The role of amphibian prey in the diet and growth of giant water bug nymphs in Japanese rice fields

Predatory insects that depend upon particular prey animals are commonly regulated by the prey animal’s abundance. Nymphs of the giant water bug Kirkaldyia (=Lethocerus) deyrolli (Heteroptera: Belostomatidae) are predators regarded as specialists in feeding on tadpoles. We studied the ontogenetic diet shift of aquatic nymphs by quantifying instar abundance and by analyzing captured prey and prey relative abundance during the period of rice irrigation in three localities. We also evaluated the contribution of major prey items (tadpoles, frogs, and Odonata nymphs) on specific growth rates of each nymphal stage in a rearing experiment. First to third-instar nymphs of K. deyrolli fed mainly on tadpoles, regardless of differences in prey availability. Nymphs of subsequent fourth and fifth instar stages shifted from tadpoles to other prey animals within each rice field. A rearing experiment demonstrated that giant water bug nymphs provided with tadpoles had greater specific growth rates at all nymphal stages, except for the final stage, than nymphs fed other prey (frogs and Odonata nymphs). The emergence of young K. deyrolli nymphs seemed to coincide with the period during which tadpoles became abundant in the rice fields. Consumption of tadpoles seems important to allow the nymph to complete its larval development in an unstable temporary habitat. An erratum to this article can be found at     

Notes on predators and their effect on the survivorship of the endangered giant water bug, <Emphasis Type="Italic">Kirkaldyia (</Emphasis>= <Emphasis Type="Italic">Lethocerus) deyrolli</Emphasis> (Heteroptera,Belostomatidae), in Japanese rice fields

A field research was carried out in Hyogo Prefecture, Japan in order to establish the role of the water-scorpion, Laccotrephes japonensis Scott as predator of nymphs of the endangered giant water bug, Kirkaldyia (= Lethocerus) deyrolli. To assess the impact of this predator, a field experiment was set up with (Control) and without L. japonensis (Removed). The survival rate of K. deyrolli in Removed treatment was higher than in the Control. Our experimental results showed that L. japonensis is an important predator for K. deyrolli nymphs in the field. Handling editor: S. Wellekens     

Density-mediated indirect effects of a common prey tadpole on interaction between two predatory bugs: <Emphasis Type="Italic">Kirkaldyia deyrolli</Emphasis> and <Emphasis Type="Italic">Laccotrephes japonensis</Emphasis>

This paper suggests that the nymphs of a specialist predator, Kirkaldyia (=Lethocerus) deyrolli (Belostomatidae: Heteroptera), are indirectly affected by their tadpoles’ prey. K. deyrolli nymphs and the predator Laccotrephes japonensis (Nepidae: Heteroptera) adults coexist in rice paddy fields. It was predicted that the difference in tadpole density may influence the K. deyrolli nymph survival rate. We first compared survival rates of the first instar nymphs of K. deyrolli in June (high tadpole density period) and July (low tadpole density period). Secondly, we investigated the survival rate of K. deyrolli nymphs at different tadpole densities and under the presence or absence of L. japonensis adults to examine whether higher tadpole density moderates predation pressure from L. japonensis adults to K. deyrolli nymphs, e.g., density-mediated indirect effects. As a result of the comparison, the survival rate of K. deyrolli nymphs in June was higher than that in July. For the field experiment, the slopes between the survival rate of K. deyrolli nymphs and tadpole density were positive under both predator presence and absence. However, the slope under the presence of a predator was steeper than that under absence of the predator (“predator-by-tadpole density interaction” was significant). These results suggest that a higher tadpole density in June provides an abundant food resource for K. deyrolli nymphs and also moderates predation pressure from L. japonensis.     

Variation in the geometry of foreleg claws in sympatric giant water bug species: an adaptive trait for catching prey?

