The Life History of the Parental Shield Bug, Parastrachia japonensis (Entomology Monographs)

This book presents the discoveries made during nearly three decades of research on the parental shield bug, Parastrachia japonensis inhabiting Kyushu Island, Japan. P. japonensis has evolved a unique and fascinating life history, characterized by extreme behavioral and physiological adaptations that have culminated in a singularly dependent relationship with its lone host tree, Schoepfia jasminodora (Olacaceae), which is a generally scarce and unreliable resource. It is expected that the evolution of parental care behaviors in the strictly semelparous P. japonensis was more directly influenced by the benefit to females that arises from enhanced survivorship of current offspring, rather than any possible cost the females might incur in terms of reduced future reproductive success, because no future reproduction is possible . The authors explain how the different parental cares in this species enhance offspring survivorship in the context of the ecological conditions it has experienced over evolutionary time. The book begins with a recap of the earliest studies, the reports through 1991, and then introduces the many fascinating aspects of the life history, neurobiology, physiology and behavior of P. japonensis that have been newly discovered since, and those aspects that have been confirmed through experimentation over the past thirty years. This comprehensive review of information will be useful for comparative studies of parental care in other semelparous and iteroparous organisms experiencing both similar and different ecological constraints. The book will be of academic interest to undergraduate and graduate students of entomology, zoology, behavior, and behavioral ecology. Foreword Preface Acknowledgments Contents About the Editors 1: General Biology of Parastrachia japonensis 1.1 Introduction 1.2 Historical Perspective of Studies on the Life History of P. japonensis 1.3 General Morphology 1.4 Classification 1.4.1 Phylogenetic Status Based on Morphology 1.4.2 Phylogenetic Status Based on Morphology and Molecular Data 1.4.3 Phylogenetic Status Based on Unique Behavioral Features 1.5 Geographic Distribution of P. japonensis and P. nagaensis 1.6 General Characteristics of the Habitat 1.7 Climate in Southern Japan 1.8 Local Field Site at Mt. Hinokuma Park 1.9 Local Habitat Required to Support a Subpopulation of P. japonensis 1.10 Distribution of Host Trees and P. japonensis and Abundance of Drupes 1.11 Non-food Resource Qualities Essential to the Microhabitat 1.12 Do P. japonensis Discriminate Habitat Based on Collective Optimality of Essential Environmental Features? 1.12.1 Most Determinant Environmental Features 1.13 Phenology of the Host Tree and Instability of the Resource 1.13.1 Variation in Drupe Quality 1.14 Toxic Drupes and Toxic Bugs 1.15 Life Cycle of Parastrachia japonensis References 2: Mechanisms for Prolonged Survival Without Food 2.1 Introduction 2.2 Pattern of Aggregation Formation 2.3 Functions of Aggregations 2.3.1 Protection Against Predators, Mate Acquisition, and Reduction of Water Loss Mate Acquisition Reduction of Water Loss 2.3.2 Increased Efficiency of Resource Use Aggregation and Reduction of Metabolic Rate 2.3.3 Effect of Group Size on Metabolic Rate 2.3.4 Effect of Physical Contact on Metabolic Rate 2.3.5 Combined Effects of Contact Pheromone and Physical Contact 2.3.6 Effect of Humidity Level on Metabolic Rate 2.3.7 Effect of Reproductive Stage on Metabolic Rate 2.3.8 Monthly Metabolic Rates from the End of Diapause until Hibernation 2.3.9 Metabolic Rate of New Adults over 20 Weeks 2.3.10 Conclusions About Formation and Functions of Aggregations in P. japonensis 2.4 The Roles of Uric Acid and the Bacterial Symbiont During Prolonged Reproductive Diapause 2.4.1 Nitrogenous Waste Levels in Active P. japonensis Nymphs and Reproductive Adults and their Excreta 2.4.2 Nitrogenous Waste Levels