Japanese Journal of Systematic Entomology, 26 (2): 191–200. December 30, 2020.

REVIEW ARTICLE Species Diversity of Aquatic and Coleoptera in Japan

Masakazu HAYASHI1), Jun NAKAJIMA2), Kazuo ISHIDA3), Tadashi KITANO4), Hiroyuki YOSHITOMI5) 1) Hoshizaki Green Foundation, Sono, Izumo, 691-0076 Japan 2) Fukuoka Institute of Health and Environmental Sciences, Fukuoka, 818-0135 Japan 3) Narashino, Chiba, 275-0012 Japan 4) Department of Human Development, School of Humanities and Culture, Tokai University, Hiratsuka, 259-1292 Japan 5) Ehime University Museum, Matsuyama, 790-8577 Japan

Abstract The species diversity of aquatic Hemiptera and Coleoptera in Japan on the water surface and in the water column during both larval and adult stages was reviewed. The list was based on the latest taxonomic knowledge, and summarized species recorded in Japan at the end of 2019. Hemiptera included 118 species in 13 families, among which 22 species (18.6%) were endemic to Japan. Coleoptera included 358 species in 12 families, among which 156 species (43.6%) were endemic to Japan. A total of 29 taxa of Hemiptera and 109 taxa of Coleoptera listed in the Red List of Japan were published in 2019. The total number of Coleoptera taxa increased from 41 to 109 from 2007 to 2019. Keywords: aquatic , aquatic true bugs, biodiversity of Japan

Introduction the water surface and in the water column during both their larval and adult stages. In Coleoptera, these are defined as The Japanese archipelago is located in the ranges of “true water beetles” (Jäch, 1998); however, there is a similarly latitude 20–46° N and longitude 122–153° E, and contains definable species in Hemiptera. The authors published a 6852 large and small islands on the east side of Eurasia bibliographical picture book summarizing these Japanese (Geospatial Information Authority of Japan, 2020). The Kuril species (Nakajima et al., 2020). During the preparation Islands, the four main islands (Hokkaido, Honshu, Shikoku, of this book, the current situation of Japanese species was and Kyushu), and the Ryukyu Islands form island arcs. reexamined. No data have been compiled on species diversity Geologically, the archipelago is dominated by continental to date; therefore, the number of known species, endemic taxa, islands formed by the separation of the continental crust into endangered species, and genetic diversity studies are discussed the Pacific Ocean during the Miocene (Otofuji & Mastuda, in the present review. In particular, the increase in endangered 1987; Barnes, 2003). The island arcs are in the subduction species of aquatic Coleoptera is a significant problem. zone of the oceanic plate, and crustal deformation is active. The main island has mountain ranges that are 2,000–3,000 Methods m above sea level and contain several volcanic fronts. In the North Pacific Ocean, the Daito, Ryukyu, and Ogasawara The species list (Nakajima et al., 2020) is mainly based on Islands are oceanic islands. Kawai & Tanida (2018) and incorporates the latest taxonomic The climate of Japan is warm and humid. From the knowledge and summarizes species recorded in Japan at Japan Meteorological Agency (2020) statistics, the average the end of 2019 (Kamite & Hayashi, 2019; Minoshima & temperature and precipitation values for the 30 years from Inahata, 2019; Nakajima, 2020). Counting was performed 1981 to 2010 were 15.4 °C and 1528.8 mm in Tokyo, and 8.9 at the species level, and taxa that were divided into multiple °C and 1106.5 mm in Sapporo, Hokkaido, respectively. The subspecies were grouped into species. average annual temperature in Naha in Okinawa Prefecture is Endangered species are based on the Red List 2019 23.8 °C, and the annual precipitation is 2099.3 mm. Surface published by the Ministry of the Environment, Japan (MOE, water is abundant due to high precipitation. Paddy fields are 2019a). The list is based on species and subspecies ranks, and mainly used as farmlands in the plains, and valleys in low does not represent the exact number of species. mountainous areas are often used as paddy fields because rice The distribution was divided into seven regions (Fig. 1): is the primary agricultural crop. Many agricultural reservoirs Hokkaido, Honshu, Shikoku, Kyushu, Nansei Islands (Ryukyu are created in areas with relatively low precipitation, and there Islands), Tsushima, and Ogasawara Islands. Of these, the are approximately 96,000 locations nationwide (Ministry of three major islands of Honshu, Shikoku, and Kyushu are often Agriculture, Forestry and Fisheries, 2020). Therefore, both lotic classified as an integrated area in terms of biogeography (e.g., and lentic water environments are abundant in Japan. In the mid- Millien-Parra & Jaeger, 1999). latitudes of the Northern Hemisphere, surface water-rich areas Non-native species were not included in the species count, are limited. Owing to the abundance of surface water, a variety which was only applicable to Rhagadotarsus kraepelini of aquatic adapt to various inland water environments. Breddin, 1905 (Hemiptera: ). This review covered species of aquatic insects that live on

