Jpn. J. Environ. Entomol. Zool. 31（1）：1－12（2020） 環動昆 第 31 巻 第 1 号：1－12（2020） Original Article

Species diversity of in Nakaikemi Marsh, Fukui Prefecture, Japan

Norio Hirai＊, Takashi Morioka and Minoru Ishii

Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-1 Gakuen-cho, Nakaku, Sakai, Osaka 599-8531 Japan

（Received: June 5, 2018; Accepted: February16, 2020）

Abstract Nakaikemi Marsh was designated as a wetland of international importance under the Ramsar Convention on Wetlands in 2012 because of its rich species diversity and the presence of threatened and endangered and plant species. Although the marsh had been maintained using traditional methods for centuries as rice paddy fields, land use has changed since the abandonment of cultivation in the 1990s. In this study, species diversity of Odonata in the marsh was investigated once a month between April and November 2012 using line-transect and point-census methods for adults and a netting method for larvae. We recorded adults and larvae of 50 Odonata species; a total of 2093 adults from 47 species and 503 larvae from 27 species were observed in the eight surveys. Most of the species found in this study were those recorded in the past, but Aeschnophlebia longistigma, Aeschnophlebia anisoptera, and Nannophya pygmaea, which had been continuously observed in the early 1990s, were not recorded. In contrast, we found increased numbers of Rhyothemis fuliginosa, Ischnura senegalensis, and Sympetrum croceolum around the newly formed Sasahana Pond. A population analysis using Kimoto’s similarity index (Cπ) revealed that the odonatan assemblage around the pond differs from those in other areas in Nakaikemi Marsh. It is possible that the Sasahana Pond has become one of the most important odonatan habitats in the marsh. We found several endangered species and the second highest species richness and diversity in the Ushirodani Valley adjoining the marsh, where traditional methods are used to maintain paddy fields. Invasive alien plant and animal species such as Solidago altissima and Procambarus clarkii were widespread across the whole area and are considered to harm native vegetation and aquatic in the marsh. Our findings indicate that P. clarkii density has a significant negative effect on the species diversity of Odonata larvae in the marsh.

Keywords: aquatic , community ecology, , , Procambarus clarkii

Introduction designated as a wetland of international importance under the Ramsar Convention on Wetlands in 2012 (The Ramsar Nakaikemi Marsh, located at an elevation of 47 m a.s.l. in Convention on Wetlands, 2012). Tsuruga City, Fukui Prefecture, Japan, is a 25-ha basin In 1990, a bypass highway was built, and excavated soil surrounded by hills (Saito, 2008). The central part of the site is from its construction was deposited in the marsh. As a result, composed of peat sediment that is approximately 40 m in depth several ponds formed by heavy soil were connected and and represents a record of climate and vegetation changes became a large pond (Nakamoto et al., 2003; Shimoda and during the past 100,000 years (Sakamaki, 2003; Ramsar Nakamoto, 2003), which is called Sasahana Pond. The Tsuruga Convention on Wetlands, 2012). This marsh is also considered City government invited a gas company to build liquified a biodiversity hotspot with more than 2000 species of animals natural gas tanks on the marsh in 1992, and cultivation of the and plants (Watanabe and Kawano, 2003; Ramsar Convention paddy fields was abandoned after the company took possession on Wetlands, 2012). For this reason, the Nakaikemi Marsh was of the marsh (Shimoda and Nakamoto, 2003). However,

*Corresponding author: [email protected]

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Fig. 1 Location of the study site, Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, and the transect route for Odonata survey. Adult survey sections are A to J; Aeshnidae observation points are K & L; and larvae survey points are Q to Z. construction of the liquified natural gas tanks was canceled in was newly recorded in 2011 (Fujino and Wada, 2011) and 2002 (Sasaji et al., 2003), and the gas company donated the Gynacantha japonica was found in 2013 (M. Uenoyama, property to Tsuruga City in 2005 (Sasaki, 2006). Prior to the personal communication), bringing the total number of abandonment of the paddy fields in Nakaikemi, the marsh recorded species to 72. However, the populations of some consisted of various aquatic and semi-aquatic environments: Odonata species declined remarkably between 1995 and 2003 cultivated paddy fields, fallow fields, abandoned fields, ponds, due to deterioration of their habitats in the marsh (Tsubaki and and channels (Wada, 2000). Since rice farming ceased, Kawano, 2003), and a comprehensive survey of Odonata however, vegetative succession has progressed, water levels species has not been carried out since Wada (2003) and have declined due to lack of management, and stagnation and Nakamoto et al. (2003) performed them. After 2003, plant deterioration of water quality have occurred as pathways have succession advanced; a large deep pond was expanded; and been constructed in the marsh (Shimoda and Nakamoto, 2003; alien species, such as Solidago altissima and P. clarkii, invaded Hoshina et al., 2007). The population of the invasive alien red more of the marsh. Therefore, we expected to find that the swamp crayfish, Procambarus clarkii, has exploded, Odonata assemblage, which previously consisted of destroying populations of native aquatic animals and plants shallow-marsh species, had shifted to that of deep-pond species. (Wada, 2001; Shimoda, 2003; Hoshina et al., 2007). To clarify whether this habitat shift was accompanied by a shift Odonata species are an important and widespread biological in the Odonata assemblage, research on the different water indicator of the condition and biodiversity of freshwater types and effects of alien species was needed. In 2012, we ecosystems (Corbet, 1962; Steytler and Samways, 1995; Wada, measured the species diversity of Odonata in Nakaikemi Marsh 2000; Inoue, 2010a). Habitat preference also varies among and analyzed recent changes in the assemblage structure as species, with some Japanese species preferring lotic water and compared with past records. others deep lentic or shallow lentic waters (e.g., Kadoya and Washitani, 2007; Kadoya et al., 2009; Inoue, 2010b). In Materials and Methods Nakaikemi Marsh, 70 species of Odonata in 11 families were recorded prior to 2002 (Nakaikemi Wetland Trust, 2002; Study sites and methods Nakamoto et al., 2003; Wada, 2003). Sympetrum croceolum The field surveys were carried out once a month from April

