The quantity and quality of prey animals strongly affect a predator’s life history and abundance. Among predacious insects, predatory species that depend upon a particular prey animal, which are known as specialists, breed when their prey animal is abundant [33-36]. Specialist development coincides with the appearance of specific prey animals, especially during the nymphal period [37]. In rice fields, K. deyrolli nymphs prey upon tadpoles more than on other kinds of prey (Figure 2). The subfamily Lethocerinae, which has the largest body size among Belostomatidae, is known to be a vertebrate specialist [38-40]. Why K. deyrolli nymphs mostly feed on tadpoles is not well understood from the viewpoint of nymphal growth and seasonal occurrence.

In general, the appearance of younger nymphs of predacious insects when prey animals are abundant is expected to moderate cannibalism due to food shortages [41-44]. Accordingly, Ohba et al. [45] studied the ontogenetic diet shift of K. deyrolli by quantifying instar abundance and analyzing captured prey and prey relative abundance in rice fields in three localities. The first to third-instar K. deyrolli nymphs mainly fed on tadpoles, regardless of differences in prey availability among the three localities (Figure 3). A rearing experiment demonstrated that K. deyrolli nymphs provided with tadpoles displayed greater growth rates at all nymphal stages, except for the final stage, than nymphs fed on dragonflynymphs. The emergence of young K. deyrolli nymphs seemed to coincide with the period when tadpoles became abundant in the rice fields (Figure 4). In addition, the appearance of younger K. deyrolli nymphs when tadpoles are abundant is expected to moderate cannibalism due to food shortages, as has been demonstrated for other predatory insects such as ladybirds [41-44]. Actually, the frequency of cannibalism in K. deyrolli nymphs is lower than that seen in A. japonicus nymphs in the field (Figure 2) [7].

Many specialists breed when certain prey are abundant in order to increase the chance of there being a sufficient amount of food to increase the growth and survival of their young, showing that a high prey density directly supports the predator population, e.g., a bottom-up effect. However, there is little information on the indirect role of higher prey density on the mediation of predation pressure on the predator from other predators within the same guild; i.e., density-mediated indirect effects, in aquatic environments including insect predator–anuran larva prey relationships. As mentioned above, K. deyrolli nymphs are considered to feed on tadpoles [45]. In addition, L. japonensis prey upon K. deyrolli nymphs [32,46] and tadpoles in rice fields [7]. Therefore, L. japonensis adults are intraguild predators of K. deyrolli nymphs. Consequently, it is predicted that the survivorship of K. deyrolli nymphs is affected by their common prey, tadpoles, via a bottom-up effect on survivorship as well as by their predator, L. japonensis adults, via a top-down effect. Thus, it is considered that density-mediated indirect relationships exist among the three animal species.

Ohba and Nakasuji [47] demonstrated that the survival of K. deyrolli nymphs, which are tadpole specialists, is affected by tadpoles (a direct bottom-up effect). We investigated the survival rates of the first instar nymphs of K. deyrolli in June (high tadpole density period) and July (low tadpole density period) using the Kiritani-Nakasuji-Manly method [48,49]. As circumstantial evidence, the survival rate of the first instar nymphs of K. deyrolli in a rice paddy field was higher in June (75.1%) than in July (54.2%) [47]. The differences in prey density between June and July probably affected the survival rates of the K. deyrolli nymphs, suggesting that bottom-up effects display seasonal variation.

To examine whether a higher tadpole density moderates the predation pressure from L. japonensis adults on K. deyrolli nymphs, a field experiment was conducted in a rice field. As a result, it was found that a higher tadpole density moderated the predation pressure from L. japonensis adults on K. deyrolli nymphs (a density-mediated indirect effect; Figures 5 and 6) [50,51]. Prey abundance is an important factor for determining the frequency of intraguild predation [52-54], especially in terrestrial aphidophagous predator–aphid prey relationships. Thus, in rice fields the incidence of intraguild predation by L. japonensis adults might increase when the tadpole density decreases.

The Japanese populations of K. deyrolli have decreased sharply during the last four decades, and this species is now included in the Red Data List of species in 45 of 47 Japanese prefectures [55,56]. Contributing factors such as decreases in suitable aquatic habitats, water pollution, and urbanization have been investigated and verified in previous studies [57-59]. In addition to these factors, it is important for the conservation of K. deyrolli to reveal the best food for them to eat. Regarding bottom-up effects, Hirai and Hidaka [60] and Hirai [61] emphasized that the frog population is very important for the conservation of the K. deyrolli population because frogs are major constituents of the diet of K. deyrolli adults.

Previous studies have only focused on direct bottom-up effects of amphibian prey. However, the present study demonstrated an indirect bottom-up effect of amphibian prey. The emergence of young K. deyrolli nymphs appeared to coincide with the period when tadpoles became abundant in the rice fields, which allowed the young K. deyrolli nymphs to achieve greater growth (Figure 4 [45]). This indicates that a high prey density directly supports K. deyrolli nymphs. In addition to such direct effects, a high tadpole density was also demonstrated to have a beneficial indirect effect on the survival of K. deyrolli nymphs (Figure 6 [47]). Therefore, an abundance of amphibian prey is indispensable for the conservation of this endangered giant water bug species.

This paper introduced that young K. deyrolli nymphs mainly feed on tadpoles in rice fields and that nymphs provided with tadpoles grow faster than nymphs provided with invertebrate prey. A higher tadpole density moderates the predation pressure from the water scorpion L. japonensis on K. deyrolli nymphs; i.e., it has a density-mediated indirect effect. These results suggest that an abundance of tadpoles provides sufficient food for K. deyrolli nymph growth (a direct bottom-up effect) and moderates the predation pressure exerted on them by L. japonensis (an indirect bottom-up effect). An abundance of amphibian prey is indispensable for the conservation of this endangered giant water bug species.