When giant water bugs (Heteroptera: Belostomatidae) encounter prey animals that are larger than they are themselves, they first hook the claw of their raptorial legs onto the animal, and then use all their legs to pin it. The claws of the raptorial legs in giant water bugs play an important role in catching larger prey, but the relationship between the claws, body lengths of predators, and prey size has not been fully investigated. To elucidate the functioning of claws in catching prey, we investigated prey body size relative to predator size in nymphs of two sympatric belostomatid giant water bug species, the vertebrate eater Kirkaldyia (=Lethocerus) deyrolli Vuillefroy and the invertebrate eater Appasus japonicus Vuillefroy, captured in rice fields. The younger nymphs of K. deyrolli caught preys that were larger than themselves, whereas those of A. japonicus caught preys that were smaller. Younger nymphs of K. deyrolli had claws that were curved more sharply than those of A. japonicus. The more curved claws of younger nymphs of K. deyrolli probably hook more easily onto larger vertebrates and thus this shape represents an adaptation for acquiring such prey.     

Prey preferences of aquatic insects: potential implications for the regulation of wetland mosquitoes

Wetlands are potential sites for mosquito breeding and are thus important in the context of public health. The use of chemical and microbial controls is constrained in wetlands in view of their potential impact on the diverse biota. Biological control using generalist aquatic insects can be effective, provided a preference for mosquito larvae is exhibited. The mosquito prey preferences of water bugs and larvae of odonate species were evaluated using chironomid larvae, fish fingerlings and tadpoles as alternative prey. Manly's selectivity (α_i) values with 95% confidence intervals (CIs) were estimated to judge prey preference patterns. Multivariate analysis of variance (manova) and standardized canonical coefficients were used to test the effects of density on prey selectivity. The α_i values indicated a significant preference (P < 0.05) in all of the insect predators tested for mosquito larvae over the alternative prey as a density‐dependent function. On a comparative scale, chironomid larvae had the highest impact as alternative prey. In a multiple‐prey experiment, predators showed a similar pattern of preference for mosquito larvae over alternative prey, reflecting a significant (P < 0.05) niche overlap. The results suggest that, in a laboratory setting, these insect predators can effectively reduce mosquito density in the presence of multiple alternative prey.     

The number of tadpoles consumed by the nymphs of the giant water bug <Emphasis Type="Italic">Kirkaldyia deyrolli</Emphasis> under laboratory conditions

Giant water bug Kirkaldyia (=Lethocerus) deyrolli (Belostomatidae: Heteroptera) nymphs consume many individuals of anuran larvae (tadpoles) before they reach adulthood. However, no quantitative data on the number of tadpoles consumed have been made available until now, despite the importance of this data for the conservation of this species. The number of tree frog, Hyla japonica (Hylidae: Anura), tadpoles consumed by nymphs of K. deyrolli was examined under laboratory conditions. The number increased according to the developmental stage of the nymphs; the fifth instar nymphs were the highest consumers. The total numbers consumed by the nymphs throughout development were 155.0 ± 12.8 (average ± SD) and 172.8 ± 9.6 for the males and the females, respectively. Thus, it might be important to maintain high densities of frogs in fields to conserve the population of K. deyrolli into the future.     

Intraguild predation of water scorpion Laccotrephes japonensis (Nepidae: Heteroptera)

Previous work on community structure of the invertebrate fauna of Japanese wetlands indicates the presence of intraguild predation between the heteropterans Laccotrephes japonensis (Nepidae) and Kirkaldyia deyrolli (Belostomatidae). We designed a series of experiments to understand the biotic interactions of several species of sympatric heteroptera and their shared prey. Adult Laccotrephes japonensis (Nepidae), first-instar nymph of Kirkaldyia (=Lethocerus) deyrolli (Belostomatidae), Hyla japonica tadpole, and fourth-instar nymph of Appasus japonicus (Belostomatidae) have been shown to be intraguild predator, intraguild prey, common prey, and prey of L. japonensis, respectively. To further understand the factors affecting prey preference by L. japonensis, we also examined the comparison of swimming speed in the three prey animals (K. deyrolli first-instar nymph, A. japonicus fourth-instar nymph, and H. japonica tadpole), and effects of prey animals on weight gain of L. japonensis adult. Despite there being no significant difference in weight gain or swimming speed of the three prey species, L. japonensis exhibited a strong preference for the 1st-instar nymph of K. deyrolli. We suggested that this may be evidence for one of elimination of a potential competitor, K. deyrolli, by L. japonensis through intraguild predation.     

