Shintaro Nomakuchi

A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource

Abstract Subsocial behavior or postovipositional parental care in insects has evolved in response to a variety of environmental stresses and ranges from briefly guarding eggs after oviposition to elaborate nidification and provisioning behaviors. Investment in parental care bears various costs, and should not continue beyond the point at which the costs to future reproductive success exceed the benefits to current reproductive effort. Progressive provisioning is a rare form of subsociality in insects. Females of the subsocial shield bug Parastrachia japonensis progressively provision their nymph-containing nests with drupes of the single resource, Schoepfia jasminodora, and this provisioning drastically enhances offspring survival. A female rears only one brood throughout her lifetime and continues provisioning the brood until about the third larval stadium, when the female dies. Thus, the females entire reproductive effort is expressed in the success of that one brood, which suggests a reproductive strategy with enormous costs and risks. Why has such an extreme life history evolved in this species? Here, to answer that question and to contribute to our understanding of the evolutionary implications of subsocial behavior, in particular, progressive provisioning, we review what we have discovered about the ecological parameters of subsociality in this species during a long-term field study. We also discuss these parameters in P. japonensis in reference to other subsocial insects and related species and conclude with a suggestion that semelparity and progressive provisioning in this species are extreme adaptations to evolving complete dependency on an unreliable resource.

Provisioned Parastrachia japonensis (Hemiptera: Cydnidae) nymphs gain access to food and protection from predators

Females of the shield bug Parastrachia japonensis Scott progressively provision nymph-containing nests with drupes of the host tree, Schoepfia jasminodora (Olicaceae: Rosidae: Santales). The majority of nests are 5-15 m from the host tree, a distance thought to have been a major impetus for the occurrence of provisioning in this species. However, the function of provisioning is not well understood. We carried out two field experiments to determine whether provisioning is nutritionally important and whether it affords protection against predation. Development of nymphs was significantly delayed and their survival was low in the absence of provisioning, even when nests were within the area of ground on to which the drupes fell, apparently because of the poor quality of the majority of the drupes. Selective provisioning of good-quality drupes by female P. japonensis, a semelparous species, was thus necessary for young nymphs to obtain enough food for their development. Furthermore, even without a female in attendance, having drupes in the nest significantly reduced early mortality in the presence of a predator. Copyright 2000 The Association for the Study of Animal Behaviour.

Pre- and post-hatch trophic egg production in the subsocial burrower bug, Canthophorus niveimarginatus (Heteroptera: Cydnidae).

In recent years, three terrestrial bugs, Adomerus triguttulus and Sehirus cinctus (Cydnidae) and the closely related Parastrachia japonensis (Parastrachiidae), have been the focus of several fascinating studies because of the remarkable, extensive parental care they were found to display. This care includes egg and nymph guarding, production of trophic eggs, unfertilized, low cost eggs that are used as food by newly hatched nymphs, and progressive provisioning of the host seed. In this study, we have investigated yet a third related Asian cydnid, Canthophorus niveimarginatus, with regard to the possible occurrence of some or all of these complex traits in order to assess how widespread these maternal investment patterns are in this group of insects and to better understand the implications of their manifestations from an evolutionary context. Manipulative experiments were carried out in the lab to determine whether females provision nests. Observational and egg removal studies were carried out to determine whether trophic eggs are produced, and, if they are, their possible impact on nymphal success. The findings revealed that C. niveimarginatus does, in fact, progressively provision young, and this species also displays all of the other behaviors associated with extended parental care in subsocial insects. Moreover, unlike the other two related species, which place trophic eggs on the surface of the original egg mass, C. niveimarginatus produces both pre- and post-hatch trophic eggs. Nymphs deprived of access to post-hatch trophic eggs had significantly lower body weight and survival rate than those that fed on them. To our knowledge, this is the first time the production of both pre- and post-hatch trophic eggs has been demonstrated in insects outside the Hymenoptera. In this paper, we qualitatively and quantitatively demonstrate the provisioning behavior and patterns of trophic egg production in C. niveimarginatus. When and how trophic eggs are produced and delivered to young should have important correlations with the ecological and life history constraints under which a species has evolved. Thus, we also discuss the possible ecological and life history factors that favor the evolution of post-hatch trophic eggs.

Selective Foraging Behavior in Nest-Provisioning Females of Parastrachia japonensis (Hemiptera: Cydnidae): Cues for Preferred Food

Females of Parastrachia japonensis (Hemiptera: Cydnidae) provision nymph-containing nests with drupes of the single host tree, Schoepfia jasminodora (Rosidae: Santales). P. japonensis feeds on the endosperm of these drupes. Foraging females approached and accepted only a few selected drupes for transport to their nests from among the hundreds of drupes scattered on the ground. The characteristics of the drupes that elicited an acceptance response under field conditions were examined. Females estimated the degree of endosperm development using volatile and nonvolatile chemicals in the outer skin as cues and selected only those drupes which had a well-developed endosperm. Although the cues that prompted approach and inspection of a drupe are in the fleshy outer skin, females presented with various substitute drupes coated with outer skin juices of acceptable drupes selected only those they could recognize as a solid mass, suggesting that they used volatile chemicals in the outer skin as cues for approaching and inspecting a drupe and then taste and tactile stimuli as cues for acceptance. Thus, this bug possesses a complex, ecologically sensitive cognitive system that enables it to recognize valuable food items by using reliable cues. The importance of selective foraging by P. japonensis females and the evolutionary significance of this behavior are discussed.

Risk‐sensitive decisions during nesting may increase maternal provisioning capacity in the subsocial shield bug Parastrachia japonensis

Abstract 1. Females of the monophagous shield bug Parastrachia japonensis Scott provision their nymph‐containing nests with high‐quality drupes of the single host tree, Schoepfia jasminodora, a resource that is poor and unstable, under an array of variable environmental constraints.

