Many phytophagous insects are known to feed on fruits and seeds. On the other hand, vertebrate-dispersed trees often have conspicuously coloured fruits. Frugivorous birds are attracted by fleshy fruits and disperse the seeds but avoid unripe, green fruits.

The focus of many classical and contemporary studies in ecology, however, has been on pairwise interactions between species: plant-insect and plant-bird interactions have been treated separately. Recently, an appreciation has been developed of how multi-species interactions synergistically or antagonistically alter the ecological outcomes of interactions from outcomes predicted by pairwise interactions. Little consideration, however, has been made for the effects of frugivorous insects on plant-bird interactions.

The seed parasitoid wasp Macrodasyceras hirsutum Kamijo (Hymenoptera: Torymidae) attacks seeds of the bird-dispersed tree Ilex integra Thunb. (Aquifoliaceae). In this plant-insect-frugivorous bird triad system, there may be three interactions among them; (1) seed consumption by the wasp, (2) seed dispersal by the birds, and (3) indirect effects of the wasp on the birds via modified berry traits. The aim of this study was to reveal the effects of the wasp on plant-insect-frugivorous bird triad system.

Selective oviposition in fertilised seeds by M. hirsutum

Oviposition of some seed parasitoid wasps induces unfertilised seeds to accumulate storage material in conifers. Therefore, it is speculated that ability of wasps to manipulate the accumulation of storage material varies depending on the temporal relationship between wasp oviposition and tree ovule fertilisation. To test the hypothesis, berries of I. integra were dissected immediately after the end of flight season of the seed parasitoid wasp in the field and the berries bearing unfertilised seeds were also dissected after being exposed to wasp females in the laboratory. Almost all the eggs were found in fertilised seeds in the field. Unfertilised seeds did not show the accumulation of storage material in them after being exposed wasps. Both results indicated that the wasp did not oviposit in unfertilised seeds, supporting the hypothesis and indicating that the substantial proportion of seedless berries did not function as an egg sink.

Egg distribution pattern among seeds and berries

Selection of oviposition sites by phytophagous insects is crucial for the fate of offspring. As M. hirsutum selectively lays the eggs into the fertilised seeds and only one larva develops in a seed, a uniform distribution pattern of wasp eggs may be expected among fertilised seeds and berries. To test the hypothesis, the wasp eggs in seeds and berries were counted for the first generations over five years. Dissection of 531 berries showed that the wasps deposited one to five eggs into a fertilised seed. Iwao's patchiness regression analysis revealed that the eggs showed a uniform distribution pattern among fertilised seeds and a random distribution pattern among berries. Destroying the connection of seeds within berries revealed that female wasps randomly selected berries for oviposition in most trees. Generalised linear mixed models (GLMM) showed that the number of fertilised seeds in a berry could not explain the number of eggs in a seed but could explain the number of eggs in a berry. Therefore, this study suggests that the wasp females did not discriminate between berries with different numbers of fertilised seeds but discriminated the egg loads in a seed.

Life cycle of M. hirsutum with relation to amount of available seeds

Facultative diapause is a strategy that decides whether insects initiate an additional generation or stop the development depending on the environmental conditions. Although food supply is assumed to dominate the most summer diapauses of phytophagous insects, very few studies have reported the influence of food supply on the induction of summer diapause. Dissection of berries at various occasions in the field showed that some individuals of the first generation of M. hirsutum emerged as an adult in early summer and formed the second generation whereas the others entered the diapause and overwintered as a larva. The GLMM showed that the proportion of summer diapause larvae was not affected by the proportions of seeds available to oviposition per berry and branch but by the proportion of available seeds per tree.

