ARTHROPOD BIOLOGY

Pollinator and Stem- and Corm-Boring Insects Associated withMycoheterotrophic Orchid Gastrodia elata
MAKOTO KATO,1, 2 KAORU TSUJI,3 AND ATSUSHI KAWAKITA1Ann. Entomol. Soc. Am. 99(5): 851Ð858 (2006)

ABSTRACT The nonphotosynthetic orchid Gastrodia elata Blume (Orchidaceae) is a mycoheterotroph associated with the wood-decomposing fungus Armillaria mellea. Here, we report thesymbiotic and parasitic associations of some insects with this orchid. The ßowers are nectarless andwere visited by females of a halictid bee, Lasioglossum sp. The bees entered the tubular ßower andcollected the tissue from the orchidÕs labellum. Pollinia were attached to the hind thorax of the bee
and transported to the stigma of receptive ßowers. The stems and corms of the orchid were infested
by two rare dipterans, Azpeytia shirakii Hurkmans (Syrphidae) and a new genus and species ofscatophagid, Orchidophaga gastrodiacola n. sp. M. Kato. Adult ßies of the latter species laid eggs in theßower. The hatched larvae infested the immature ovary, bored downward into the ßowering stem, andoccasionally entered the underground corms. The high rate of infestation by these dipterans suggeststhat the robust ßower stem of the orchid has evolved as counteradaptation against these particular
stem-boring dipterans. A molecular phylogenetic analysis suggests that O. gastrodiacola belongs toDelininae, which is one of the basal groups of Scatophagidae.
KEY WORDS Scatophagidae, Gastrodia, orchid, pollination, mycoheterotrophy

The orchid Gastrodia elata Blume (Orchidaceae),
lacking green leaves and chlorophyll, is a characteristic member of understory plants in Asian temperate
deciduous forests. It depends on the fungus Armillaria
mellea (Vahl.:Fr.) Kummer, a key wood decomposerin these forests, for nutrients (Kusano 1911). The
fungus invades the nutritive or primary corm of theorchid, arresting and digesting the fungal hyphae inthe cortical layer of the corm (Zhou et al. 1987). The
primary corm produces a secondary terminal cormthat is resistant to the fungal infection and will produce a ßowering stem (Jintang and Shunxiang 2000).
Small embryos of the orchid are also symbiotic withlitter-decomposing fungi such as Mycena osmundicola
Lange, because the fungal hyphae invade the embryonic cells and provide the nutrients necessary forsprouting (Xu et al. 1989). The symbiotic relationshipof the orchid with these fungi may have led to theevolution of antifungal proteins, which are importantin medicine and agriculture (Zhou et al. 1987, Hu andHuan 1994, Wang et al. 2001).
Compared with fungal relationships, mutualisticand parasitic relationships of G. elata with insects havebeen little studied. Our preliminary survey of thebiology of the orchid showed that the stems and corms
were often infested by taxonomically unknown
1 Graduate School of Human and Environmental Studies, Kyoto
University, Yoshida-Nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501,Japan.
2 E-mail: kato@zoo.zool.kyoto-u.ac.jp.
3 Department of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo-ku, Kyoto 606-8502, Japan.

dipteran larvae. We reared larvae collected from thestems and corms and identiÞed them as rare, undescribed syrphid and scatophagid dipterans. Five genera of Syrphidae are phytophagous, namely, Taxomerus, Cheilosia, Portevinia, Eumerus, and Merodon(Ferrar 1987). However, the syrphid species collectedfrom Gastrodia corms did not belong to of any of thesegenera. Scatophagidae includes a variety of phytophagous genera, e.g., Gymnomera, Hydromyza, Norellisoma, Cordilura, Nanna, Norellia, Hexamitochera,
Neochirosia, Delina, and Parallelomma, the last sevenof which are associated with monocots (Ferrar 1987),
and the last two with orchids (Meijere 1940, de Jong
2000). The scatophagid ßy collected from Gastrodia
stems and corms did not belong to any of these genera.
In general, orchids have evolved characteristic pollination systems associated with speciÞc insects. According to one brief report, the pollinator of G. elata
in China is a “reed bee” (species name not given; Zhouet al. 1987). The frequent infestation of fruiting stems
by the dipterans described above suggests that adultfemales of the phytophagous dipterans may pollinate
the ßowers to improve Þtness of their progeny as in Þg
wasps (Wiebes 1979), yucca moths (Riley 1892), andGlochidion-associated gracillariid moths (Kato et al.
2003). To identify the pollinator of this orchid, weobserved the insects that visited its ßowers in a naturalforest in Japan.
We found that the orchid is pollinated by small
halictid bees. We also found that two insect species
infest the stems and corms of the orchids, and we
describe one of these as a new species and genus of0013-8746/06/0851Ð0858$04.00/0 䉷 2006 Entomological Society of America