Notes on paternal care and sibling cannibalism in the giant water bug, Lethocerus deyrolli (Heteroptera: Belostomatidae)

Males of the giant water bug, Lethocerus deyrolli, care for egg masses on vegetation above the water surface. They supply the developing eggs with water and guard them against predators. In the present study, mechanisms by which paternal care is extended were found. Males were found situated just below the water on the natal substrate (usually a stick), and the first instar nymphs were aggregated around the substrate. When disturbed, the males showed aggressive behavior, threatening the intruder with their forelegs. Nymphs up to 12 h old did not attack the offered sibling nymphs or anuran larvae, which are common prey in the field. The 24 h‐old nymphs attacked both prey animals; however, they preferred anuran larvae. Cannibalistic behavior in the nymphs was well developed 72 h after hatching, when the nymphs had already dispersed from the natal substrate. The suppression of sibling cannibalism in younger nymphs would promote the maintenance of tight nymphal aggregations and consequently extend male care in this predatory species.     

Tadpoles of three common anuran species from Thailand do not prey on mosquito larvae

Tadpoles are often considered to be predators of mosquito larvae and are therefore beneficial for the control of certain disease vectors. Nevertheless, only a few species have actually been recorded to prey on mosquito larvae. The mosquito larvae predation rates of tadpoles of three common Thai anuran species (Bufo melanostictus, Kaloula pulchra and Hylarana raniceps) were experimentally tested. Tadpoles in varying developmental stages were used to assess a size/age effect on the predation rate. In addition, different instars of Culex quinquefasciatus were used in order to assess a prey size effect on the predation rates. All three species failed to show any evidence of mosquito larvae predation. Neither small nor large tadpoles fed on mosquito larvae. Prey size also did not affect predation. Although tadpoles do not feed on mosquito larvae, there may be other direct or indirect inter‐specific interactions that adversely impact the development of larvae in shared habitats with tadpoles.     

Relationships between predatory aquatic insects and mosquito larvae in residential areas in northern Thailand

In order to elucidate the poorly understood relationships between mosquito larvae and their predatory aquatic insects in urban and suburban areas of tropical Southeast Asia, where vector‐borne diseases are prevalent, aquatic insects were sampled from 14 aquatic habitats in residential areas of Chiang Mai, northern Thailand, during the rainy season (July to November) in 2016. Correlations among biological variables, densities of major predatory aquatic insect groups (i.e., Odonata, Coleoptera, and Hemiptera: OCH group) in wetlands and artificial lentic habitats, and the density of mosquito larvae were analyzed. Among the sampled mosquito larvae, Culex spp. were the most abundant, and both OCH density and water quality were major determinants of Culex spp. density (r_s = ?0.302 and ?0.396, respectively). Logistic regression analyses indicated that the probability of Culex spp. occurrence was significantly and negatively correlated with OCH density. Furthermore, high macrophyte abundance was associated with higher predator density, potentially reducing mosquito density. Hemipteran predators were most negatively correlated with Culex spp. density, regardless of whether macrophyte abundance was high or low (r_s = ?0.547 and ?0.533, respectively). Therefore, hemipteran predators were the most important aquatic insect predators in the urban and suburban residential areas of Chiang Mai, Thailand, and OCH species, such as the hemipteran Micronecta scutellaris, could be used as biological control agents against mosquitoes in the region.     

Effect of loach consumption on the reproduction of giant water bug Kirkaldyia deyrolli: dietary selection, reproductive performance, and nutritional evaluation

Rice fields provide major habitats for lentic aquatic insects including the giant water bug Kirkaldyia (=Lethocerus) deyrolli (Heteroptera: Belostomatidae) in Japan. Previous researchers have emphasized that conserving populations of the frogs, Hyla japonicus and Rana nigromaculata, is very important for preserving K. deyrolli because these frogs were found to be a major component of the diet of K. deyrolli adults. However, these previous studies were carried out in rice fields with no loaches, Misgurnus anguillicaudatus, which were probably been inhabited by loaches in the past. A series of field surveys and laboratory experiments were conducted to determine the dietary preference of K. deyrolli adults for loaches, frogs, and aquatic insects; the reproductive effects of consuming these foods; and their protein content. In the rice fields, K. deyrolli adults ate loaches when they were available. When the three prey species (frog: R. nigromaculata, loach: M. anguillicaudatus, and dragonfly: Orthetrum albistylum speciosum) were supplied in laboratory conditions, K. deyrolli adults ate more loaches than frogs or dragonflies. In addition, K. deyrolli adults provided with loaches or frogs laid more egg masses within the limited breeding season than when provided with dragonflies. The edible parts of the loach bodies were the largest of the three prey types. It is possible that K. deyrolli adults have been forced to eat frogs due to reductions in the population density of loaches because modern rice cultivation obstructs loach migration routes and reduces their spawning grounds.     