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Table 1 Description of Odonata survey location sections, landscape, and vegetation components of

the study area, Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan in 2012.

Survey place Landscape component Vegetation Section AB Gravel path between Sasahana Pond and deciduous forest Tall herbaceous plants such as the common reed Phragmites [Points Q, R and S] communisand reedmace, Typha spp., were growing in the deep Transect length: 456 m ponds.

Section BC Gravel path along the western edge of the marsh Tall herbaceous plants such as the common reed, Phragmites [Point T] communis, and the invasive introduced goldenrod, Solidago Transect length: 341 m canadensis, were growing in shallow mud.

Section CD&EG Soil path along the northeastern edge of the marsh. Northern side Tall herbaceous plants such as the common reed, Phragmites [Points U and W] was deciduous forest and southern side was wet mud flats. communis, and the invasive goldenrod, Solidago canadensis, Transect length: 686 m were growing in the shallow mud.

Section DE Soil path between a shallow small pond and the marsh. Short herbaceous plants such as cogongrass, Imperata [Point V] cylindrica, were growing along edge of the small pond. Transect length: 46 m Section EF Slope behind the small pond with water exudation from forest. Shrubs and short herbaceous grass. Transect length: 111 m

Section GH Ushirodani Valley, comprising branched waterways and paddy Almost all areas were abandoned paddy fields traces covered [Points X, Y and Z] fields. with tall herbaceous plants, but the most eastern area had always Transect length: 859 m had water and tall and low herbaceous plants. Section IA&AJ One-meter wide waterways with bottoms covered with slime. Short herbaceous grass. Transect length: 299 m to November 2012 in Nakaikemi Marsh, Tsuruga City, Fukui basin. Physical details of the adult survey transect sections are Prefecture, Japan (35°39’N, 136°05’E; Fig. 1). given in Table 1. To assess the relationship between environmental factors To identify whether Odonata species are breeding in the and the Odonata assemblage, Odonata adults were recorded marsh, Odonata larvae were captured by sweeping a D-frame along seven line transects and at two point-census locations. In aquatic net (40 cm wide; 1-mm mesh) through the water the transect-census method, the study area was divided into at 10 locations (points Q to Z) in the study area on the same two landscapes: basin and valley. In the basin landscape, a days as the adult surveys were conducted (Fig. 1). The insect 1.8-km route that circled through major landscape components net was then moved 1 m, and this sampling was repeated 10 was fixed and divided into six sections according to times per point as a rule. When the water depth was reduced, surrounding landforms. In the narrow 0.8-km-long valley we decreased the number of sweeps. The density of larvae landscape (Ushirodani Valley), we fixed a single transect. (number / 10 netting sample) was calculated by dividing the Water flows out from the basin area into Ushirodani Valley, total number observed by the total number of sweeps at each which is separated from the rest of the marsh and contains point (for the total number of sweeps conducted in each survey, cultivated and fallow paddy fields surrounded by deciduous see Table 4). Unidentified individuals not belonging to the forests (Fig. 1). commonly captured families or genera were placed in Odonata adults were counted monthly from April to screw-top bottles filled with 99% ethanol and brought to the November 2012 in all sampling areas, for a total of nine times. laboratory for identification. We also recorded the number of P. Each count was conducted for 2 to 3 h between 09:00 and clarkii captured at each netting site during sampling. 14:00 h local time under fine weather conditions. We recorded adults of each species that were sighted within an area 10 m Data analysis wide (5 m to each side of the recorder) and up to 5 m high We used the Simpson diversity index (1 – λ), the Sörensen along the route. Species not readily identified were captured quotient of similarity index (QS), and the Kimoto Cπ index to with an insect net and released immediately after identification. compare the species diversity of adults and larvae in each The density of adults was calculated by dividing the total transect, the total number of species, and species (population) number observed by the total length of each section (section structure, respectively. length × 8 survey times). Because some Aeshnidae species are The Simpson index was calculated by using the following difficult to find in the daytime (e.g., Corbet, 1999; Katatani, equation (Simpson, 1949): 2010), they were monitored at twilight between June and ni ( ni 1) August by using a point-census method at two locations in the 1λ 1  N ( N 1)

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Table 2 Density (No./km; see text) and the actual total number (in parentheses) of Odonata species adults recorded using a line transect census method in the Nakaikemi Marsh, Tsuruga City, Fukui Prefecture,

Japan between April and November 2012.