Insemination success discrepancy between long-term and short-term copulations in the provisioning shield bug, Parastrachia japonensis (Hemiptera: Cydnidae).

Abstract The duration of copulation in the gregarious shield bug, Parastrachia japonensis Scott (Hemiptera: Cydnidae), is of two types, the far more prevalent short-term copulation (average, 15 s) and the long-term coupulation (average, 23 min). Both types were thought to be equally effective in inseminating females. Recent evidence has suggested that there is, in fact, a discrepancy in insemination success between the two duration types of copulations. We carried out manipulated field studies to clarify the difference in insemination success between the two duration types and to determine whether there is some physical or physiological variability in females or males that might affect female receptivity to a long-term copulation. The findings indicated that, although a small percentage of short-term copulations resulted in some sperm transfer, long-term copulations were a far more effective way for males to inseminate females. Further, females experiencing long-term copulations were found to be at a slightly more advanced stage of ovarian development than those experiencing only short-term copulations, and may be deciding whether a long-term copulation occurs. Male size does not appear to affect copulation duration. It is concluded that the long-term type of copulation is the actual effective copulation duration in this species and the objective of all females. Possible factors that might contribute to the prevalence of these two copulation durations are discussed.

Competitive habitat utilization in the damselfly,Mnais nawai (Zygoptera: Calopterygidae) coexisting with a related species,Mnais pruinosa

Reproductive behaviors related to habitat utilization were studied in males of the damsefly,Mnais nawai, which has two male forms, territorial orange-winged males (nawai) and non-territorial pale-orange-winged males (sahoi), at the upper part of a mountain stream where they partiallycoexist with a related species,Mnais pruinosa, which also has two male forms, territorial orange-winged males (esakii) and non-territorial hyaline-winged males (strigata). These two species showed parapatric distribution; the lower part of the stream was occupied byM. nawai, and the upper part byM. pruinosa. In the present study, cross-matings occurred between bothMnais species, although normal intraspecific matings occurred more frequently than cross-matings. Territorial males of both species copulated with conspecific females that entered their territory and guarded the ovipositing females, probably to avoid sperm displacement resulting from subsequent copulations. Severe competition for oviposition sites by territorial males even occurred between the two species. On the other hand, non-territorial males of both species have alternative mating strategies (including several tactics such as sneaking, takeover and interception). The possible benefits from conflict among territorial males of both species is discussed.

Trophic eggs compensate for poor offspring feeding capacity in a subsocial burrower bug

Various animals produce inviable eggs or egg-like structures called trophic eggs, which are presumed to be an extended maternal investment for the offspring. However, there is little knowledge about the ecological or physiological constraints associated with their evolutionary origin. Trophic eggs of the seminivorous subsocial burrower bug (Canthophorus niveimarginatus) have some unique characteristics. Trophic eggs are obligate for nymphal survival, and first-instar nymphs die without them. To identify the cause of nymphal death, we hypothesized that first-instar nymphs starve to death because they cannot feed on anything but trophic eggs. Although first-instar nymphs fed on artificially exposed endosperm did survive, nymphs that were provided with intact seed were not able to penetrate the seed vessel and starved to death. Another hypothesis that trophic eggs play a role in transferring the midgut symbiont, essential for survival in heteropteran bugs, from mother to offspring was rejected because almost all nymphs had retained the symbiont without feeding on trophic eggs. These results suggest that poor feeding capacity of the offspring is the cause of nymphal death, and the important constraint that promotes the evolution of the curious trophic egg system in C. niveimarginatus.

Maternal-Care Behaviour in Adomerus variegatus (Hemiptera: Cydnidae)

Abstract Subsociality involving provisioning for offspring has been reported for one shield bug and three burrower bug species (Hemiptera: Pentatomoidea: Parastrachiidae and Cydnidae: Sehirinae). We present the first report of subsocial behaviour in the burrower bug Adomerus variegatus (Signoret), focusing on manifestations of maternal-care, specifically the production of trophic eggs, guarding of offspring, and progressive provisioning. In our study, each female produced an egg mass that included some trophic eggs. Prior to nymphal hatch, females remained in their nests and showed egg mass guarding behaviour. Mothers started provisioning behaviour a few hours after nymphal hatch. Each mother dragged a seed (larger than her body) with her proboscis to the nest as food for the nymphs. These findings suggest that A. variegatus shows maternal-care behaviours similar to those reported in some other pentatomoid species and that trophic egg production and nest provisioning have evolved as interrelated processes.

Kleptoparasitism and the Effect of Nest Location in a Subsocial Shield Bug Parastrachia japonensis (Hemiptera: Parastrachiidae)

Abstract Females of the subsocial shield bug Parastrachia japonensis Scott progressively provision nymph-containing nests with drupes of the single host tree Schoepfia jasminodora Sieb. et Zull. The resource is unreliable and typically poor, and females invest considerable time in searching for suitable drupes. Earlier observations have indicated that although some females nest under the host tree, most prefer to nest far from the food source, despite the difficulty involved in transporting drupes to a distant nest. Because we have observed females stealing drupes from other females’ nests, we considered that kleptoparasitism might be a factor in determining nest site preference. A manipulated field study was carried out to clarify the prevalence of kleptoparasitism in nests close to and far from the host tree and to determine how these factors affect nest success. Surprisingly, in the year of this study, when drupes were particularly scarce, more drupes were stolen, but females still collected significantly more drupes and had greater nest success, in nests located under the host tree than in those that were 5 m away. The ecological factors relevant to kleptoparasitism and nest site choice are discussed.