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Inventory of the Heteroptera (Insecta: Hemiptera) in Komaba Campus of the University of Tokyo, a highly urbanized area in Japan

Abstract Background The Heteroptera, or true bugs, forms one of the major insect groups with respect to the very diverse habitat preferences, including both aquatic and terrestrial species, as well as a variety of feeding types. The first comprehensive inventory of the Heteroptera at Komaba Campus of the University of Tokyo, or an urban green space in the center of the Tokyo Metropolis, Japan, was conducted. New information A total of 115 species in 29 families of the suborder Heteroptera were identified. The area had a high species richness compared with other urbanized and suburbanized localities in Tokyo. The campus is found to show a substantial difference in heteropteran species compositions, despite being close to the other localities surrounded by highly urbanized zones in central Tokyo.


Introduction
Although central part of the Tokyo Metropolis is a highly urbanized area, it contains several large green spaces for landscaping, such as the Imperial Palace and Meiji Jingu (Shinto Shrine), where well-preserved and managed vegetation is present (Tomokuni et al. 2000, Ishikawa andHayashi 2013). For some of these spaces, intensive inventories on various animal groups have been conducted over the last two decades; these efforts evidently suggest substantially high species diversity even in the highly urbanized zones.
The hemipteran suborder Heteroptera (true bugs) is one of the major insect groups with respect to the habitat preferences, including aquatic, semi-aquatic, and terrestrial species with a variety of feeding types represented by varying degrees of herbivory, predation (including sucking vertebrate blood), mycophagy, and polyphagy (Schuh and Slater 1995). Due to the high habitat diversity and the relatively high environment specificity, heteropterans can be a useful bio-indicator of various environmental parameters, such as habitat structure and vegetation coverage.
The approximately 1,300 known heteropteran species of Japan are estimated to represent more than 80% of the possible total number of species Miyamoto 2005, Ishikawa et al. 2012). Of these, 348 species have been recorded in the administrative districts of Tokyo from coastal plains to mountainous regions (excluding islands belonging to the metropolis), and approximately 30% of the 348 species have been found in central Tokyo . In faunal investigations of green spaces, 133 species have been detected at the Imperial Palace (Tomokuni et al. 2000, Tomokuni 2006) and 83 at the Meiji Jingu (Ishikawa and Hayashi 2013); these results evidently suggest that the fauna has been maintained by the diverse and well-preserved vegetation even in the highly urbanized zones. However, little is known about the fauna of relatively small green spaces, such as university campuses, parks and/or gardens.
Komaba Campus of the University of Tokyo provides the comparatively small green spaces surrounded by a highly urbanized zones in central Tokyo. Within the campus, appropriately maintained forests, shrubs and grasslands fill spaces among a number of buildings and athletic fields. Recently, two remarkable true bug species were found from broadleaf angiosperms in this campus; one was reported as a new species (Yasunaga et al. 2013) and the other as a true bug that was rediscovered after being undetected for 59 years . Both belong to the plant bug family Miridae of the Heteroptera. These findings clearly demonstrate that further inventory surveys in such green spaces remaining in central Tokyo as Komaba Campus (apparently much smaller than the Imperial Palace or Meiji Jingu), are required. However, any comprehensive evaluation on the campus fauna or the local biodiversity of the Heteroptera is yet to be carried out.
The present paper documents the first comprehensive inventory for the heteropteran fauna in the Komaba Campus, which represents a model case of extensive research on the fauna of small green spaces in central Tokyo. We also discuss the characteristics of the heteropteran fauna on the campus in comparison with those exhibited in other urbanized or suburbanized localities in Tokyo.

Study site
This research was carried out at Komaba Campus (35.66006N 139.68521E; at an altitude of approximately 35 m above sea level) of the University of Tokyo, Meguro City, Tokyo, Japan, which is situated within the center of Tokyo and surrounded by highly urbanized environments including residential quarters and business complexes (Figs 1, 2). The total site area of the campus is 25.4 ha, within which approximately 50 buildings, four athletic fields, and a few artificial pools are present. The study site was located in a warmtemperate climate zone and had an annual mean temperature of 15.4°C and annual mean precipitation of 1,528.8 mm (Japan Meteorological Agency 2014). The vegetation is generally mosaic and characterized by various species of herbs as well as deciduous/ evergreen and broadleaf/coniferous trees (Figs 2,3,4,5,6).     Inventory of the Heteroptera (Insecta: Hemiptera) in Komaba Campus of the ...

