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Invasion Pathway and Potential Risks of a Bamboo-Nesting Carpenter Bee

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Invasion Pathway and Potential Risks of a Bamboo-Nesting Carpenter Bee Appl. Entomol. Zool. 45 (2): 329–337 (2010) http://odokon.org/ Invasion pathway and potential risks of a bamboo-nesting carpenter bee, Xylocopa tranquebarorum (Hymenoptera: Apidae), and its micro-associated mite introduced into Japan Kimiko OKABE,1,* Hayato MASUYA,1 Kazuhide KAWAZOE2 and Shun’ichi MAKINO1 1 Forestry and Forest Products Research Institute; Tsukuba, Ibaraki 305–8687, Japan 2 JR Tokai Takashimaya Co., Ltd.; Nagoya, Aichi 450–6001, Japan (Received 7 January 2010; Accepted 1 March 2010) Abstract Despite plant quarantine systems, many organisms have been unintentionally introduced by the rapid expansion of in- ternational trade. Xylocopa tranquebarorum, a large species of carpenter bee that nests in bamboo shoots, was intro- duced into Japan approximately 5 years ago and, along with its specifically associated mite, has established popula- tions in Toyota and Nagoya in Aichi Prefecture and Anpachi in Gifu Prefecture. Because X. tranquebarorum only nests in dead bamboo shoots and because its associated mite differs from the mite species associated with X. tranque- barorum in Taiwan but is morphologically similar to the species described in India, Indonesia, and China, we suspect that X. tranquebarorum and its mite were introduced via processed bamboo shoots from continental Asia. Because the most probable pathway of associated microorganisms is host introduction, biological and ecological information, such as an inventory of symbionts, is crucial to avoid the risk of invasive symbiotic microorganisms. Although X. tranque- barorum may become a pest in the bamboo industry if its distribution is expanded by human transport, its associated mite is suspected to be of low risk as house dust but to have a high contamination risk for the Japanese endemic mite, Sennertia alfkeni, associated with native Japanese carpenter bees. Key words: Cleptoparasite; fungivore; house dust; phoresy; symbiont tine offices in Japan based on their pest status, INTRODUCTION small organisms have been unintentionally intro- International trade has rapidly expanded world- duced because searches of associated organisms wide, resulting in the concomitant transport of (usually called hosts) and assessments of their po- alien species (Meyerson and Mooney, 2007; tential pest risk have never been conducted as quar- Hulme, 2009). Although quarantine systems cover antine targets (Goka et al., 2001; Okabe and Goka, many traded goods, microorganisms are often un- 2008). Due to the extreme difficulty of controlling intentionally introduced, frequently causing devas- and eradicating such organisms, important preven- tating consequences within the novel environment. tative measures should include both potential risk Whereas plants and vertebrates tend to be inten- assessments in terms of crops, hygiene, and eco- tionally introduced across borders as crops and/or logical impacts and pathway analysis to develop ef- pets, invertebrates and microorganisms are typi- fective control measures, reexamine the current cally introduced because the quarantine system quarantine system, and determine effective eradica- failures or because of a lack of knowledge (e.g., tion measures (Pimentel, 2002; Perrings et al., horticultural plants: Reichard and White, 2001; mi- 2005). croorganisms and others in China: Xu et al., 2006; Large carpenter bees belonging to the genus Xy- forest herbivorous insects: Gandhi and Herms, locopa have diversified within tropical and sub- 2009). Although microorganisms such as fungi, ne- tropical regions and expanded their distributions to matodes, and mites are monitored by plant quaran- temperate regions (Hurd and Moure, 1963). Sev- * To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2010.329 329 AEZ45-2_329-337.pdf 1 10.5.26 1:52:45 PM 330 K. OKABE et al. eral species are suspected to have invaded oceanic exact distributions of carpenter bees of Xylocopa islands, as only a few species exist within island subgenus Biluna and their associated mites are un- groups and the distances between the original and known. An additional bamboo-nesting carpenter close relative’s habitats are relatively short. For ex- bee, X. tranquebarorum, was recently introduced ample, Xylocopa sonorina Smith was allegedly into Japan; in 2006, this species was collected in transferred by humans from North America to Aichi and Gifu prefectures, where the native large tropical Pacific islands, including Hawaii (Hurd, carpenter bee, Xylocopa appendiculata circum- 1958). Mites are associated with most species of volans, is distributed (Kamio, 2007; Yata, 2007). carpenter bees, often exhibiting host specificity or The exotic bee has established populations in To- at least narrow host ranges; these mite species be- yota, Aichi Prefecture (Okada and Takeda, 2009; long to the Mesostigmata (Dinogamasus and Hy- this study) and has likely expanded its distribution poaspis of Laelapidae), Prostigmata (Cheletophyes to Nagoya (Ohkusa, personal communication) (Fig. of Cheyletidae and Tarsonemus of