Ⓒ Japanese Society of Systematic Entomology 192 Hayashi, M., J. Nakajima, K. Ishida, T. Kitano and H. Yoshitomi

400

45°

350

300 Hokkaido

40° 250 Coleoptera 200

35° 150

Tsushima Honshu 100 Hemiptera Shikoku 50

30° Kyushu

0 Nansei Isls Ogasawara Isls 1750 1800 1850 1900 1950 2000 Fig. 2. Cumulative number of described species and subspecies by

25°N 0 250 500 year. Only valid names are counted. Km

125°E 130° 135° 140° 145° Fig. 1. Biogeographical division in this study.

Hemiptera Coleoptera

Sharp , 64 Miyamoto, 21

Others, 163 M.Satô , 36 Others, 59 Esaki, 15

Nomura , 31

Matsumura, 12 Jäch , 28

Horváth, 10 Nakane , 21 Clark, 10

Regimbart, 11 Díaz , 17 Fig. 3. Number of described species/ S.Uéno , 11 Scott, 5 Kamite , 15 subspecies per author. Only valid Fieber, 5 Fabricius, 6 Matsui , 11 Kamiya , 11 Fabricius , 12 names are counted.

Habitat of aquatic species the families , , , , Aphelocheiridae, , , Helotrephidae, Nakajima et al. (2020) classified the habitat of aquatic Mesoveliidae, , , Gerridae, and insects into ponds, rivers, puddles, paddy fields, wet rocks, Hermatobatidae. The families of other groups are semi- sea, and groundwater. aquatic, for example, Hebridae, , and . Ponds include natural waters such as ponds, lakes, marshes, and agricultural reservoirs. Taxonomic history Rivers include running water environments such as rivers The first species of aquatic Hemiptera described in Japan and streams. was Appasus japonicus Vuillefroy, 1864. Then, Ilyocoris Puddles are temporary small water bodies or very small cimicoides exclamationis (Scott, 1874), Hydrometra water bodies recharged by springs. albolineata (Scott, 1874), Laccotrephes japonensis Scott, Paddy fields are farmland where rice is grown; dry rice 1874, Ranatra unicolor Scott, 1874, and Microvelia douglasi fields are dry from autumn to winter, and wet rice fields are Scott, 1874 were described as Japanese species of Hemiptera damp all year. by Scott (1874). Wet rocks, also known as hygropetric environments, are According to Hayashi & Miyamoto (2018), the study environments in which the surface of the rocks is constantly of Hemiptera was begun by a Japanese taxonomist after moist due to currents and splashes flowing through the rock. 1900. Shônen Matsumura described Aphelocheirus vittatus Sea includes intertidal zones such as tidal flats and rocky Matsumura, 1905, Anisops ogasawarensis Matsumura, 1915, reefs, inner bays, and coastal waters. and 10 other species (Matsumura, 1905, 1915). During the Groundwater is a water environment that exists in 1950s and 1960s, 21 species were described by Teiso Esaki and underground gravel deposits and fractured zones. Syôiti Miyamoto (Esaki & Miyamoto, 1955; Miyamoto, 1958). While the valid species and subspecies were accrued each Hemiptera year, the increase was remarkable during the 1950s–1960s The taxa of Japanese species that inhabit the water surface (Fig. 2), which was due to the research undertaken by Esaki and water column during their larval and adult stages include and Miyamoto. However, since the 1980s, the increase in the

December 30, 2020, JJSE 26 (2) Review: Species Diversity of Aquatic Hemiptera and Coleoptera in Japan 193

Fig. 4. Known species number for each family of aquatic Hemiptera.

Table 1. Species number for each area of aquatic Hemiptera, and endemic species number in parentheses. HSK shows major three islands, Honshu, Shikoku and Kyushu.