Sampling methods
All specimens were collected by our research group (TI, MUS, KKY, and TK) using the following methods: net sweeping (including visual searches), UV light trap (using a highintensity discharge lamp), and Tullgren funnels. The net sweeping method was used 41 times from April 2013 to May 2014 for a maximum of two hours per day in the daytime. The light trap method was carried out eight times from May 2013 to February 2014 for 1-1.5 hours per day shortly after sunset. Insects collected by the net sweeping and light trap methods were killed with ethyl acetate soon after capture. Sampling of the leaf litter fauna was carried out on November 28, 2013. Shortly after sampling, the leaf litter heteropterans were extracted from the sample by using Tullgren funnels, and fixed in plastic bottles filled with 60-70% ethanol. The extraction period was two days. All specimens were dried at room temperature and mounted for morphological examination.

Identification methods
Species identification and the determination of postembryonic developmental stage and sex were performed under a stereoscopic microscope (Olympus SZ61, Tokyo, Japan) by TI, using , Hayashi and Miyamoto (2005), Yasunaga et al. (1993), and Yasunaga et al. (2001) as primary references, together with the original descriptions and/or redescriptions of each species, as necessary. For accurate identification, observations of the genitalia, if needed, were made under the stereoscopic microscope and an optical microscope (Olympus BX41) after dissection. The genitalia were preserved in small plastic tubes containing glycerin and mounted on pins with their respective specimens. All specimens examined are preserved in the Insect Collection (IC) at the Komaba Museum, the University of Tokyo, Meguro City, Tokyo, Japan (KMUT). Classification and nomenclature of taxa follow Aukema and Rieger (1995), Aukema and Rieger (1996), Aukema and Rieger (1999), Aukema and Rieger (2001), Aukema and Rieger (2006) and Aukema et al. (2012), and the family level classification within the superfamily Lygaeoidea follows Henry (1997). The arrangement of higher taxa from infraorder to family follows  and is in alphabetical order within families.

Data analysis
The similarities in species composition (occurrence or absence) were examined using a similarity index, Jaccard distances of assemblage, for the Komaba Campus and six localities in Tokyo as reference sites (Table 1). Based on the Jaccard distances, the species compositions were compared among sites by cluster analysis with group averaging. These analyses were conducted using the 'vegdist' function in the 'vegan 2.0-9' package and 'hclust' function in the 'stats 3.0.2' package implemented in the R 3.0.2 software environment (R Core Team 2013

Data resources
In this study, a total of 1,541 specimens were collected and 115 species in 29 families of Heteroptera were detected on the Komaba Campus. Of these specimens, 1,451 individuals were captured by net sweeping, 75 individuals by light traps, and 15 individuals by Tullgren funnels (Table 2). Four species, Hydrometra procera Horváth, Physopleurella armata Poppius, Botocudo japonicus (Hidaka) and Stigmatonotum geniculatum (Motschulsky), Table 1.
Detailed characteristics of each reference site. All sites are situated in Tokyo (see Fig. 1).
Inventory of the Heteroptera (Insecta: Hemiptera) in Komaba Campus of the ...

Notes:
Known as a recent alien species to Japan (Tomokuni 2002) and recorded in Tokyo for the first time by Ishikawa and Hayashi (2013).

Analysis
Cluster analysis based on Jaccard distances revealed two major assemblage groups; one consisted of highly to moderately urbanized localities (Meiji Jingu, Akasaka Imperial Gardens, Imperial Palace, Mizumoto Park, and the campus) and the other of suburbanized localities (Kusabana Hills and Ome City) (Fig. 7).

Discussion
In our qualitative survey, we recorded 115 species of Heteroptera on the Komaba Campus of the University of Tokyo (Table 2). The species richness at campus locations tends to be higher than that of other references sites (Table 1), even though the campus is situated in an urban area within the center of Tokyo and has the smallest area of all sites. The rich campus vegetation presumably derived from effective landscaping managements. These activities may have enhanced heteropteran species diversity. It is, however, possible that the surveys for the majority of reference sites were insufficient, both in terms of quantity and quality, resulting in the relatively low documented species richness. Faunal surveys are often affected by biases related to season, research frequency, collection method, and sampling effort (Tomokuni 2005). More intensive surveys may reveal similar species richness to that of the campus, even in green spaces in highly urbanized zones.
Cluster analysis of assemblages revealed two major groups (Fig. 7). This indicates that the heteropteran fauna detected on the campus was more similar to those of highly urbanized localities than to those of suburbanized localities. However, the analysis also indicated differences in species composition among the five urbanized localities, including the Cluster analysis of Heteroptera assemblages in Komaba Campus and the six reference sites based on Jaccard distances. campus (Fig. 7), irrespective of the distance between the respective urbanized localities, even for the closest two locations, the campus and Meiji Jingu. The differences might reflect that each of the green spaces has a peculiar ecosystem in terms of the heteropteran fauna. However, it is also necessary to consider the relative sufficiency of the surveys for accurately evaluating the urban faunae and ecosystems. Further surveys will clarify the attributes of the urban fauna and biodiversity, and suggest appropriate, sustainable urbanization, or exploitation.