Yearly fluctuation in berry productions and seed parasitism by M. hirsutum

Production of fruits and seeds fluctuate from year to year in many tree species. As flower buds of I. integra are formed in the previous year and the berries grow in the current year, the production of fruits and seeds are closely related to environmental conditions such as sunlight, water, and nutrients in the previous and current years. To determine the relationship of the production of I. integra seeds and berries to seed parasitism by M. hirsutum, berry density per one-year-old twig and seed parasitism by M. hirsutum were investigated over five years. Some trees changed the sex. Any female trees showed marked, yearly fluctuation in berry density per twig, which was not in synchronisation among trees in a plantation. There was a difference in the mean number of wasp-parasitised seeds per berry among trees in each spring, but there was no relationship between berry density per twig and percent seed parasitism. The GLMM showed that the percent seed parasitism in autumn was not related significantly to the berry production in the following year. These suggest that yearly fluctuations in the berry production of I. integra trees are not determined by M. hirsutum populations.

Trait-mediated indirect effects by M. hirsutum on frugivorous birds

Frugivorous and seed-feeding insects may alter the traits of fruits, such as shape and size, which may influence fruit attractiveness to frugivorous birds. Consequently, trait-mediated interactions may occur in systems where plants, seed-dispersing frugivorous vertebrates and frugivorous or seed-feeding insects interact. I investigated colour manipulation in I. integra berries caused by the seed parasitoid wasp and how the manipulation relates to fruit attractiveness for frugivorous birds. Observation in winter showed that the colour of I. integra berries varied from green to red, but most berries were greenish, indicating that the berries were immature. Berry dissection indicated that the number of live parasitoid larvae present within each berry was closely related to berry colour-greater the number of live larvae, more intense is the green colour of the berry. However, the wasp larvae did not modify the shape or size of the berries. More than 98% of berries that were protected from the insects by gauze bags ripened and turned red. In this study, berries with unfertilised seeds alone turned red. Field feeding preference tests showed that the frugivorous birds preferred red berries to green berries. I demonstrated that the seed parasitoid wasp manipulates the berry colour, but not its shape or size, in a density-dependent manner. Because green berries suffered less from bird foraging, I believe that this colour manipulation helps the wasps to avoid being killed by the birds. The present study indicates that manipulation by wasps may reduce the level of mutualism between the tree and seed-dispersing birds.

Conclusion

Insect seed parasitoids and predators have received relatively little attention in the context of the organisation and functioning of natural and agricultural ecosystems compared to other functionally important insect groups such as pollinators. Although insect seed predators frequently kill >90% of developing seeds, it has been considered that a high rate of seed parasitism does not necessarily have a substantial effects on the plant populations due to critical action of post-dispersal mortality factors on the recruitments, leading to a underestimate of insect seed predators. In addition, both plant-insect and plant-bird interactions have been studied separately and little attention has been attracted to the effects of frugivorous and seed-feeding insects on plant-bird interactions. The doctoral thesis, however, is the first report to indicate that the seed parasitoid inhibits the seed dispersal through a trait-mediated indirect effect of the seed parasitoid wasp on frugivorous birds in addition to seed predation. It also shows that insect seed predators may cause far heavier losses in plant reproduction than expected by direct seed mortality. Full understanding of the ecology of insect seed predator-plant interactions will be valuable to conservation and management in a range of natural and agricultural systems.

昆虫には樹木の種子や果実を食べ,木の繁殖に悪影響を与えるものがいる。他方,樹木には目立つ色の果実を着けて脊椎動物を誘引し,それらに果実を食べさせることによって種子を分散するものがある。このような植物と昆虫あるいは植物と鳥類の2者系の関係によって起こる生態学的な結果は,3種以上の相互作用が働く場面では,2種間の直接的な効果とともに第3の種を通して生起される間接的な効果によって2種間の相互作用から予測されないことが起こる場合がある。本論文では,樹木と鳥類の相互作用(種子伝播)に及ぼす種子食性昆虫の効果を明らかにするために,間接効果に焦点を当てながら,モチノキタネオナガコバチ―モチノキ―果実食性鳥類の相互作用系を解析したものである。