Family Japan Hokkaido Honshu Shikoku Kyushu Nansei Isles Tsushima Ogasawara Isles HSK Nepidae 7(0) 2(0) 4(0) 4(0) 3(0) 6(0) 2(0) 0(0) 4(0) Belostomatidae 5(0) 3(0) 3(0) 3(0) 3(0) 3(0) 2(0) 0(0) 3(0) Corixidae 29(3) 10(1) 20(0) 15(0) 17(0) 11(1) 4(0) 0(0) 21(0) Naucoridae 1(0) 0(0) 1(0) 0(0) 1(0) 0(0) 0(0) 0(0) 1(0) Aphelocheiridae 3(1) 0(0) 3(1) 1(0) 2(0) 0(0) 0(0) 0(0) 3(1) Notonectidae 11(0) 2(0) 4(0) 3(0) 4(0) 9(0) 2(0) 1(0) 5(0) Pleidae 3(0) 0(0) 2(0) 2(0) 2(0) 2(0) 1(0) 0(0) 2(0) Helotrephidae 1(1) 0(0) 0(0) 0(0) 0(0) 1(1) 0(0) 0(0) 0(0) Mesoveliidae 6(1) 4(0) 6(0) 5(0) 4(0) 3(0) 1(0) 1(0) 6(0) Hydrometridae 5(0) 2(0) 4(0) 3(0) 3(0) 3(0) 3(0) 0(0) 4(0) Veliidae 19(12) 2(0) 9(1) 7(0) 8(0) 15(7) 6(0) 2(1) 9(1) Gerridae 27(3) 11(0) 16(0) 10(0) 14(1) 13(0) 9(0) 1(1) 17(1) Hermatobatidae 1(1) 0(0) 0(0) 0(0) 0(0) 1(1) 0(0) 0(0) 0(0) Total 118(22) 36(1) 72(2) 53(0) 61(1) 67(10) 30(0) 5(2) 75(3) number of species described has not occurred, yet the number of Gerridae, 19 species of Veliidae, and 11 species of of species in Japan has increased. This is because species Notonectidae. Corixidae includes 12 species of Sigara, and 9 described overseas are often found in Japan. Comparing the species of Micronecta. number of authors for species/subspecies, Miyamoto, Esaki, The total number of Japanese endemic species is 22, and Matsumura accounted for approximately one-third of the which is 18.6% of the total number of species. The taxa total (Fig. 3). including endemic species are Corixidae, Aphelocheiridae, Helotrephidae, Mesoveliidae, Veliidae, and Gerridae. Veliidae Known species contains 12 endemic species. The total number of Japanese species in the 13 families Counting common species in the surrounding area, there is 118 (Table 1; Fig. 4). In descending order of the number were 85 species from East Asia; 40 species from Siberia, of species, there are 29 species of Corixidae, 28 species Sakhalin, and Kuril; 35 species from southeast Asia; 10

December 30, 2020, JJSE 26 (2) 194 Hayashi, M., J. Nakajima, K. Ishida, T. Kitano and H. Yoshitomi

Table 2. Distribution pattern of aquatic Hemiptera and Coleoptera. Total number of common species each distribution area and Japan.

All species in Siberia, Sakhalin Region Endemic species E Asia SE Asia Oceania Europe N America Japan & Kuril Hemiptera 118 22 85 35 10 40 10 1 Coleoptera 358 156 169 69 13 96 29 11

Table 3. Habitats for each species of aquatic Hemiptera. Data from Nakajima et al. (2020).

Ground- Family Ponds Rivers Puddles Paddies Wet rocks Sea water Nepidae 7225 Belostomatidae 5 1 5 Corixidae 23 9 13 16 Naucoridae 1 Aphelocheiridae 3 Notonectidae 11 2 7 4 Pleidae 3 1 1 Helotrephidae 1 Mesoveliidae 5 2 1 2 Hydrometridae 5114 Veliidae 10 13 10 5 1 Gerridae 17 10 6 4 7 Hermatobatidae 1 Total 87 45 39 45 0 11 0 Ratio % 38.3 19.8 17.2 19.8 0 4.8 0

Table 4. Endangered species of aquatic Hemiptera and Coleoptera listed in Red List 2019 by MOE, Japan. Family EX CR EN VU NT DD Total Nepidae 0000202 Belostomatidae 0201104 Corixidae 0000527 Naucoridae 0010001 Aphelocheiridae 0101002 Notonectidae 0000101 Pleidae 0000000 Helotrephidae 0001001 Mesoveliidae 0000000 Hydrometridae 0001001 Veliidae 0001102 Gerridae 0003407 Hermatobatidae 0000101 Total (2019RL) 031815229 Total (2007RL) 0 2(CR+EN) 9 14 4 29 species from Europe; and one species from North America Species in each area (Table 2). There is a high degree of commonality with species The number of species in each region is shown in Table distributed in the Oriental Region and the eastern part of the 1. Hokkaido accounts for 30.5% of all species, with the three Palaearctic Region. major islands (Honshu, Shikoku, and Kyushu) accounting for 63.6%, and the Nansei Islands accounting for 56.8%. The Ogasawara Islands contained only Notonectidae,

