English Summary

INTRODUCTION

Welcome. Here, I (Shigeki Kishi) summarize my researches, which can be majorly separated into three parts.

In chronological order, the first one is associated with "parental care in Onthophagus dung beetles", the second associated with "reproductive interference", and the last with "pollination network". Each of them is summarized below.

If you have any questions or notices, please tell me via e-mail

(Address: kishisgk [at] gmail.com, please substitute "at sign (@)" for [at]).

Parental Care

Onthophagus (Scarabaeidae, Scarabaeinae) dung beetles have unique reproductive behaviors. A pair of onthophagini beetles dig a main-burrow beneath the mammal's dung pat and branch a sub-burrow. Then they cooperatively produces a dung brood ball by repeatedly packing a piece of dung into the sub-burrow. A female of the pair lay a single egg on the head of a brood ball, and seal the small egg chamber. After that, parents start to produce another brood ball in another sub-burrow. A hatched larva feed on the brood ball which is a whole food for a larva to grow up to adult. Therefore, the brood ball size crucially affects larval fitness, and then fitness return to parents.

1 Kishi, S. & Nishida, T. (2006) Adjustment of parental investment in the dung beetle Onthophagus atripennis (Col., Scarabaeidae).

Ethology 112:1239‒1245. DOI: 10.1111/j.1439-0310.2006.01284.x

Onthophagus atripennis is one of the most common dung beetles in Japan. This species uses various mammal's dung, which differs in ingredient between mammal species. In this study, I examined if beetle parents adjust brood ball size in response to dung quality. If a dung has rich nutrients, a smaller brood ball is enough for a larva to grow up to adult. On the other hand, if a dung has poor nutrients, a larger brood ball is necessary for a larva. I provided each of three dung types for each pair of beetles; monkey dung with rich nutrients, cow dung with poor nutrients, and the mixed dung with the intermediate. After 1 week, I measured the brood ball size that parents produced.

As a result, parents produced smaller brood balls when provided with monkey dung, and produced larger brood balls when provided with cow dung, and produced the middle size when provided with the mixed dung. Thus, we showed that the beetle parents can assess dung quality and adjust the brood ball size.

2 Kishi, S. & Nishida, T. (2008) Optimal investment in sons and daughters when parents do not know the sex of their offspring. Behavioral Ecology and Sociobiology 62:607‒615. DOI: 10.1007/s00265-007-0485-0

In sexual animal species, optimal parental investment per offspring often differs between sons and daughters. Theories of parental investment predict that parents should adjust quality and quantity of their investment in response to offspring sex, to maximize their fitness return. In fact, many studies have reported the differential parental investment between sons and daughters. However, many species seems not differentiate their investment between offspring sexes. In Onthophagus beetles, because the sex is determined by XY genetic sex determination system, as like human, females would not know the offspring sex during brood ball construction. However, the optimal brood ball size is larger in a son than in a daughter due to male-male competition. I researched how large brood ball is evolutionarily stable in a dung beetle, O. atripennis.

A series of experiments showed that parents of this species provide optimal brood ball size for a son to both of sons and daughters. Thus beetle parents invest optimally for sons, but excessively for daughters. If the brood ball size is optimal for daughters and smaller for sons, fitness return from sons results in nearly zero because smaller adult sons from smaller brood balls lose male-male combats.

Furthermore, the observed brood ball size was exactly consistent with the expected brood ball size, which is the optimal for a son. Thus, this study can be a demonstration of the optimal parental investment (Smith and Fretwell 1974). This study also indicates that critical parental investment of this species constraints sexual size dimorphism, but does not constrain the evolution of sexual dimorphism.

3 Kishi, S. & Nishida, T. (2009) Adjustment of parental investment in sympatric Onthophagus beetles (Coleoptera: Scarabaeidae). Journal of Ethology 27: 59‒65. DOI: 10.1007/s10164-008-0084-1

In this study, I researched interspecific difference of the parental capability between two sympatric and sibling Onthophagus beetles, O. ater and O. fodiens. Results, though complicated, showed that O. ater adjusted brood ball size in response to four dung types (dog, monkey, deer and cow), but O. fodiens did not. Dung quality descends with time after the excretion. Then, the available period of dung is longer for O. ater than O. fodiens. We suggest that O. fodiens uses more nutritious but rarer monkey dung, while O. ater uses lesser nutritious but abundant dung, such as cow dung and deer dung. This different resource use pattern may allow the two species to keep coexistence at the central Japan.

10 Kishi, S. (2014) Brood ball size but not egg size correlates with maternal size in a dung beetle, Onthophagus atripennis. Ecological Entomology 39:355‒360. DOI: 10.1111/een.12102

Theory of optimal parental investment (or, marginal value theorem) predicts that the optimal amount of parental investment per offspring depends on fitness curve of an offspring, but not depends on the total amount of parental resource. However, conflicting results have been reported. In some cases the constant size of progeny did not correlate with parental body size (an index of parental resource), while in other cases the progeny size correlated with parental body size. This conflicting results may be explained by different investment components, because parental body size should give different effect on those components. Using an dung beetle, O. atripennis, I examined two relationship: between parental body size and egg size, and between parental body size and brood ball size. A brood ball, made by beetle parents, is the total amount of food resource for a larva to grow up to adult. As a result, egg size did not correlated with maternal body size, but brood ball size significantly correlated with maternal body size. No significant effect of paternal body size was detected. Then, this study demonstrated that effect of parental body size differs between the components of parental investment. Accounting that beetle mothers adjust brood ball size in response to dung quality, the adjusting process may inevitably involve the correlation between maternal size and brood ball size.