Transect section Point census Family and species name Total AB BC CD&EG DE EF GH IA&AJ K&L D/S/L1) Forest Les tidae peregrinus 2.72 (1) 0.04 (1) S +2) temporalis 1.09 (6) 13.59 (5) 0.15 (1) 0.54 (12) S + Calopterygidae Mnais costalis 1.31 (9) 0.40 (9) L + Mnais pruinosa 4.07 (28) 2.18 (4) 1.43 (32) L + Atrocalopteryx atrata 0.36 (2) 0.73 (5) 0.31 (7) L + Platycnemididae Copera annulata 0.27 (1) 0.55 (3) 0.18 (4) D + Coenagrionidae Ceriagrion melanurum 1.92 (7) 0.31 (7) S Paracercion calamorum 1.64 (6) 0.73 (2) 0.36 (8) D, S + Paracercion hieroglyphicum 3.56 (13) 0.55 (1) 0.63 (14) D, S Paracercion sieboldii 0.55 (2) 2.18 (4) 0.27 (6) D, S Mortonagrion selenion 0.73 (5) 0.22 (5) S Ischnura senegalensis 13.98 (51) 0.73 (2) 0.55 (1) 2.42 (54) D, S Ischnura asiatica 24.95 (91) 1.47 (4) 1.13 (1) 6.00 (11) 4.79 (107) D, S Aeshnidae Anaciaeschna martini (20) D, S Polycanthagyna melanictera (7) D Sarasaechna pryeri 0.37 (1) 1.09 (6) 0.31 (7) S + Planaeschna milnei 0.18 (1) 0.15 (1) 0.09 (2) L + Aeshna crenata 1.10 (4) 2.72 (1) 0.15 (1) 0.27 (6) D + Anax parthenope 6.03 (22) 0.37 (1) 0.29 (2) 0.55 (1) 1.16 (26) (12) D Anax nigrofasciatus 0.27 (1) 0.15 (1) 0.55 (1) 0.13 (3) (2) D + Gomph idae Sinictinogomphus clavatus 0.27 (1) 0.04 (1) D Trigomphus melampus 6.30 (23) 0.37 (1) 0.55 (3) 1.64 (3) 1.34 (30) D, S + Asiagomphus pryeri 1.09 (2) 0.09 (2) L Asiagomphus melaenops 0.27 (1) 0.37 (1) 1.31 (9) 0.55 (1) 0.54 (12) L Petaluridae Tanypteryx pryeri 0.18 (1) 2.25 (2) 0.13 (3) S + Cordulegastridae Anotogaster sieboldii 0.37 (1) 2.37 (13) 2.72 (1) 2.25 (2) 1.31 (9) 1.16 (26) L + Corduliidae Somatochlora viridiaenea 1.46 (8) 2.72 (1) 1.13 (1) 0.45 (10) S + Macromiidae Epophthalmia elegans 1.37 (5) 0.22 (5) D Libellulidae Rhyothemis fuliginosa 22.75 (83) 0.73 (2) 0.73 (4) 8.15 (3) 0.44 (3) 1.09 (2) 4.35 (97) D + Sympetrum darwinianum 9.59 (35) 7.70 (21) 9.66 (53) 5.43 (2) 9.90 (68) 3.82 (7) 8.33 (186) S + Sympetrum risi 0.27 (1) 0.37 (1) 3.38 (3) 0.15 (1) 0.27 (6) D + Sympetrum infuscatum 8.77 (32) 3.30 (9) 10.93 (60) 5.43 (2) 2.25 (2) 3.78 (26) 1.64 (3) 6.00 (134) D, S + Sympetrum frequens 10.14 (37) 9.90 (27) 8.75 (48) 10.87 (4) 27.03 (24) 6.84 (47) 7.10 (13) 8.96 (200) D, S Sympetrum baccha 0.55 (3) 2.72 (1) 0.15 (1) 0.22 (5) D, S + Sympetrum parvulum 4.19 (23) 2.72 (1) 14.64 (13) 0.58 (4) 1.84 (41) S + Sympetrum eroticum 0.55 (2) 0.73 (2) 0.91 (5) 2.25 (2) 2.91 (20) 1.09 (2) 1.48 (33) D, S + Sympetrum speciosum 5.21 (19) 0.55 (1) 0.90 (20) D + Sympetrum croceolum 2.74 (10) 0.37 (1) 0.49 (11) D Pseudothemis zonata 18.37 (67) 2.57 (7) 2.00 (11) 5.43 (2) 0.58 (4) 4.37 (8) 4.44 (99) D + Deielia phaon 5.21 (19) 0.37 (1) 0.55 (1) 0.94 (21) D Crocothemis servilia 4.39 (16) 0.37 (1) 0.29 (2) 0.85 (19) D, S Pantala flavescens 4.66 (17) 8.06 (22) 1.09 (6) 2.72 (1) 6.76 (6) 0.29 (2) 0.55 (1) 2.46 (55) S Lyriothemis pachygastra 3.56 (13) 3.30 (9) 10.20 (56) 4.50 (4) 4.07 (28) 1.09 (2) 5.02 (112) S + Orthetrum albistylum 18.09 (66) 11.73 (32) 10.02 (55) 152.17 (56) 11.26 (10) 7.13 (49) 16.38 (30) 13.35 (298) D, S Orthetrum japonicum 1.10 (4) 12.46 (34) 12.39 (68) 19.02 (7) 18.02 (16) 0.73 (5) 2.73 (5) 6.23 (139) S + Orthetrum melania 4.66 (17) 5.87 (16) 12.21 (67) 43.48 (16) 13.51 (12) 4.66 (32) 1.09 (2) 7.26 (162) D, S Libellula quadrimaculata 4.11 (15) 0.67 (15) D, S + Total 186.7 (681) 72.6 (198) 91.5 (502) 282.6 (104) 110.4 (98) 52.8 (363) 57.9 (106) 91.9 (2,052) 1) Typical larval habitat based on Inoue and Miyatake (2010) and Yamamoto et al . (2009): D, lentic deep water; S, lentic shallow water; L, lotic water. 2) Species in which adults inhabit forests or forest edge based on Inoue and Miyatake (2010) and Yamamoto et al. (2009).

