

The Eye and the Light Organ 17

Reproduction, Larval and Light Organ Development 18

The Photophobic Response 20

The Use of Light by Flashlight Fishes 21

School Formation 22

Territorial Defense 22

Sexual Signaling 22

Deep Sea Ceratioid Anglerfishes 24

Structure, Diversity and Distribution 24

Reproductive Strategies 25

Obligatory Sexual Parasitism 26

Temporary Associations 28

Facultative Sexual Parasitism 29

Light Organ Structure and Development: Light and the Mechanisms Controlling its Emission 29

The Use of Lures by Anglerfishes 34

Ponyfishes 37

Structure, Distribution and Taxonomy 37

The Light Organ System (LOS) and Diversity of the Generated Light Patterns 38

Disruptive Illumination 40

Discrete Projected Luminescence (DPL) 41

Ventral Body Flash 41

Opercular Flash 42

Buccal Luminescence 42

Sex-Specific Signaling 43

Inception of the Association between Luminescent Bacteria and Ponyfishes 43

Sexual Dimorphism of the LOS, Sex-Specific Signaling and the Role of Sexual

Selection in the Evolution of Leiognathid Fishes 44

Specificity of the Partnerships between Luminescent Bacteria and Fishes 47

Optimization of the Benefits to Fishes from their Association with Bacteria 48

The Evolution of the Partnerships between Fishes and Luminescent Bacteria 49

References 52

2 The Associations between Fishes and Sponges 58

Sponges 58

Predator Deterrence by Sponges 59

Multiple Species Assemblages in Sponges 61

Obligatory Fish Symbionts and Adaptations for Living in Association with Sponges 62

Nutrition, Reproduction and Sponge Occupation by Obligatory Symbiotic Fishes 68

Partner Specificity and Sponge Sharing by Obligatory Symbiotic Fishes 69

Evolution of the Partnership Between Obligatory Fish Symbionts and Sponges 70

Sponges as Living Incubators of Fish Eggs 72

Facultative Partnerships Between Fishes and Sponges 74

References 75

3 The Associations between Fishes and Anthozoans 79

Sea Anemones 79

The Stinging Cells and their Release Mechanism 80

Obligatory Associations with Sea Anemones of Fishes of the Genera Amphiprion and Premnas 81

The Taxonomy, Distribution and Ecology of Host Sea Anemones and their Associated Fishes 81

The Protection of Anemone Fishes from Sea Anemones 86

Recognition, Attraction to and Selection of Sea Anemones by Anemone Fishes 93

Partner Specificity 104

Host Preference 106

Competitive Interactions 106

Stochastic Processes 109

Habitat Preference 109

Geographical Overlap 109

Protection from Sea Anemones 109

Species Coexistence 110

Adaptations of Anemone Fishes for Living with Sea Anemones 111

Protandric Sex Reversal 111

Monogamy and Mate Recognition 114

Step-fathering 118

Social Control of Growth and the Tolerance of Nonbreeders by the Breeders 118

Fish Territoriality, Aggression and the Sea Anemone 121

Limited Larval Dispersal and Natal Recruitment 124

Benefits and Costs to Anemone Fishes and Sea Anemones from being Associated and their Short-term Mutual Impacts 128

The Evolution of the Anemone Fish–Sea Anemone Partnership 134

The Facultative Associations Between Fishes and Sea Anemones 135

Protection from Sea Anemones 140

Partner Specificity 141

Settlement and Recruitment of D. trimaculatus to Sea Anemones 142

The Sharing of Sea Anemones with Anemone Fishes 143

Benefits and Costs to Facultative Fish Partners and Sea Anemones 144

The Associations Between Fishes and Scleractinian Corals 145

Scleractinian Corals 145

Microhabitat Selection by Coral Dwelling Fishes 146

Attraction of Pomacentrid Fishes to Corals 146

Attraction of Pomacentrids to Corals Inhabited by Conspecifics 150

Coral Occupation, Competiton and Coexistence of Coral dwelling Gobies 153

Adaptations to Habitat by Coral Dwelling Gobies 157

Small Size and Morphology 157

Noxious Skin 158

Hypoxia Tolerance and Air Breathing 158

Bidirectional Sex Reversal 159

Monogamy 161

Social Control of Growth 162

Multiple Species Assemblages Involving Coral Dwelling Gobies and Crustaceans 164

Benefits and Costs to Fishes and Corals for being Associated 169

Benefits to Fishes 169

Costs to Fishes 173

Benefits to Corals 177

Costs to Corals 180

Social Structure and Mating System Evolution in Coral Dwelling Damselfishes of the genus Dascyllus 181