Reproductive Interference

Reproductive interference is interspecific sexual interaction that gives negative effect on female reproductive success. Reproductive interference does not only include interspecific mating and hybridization, but also includes many more events of lighter interspecific sexual interactions. For example, when many heterospecific frogs sing loudly, female frogs spend longer time to locate conspecific males (Amézquita et al. 2006. Evolution 60:1874–1887). Negative effect of reproductive interference on female reproductive success depends on the relative frequency of heterospecific males to conspecific females, though further study needs to examine the frequency dependence. Then this positive frequency dependent effect of reproductive interference enhances the population growth rate of major species, but diminishes population growth rate of minor species , and then is likely to cause species extinction (Kuno 1992. Popul Ecol 34:275–284).

4 Kishi, S., Nishida, T. and Tsubaki, Y. (2009) Reproductive interference determines persistence and exclusion in species interactions. Journal of Animal Ecology 78:1043‒1049. DOI: 10.1111/j.1365-2656.2009.01560.x

We researched reproductive interference of Callosobruchus bean beetles, which have been typical model insects for interspecific competition experiments. Females of both C. chinensis and C. maculatus lay eggs on the surface of (post-harvest) adzuki beans. Hatched larvae dig into a bean and feed on it. It takes about 3 weeks until larvae grow up to adult under the air temperature 30 degree centigrade. To examine reproductive interference, I set three treatments for each species female, which stayed with no male, stayed with a conspecific male, or stayed with a heterospecific male.

We found that reproductive interference between two beetle species is asymmetric.When stayed with C. maculatus males, C. chinensis females laid equal eggs to eggs laid in other treatments. However, when stayed with C. chinensis male, C. maculatus females laid far fewer eggs than eggs laid in other treatments. Thus, C. maculatus is far more vulnerable to reproductive interference than C. chinensis.

As a result of the multiple-generation competition experiments, C. chinensis strongly excluded C. maculatus, but when C. maculatus was many more than C. chinensis in the initial ratio, C. maculatus excluded C. chinensis. These competition results are consistent with the asymmetric reproductive interference, but inconsistent with interspecific resource competition in which a C. maculatus larva is superior. Thus, reproductive interference is a more dominant driver to determine the competition outcome, compared to resource competition.

8 Kishi, S. & Nakazawa, T. (2013) Model analysis for interspecific interaction co-mediated by resource competition and reproductive interference. Population Ecology 55:305‒313. DOI: 10.1007/s10144-013-0369-2

We built a mathematical model in which both reproductive interference and interspecific resource competition occur between two closely related species. Analyzing the model, we studied the population dynamics of two species. We found that reproductive interference and interspecific resource competition synergetically enhance species extinction. Further, we analyzed situations that the two factors were asymmetric. As a result, one species that is superior in reproductive interference but inferior in interspecific resource competition keep coexistence, and even exclude the other.

Increasing biological invasions have been reported in the world. In some of them, invasive species is displacing native closely related species. We suggest that in those cases invasive species is superior in reproductive interference, probably inferior in interspecific resource competition, in which native species should be more adaptive than invasive species.

9 Kishi, S. & Tsubaki, Y. (2013) Avoidance of reproductive interference causes resource partitioning in bean beetle females. Population Ecology 56:73‒80. DOI: 10.1007/s10144-013-0390-5

Reproductive interference is expected to cause species exclusion, rather than coexistence, when two closely related species competes for a single resource. Then, when they competes for multiple resources, reproductive interference is expected to cause resource partitioning between them, or species exclusion. Using bean beetles, Callosobruchus chinensis and C. maculatus and two oviposition resources (i.e., normal and split adzuki beans), we examined if reproductive interference causes resource partitioning between these species. In a two-compartmented dish, 10 grains of normal beans are placed on one side, while 20 hemispherical splits made of 10 beans are placed upward on the other side.

As a result, we observed resource partitioning between these two species even in a dish! In a treatment that males and females of two species were introduced into the dish, more C. chinensis adults emerged from split beans and more C. maculatus adults emerged from normal beans in next generation. We analyzed the number of eggs on two bean types and the number of emerged adults from these beans in several treatments in which different combinations of two species males and females are introduced. Results showed 1) reproductive interference changes egg-laying behavior of two species females, particularly of C. maculatus females, which laid more eggs on normal beans when stayed with heterospecific males, 2) this avoiding behavior from reproductive interference and asymmetric resource competition are critical determinants of the observed resource partitioning.

We demonstrated that reproductive interference caused resource partitioning in combination with resource competition. The fact that resource partitioning occurred only through female behavioral change against reproductive interference, but not through any evolutionary change, indicates that resource partitioning can be established by behavioral change. Therefore, evolutionary change can occur after the initiation of resource partitioning.

12 Kishi, S. Reproductive interference in laboratory experiments of interspecific competition. Population Ecology, published online DOI: 10.1007/s10144-014-0455-0

This paper is a review of interspecific competition especially studied in laboratory in view of reproductive interference. Using Callosobruchus bean beetles, Drosophila fruit flies, and Tribolium flour beetles, many competition experiments have been carried out. Results of them have been considered as the important basis of interspecific competition (e.g., Tribolium by T. Park and his fellows). However, in the competition dynamics of those results, some studies have noticed the frequency dependence, which could not be caused by resource competition and cannibalism. This study focused on reproductive interference, which causes the frequency dependence, and reviewed those competition studies. I found that reproductive interference occurred in every competition between Callosobruchus species, between Drosophila species and between Tribolium species, and furthermore, reproductive interference was a dominant determinant of the competition outcome in conjunction with resource competition in Callosobruchus and Drosophila, though an assistant determinant in Tribolium. Nevertheless, the initial-frequency dependence of the competition outcome can be explained by reproductive interference in Tribolium. At the end, I remarked the further possibility of reproductive interference to contribute our understanding of interspecific competition.