December 30, 2020, JJSE 26 (2) Review: Species Diversity of Aquatic Hemiptera and Coleoptera in Japan 195

Hemiptera Coleoptera 35 120

30 100 25 80 20 60 15 40 10

5 20

0 0 EX CR & EN VU NT DD Total EX CR & EN VU NT DD Total

2007 2019 2007 2019

Fig. 5. Species number listed in Red Lists 2007 and 2019 by MOE, Japan.

Mesoveliidae, Veliidae, and Gerridae, with a total of five Genetic diversity species, and a percentage of only 3.4%. These latter islands Few species or genera have been studied for genetic are oceanic islands; therefore, the aquatic Hemiptera has diversity. Appasus has been examined most closely (Suzuki limited opportunities for dispersal and settlement. et al., 2013, 2014). Kirkaldyia deyrolli (Vuillefroy, 1864) has Only a few Japanese endemic species are further limited been reported to be no different from its counterparts on the to each region. Sigara toyohirae (Matsumura, 1905) was Korean Peninsula (Sareein et al., 2019); however, the sample recorded only from Hokkaido. There were four species in size was small and more detailed studies are required. the three major islands, including Aphelocheirus kawamurae Matsumura, 1915 and Xiphovelia japonica Esaki & Miyamoto, Coleoptera 1959. Xiphovelia boninensis Esaki & Miyamoto, 1959 and The taxa of Japanese species that inhabit the water Neogerris boninensis Matsumura, 1913 are endemic to the surface and water column during both larval and adult Ogasawara Islands, whereas 10 endemic species to Nansei stages include families Haliplidae, Noteridae, , Islands have been recorded, including Micronecta japonica Gyrinidae, Torridincolidae, Hydraenidae, Hydrochidae, Chen, 1960, Heterotrephes admorsus Esaki & Miyamoto, Helophoridae, Hydrophilidae, Spercheidae, Dryopidae, and 1959, and Rhagovelia esakii Lundblad, 1937. The percentage Elmidae. Hydrophilidae contains terrestrial species, and this of endemic Hemiptera species is lower than that of Coleoptera review excludes such species. Other aquatic species such as because many Hemiptera species have high dispersal ability. Psephenidae, Scirtidae, and Ptilodactylidae live in water only Hemiptera has many wing polymorphisms, with macroptery during the larval stage; therefore, these families were also not enabling flying and thus dispersal (Fujisaki, 1994). included. Habitats Taxonomic history Nakajima et al. (2020) classified the main habitats and The taxonomic study of aquatic Coleoptera in Japan began listed each species, which were in descending order of 38.3% with David Sharp. The first report, Sharp (1873), described in ponds, 19.8% in rivers and paddy fields, 17.2% in puddles, 26 species of Dytiscidae, 2 species of Gyrinidae, and 21 4.8% in the sea, and 0% in wet rocks and groundwater (Table species of Hydrophilidae (including terrestrial species). Then, 3). Hemiptera, which inhabits Japanese wet rock habitats, 37 species were described by Sharp (1882, 1884). Most of is semi-aquatic and was excluded from the list. Overseas, the genus he described have been used after the original Naucoridae living on wet rocks has been reported (Sites, description, and their classification accuracy is noteworthy. 2015; Sites & Vitheepradit, 2011). The work of Japanese taxonomists, Kazuo Kamiya, Takehiko Nakane, and Masataka Satô was developed based on Sharp’s Endangered taxa work and helped understand the species diversity. In the Red List published by the MOE (2019a), zero The valid species and subspecies have accrued each year, species are classified as Extinct, three species as Critically with increases being remarkable in the 1870s–1880s and Endangered, one species as Endangered, eight species as 1950s–1960s (Fig. 2), with Sharp greatly contributing to these Vulnerable, fifteen species as Near Threatened, and two increases and him describing the largest number of species to species as Data Deficient (Table 4), with a total of 29 date (Fig. 6). In a particular family, Shizumu Nomura described species. Lethocerus indicus (Lepeletier & Serville, 1775) and 31 species of Elmidae in the 1950s–1960s, and recently nine Aphelocheirus kawamurae Matsumura, 1915 have not been species were described by Yuuki Kamite. Manfred A. Jäch has recorded recently. described 29 Hydraenidae species since 1988. Compared to the Red List 2007 (MOE, 2007), the total number of species is 29. The total number of endangered Known species species (Critically Endangered, Endangered, and Vulnerable ) A total of 358 Japanese species are included in the 12 has increased slightly from 11 to 12 (Table 4).