Food shortage affects flight migration of the giant water bug Lethocerus deyrolli in the prewintering season

The endangered giant water bug Lethocerus deyrolli (Vuillefroy) is frequently attracted in large numbers to artificial lights in Japan. To examine factors enhancing flight migration for L. deyrolli, we carried out field work in western Hyogo Prefecture, central Japan, in September during the nonreproductive and prewintering season. The body weight of specimens collected under flight migration (flight bugs) was significantly less than that of those collected in ponds (pond bugs). A field experiment using open cages in a rice paddy field was carried out with two treatments, with and without a food supply. The remaining rate of L. deyrolli for the food present treatment was significantly higher than that for the food absent treatment for the first two days. These results suggest that L. deyrolli would fly in search of food when the food supply of the present habitat becomes unsuitable.     

Diet composition of the endangered giant water bug Lethocerus deyrolli (Hemiptera: Belostomatidae) in the rice fields of Japan: Which is the most important prey item among frogs,fish, and aquatic insects?

The food habits of the endangered giant water bug, Lethocerus deyrolli, were studied in the rice fields of Nose, in the north of Osaka Prefecture, Japan. Field observations revealed that frogs were the most important prey item. Frogs represented 86.4% and 78.6% in the diet of L. deyrolli in spring and summer, respectively. Among seven species of three families (Hylidae, Rhacophoridae, and Ranidae) exploited by L. deyrolli, the most important food item was adult Hyla japonica in spring and juvenile Rana nigromaculta in summer. Fish and aquatic arthropods were not considered important foods for L. deyrolli. The frog‐dependent food habits indicate that the recovery and conservation of frogs should be prioritized to protect L. deyrolli from extinction.     

Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type

Many species alter their activity, microhabitat use, morphology and life history in response to predators. Predation risk is related to predator size and palatability of prey among others factors. We analyzed the predation risk of three species of tadpoles that occur in norwestern Patagonia, Argentina: Pleurodema thaul, Pleurodema bufoninum and Rhinella spinulosa. We sampled aquatic insect predators in 18 ponds to determine predator–tadpole assemblage in the study area. In laboratory conditions, we analysed the predation rate imposed by each predator on each tadpole species at different tadpole sizes. Finally, we tested whether tadpoles alter their activity in the presence of chemical and visual cues from predators. Small P. thaul and P. bufoninum tadpoles were the most vulnerable prey species, while small R. spinulosa tadpoles were only consumed by water bugs. Dragonflies and water bugs were the most dangerous tadpole predators. Small P. thaul tadpoles reduced their activity when they were exposed to all predators, while large tadpoles only reduced the activity in the presence of large predators (dragonfly larvae and water bugs). Small P. bufoninum tadpoles reduced the activity when they were exposed to beetle larvae and dragonfly larvae, while large tadpoles only reduced activity when they were exposed to larger predators (water bugs and dragonfly larvae). R. spinulosa tadpoles were the less sensitive to presence of predators, only larger tadpoles responded significantly to dragonfly larvae by reducing their activity. We conclude that behavioural responses of these anuran species were predator-specific and related to the risk imposed by each predator.     