where ni is the number of individuals of each species (i) and N is total number of individuals recorded in a transect section. 2n1i n2i QS was used to compare species structure between each C  2 2 ( 1  2 ) N1  N2 transect and was calculated by using the following equation  , (Kimoto and Takeda, 1989): (n )2 2  1i 2c 1  QS   N 2 a  b , 1 , where a and b are the total number of individuals observed in (n )2 2  2i each transect and c is the number of species in common  2   N 2 between the two transects being compared. 2 ,

Cπ was used to compare the assemblage structure in each where N1 and N2 are the total number of individuals recorded transect and was calculated by using the following equations in the two transects being compared (i.e., transects 1 and 2),

(Kimoto, 1967): and n1i and n2i are the number of individuals of each species (i)

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Table 3 Density (No./km) and the actual number (in the parenthesi s) of 5 dominant species of Odonata of each transect section in Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, recorded between April and November 2012.

Order of the No. of AB BC CD&EG DE EF GH IA&AJ species

1 Ischnura asiatica Orthetrum japonicum Orthetrum japonicum Orthetrum albistylum Sympetrum frequens Sympetrum darwinianum Orthetrum albistylum 25.0 (91) 12.5 (34) 12.4 (68) 152.2 (56) 27.0 (24) 9.9 (68) 16.4 (30) 2 Rhyothemis fuliginosa Orthetrum albistylum Orthetrum melania Orthetrum melania Orthetrum japonicum Orthetrum albistylum Sympetrum frequens 22.8 (83) 11.7 (32) 12.2 (67) 43.5 (16) 18.0 (16) 7.1 (49) 7.1 (13) 3 Pseudothemis zonata Sympetrum frequens Sympetrum infuscatum Orthetrum japonicum Sympetrum parvulum Sympetrum frequens Ischnura asiatica 18.4 (67) 9.9 (27) 10.9 (60) 19.0 (7) 14.6 (13) 6.8 (47) 6.0 (11) 4 Orthetrum albistylum Pantala flavescens Lyriothemis pachygastra Lestes temporalis Orthetrum melania Orthetrum melania Pseudothemis zonata 18.1 (66) 8.1 (22) 10.2 (56) 13.6 (5) 13.5 (12) 4.7 (32) 4.4 (8) 5 Ischnura senegalensis Sympetrum darwinianum Orthetrum albistylum Sympetrum frequens Orthetrum albistylum Mnais costalis Sympetrum darwinianum 14.0 (51) 7.7 (21) 10.0 (55) 10.9 (4) 11.3 (10) 4.1 (28) 3.8 (7)

The number of 6595575 families The number of 31 23 22 16 14 26 23 species

Density (actual 186.7 (681) 72.6 (198) 91.5 (502) 282.6 (104) 110.4 (98) 52.8 (363) 57.9 (106) number)

1–λ 0.93 0.89 0.90 0.68 0.87 0.90 0.88 in transects 1 and 2, respectively. lowest number of species (14) was found in transect EF, the Dendrograms of Cπ and QS were obtained by using UPGMA lowest density (58 individuals/km) in transect IA&AJ, and the cluster analysis. We calculated Cπ and QS for both adult and lowest diversity index (0.68) in transect DE (Table 4). Large larval assemblages and compared them to assess whether numbers of Orthetrum albistylum were found in all transects differences exist between their distributions. (Table 4). The dominant species observed in individual The relationships between P. clarkii density and the densities, transects were Rhyothemis fuliginosa and Ischnura species richness, and species diversity (1 – λ) of Odonata senegalensis (AB); Pantala flavescens (BC); Sympetrum larvae were analyzed by using Pearson’s correlation analysis. infuscatum and Lyriothemis pachygastra (CD&EG); Lestes To assess the relationship between the changes in species temporalis (DE); Sympetrum parvulum (EF); and Mnais composition and environmental parameters, we categorized costalis (GH). Those species recorded in only one transect or species according to their habitat preference. Based on Inoue census point were Ceriagrion melanurum, Sinictinogomphus (2010b) and Yamamoto et al. (2009), typical larval habitats of clavatus, and Libellula quadrimaculata (AB); Indolestes Odonata species found in this study were classified into three peregrinus (DE); Mnais pruinosa and Mortonagrion selenion patterns: lentic deep water, lentic shallow water, or lotic water. (GH); Asiagomphus pryeri (IA&AJ); and Anaciaeschna Those Odonata species with adults that use forests or forest martini and Polycanthagyna melanictera (Aeshnidae edge were also classified based on Inoue (2010b) and observation). Yamamoto et al. (2009). Odonata larvae Results A total of 503 Odonata larvae comprising 27 species in 8 families were collected in this study (Table 3). The highest Characteristics of the Odonata adult assemblage in the number and density of individuals was found at sampling point study site V, which contained mainly Orthetrum species. The largest A total of 2093 adults, comprising 47 species in 11 families, number of species recorded was at sampling point S, whereas was recorded by both the line-transect and point-census the smallest number of species was observed at sampling methods. The line-transect method yielded a total of 2052 points T and U. The three species Boyeria maclachlani, adults comprising 45 species in 11 families (Table 2), and the Sieboldius albardae, and Macromia amphigena were recorded point-census method yielded a total of 41 adults comprising 4 only as larvae. pecies in 1 family (Table 2). The larval habitat of each species We recorded 337 individuals (mean = 3.9 individuals/netting is also shown in Tables 2 and 3. The highest number of sample) of P. c l a rki i during larval sampling; P. clarkii density individuals (681) was found in transect AB; the highest number was highest at sampling point Z (mean = 11.3 of families (9) in transect CD⪚ the most species (31) and individuals/netting sample). There were no significant the highest diversity index (0.93) in transect AB; and the relationships between Odonata larval density (R = 0.49, P > greatest density (283 individuals/km) in transect DE. The 0.05) or species richness (R = 0.57, P > 0.05) and P. cl a rk ii