December 30, 2020, JJSE 26 (2) 196 Hayashi, M., J. Nakajima, K. Ishida, T. Kitano and H. Yoshitomi

Fig. 6. Known species number for each family of aquatic Coleoptera.

Table 5. Habitats for each species of aquatic Coleoptera. Data from Nakajima et al. (2020).

Ground- Family Ponds Rivers Puddles Paddies Wet rocks Sea water Haliplidae 11 2 6 Noteridae 9 3 7 Dytiscidae 96 26 33 57 1 5 Gyrinidae 9 14 1 4 Torridincolidae 1 Hydraenidae 2 32 6149 Hydrochidae 4 1 1 Helophoridae 5 3 1 Hydrophilidae 49 25 20 32 6 3 Spercheidae 1 Dryopidae 1 4 Elmidae 2 51 1 Total 189 154 64 105 11 13 13 Ratio % 34.4 28.1 11.7 19.1 2 2.4 2.4 families (Table 6; Fig. 6). There are 128 species of Dytiscidae, Counting common species in the surrounding area, there 76 species of Hydrophilidae, 57 species of Elmidae, and 39 were 169 species from East Asia; 96 species from Siberia, species of Hydraenidae. Sakhalin, and Kuril; 69 species from southeast Asia; 29 The total number of Japanese endemic species is 156, species from Europe; and 11 species from North America accounting for 43.6% of the total Japanese species. The only (Table 2). taxa that do not contain endemic species are the families Helophoridae and Spercheidae.

December 30, 2020, JJSE 26 (2) Review: Species Diversity of Aquatic Hemiptera and Coleoptera in Japan 197

Table 6. Species number for each area of aquatic Coleoptera, and endemic species number in parentheses. HSK shows major three islands, Honshu, Shikoku and Kyushu.

Family Japan Hokkaido Honshu Shikoku Kyushu Nansei Isles Tsushima Ogasawara Isles HSK Haliplidae 11(2) 5(0) 8(1) 6(0) 6(0) 5(0) 5(0) 0(0) 8(1) Noteridae 16(8) 3(0) 8(3) 7(3) 5(1) 6(0) 1(0) 0(0) 12(7) Dytiscidae 128(32) 57(2) 78(5) 47(3) 52(0) 53(4) 15(0) 4(1) 83(19) Gyrinidae 16(6) 6(0) 10(1) 7(0) 8(1) 6(2) 2(0) 0(0) 11(3) Torridincolidae 1(1) 0(0) 1(0) 1(0) 0(0) 1(0) 0(0) 0(0) 1(0) Hydraenidae 39(31) 7(1) 24(12) 7(0) 8(0) 14(10) 1(1) 1(1) 25(16) Hydrochidae 4(2) 1(0) 3(1) 2(0) 2(0) 1(0) 0(0) 0(0) 3(2) Helophoridae 5(0) 4(0) 3(0) 0(0) 0(0) 0(0) 1(0) 0(0) 3(0) Hydrophilidae1) 76(22) 23(0) 51(2) 34(0) 40(0) 43(9) 9(0) 4(0) 54(5) Spercheidae 1(0) 0(0) 0(0) 0(0) 0(0) 1(0) 0(0) 0(0) 0(0) Dryopidae 4(1) 1(0) 3(0) 1(0) 1(0) 2(1) 1(0) 0(0) 3(0) Elmidae 57(51) 7(0) 33(7) 22(2) 26(2) 23(17) 4(1) 0(0) 38(24) Total 358(156) 114(3) 222(32) 134(8) 148(4) 155(43) 39(2) 9(2) 241(76) 1)Except for terrestrial species

Table 7. Species number of aquatic Coleoptera listed in Red List 2007 & 2019 by MOE, Japan Family EX CR EN VU NT DD Total Haliplidae 0013116 Noteridae 0042039 Dytiscidae1) 1 6 5 11 20 8 51 Gyrinidae 01234212 Torridincolidae 0000000 Hydraenidae 0000325 Hydrochidae 0011114 Helophoridae 0011002 Hydrophilidae2) 00117211 Spercheidae 0000000 Dryopidae 0000000 Elmidae 0034029 Total (2019RL) 1 7 18 26 36 21 109 Total (2007RL) 0 13(CR+EN) 8 15 5 41 1)Includes subspecies number 2)Except for terrestrial species