Tarsonemidae), 1). Xylocopa tranquebarorum is associated with a and Astigmata (Sennertia of Caetodactylidae and mite belonging to Sennertia, the deutonymph of Horstia of Acaridae) (OConnor, 1993; Eickwort, which is morphologically similar to but genetically 1994; Klimov and OConnor, 2008). Mutualisms different from the Japanese large carpenter bee may exist between carpenter bees with acarinaria mite, S. alfkeni (Kawazoe et al., 2010). Hereafter, (external pouch-like structures that facilitate phoretic mite transfer with the bees) and their asso- ciated mites, but most interactions are considered cleptoparasitism, with mites feeding on the host pollen loaf and feces (Abrahamovich and de Alzuet, 1990; Eickwort, 1994; Okabe et al., 2008). The mite life cycle is well synchronized with that of its host: mites leave a host to migrate into a nest during the initial stage to anytime afterward, molt to a feeding stage to consume provisioned pollen and host feces after the host larva has consumed the pollen loaf, molt to deutonymphs during host pupation, and attach to the host for dispersal (Abrahamovich and de Alzuet, 1990; Okabe et al., 2008). In Japan, five species large carpenter bees are associated with one mite species, Sennertia alfkeni (Oudemans) (Okabe and Makino, 2005; Okabe et al., 2008); however, molecular analyses have revealed five host-specific genetic lineages of the mite, suggesting long evolutionary associations between each pair (Kawazoe et al., 2008a, b). Sennertia dissimilis Zakhvatkin, associated with Xylocopa nasalis Westwood (from Japan and prob- ably originating from a Southeast or East Asian country occupied by Japan at the collection time), Sennertia horrida (Vitzthum) with X. nasalis (from India, Indonesia, and Japan at the time of collec- tion), and Sennertia potanini Zakhvatkin with Xy- Fig. 1. Collection sites of introduced Xylocopa tranque- locopa tranquebarorum (Swederus) (from western barorum in Japan. Top diagram shows the regions of sites in China) are all described as species of bamboo-nest- Japan, and the bottom diagram indicates each site with a cir- cle. Bee and mite samples were collected in Toyota (white cir- ing large carpenter bees of the subgenus Biluna cle), and bees were also reported in Nagoya and Anpachi (Zakhvatkin, 1941; Klimov and OConnor, 2008). (eastern and western black circles, respectively). Gray lines in Currently, the biology and ecology, including the the bottom diagram indicate large rivers. AEZ45-2_329-337.pdf 2 10.5.26 1:52:45 PM Invasion of Xylocopa tranquebarorum with Mite 331 the introduced species is referred to as Sennertia nr Cut shoots with or without mites were stored sepa- alfkeni. Although the original habitat(s) is un- rately in a closed container and maintained out- known, this bee is unlikely to have originated from doors under a roof at ambient temperature until Taiwan (although the Japanese name of X. tranque- adult bee emergence. To use living mites in experi- barorum is directly translated to “Taiwanese bam- ments, adult carpenter bees were maintained with boo-nesting large carpenter bee”), where X. tran- phoretic mites in a cage (45 cm per side, con- quebarorum is associated with S. horrida; instead, structed of a wooden frame and synthetic fiber based on its associated mite species, it probably ar- mesh) and were provided diluted honey and sugar rived from Southeast and/or East Asia (Kawazoe et water soaked in cotton. al., 2010). We conducted three laboratory experiments to Although the introduced X. tranquebarorum at- examine the potential risks of the mite: compar- tacks commercial bamboo products for nesting isons of the developmental period of S. nr alfkeni purposes, the risks posed by the associated mite are to that of S. alfkeni, which was originally associ- not as direct because thus far no Sennertia mites ated with the Japanese carpenter bee X. a. circum- have been considered pests. However, potential volans to investigate the possibility of a host switch mite problems include the following: introduced by the invasive mite; fungal sampling in nests to mites may lead to the collapse of the interaction evaluate the potential house dust risk via a mite between endemic X. a. circumvolans (Smith) and vector; and assessments of the necessary condi- S. alfkeni, perhaps via a mite host switch, and S. nr tions for the deutonymphal molt to determine the alfkeni may become house dust by surviving with- risk of both a host switch and to contributing to out the host and vectoring fungi. Therefore, as a house dust. risk assessment of S. nr alfkeni, we investigated the To assess the mite developmental periods, pairs life cycle of the introduced mite to examine the of S. nr alfkeni were isolated from bee nests and possibility of an association between X. a. circum- placed in transparent plastic vials (1.6 cc, 35 mm in volans and S. nr alfkeni, and to determine if the length) with a small piece of wet filter paper and mite could survive without the host, with particular about 1 g fresh pollen loaf from a X. tranquebaro- focus on deutonymphal molt to tritonymphs in the rum cell. Ten vials were prepared and maintained absence of the host. We also investigated the poten- at 25°C.
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