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Fig. 2 Relationships between (A) density and (B) species richness of Odonata larvae and density of the crayfish Procambarus clarkii. Data were recorded in netting surveys of Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, between April and November 2012.

water. Among species that use only deep or shallow lentic water, a high proportion were species whose adults use forest and forest edge habitats.

QS and Cπ of adult and larval Odonatan assemblages The QS and Cπ values among the 7 adult survey transects and 10 larval census points are shown in Tables 5 and 6, respectively. The species composition of adult Odonata along transects was separated into two groups at QS = 0.54 (Fig. 4), one having deep and/or open-water species (IA&AJ, AB, and BC) and the other containing species that inhabit water in or near forest (EF, GH, CD&EG, and DE). The population structure of adults along transects was classified into three groups according to Cπ values (Fig. 5). Transects DE and IA&AJ, with poor vegetation environments, were distinguished Fig. 3 Relationship between species diversity of Odonata at Cπ = 0.55 from transects EF, GH, BC, and CD&EG, which larvae and density of the crayfish Procambarus clarkii. are classified as wetland environments. Transect AB along the Data were recorded in netting surveys of Nakaikemi large pond was distinguished from all other transects at Cπ = Marsh, Tsuruga City, Fukui Prefecture, Japan, between 0.45. April and November 2012. The species composition of Odonata larvae formed three groups: a cluster dominated by Orthetrum species (T, U, and density (Fig. 2). However, P. c l a rk i i density did have a W), a lotic species cluster (X and Y), and a deep and/or significant negative effect on species diversity of Odonata (y = open-water species cluster (Q and R; Fig. 6). The population –0.062 x + 0.671, R = 0.653, P < 0.05; Fig. 3). structure of Odonata larvae was classified into four groups: The number of species and density of Odonata species points T, U, V, Z, and W composed a group above Cπ = 0.98; according to larval habitat preferences are shown in Table 5. points R, S, and Q composed a group above Cπ = 0.67; and Among the 39 species whose adults use lentic water, 11 use points Y and X each had a unique assemblage (Fig. 7). only shallow water and 28 can use deep water as well. In the larval survey, we collected two species that use only shallow

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Table 4 Density (no./ 10 netting sample) and actual number (in parentheses) of Odonata larvae and a crayfish, Procambarus clarkii, recorded in netting surveys of Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, between April and November 2012