Species in each area commonality between Sakhalin and Siberian species. There The species numbers in each region are shown in Table are 76 endemic species in the three major islands including 6. Hokkaido accounts for 31.8% of all species, with the three Haliplus kamiyai Nakane, 1963, Copelatus kammuriensis major islands (Honshu, Shikoku, and Kyushu) contributing Tamu & Tsukamoto, 1955, Orectochilus agilis Sharp, 1884, 67.3% and Nansei Islands contributing 43.3%. The Ochthebius japonicus Jäch, 1998, Orientelmis parvula Ogasawara Islands contain only Dytiscidae, Hydraenidae, and (Nomura & Baba, 1961), and Zaitzeviaria sotai Hayashi & Hydrophilidae, with a total of nine species, and a percentage Yoshitomi, 2015. Another characteristic of this area is the of only 2.5%. The Ogasawara Islands are oceanic islands; presence of groundwater species such as Phreatodytes relictus therefore, the aquatic Coleoptera have limited opportunities S. Uéno, 1957 and Morimotoa phreatica S. Uéno, 1957. for dispersal and settlement. Copelatus ogasawarensis Kamiya, 1932 and Ochthebius The distribution of endemic species in each region sasakii Yoshitomi, Karube & Hayashi, 2019 are endemic is shown in Table 6. Many endemic Japanese species are to the Ogasawara Islands. There are 43 species endemic to further restricted to each region. Hokkaido contains only the Nansei Islands, including Allopachria bimaculate (M. three endemic species, including Hydroporus ijimai Nilsson Satô, 1972), Gyrinus ryukyuensis M. Satô, 1971, Hydraena & Nakane, 1993 and Ochthebius hokkaidensis Jäch, 1998. okinawaensis Jäch & Díaz, 1999, and Ochthebius amami The lack of endemic species in Hokkaido is due to the high Yoshitomi & M. Satô, 2001. There are two species endemic

December 30, 2020, JJSE 26 (2) 198 Hayashi, M., J. Nakajima, K. Ishida, T. Kitano and H. Yoshitomi

regional populations (Nagata et al., 2018). In species, intraspecific mutations of Horelophopsis hanseni (Minoshima et al. 2013) and Enochrus vilis (Sharp, 1884) have been reported (Minoshima, 2019). Although the phylogenetic relationships of Elmidae have been investigated (Hayashi et al., 2013, 2016, 2019), no consideration has been given to regional populations.