and Total Nitrogen in Diapausing P. japonensis Adults and their Excreta 2.4.3 Involvement of the Midgut Symbiont in Uric Acid Metabolism 2.5 Unique Mechanism of Vertical Symbiont Transmission References 3: Mating Behavior 3.1 Introduction 3.2 Mating Systems That Involve Polygyny 3.2.1 Female Defense Polygyny 3.2.2 Resource Defense Polygyny 3.2.3 Scramble Competition Polygyny 3.3 Mating System in Parastrachia japonensis 3.3.1 Flight by Males and Mating Behaviors in the Field 3.3.2 Copulation Frequency and Success Rate by Males in Aggregations and at Isolated Sites 3.3.3 Duration of Copulation in Aggregated and Isolated Conditions 3.3.4 Change in Numbers of Males and Females at the Aggregation Site over the Mating Season 3.4 Ovarian Development and Fat Body Content Throughout the Mating Season 3.5 Male Intrasexual Competition 3.6 Conclusions of Initial Mating Study 3.7 Observations of Manipulated Mating Behavior in the Field 3.8 Patterns of Short- and Long-Term Matings over the Mating Season 3.9 Frequency, Duration, and Insemination Success Rate of Short- and Long-Term Matings 3.10 Effect of Female Body Size, Weight, and Ovarian Development on Mating Duration and Insemination Rate 3.11 Effect of Male Body Size on Long-Term Mating Success References 4: Parental Care 4.1 Introduction 4.2 Nesting and Maternal Care of Eggs 4.3 Provisioning Behavior 4.3.1 Method of Provisioning 4.3.2 Relationship Between Nest Distance and Provisioning Rate 4.3.3 Conclusions of Our Earliest Study on Parental Care in P. japonensis 4.4 Thinking About the Big ``Whys ́ ́ 4.5 Nesting Pattern and Longevity of Nests in 1994 4.6 Maternal Egg Guarding Behavior 4.7 Kin Recognition and Nest Fidelity 4.8 Provisioning Behavior 4.9 Variation in Number of Provisioned Drupes and Nymphal Nesting Stage 4.10 Effects of Drupes and Female Presence 4.11 Conclusions from This Study 4.12 Testing the Speculated Functions of Progressive Provisioning 4.12.1 Testing the Resource Constraint Hypothesis Drupe Availability Development Rate Survivorship 4.12.2 Testing the Predation Hypothesis 4.13 Conclusions from These Studies 4.14 Predation Risk to Nymphs of Different Stages 4.15 Impact of Female Provisioning Capacity on Duration of Nymphal Stage 4.15.1 Experiment 1: Determining the Timing of Nymphal Independence 4.15.2 Experiment 2: Impact of Provisioning Capacity on Timing of Nymphal Independence 4.15.3 Experiment 3: Distance and Success Rate of Nymphal Instars Reaching the Foraging Area 4.16 Conclusions About the Impact of Provisioning on the Nymphal Nesting Period 4.17 Provisioning of Nutrition Before Provisioning Drupes: Production of Trophic Eggs 4.17.1 Are Eggs Fed on by New Hatchlings Morphologically Different from Viable Eggs? 4.17.2 Numbers/Proportions of Fertile and Unfertilized Eggs 4.17.3 Impact of Feeding on Unfertilized Eggs on Nymphal Weight at 24 h 4.17.4 Impact of Access to Unfertilized Eggs on Nymphal Development Rate and Survivorship 4.17.5 Risk-Sensitive Decision-Making as the Source of Variation in Trophic Egg Production 4.17.6 Temporal Variation in Female and Egg Parameters During the Nesting Season 4.17.7 Impact of Body Size on the Number of Eggs Produced 4.18 Timing and Manner of Trophic Egg Deposition in the Cydnid Relatives of P. japonensis 4.19 Verifying Risk-Sensitive Decision-Making by Nesting Mothers 4.19.1 Variation in Duration of Provisioning Season and Individual Provisioning Activity 4.19.2 Variation in S. jasminodora Drupe Availability and Weather During the Provisioning Season 4.19.3 Intensity of Competition for the Resource, Weather, and Provisioning Capacity of Females 4.19.4 Variation of Nest Distribution over the Four Nesting Seasons 4.19.5 Variation in Provisioning Capacity Based on Nest Location and Active Timing 4.19.6 Conclusions Regarding Risk-Sensitive Decision-Making References 5: Parent-Offspring Communication 5.1 Introduction 5.2 Parent-Embryo Communication 5.2.1 Maternal Substrate Vibrations as Cues of Exquisite