Survey points QRSTU VWXY ZTotalD/S/L1) Species name /Time of netting 98 97 119 74 68 85 83 72 89 87 872 Les tidae Lestes temporalis 0.94 (8) 0.09 (8) S Calopterygidae Mnais costalis 2.92 (21) 0.24 (21) L Mnais pruinosa 0.42 (3) 0.11 (1) 0.05 (4) L Mnais spp. 2.36 (17) 0.19 (17) L Coenagrionidae Paracercion calamorum 0.21 (2) 0.08 (1) 0.03 (3) D, S Paracercion sieboldii 0.12 (1) 0.01 (1) D, S Ischnura senegalensis 0.20 (2) 0.31 (3) 0.17 (2) 0.08 (7) D, S Ischnura asiatica 0.10 (1) 0.31 (3) 0.08 (1) 0.06 (5) D, S Coenagrionidae spp. 0.31 (3) 1.03 (10) 3.45 (41) 0.62 (54) - Aeshnidae Boyeria maclachlani 0.34 (3) 0.03 (3) L Planaeschna milnei 0.11 (1) 0.01 (1) L Anax parthenope 0.20 (2) 0.72 (7) 0.59 (7) 0.23 (2) 0.21 (18) D Anax nigrofasciatus 0.08 (1) 0.01 (1) D Anax spp. 0.10 (1) 0.31 (3) 0.05 (4) D Sieboldius albardae 0.14 (1) 0.01 (1) L Trigomphus melampus 0.51 (5) 0.52 (5) 0.67 (8) 0.11 (1) 0.22 (19) D, S Asiagomphus pryeri 0.14 (1) 0.45 (4) 0.06 (5) L Asiagomphus melaenops 0.28 (2) 0.02 (2) L Cordulegastridae Anotogaster sieboldii 0.72 (6) 0.69 (5) 4.16 (37) 0.55 (48) L Macromiidae Epophthalmia elegans 0.10 (1) 0.10 (1) 0.02 (2) D Macromia amphigena 0.28 (2) 0.02 (2) L Libellulidae Sympetrum risi 0.17 (2) 0.02 (2) D Sympetrum eroticum 0.12 (1) 0.01 (1) D, S Sympetrum croceolum 0.08 (1) 0.01 (1) D Pseudothemis zonata 0.10 (1) 0.62 (6) 0.67 (8) 0.17 (15) D Deielia phaon 0.08 (1) 0.01 (1) D Crocothemis servilia 0.34 (4) 0.05 (4) D, S Orthetrum albistylum 1.02 (10) 0.52 (5) 1.34 (16) 2.97 (22) 0.15 (1) 1.65 (14) 3.37 (28) 1.24 (11) 1.38 (12) 1.36 (119) D, S Orthetrum japonicum 0.41 (3) 0.74 (5) 0.48 (4) 0.46 (4) 0.18 (16) S Orthetrum melania 0.14 (1) 0.15 (1) 0.24 (2) 1.08 (9) 0.22 (2) 0.69 (6) 0.24 (21) D, S Orthetrum spp. 0.14 (1) 4.41 (30) 7.06 (60) 0.48 (4) 0.23 (2) 1.11 (97) - Odonata total 2.65 (26) 4.64 (45) 7.82 (93) 3.65 (27) 5.44 (37) 10.12 (86) 6.14 (51) 7.22 (52) 6.63 (59) 3.10 (27) 5.77 (503) 1-λ 2） 0.78 0.76 0.72 0.00 0.00 0.21 0.21 0.73 0.57 0.21 Procambarus clarkii 3.60 (35) 1.40 (14) 1.30 (15) 4.30 (32) 8.40 (57) 2.60 (22) 4.50 (37) 0.70 (5) 2.40 (21) 11.40 (99) 3.85 (337) 1) Typical larval habitat based on Inoue (2010b) and Yamamoto et al. (2009): D, lentic deep water; S, lentic shallow water; L, lotic water. 2) calculated the which includes spp. as 1 species.

Table 5 Number of species and density of Odonata sp ecies which have different larval habitat preferences summerized from Tables 2 and 4.

Lentic water Deep Shallow Both deep and shallow Lotic water Total Adult No. species 13 (7)2) 11 (9) 15 (6) 7 (5) 46 (27) Density 13.4 (10.5) 25.9 (22.9) 48.6 (10.1) 4.0 (3.4) 91.9 (46.1)

Larva1)

No. species 7 (5) 2 (2) 9 (3) 9 (7) 27 (19)

Density 0.51 (0.48) 0.28 (0.28) 2.06 (0.26) 1.19 (1.11) 4.05 (2.13) 1) Larvae of Coenagrionidae spp. and Orthetrum spp. are excluded because several types of species could be included. 2) Numbers in parenthes are numbers or density of species in which adults inhabit forests or forest edge.

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Table 6 Values for QS (above diagonal) and Cπ (below diagonal) among seven adult odonatan survey transects

Cπ ＼QS AB BC CD/EG DE EF GH IA/AJ AB - 0.75 0.49 0.43 0.44 0.60 0.78 BC 0.50 - 0.64 0.54 0.61 0.67 0.76 CD/EG 0.41 0.82 - 0.70 0.67 0.71 0.53 DE 0.31 0.53 0.46 - 0.62 0.63 0.47 EF 0.27 0.77 0.75 0.47 - 0.55 0.49 GH 0.45 0.71 0.78 0.45 0.46 - 0.61 IA/AJ 0.67 0.74 0.56 0.71 0.49 0.67 -

Table 7 Values for QS (above diagonal) and Cπ (below diagonal) among 10 larval survey points

Cπ ＼QS QRSTUVWXYZ

Q - 0.94 0.40 0.22 0.22 0.17 0.20 0 0.14 0.36 R 0.69 - 0.76 0.20 0.20 0.15 0.18 0 0.13 0.50 S 0.31 0.81 - 0.15 0.15 0.13 0.14 0 0.11 0.40 T 0.63 0.19 0.28 - 1.00 0.40 0.67 0 0.29 0.50

U 0.63 0.19 0.28 1.00 - 0.40 0.67 0 0.29 0.50 V 0.67 0.21 0.29 0.99 0.99 - 0.33 0 0.20 0.29 W 0.67 0.21 0.29 0.98 0.98 0.98 - 0.25 0.50 0.40 X0000000.02-0.500.00