Discussion Species diversity Tojo et al. (2017) stated seven factors for diversity in Japan: 1) the extended latitudinal range from north to south, 2) the rugged terrain and geography, 3) the humid climate and abundant precipitation resulting from the Asian monsoon Fig. 7. Hydaticus satoi Wewalka, 1975. Collected in Mastuyama, climate, 4) the complex formation of the Japanese islands and Ehime Prefecture, Shikoku, Japan (3 Oct, 1935; collected by its geological history, 5) dispersal via land bridges, 6) dispersal Mutsuo Miyatake). of long distances by aerial flight and oceanic floating, and 7) climatic changes in glacial and interglacial cycles. All of these to Tsushima: Hydraena tsushimaensis Jäch & Díaz, 2012 and factors contribute to the diversity of aquatic Hemiptera and Zaitzeviaria kuriharai Kamite, Ogata & M. Satô, 2006. Coleoptera in Japan. The climate is particularly important; however, the abundance of endemic species is greatly Habitats influenced by other factors. Molecular phylogeographic studies Nakajima et al. (2020) classified the main habitats and on aquatic insects have been conducted on two species of listed each species, in descending order of 34.4% in ponds, Appasus (Belostomatidae), and their divergence between the 28.1% in rivers, 19.1% in paddies, 11.7% in puddles, 2.4% continental and Japanese clades was estimated (Suzuki et al., in the sea and groundwater, and 2.0% in wet rocks (Table 2013, 2014). Hydraena (Hydraenidae), which describes many 5). Compared to Hemiptera, Coleoptera is characterized by species and contains several undescribed species, is expected a higher proportion found in rivers and the presence of 11 to be a useful taxa for molecular phylogeographic studies. In species in the groundwater. Coleoptera, Quaternary fossil record have accumulated, and it is known that two species of Dytiscidae, Ilybius apicalis Sharp, Endangered taxa 1873 and Ilybius nakanei Nilsson, 1994, were distributed in The Red List published by the MOE (2019a) lists one Honshu during the last glacial period (Hayashi, 2007). These species as Extinct, 7 taxa as Critically Endangered, 18 taxa two species are thought to have become extinct in Honshu due as Endangered, 26 taxa as Vulnerable, 36 taxa as Near to the warming at the end of the glacial period. Fossils are the Threatened, and 21 taxa as Data Deficient, for a total of 109 most reliable record of how regional differences in species taxa (Table 7; Fig. 5). Hydaticus satoi Wewalka, 1975 has composition have emerged within the Japanese archipelago. been found to be extinct (Fig. 7). Orectochilus teranishii Focusing on aquatic Coleoptera, Short (2018) summarized Kamiya, 1933 has not been recorded since it was originally the described species for each family worldwide. When described and Hydaticus thermonectoides Sharp, 1884 has not limited to families distributed in Japan, the total number been confirmed in recent years. of described species worldwide is 12,485. There are 358 Several species have been rediscovered because Japanese varieties, totaling at different times, but the Japanese increasing number of researchers have been investigating species numbers are estimated to be less than 3%. Given that aquatic Coleoptera. Examples include Copelatus parallelus the land area of the Japanese archipelago is only 0.25% of the Zimmermann, 1920, Dytiscus sharpi Wehncke, 1875, Gyrinus world and it is a mid-latitude region, the number of species is niponensis Brinck, 1941, and Orientelmis parvula (Nomura & large. Bilton et al. (2019) reviewed the ‘Models in Ecology Baba, 1961). and Evolution’ using aquatic beetles and introduced some Compared to the Red List 2007 (MOE, 2007), the total important areas of historical biogeography, such as Gondwana, number of taxa increased from 41 to 109 by 2019. The but did not mention East Asia, including the Japanese islands. total number of endangered species (Critically Endangered, This is because few studies have been conducted on aquatic Endangered, and Vulnerable) has more than doubled from beetles. The Japanese islands were formed by a complex 21 species to 52 species (Table 7). In Japan, the number of geological history, and are among the most tectonically active species of Gyrinidae and Dytiscidae has been decreasing regions worldwide. Thus, further studies are required for the since the beginning of the 2000s, and the number of Red List speciation of many endemic species in Japan. species has been increasing. Conservation Genetic diversity Many aquatic insects are considered endangered in Few species or genera have been studied for genetic Japan. In Hemiptera, of the 29 species on the Red List diversity. Dytiscus sharpi Wehncke, 1875 has been studied in

December 30, 2020, JJSE 26 (2) Review: Species Diversity of Aquatic Hemiptera and Coleoptera in Japan 199