References 186

4 The Associations between Fishes and Siphonophores 202

Siphonophores 202

Physalia physalis −the Portuguese Man-of-War 203

Fishes Associated with Siphonophores other than Physalia physalis 204

Fishes Associated with Physalia physalis 207

References 209

5 The Associations between Fishes and Scyphozoan Medusae 212

Scyphozoan medusae 212

Predation on Scyphozoan Medusae and their Structural and Behavioral Antipredator Defenses 214

Fishes Associated with Scyphozoan Medusae 215

The Protection of Fishes from Scyphozoan Medusae 217

Recognition and Attraction to Scyphozoan Medusae by Associated Fishes 217

Partner Specificity, Duration of the Medusa–Fish Bond and the Effects of the Medusae Size on the Associated Fishes 219

Benefits and Costs to Fishes and Medusae from being Associated 221

The Effects of Medusae on Fish Recruitment 225

The Association of Fishes with Floating Objects and the Fish–Medusa Partnership 226

References 227

6 The Associations between Fishes and Molluscs 230

The Association between Fishes and Cephalopods 230

Cephalopods 230

Octopus Dens, Foraging and Antipredatory Behavior 231

Scavenging Fishes Associated with Octopus Dens 233

Fishes Associated with Foraging Octopuses 234

Octopuses and Cleaning Symbiosis 238

Transport Associations between Octopuses and Fishes 239

Fishes Associated with Squid Schools 239

The Association between Fishes and Gastropods 241

Gastropods 241

Predation on Conchs, Antipredatory Strategies and Foraging in Conchs 241

The Association between Cardinal Fishes and Conchs 242

The Association between Nudibranchs and Gobiid Fishes 245

The Association between a Pearlfish and an Opisthobranch Gastropod 246

The Association between Fishes and Bivalves 246

Bivalves 246

The Glochidia Larvae of Freshwater Mussels and their Host Fishes 247

Bitterlings and their Freshwater Mussel Hosts 248

Attraction of the European Bitterling to Mussels and Choice of Oviposition Sites 250

Adaptations of Bitterling for Development Inside Freshwater Mussels 252

Male Reproductive Behavior and the Mussel 254

Female Reproductive Behavior and the Mussel 257

Host Utilization by Sympatric Bitterling Species 260

Costs and Benefits for the Mussel and Possible Coevolution of the

Bitterling–Mussel Partnership 263

Pearl Fishes Associated with Bivalves 265

The Association of Snailfish and Red Hake with Sea Scallops 265

References 269

7 The Associations between Fishes and Crustaceans 276

The Associations between Fishes and Cleaner Shrimps 276

Cleaning Symbiosis and Shrimp 276

Taxonomy, Morphology, Coloration and Distribution of Cleaner Shrimp 276

Cleaner Shrimp Activity 287

Associations between Cleaner Shrimp and Sea Anemones 288

Communication between Fishes and Cleaner Shrimp 292

Removal of Parasites versus Mucus by Cleaner Shrimp 294

Costs and Benefits for Cleaner Shrimp and Fish Clients and the Proximate Mechanisms for Cleaning 296

The Evolution of the Cleaner Shrimp–Fish Partnership 298

Feeding associations between fishes and crustaceans 299

Mixed Species Schools of Fishes and Crustaceans 300

Liparid Fishes Associated with Lithodid Crabs 301

The Associations between Fishes and Burrowing Brachyuran Crabs 303

Gobiid Fishes Associated with Burrowing Thalassinid Shrimp 305

Thalassinid Shrimp and their Burrows 305

The Facultative Association of Clevelandia ios with Callianassa californiensis and Upogebia pugettensis 307