Y 0.25 0.08 0.11 0.30 0.30 0.31 0.44 0.14 - 0.22 Z 0.69 0.25 0.31 0.99 0.99 0.99 0.99 0 0.31 -

Discussion

Prior to this study, 72 Odonata species in 11 families have been recorded in Nakaikemi Marsh (Nakamoto et al., 2003; Wada, 2003; Fujino and Wada, 2011). We recorded adults and larvae of 50 species in 11 families. Among the 72 species recorded in the past, 18 were considered to be accidentally recorded species, those flying from distant habitats, or both. For 23 species we found both larvae and adults in this study, for 24 we found only adults, and for 4 we found only larvae. The four species for which we found only larvae (Boyeria Fig. 4 Dendrogram showing the result of UPGMA cluster maclachlani, Sieboldius albardae, Asiagomphus melaenops, analysis based on QS index among adult odonatan fauna in and Macromia amphigena) are all lotic species. Although more Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, in species were recorded in the adult survey than in the larval 2012. survey, some of the adults were thought to come from other habitats. In the larval survey, the breeding of species in the study site could be confirmed, but some genera such as Anax, Mnais, and Orthetrum were difficult to identify to the species level. Although the larval habitat of species such as Pseudothemis zonata, Anax nigrofasciatus, and Asiagomphus melaenops were restricted in the marsh, adults of these species

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had wider ranges. These differences in the distributions of adults and larvae were the result of dispersal by adults and different environmental preferences. Adults and a larva of S. croceolum, first recorded in the marsh in 2011 (Fujino and Wada, 2011), were found at the Sasahana Pond site in our study. This species prefers ponds in hilly areas with woods (Inoue and Tani, 1999). Wada (2000) noted that R. fuliginosa and I. senegalensis numbers were increasing around the Sasahana Pond, and both species were abundant in that location in our study. We attribute the population increases of S. croceolum, R. fuliginosa, and I. senegalensis to the formation of the Sasahana Pond. Aeschnophlebia longistigma, A. anisoptera, and Fig. 5. Dendrogram showing the result of UPGMA cluster Nannophya pygmaea, which prefer wetlands with analysis based on Cπ index among adult odonatan graminaceous plants, were present in the early 1990s (Wada, assemblages in Nakaikemi Marsh, Tsuruga City, Fukui 1995), but were not observed in our study. A few specimens of Prefecture, Japan, in 2012. Sympetrum kunckeli were observed in 1994 and 2001 (Wada,

2003) and those of Somatochlora uchidai in 1996, 2001 (Sasaji

and Kishimoto, 1996; Wada, 2003), and 1998–2002 (Nakamoto

et al., 2003); however, these species were not recorded during

our study. Other than these five species, the species structure at

the marsh was similar to that observed 10 years before. Kadoya

et al. (2009) noted that Japanese lentic dragonfly species that

depend on paddy fields have extensively decreased, whereas

lotic species have not. In this study, all five unrecorded taxa

are lentic species as well.

According to our cluster analyses, the population structure

Fig. 6. Dendrogram showing the result of UPGMA cluster of adult Odonata along transects was classified into three analysis based on QS index among larval odonatan fauna in groups: poor vegetation, wetland, and pond environment. The Nakaikemi Marsh, Tsuruga City, Fukui Prefecture, Japan, in assemblage recorded in transect AB, which goes along 2012. Sasahana Pond, is singular and was not seen in the past. The

cluster analyses of larval Odonata indicate that the species’

habitat types clearly correspond to water types. For example,

survey points Q, R, and S located near Sasahana Pond contain

species that prefer deep water and are to close each other in the

dendrogram.

According to Wada (1995), Nakaikemi Marsh comprised

various types of wetlands with tall and low vegetation, paddy

fields, and waterways, and Odonata species that prefer

wetlands with low vegetation (e.g., N. pygmaea and M.

selenion) could be found there. Kadoya et al. (2009) also noted

the significance of habitat complexes maintained in rice paddy

systems. However, in our study, the marsh was covered with

tall vegetation like S. altissima and Poaceae species. Solidago Fig. 7. Dendrogram showing the result of UPGMA cluster altissima, which is designated as an invasive alien species analysis based on Cπ index among larval odonatan assemblages in Nakaikemi Marsh, Tsuruga City, Fukui (Ministry of the Environment, 2017a) and one of the worst 100 Prefecture, Japan, in 2012. invasive foreign species in Japan (Murakami and Washitani, 2003), was first found in the marsh in 1997. This species grows