(MOE, 2019a), four species (13.8%) live mainly in the lotic is being undertaken by the Conservation Society for D. environment and three species (10.3%) live in the sea, with sharpi in Chiba Prefecture (Nishihara, 2019). However, the the remaining 22 species found in the lentic environment. In situation has not improved for some species due to ongoing Coleoptera, of the 109 species on the Red List, 22 species habitat degradation and dispersion by invasive species. In this (20.2%) live mainly in the lotic environment and six species context, university laboratories and insect breeding facilities (5.5%) live in the groundwater, with the remaining 80 species collaborated to conserve habitat (Kitano & Watanabe, 2016; found in the lentic environment. Anthropogenic modification Nishihara, 2019). Conservation both inside and outside of the river environment is a significant factor in the decline habitats requires the elucidation of the life histories of each of species inhabiting the lotic environment (Kamite, 2016; target species and the establishment and coordination of Nishihara, 2016). In Japan, rivers have had increasing water organizations to carry out this work on an ongoing basis. The quality since the 1970s and, as of 2017, the achievement rate establishment of efficient breeding techniques and the creation of water quality standards was 94% (MOE, 2019b). Therefore, of manuals are also important for ex situ conservation. the habitat status of endangered species could be improved by The ultimate goal of conservation is to recover as many changing the way rivers are utilized. endangered species as possible. Nishihara (2016) cited large-scale development, land development, pesticide use, field maintenance, reservoir Acknowledgements renovation, the abandonment of cultivation, the introduction of We are indebted to Mr. Tomohiro Nakamura (Bun-ichi invasive alien species, and the collection of species as factors Sogo Shuppan, Tokyo) for his help in preparing our book, contributing to the decline of species since 2000, with climate ‘Aquatic Coleoptera and Hemiptera of Japan,’ on which this change also being a factor. In reservoirs, native aquatic insects review was based. have been heavily affected by non-native species, Micropterus salmoides Lacépède, 1802, Lepomis macrochirus Rafinesque, 1819, Procambarus clarkii (Girard, 1852), and Lithobates References catesbeianus (Shaw, 1802). Common species such as Gyrinus Anastacio, P. M., V. S. Parente, & A. M. Correia, 2005. Crayfish japonicus Sharp, 1873, Hyphydrus japonicus Sharp, 1873, effects on seeds and seedlings: identification and quantification and Laccophilus difficilis Sharp, 1873, which were common of damage. Freshwater Biology, 50: 697–704. on the main islands of Japan until 1990, are found in paddy Barnes, G. L., 2003. Origins of the Japanese Islands: the new “Big Picture”. Japan Review, 15: 3–50. fields and reservoirs, and have been rapidly declining since Bilton, D. T., I. Ribera, & A. E. Z. Short, 2019. Water beetles 2000 (Ichikawa, 2016). The area of paddy fields in Japan has as models in Ecology and Evolution. Annual Review of been declining since its peak in the 1960s (MAFF, 2019). The Entomology, 64: 359–377. impact of the decline is pronounced, particularly in the Nansei Esaki, T. & S. Miyamoto, 1955. Veliidae of Japan and adjacent Islands, because of the limited cultivable paddy fields on the territory (Hemiptera-). I. Microvelia Westwood narrow islands, and the breeding sites being greatly reduced and Pseudovelia Hoberlandt of Japan. Sieboldia, Fukuoka, 1: (Nishihara, 2016). 169–204, pls 24–29. In Japan, M. salmoides, L. macrochirus and Lithobates Fujisaki, K., 1994. Adaptive significance and evolution of dispersal polymorphisms in insects. Scientific Reports of the Faculty of catesbeianus have been designated as invasive species since Agriculture, Okayama University, (83): 113–132. (in Japanese the Alien Species Act was enforced in 2004. L. catesbeianus with English abstract) can move over land by walking, and M. salmoides and Geospatial Information Authority of Japan, 2020. Welcome to GSI. L. macrochirus are transported by humans. In addition, https://www.gsi.go.jp/ENGLISH/index.html (accessed: 7 Jan Procambarus clarkii is widely established in Japan, but 2020) has not been designated as a specified invasive organism. Hayashi, M., 2007. Beetle records: Late Pleistocene of Japan. In Elias However, P. clarkii has significant effects on aquatic insects ed. Encyclopedia of Quaternary Science, 1: 196–212. Elsevier. Hayashi, M., & S. Miyamoto, 2018. Hemiptera. In Kawai T, Tanida and plants (Anastacio et al., 2005; Nishijima et al., 2017). K (eds) Aquatic insects of Japan: Manual with keys and They live in shallow water and burrow deep into the mud; illustrations, Second Edition: 329–427. Tokai University Press, therefore, they are difficult to eradicate. This species should Hadano. be designated by the act before further expansion of its Hayashi, M., S. D. Song, & T. Sota, 2013. Patterns of hind-wing distribition. degeneration in Japanese riffle beetles (Coleoptera: Elmidae). The Species Protection Act in Japan was enacted in 1993 European Journal of Entomology, 110: 689–697. https://doi. and, as at the end of 2019, Dytiscus sharpi Wehncke, 1875, org/10.14411/eje.2013.092 Acilius kishii Nakane, 1963, Cybister lewisianus Sharp, 1873, Hayashi, M., Y. Kamite, T. Kobayashi, & T. Sota, 2016. Description of larvae of genera Stenelmis, Ordobrevia and Nomuraelmis Cybister limbatus (Fabricius, 1775), and H. thermonectoides (Coleoptera: Elmidae: Elminae) of Japan with their molecular Sharp, 1884 were designated (EOE, 2019c). Among these, . Zootaxa, 4178: 451–480. https://doi.org/10.11646/ specific conservation plans have been implemented for two zootaxa.4178.4.1 species, A. kishii and D. sharpi (EOE, 2019c). The designation Hayashi, M., H. Yoshitomi, Y. Kamite, T. Kobayashi, & T. Sota, prohibits collection; therefore, there is a certain conservation 2019. Description of adults and larvae of Orientelmis parvula effect. Depending on the legal basis, there are examples of (Nomura & Baba, 1961) (Coleoptera: Elmidae) with their cooperation between the government and private organizations molecular phylogenetic analysis. Zootaxa, 4568: 483–500. Ichikawa, T., 2016. The crisis of water bugs and water beetles. The regarding conservation. 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