Habitat complexity reduces prey vulnerability: An experimental analysis using aquatic insect predators and immature dipteran prey

The effects of alternative prey and structural complexity of habitat on the selection of mosquito larvae by aquatic insect predators were evaluated in the laboratory. The water bugs Anisops bouvieri, Diplonychus (= Sphaerodema) rusticus, and D. annulatus, and the odonate nymphs, Ceriagrion coromandelianum and Brachydiplax chalybea chalybea, selected mosquito larvae based on their abundance relative to chironomid larvae and on the levels of habitat complexity. The effect of one prey species on the other was asymmetrical, as indicated through prey selectivity values. Compared to open habitat, the presence of macrophytes reduced the vulnerability of mosquito larvae while the effect was reverse in the presence of sediments. When both sediment and macrophytes were present in habitats, all the predators except D. annulatus consumed more mosquito larvae than chironomid larvae. The clearance rate, an indicator of predatory efficiency, varied among the predator species and habitat types. The results suggest that the outcome of the interactions between insect predators and mosquito immatures was context-dependent and that it was mediated by the presence of alternative controphic species and the habitat complexity.     

Mosquitoes and other aquatic insects in fallow field biotopes and rice paddy fields

Fallow field biotopes that develop from abandoned rice fields are man‐made wetlands that provide new habitats for various aquatic animals. Although consideration of such biotopes generally focuses on their positive aspects, this study evaluated the negative aspects of establishing fallow field biotopes with regard to mosquito breeding sites. To determine whether fallow field biotopes become breeding habitats for vector mosquitoes, we evaluated mosquito fauna in fallow field biotopes and adjacent rice fields. We found larvae of Anopheles lesteri, Anopheles sinensis and Culex tritaeniorhynchus (all: Diptera: Culicidae) in the biotopes. Although abundances of mosquito larvae in the biotopes and rice fields were statistically similar, mosquito abundances in rice fields increased dramatically in August when the water level reduced after the rainy season. The abundance and variety of the mosquitoes' natural predators were greater in biotopes than in rice fields because the former are a permanent and stable aquatic environment. A generalized linear mixed model showed a negative effect of predator diversity on mosquito larvae abundance in both habitats. Although fallow field biotopes become breeding habitats for vector mosquitoes, establishing biotopes from fallow fields in order to protect various aquatic animals, including mosquito insect predators, may help to control mosquito breeding.     

Do nymphs of Parameletus chelifer and P. minor (Ephemeroptera) reduce mortality from predation by occupying temporary habitats?

Summary The possible effect of predation on the habitat selection of nymphs of the two mayfly species Parameletus chelifer Bengtsson and P. minor (Bengtsson) was investigated for different habitats of a North Swedish boreal river. In spring, these two species migrate to river margins and subsequently, in different proportions, to adjacent seasonal ponds. Feeding rates on mayfly nymphs and mosquito larvae by some dytiscid beetles and larvae, a corixid waterbug and a caddisfly larva were studied in the laboratory. In the seasonal pond, the consumption rate of invertebrate predators on Parameletus nymphs was below that expected from their relative abundance, and mosquito larvae were preferred. At the river margin, where mosquito larvae were absent, Parameletus nymphs were consumed in agreement with their relative abundance. The absolute abundance of macroinvertebrate predators was similar at the river margin and in the pond. Fish predators visited the seasonal pond only during a short time of flood, while at the river margin their presence was continuous. In the seasonal pond, minnow and roach consumed nymphs of both P. chelifer and P. minor in a lower proportion than expected. At the river margin, nymphs of P. chelifer were consumed by minnow and ten-spined stickleback in a higher proportion than expected. Nymphs of P. minor were consumed according to expectance. Imagines of P. minor emerged early, and nymphs were equally abundant in the river and in the seasonal pond. In contrast, almost all nymphs of P. chelifer migrated to the seasonal pond. The later emergence of P. chelifer would probably result in a very high mortality from predation if it remained at the river margin.     

Cannibalistic Interactions Resulting from Indiscriminate Predatory Behavior in Tadpoles of Poison Frogs (Anura: Dendrobatidae)1