- 9 - Hirai et al primarily in areas with a low water table (Ikegami et al., 2011). needed in the marsh, especially to eliminate tall vegetation. By We found it widely distributed throughout the marsh, controlling water levels of waterways and Sasahana Pond, particularly along the western edge near the bypass highway suitable wetlands can be reestablished that Odonata adults can where little water remained. Most aquatic insects, including recognize and Odonata populations can be conserved while Odonata species, are thought to find their habitat by using the controlling invasive alien species. polarization of the reflectance of light from water surfaces (Schwind, 1991; Corbet, 1999); the presence of tall vegetation Acknowledgements such as S. altissima and Phragmites australis throughout the marsh obscures suitable oviposition sites from Odonata adults. We are grateful to the members of Nakaikemi Net NPO for Procambarus clarkii is also designated as an invasive alien their kind help. We thank Mr. Shigeki Wada for providing species (Ministry of the Environment, 2017b) and one of the literature. We are also indebted to the Tsuruga City government worst 100 invasive foreign species in Japan (Murakami and for permission to conduct this study and funding. Washitani, 2003). Although P. clarkii can be a major food source for waterbirds (Montesinos et al., 2008), the crowded References vegetation of the marsh makes it difficult for birds to find them. Populations of P. clarkii impact multiple levels of food webs, Corbet, P. S. (1962) A Biology of . H. F. & G. disrupting natural prey–predator relationships by preying on Witherby, London. the larvae of amphibians and aquatic insects, including Corbet, P. S. (1999) Dragonflies, Behavior and Ecology of Odonata species (Ficetola et al., 2012), and damaging rare Odonata. Cornell University Press, New York. plant species in the marsh like Hydrocharis dubia and Trapa Ficetola, G. F., M. E. Siesa, F. De Bernardi and E. incisa (Shimoda, 2003). Fukui (2010) also reported that the Padoa-Schioppa (2012) Complex impact of an invasive introduction of P. clarkii caused the decline of a variety of crayfish on freshwater food webs. Biodivers. Conserv. 21: Odonata species. In this study, we observed a significant 2641–2651. negative effect of P. clarkii density on the species diversity of Fujino, Y. and S. Wada (2011) Records of Sympetrum Odonata larvae. Since the introduction and subsequent croceolum (Selys, 1883) (Odonata: Libellulidae) at population increase of P. clarkii in Nakaikemi Marsh, A. Nakaikemi Marsh, Tsuruga, Fukui Prefecture, Japan. longistigma or A. anisoptera have not been recorded (Tsubaki Bulletin of the Fukui City Museum of Natural History and Kawano, 2003), nor were these species found in our study. (58): 65–66 (in Japanese). The abandonment of paddy field cultivation allowed for natural Fukui, J. (2010) Conservation of a dragonfly, Libellula succession to occur, and caused a decrease in the Odonata angelina at the Okegaya Pond, Shizuoka Prefecture, Japan. species A. longistigma, A. anisoptera, Nannophya pygmaea, In “Decline and conservation of Japanese Insects” (Ishii, and Mortonagrion selenion; which prefer to inhabit shallow M. ed), pp. 135–142. Hokuryukan, Tokyo (in Japanese). wetlands with short graminaceous vegetation. Conversely, Hoshina, H., H. Uomi, M. Terashima and C. Yamada (2007) Odonata species that prefer deep ponds, such as Rhyothemis Notes on aquatic insects inhabiting Nakaikemi Wetland, fuliginosa, Ischnura senegalensis, and Sympetrum croceolum, Tsuruga City, Fukui Pref., Honshu, Japan. Nature and increased around the newly formed large artificial Sasahana environment of the Sea of Japan districts (14): 1–16 (in Pond, where species richness and diversity were highest in Japanese). Nakaikemi Marsh. In the Ushirodani Valley where traditional Ikegami, Y., J. Nishihiro and I. Washitani (2011) Vegetation of methods are used to maintain paddy fields, Odonata species abandoned rice fields in the head areas of small valley richness and diversity were second highest and we found some bottoms (‘yatsu’) in the Lake Kitaura watershed, Ibaraki, endangered species. Japan. Jpn. J. Conserv. Ecol. 16: 1–15 (in Japanese with Kadoya and Washitani (2007) proposed an adaptive English summary). management scheme for wetland restoration by using Inoue, K. (2010a) Bio-indicator. In “Survey manual of dragonflies as indicator taxa. To restore Odonata diversity in Odonata” (Japanese Society of Environmental the Nakaikemi Marsh, management practices that imitate the Entomology and Zoology, ed), pp. 233–235, Bunkyo rice paddy system are needed across a wider range of the area. Shuppan, Osaka. If possible, appropriate artificial management methods are Inoue, K. (2010b) Distribution and biology of and

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福井県中池見湿地におけるトンボ類の種多様性

平井規央＊・森岡賢史・石井 実 大阪府立大学大学院生命環境科学研究科

福井県敦賀市の中池見湿地は多くの希少種を含む多様な動植物がみられることなどから， 2012 年にラムサール 湿地に登録された．しかし，1990 年代の水田放棄以降は環境が大きく変化した．本研究では，2012 年 4 月から 11 月にトンボ類成虫のルートセンサス法，幼虫のすくい採り，ヤンマ類の定点調査により種多様性を把握する調 査を行った．その結果，50 種のトンボ類を確認した．成虫は 47 種 2,093 個体，幼虫は 27 種 503 個体であった． 過去に記録された種の多くは確認されたが，1990 年初頭に安定して発生したとされる，アオヤンマ，ネアカヨシ ヤンマ，ハッチョウトンボは確認できなかった．逆に，池沼を好むとされるアオモンイトトンボ，チョウトンボ， キトンボは増加したと考えられる．重複度 Cπ を用いた群集解析では，近年形成された笹鼻池周辺で特異となっ た．現在の中池見湿地においては，笹鼻池がトンボ類にとって主要な生息地となっていることが明らかとなった． 水田を模した管理がなされているうしろ谷では，種数と個体数が 2 番目に高く希少種も発見された．湿地に侵入 し，拡散したセイタカアワダチソウやアメリカザリガニのような外来種も在来の水生動植物に悪影響を与えてい ると考えられた．特に，トンボ類の幼虫の多様度に関しては，アメリカザリガニの密度との間に負の相関が認め られた．

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