Synchronous Hatching Exquisite Synchronous Hatching Vibrating Behavior by Mothers 5.2.2 Effect of Maternal Vibration on Hatching Pattern 5.2.3 Maternal Care as a Necessary Cue for Embryo Hatching 5.2.4 Maternal Vibration and Synchronous Hatching in Closely Related Species 5.2.5 Adaptive Function of Maternal Care at the Moment of Hatching 5.2.6 Conclusions About Parent-Embryo Communication in Subsocial Stinkbug 5.3 Parent-Nymph Communication 5.3.1 Provisioning Call Discovery of the Provisioning Call 5.3.2 When Do Females Emit the Call? 5.3.3 Vibrational Characteristics of the Provisioning Call 5.3.4 Function of the Provisioning Call References 6: Foraging Strategies 6.1 Introduction 6.2 Visual and Chemical Orientation in the Provisioning Excursion 6.2.1 Navigating the Provisioning Trip 6.2.2 Outbound Trip 6.2.3 Inbound Trip 6.2.4 Chemical Cue Used in Nest Searching 6.2.5 Path Integration System 6.2.6 Visual Compass Mechanism 6.2.7 Canopy Cue in Nocturnal Homing 6.2.8 Conclusion: Navigation Ability in Subsocial Bugs 6.3 Process Used by Females to Identify a ``Good ́ ́ Drupe 6.3.1 Relationship Between Drupe Features and Acceptability to Provisioning Females 6.3.2 Initial Cues Used by Provisioning Females that Led to Approaching a Drupe 6.3.3 Weight as a Possible Cue to Accept a Drupe 6.3.4 Nonvolatile Juices in the Outer Skin as a Possible Cue to Accept a Drupe 6.3.5 Consistency of Drupe as a Possible Cue for Its Acceptability 6.3.6 Can Females Recognize Just the Endosperm with No Chemical Cues from the Outer Skin? 6.3.7 Conclusions About Drupe Selection Process 6.4 Alternative Foraging Behavior: Kleptoparasitism 6.4.1 Factors Related to Rate of Kleptoparasitism Pattern of Drupe Availability 6.4.2 Effect of Energetic Reserves on Provisioning Capacity 6.4.3 Development and Survival Rates of Nymphs Inside and Outside the Foraging Area 6.4.4 Persistence of Nests Inside and Outside the Foraging Area 6.4.5 Conclusions of This Study 6.5 Guarding Behavior Against Intraspecific Kleptoparasites 6.5.1 Guarding Behaviors Displayed 6.5.2 Effectiveness of Guarding Behavior Against Intruders 6.5.3 Summary of Guarding Behavior 6.6 Kleptoparasitism: An Opportunistic Behavior or an Evolved Alternative Tactic? 6.6.1 Are Females Attracted to Other Female ́s Nests? 6.6.2 Testing the Attractiveness of a Good Drupe vs a Conspecific 6.6.3 Could Females Be Entering a Conspecific Nest for Some Other Reason? 6.6.4 Does the Female Find Her Own Nest and Other Nests by Location or by Odor? 6.6.5 Conclusions References 7: Nematodes Exploiting P. japonensis 7.1 Introduction 7.2 Parasitic Nematode: Mermithid Nematodes 7.2.1 Prevalence of Mermithids in P. japonensis 7.2.2 Synchronization of Life Cycle 7.2.3 Impact of Mermithid Parasitism on P. japonensis 7.3 Phoretic/Necromenic Nematode: Caenorhabditis japonica 7.3.1 The Genus Caenorhabditis and Phylogenetic Relationship 7.3.2 Distribution 7.3.3 Life Cycle 7.3.4 Synchronized Life History with P. japonensis 7.3.5 Species Specificity and Adult Female P. japonensis-Biased Association of C. japonica 7.3.6 Characteristic Behavior of C. japonica Dauer Larva Nictation, Waving, and Jumping Negative Gravitaxis Odor Recognition and Host Orientation Behavioral Changes After Association with P. japonensis 7.3.7 Characteristic Physiology of C. japonica Dauer Larvae 7.3.8 Longevity of Dauer Larvae Desiccation Tolerance Influence of C. japonica on P. japonensis 7.4 Conclusion References 8: Future Directions: Where Do We Go from Here? 8.1 Introduction 8.2 Similarities and Differences Among Members of the Parental Cluster 8.3 Future Directions 8.3.1 Describing the Sister Species 8.3.2 Ecological Cues, Suppression of Metabolic Rate, and Physiological Innovations Using Bacterial Symbionts 8.3.3 Lingering Questions About Mating Behavior 8.3.4 Regulation of Trophic Egg Production 8.3.5 Parent-Offspring Conflict and Sibling Rivalry 8.3.6 Navigating at Night 8.3.7 Mitigation of Sibling Cannibalism References Index