Poison frogs in the genus Dendrobates have very small clutch sizes (2–6 eggs among species for which there are data) and typically transport their tadpoles singly to small phytotelmata, such as bromeliad tanks, leaf axils, fallen fruit capsules, and treeholes. Tadpoles of many species are predaceous, consuming larvae of insects that use the same microhabitat for breeding, such as giant damselflies and mosquitoes. Previous studies and observations on the behavior of poison frog tadpoles led us to question whether tadpoles might be cannibalistic. We studied a population of Dendrobates castaneoticus in lowland rainforest in Pará, Brazil; additional data were collected on Dendrobates auratus in Nicaragua. At the study site in Brazil, we established a grid of 40 Brazil nut capsules, the microhabitat used by D. castaneoticus for tadpole deposition. Of 42 tadpoles deposited during the 55 days of the study, 20 were killed or died; 16 of these were presumably killed by conspecific tadpoles. Growth rate and time to metamorphosis was higher among tadpoles that consumed three or more tadpoles or relatively large larvae of the mosquito Trichoprosopon digitatum, a colonist of newly opened Brazil nut capsules. We propose that selection has favored the development of predatory behavior in poison frog tadpoles primarily as a mechanism to eliminate predators from the small phytotelmata in which they develop and that cannibalism is a secondary outcome of this behavior. Predatory behavior also provides tadpoles with a source of food, which is frequently limited in these microhabitats. Additional studies of the biology of tadpoles of other species of Dendrobates are needed to determine the evolution of predatory and cannibalistic behavior in the clade.     

Diving beetle assemblages of flooded wetlands in relation to time,wetland type and Bti-based mosquito control

We investigated the abundance and taxonomic composition of the aquatic predatory insect fauna, with focus on adult diving beetles (Coleoptera: Dytiscidae), in eight temporary flooded wet meadows and two alder swamps in the River Dalälven floodplains, central Sweden from 2002 to 2006. Diving beetles are generalist predators and often abundant in various waters, including temporary wetlands. In the River Dalälven floodplains, recurrent floods induce massive hatching of flood-water mosquitoes (Diptera: Culicidae), which constitute a superabundant patchy and irregular food resource for aquatic predatory insects. Our aims were (1) to characterize the assemblage of adult diving beetles occurring in the wetlands during floods in relation to time and wetland type and (2) to evaluate the effect on the aquatic predator assemblage of strongly reducing the abundance of a potential prey, flood-water mosquito larvae with Bacillus thuringiensis var. israelensis (Bti) during floods. We found diving beetles to be the dominating aquatic predatory insect taxa in all 10 wetlands. There was a difference in Dytiscidae species richness but not in diversity between wet meadows and alder swamps after rarefaction. The cluster analysis based on dytiscid species and abundances showed very high similarities between the wetlands. The variance component analysis was unable to distinguish any factor that could explain more than 7.4% of the variation in the dytiscid species assemblages. The only effect of Bti-treatment against flood-water mosquito larvae, potential food for the predatory dytiscids, was a slight increase in abundance of the medium-sized dytiscid species. Our results are in accordance with previous studies, suggesting that irregular and recurrent flood dynamic structure the dytiscid fauna more than food limitations and environmental factors.     

Oral Ingestion of Transgenic RIDL Ae. aegypti Larvae Has No Negative Effect on Two Predator Toxorhynchites Species

Dengue is the most important mosquito-borne viral disease. No specific treatment or vaccine is currently available; traditional vector control methods can rarely achieve adequate control. Recently, the RIDL (Release of Insect carrying Dominant Lethality) approach has been developed, based on the sterile insect technique, in which genetically engineered ‘sterile’ homozygous RIDL male insects are released to mate wild females; the offspring inherit a copy of the RIDL construct and die. A RIDL strain of the dengue mosquito, Aedes aegypti, OX513A, expresses a fluorescent marker gene for identification (DsRed2) and a protein (tTAV) that causes the offspring to die. We examined whether these proteins could adversely affect predators that may feed on the insect. Aedes aegypti is a peri-domestic mosquito that typically breeds in small, rain-water-filled containers and has no specific predators. Toxorhynchites larvae feed on small aquatic organisms and are easily reared in the laboratory where they can be fed exclusively on mosquito larvae. To evaluate the effect of a predator feeding on a diet of RIDL insects, OX513A Ae. aegypti larvae were fed to two different species of Toxorhynchites (Tx. splendens and Tx. amboinensis) and effects on life table parameters of all life stages were compared to being fed on wild type larvae. No significant negative effect was observed on any life table parameter studied; this outcome and the benign nature of the expressed proteins (tTAV and DsRed2) indicate that Ae. aegypti OX513A RIDL strain is unlikely to have any adverse effects on predators in the environment.