The Obligatory Association of the Blind Goby Typhlogobius californiensis with Callianassa affinis 311

The Obligatory Association of Austrolethops wardi with Neaxius acanthus 313

The Obligatory Association of Didogobius amicuscardis with Axiopsis serratifrons 314

Gobiid Fishes Associated with Burrowing Alpheid Shrimps 316

Systematics of Gobies and Shrimps 316

Biogeography 318

Diet and Feeding Behavior 319

Habitat Specificity 322

Population Structure and Dynamics 324

Burrow Structure, Construction and Dynamics 326

Activity Rhythms 330

Aggressive Behavior and Territoriality of Goby and Shrimp 334

Reproduction of Goby and Shrimp 336

Interspecific Communication 338

Communication under Natural Conditions in Indo-Pacific Partnerships 338

Warning Signal Generation by Indo-Pacific Gobies in Response to

Predators and Models of Predators 340

Sequence and Information Analyses in Indo-Pacific Partnerships 342

Film Analysis of the Communication between the Goby Amblyeleotris steinitzi and the Shrimp Alpheus purpurilenticularis 344

Communication between Gobies and Shrimp in the Western Atlantic 347

Partner Specificity 349

Field Observations 349

Laboratory Experiments 350

The Mechanism Regulating Specificity 352

Goby–Shrimp Phylogeography 353

Costs and Benefits for Goby and Shrimp 357

Evolution 358

References 360

8 The Associations between Fishes and Echinoderms 371

The Association between Fishes and Sea Urchins 371

Sea Urchins 371

Sea Urchin Structural Defenses, Predation by Fishes and Antipredatory Strategies 371

Associated Fishes, their Size, Coloration and Sea Urchin Hosts 373

The Attraction of Associated Fishes to Sea Urchins 386

Benefits and Costs of the Fish–Sea Urchin Partnership 388

Partner Specificity in the Fish–Sea Urchin Association 390

The Evolution of the Fish–Sea Urchin Partnership 390

Mimicry of Sea Urchins by Fishes 391

The Association between Fishes and Crinoids 392

Crinoids 392

Predation on Crinoids by Fishes and Antipredatory Strategies of Feather Stars and Sea Lilies 393

Multiple Species Assemblages in Crinoids 394

Associated Fishes and Adaptations for Living with Crinoids 395

Attraction of Associated Fishes to Crinoids and Partner Specificity 398

Benefits and Costs of the Fish–Crinoid Partnership 398

Scarcity of Knowledge 398

The Association between Fishes and Sea Cucumbers 399

Sea Cucumbers 399

Predation on Sea Cucumbers by Fishes and their Structural and

Behavioral Antipredatory Defenses 400

Fishes Associated with Sea Cucumbers and their Life Cycles 401

Host Location, Penetration and Occupation by Pearlfishes 405

Pearlfish Nutrition 406

Pearlfish Reproductive Biology 408

Ecology and Partner Specificity of Pearlfish–Holothurian Associations 410

Acoustic Communication in Pearlfishes 414

Morphological and Physiological Adaptations to Inquilism 415

Benefits and Costs of the Pearlfish–Sea Cucumber Partnership 417

The Evolution of the Partnership between Pearlfishes and their Hosts 417

The Association between Fishes and Sea Stars 418

Sea Stars 418

Sea Star Structural and Behavioral Antipredatory Defenses 419

Feeding Associations between Sea Stars and Fishes 420

Cardinal Fishes Sheltering among Sea Star Spines 421

Pearlfishes Associated with Sea Stars 421

References 423

Species Index 431

Subject Index 443

“Overall, Symbiosis in Fishesis a valuable scientific contribution because although symbiotic interactions interactions involving fish are common worldwide and can affect the dynamics of many ecosystems, this is the first comprehensive review of the topic.”  (The Quarterly Review of Biology, 1 June 2015)  

"Overall, the book reflects an exceptional breadth of knowledge and depth of integrative thinking, together with a deep appreciation for the subject of interspecific partnerships in fishes. As such, the book provides a superb resource and foundation for learning, teaching and further scientific inquiry." ( Journal of Fish Biology, 2015)