本論文は9章から構成されている。1章は序論であり,この研究の意義を述べるとともに,モチノキタネオナガコバチがモチノキ果肉内の種子だけに産卵すること,モチノキの果実には4内果皮があり,その中に一つずつ胚珠があること,種子は鳥によって散布されることなどの生態が概説されている。2章では調査地の概要と各章に共通の方法を示している。

モチノキは雄花と雌花を生産し,木は雌株と雄株に分かれることが知られていた。3章では,個体別に花の雌雄を3年間記録し,本種に性転換があることを明らかにした。その場合,性転換は木単位で起こり,枝単位でないことを示した。

4章はモチノキタネオナガコバチ越冬世代の産卵選択を取り扱っている。針葉樹の種子に産卵するタネバチは未受精の種子に産卵することがあり,コバチの幼虫は木を操作して未受精の種子に貯蔵物質を蓄積させることが知られている。これに対して,広葉樹の種子に寄生するモチノキタネオナガコバチは受精した種子にしか産卵しないこと,野外では未受精種子はかなり高い割合であることが示された。これらのことから,未受精種子への産卵がコバチのコストになることが示唆された。このコバチは種子内で1個体しか発育を完了できない。5章では,越冬世代がモチノキの種子内と果実内に産む卵数を調べ,卵は種子間では一様分布を示すが,果実間ではランダム分布を示すことを明らかにし,ハチが種子内の卵数を識別する可能性を示唆した。モチノキタネオナガコバチの生活史は2化であると報告されてきた。しかしながら,6章では第一世代成虫の産卵直後の調査によって,種子内には終齢幼虫と卵が存在することを明らかにし,一部の幼虫が発育停止をして越冬することを示した。つまり部分2化であることを示すとともに,発育停止した幼虫の割合が木内の産卵可能な種子の割合と負の相関があることを示した。

7章はモチノキの果実と種子の生産とモチノキタネオナガコバチの寄生率の関係を取り扱っている。1植林地における4年間の調査の結果,全てのモチノキが毎年開花する訳ではないこと,木の果実生産の年次パターンによって木は3グループ―ほぼ毎年着果する木,調査期間の後半に着果した木,4年間ほとんど着果しなかった木―に分割できることを示した。このようなグループは林内で集中分布を示さず,樹木個体間の果実の豊凶(masting)に似た現象は認められなかった。木の着果パターンに対応してコバチの種子寄生率の年次変動も3グループに分けることができた。前年のコバチの種子寄生率はモチノキの当年着果量に影響を及ぼすことはなく,前年の着果量が当年の種子寄生率に影響を及ぼさないことが示された。

8章はハチの間接効果を取り扱っている。モチノキの果実は秋から冬に緑から赤に変色し,果実食性の鳥類は赤い果実を食べて種子散布することが知られていた。ところが,野外調査から冬は赤い果実だけでなく緑色の果実があること,緑色が強い果実ほど果実内のハチ幼虫数が多いこと,コバチの寄生は果実の大きさに影響しないこと,袋掛けによって赤い果実は失われないこと,未受精の種子だけの果実が赤くなることを示した。さらに,餌台に赤い果実と緑の果実を置いた時,鳥(ヒヨドリ)は赤い果実を選択的に食べることを示した。これらのことから,タネバチが果実の変色を妨げて鳥の捕食を免れ,その結果,モチノキと鳥の共生関係が阻害されることを論議している。

9章は総合考察であり,これまでの結果をまとめるとともに,種子食性昆虫の間接効果を考慮しながら,それらが森林に及ぼす影響を論議している。

このように,本論文は,モチノキの性転換,モチノキタネオナガコバチによる宿主形質の操作,利用資源量に対するコバチの生活史反応,コバチの種子寄生率とモチノキ果実の生産量の年次変動の関係,およびモチノキと鳥類の共生系に及ぼすコバチの間接効果を調べた労作であり,多くの新知見とともに森林生態系における種子食性昆虫の影響が論じられている。よって審査委員一同は,本論文が学術的にも応用的にも価値が高く,博士(農学)の学位論文として価値あるものと認めた。