Appl. Entomol. Zool. 38 (4): 449–459 (2003)

Ground (Coleoptera: Carabidae) and other predators overwintering in arable and fallow fields in central Japan

Kazuo YAMAZAKI,1,* Shinji SUGIURA2 and Koji KAWAMURA2 1 Osaka City Institute of Public Health and Environmental Sciences; Tennoji, Osaka 543–0026, Japan 2 Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University; Kyoto 606–8502, Japan (Received 5 February 2003; Accepted 26 May 2003)

Abstract To clarify assemblage patterns of overwintering ground beetles (Coleoptera: Carabidae) and other insect predators in farmland habitats for the purpose of proper land management to enhance beneficial predators, we collected carabid and other insect predators at eight plots including arable and fallow rice and vegetable fields and a bank of an adjacent irrigation pond in central Japan. In total, 159 adults and 268 larvae of 33 carabid species, and 178 individuals of at least 17 species of other insect predators were collected by the quadrat sampling method. In rice fields, both the num- ber of species and no. of individuals of overwintering carabid beetles increased as the soil became dry and vegeta- tional succession proceeded, whereas in fallow vegetable fields carabids decreased according to succession. Similar trends were confirmed in other insect predators. Variations of carabid species richness and abundances among the plots might be attributed to soil water content, vegetation and prey availability. In early-successional fallow vegetable fields, the larvae of the carabid Harpalus overwintered with high density; this appeared to be because the fin- gergrass Digitaria ciliaris (Poaceae), whose seeds were a potential food for Harpalus, were densely vegetated there. In a dry fallow rice field and early-successional vegetable fields, beneficial predators such as Dolichus halensis (Coleoptera: Carabidae), Agrypnus binodulus (Coleoptera: Elateridae), and soldier (Coleoptera: Cantharidae) larvae hibernated with high densities. For proper farmland management to augment insect predators, it is desirable to maintain fallow rice and vegetable fields as relatively dry habitats and at early successional stages. Ploughing fallow fields in winter may reduce overwintering predacious insect larvae.

Key words: Carabidae; hibernation; beneficial predators; pest control; habitat preference

and Marshall, 1999; Pfiffner and Luka, 2000). INTRODUCTION Some studies have shown that predatory epigaeic In agroecosystems, polyphagous beneficial ar- which had overwintered in field margins thropod predators such as carabid and staphylinid emigrated into adjacent farmland in spring beetles and spiders can efficiently reduce the popu- (Coombes and Sotherton, 1986; Thomas et al., lations of some pest insects and slugs (Best and 1991, 2002). However, these studies were restricted Beegle, 1977; Edwards et al., 1979; Chiverton, to cereal and forage crop fields in Europe and 1986; Clarke et al., 1994; Kromp, 1999). Thus, North America (Kromp, 1999). emphasis has recently been placed on studies to In Japan and other temperate Asian regions, rice, create and manage farmland habitats for augmenta- vegetables and fruits are intensively cultivated on tion of such beneficial predators (Thomas et al., narrow plains and foothill areas of mountains. 1991; Lys and Nentwig, 1992; Lys et al., 1994; Farmland management practices in Japan are dif- Kromp, 1999). These studies indicate that field ferent from those in Europe and North America. margins and semi-natural habitats with dense vege- Assemblages of carabids and other predators in tation harbor high abundance and species richness Japan thus may be distinct from those in other of beneficial predators. These habitats not only world areas, although Luff (2002) compared the support feeding and reproductive activity but also carabid assemblages of various world farmlands in- function as overwintering refuges for the predators cluding Japan mainly at the genus level and dis- (Desender, 1982; Sotherton, 1984, 1985; Thomas cussed how dominant genera were common among

* To whom correspondence should be addressed at: E-mail: [email protected]

449 450 K. YAMAZAKI et al. temperate world farmlands. Therefore, in order to gation ponds in central Japan. Firstly, assemblages use carabid beetles and other beneficial predators of carabids and other predators in each habitat are as biological control agents in Japan, the assem- described, and the habitats with high abundance blage patterns in each habitat and habitat prefer- and species richness of the predators are explored. ences of component species should be clarified. Similarities between assemblages are also ana- In Japan, Habu and Sadanaga (1961, 1963, lyzed. Overwintering developmental stages and 1965, 1969, 1970a, b, 1971) described larval mor- breeding seasons of the sampled carabid beetles phology of carabid beetles and noted their biology are compared among habitats. Then, habitat prefer- in cultivated fields and paddy fields based on labo- ences for beneficial species are examined, and in ratory rearings. Carabid assemblages and faunae turn land management practices to enhance benefi- have been described from paddy fields, forage crop cial insect predators against pest insects in Japa- field, cabbage field, fig orchards and vineyards dur- nese agroecosystems are discussed. ing the warm season using pitfall-trapping (Torii, 1974; Yano et al., 1989, 1995; Yahiro et al., 1992; MATERIALS AND METHODS Ishitani et al., 1994; Ishitani and Yano, 1994; Ishi- tani, 1996; Suenaga and Hamamura, 2001; Yano, Study site. The study site was located in a rural 2002). Yahiro and Yano (1997) reported long-term area of Son-enji (34°48ЈN, 135°43ЈE, ca. 100 m data on a carabid assemblage caught by a light trap above sea level), Hirakata City, Osaka Prefecture, set at a farmland area which comprised rice, cereal central Japan (Fig. 1). The landscape of this area is and vegetable fields, orchards and irrigation ponds. well preserved, comprising mosaics of coppice However, in Asia including Japan, no quantitative woodlands, rice and vegetable fields, irrigation study on overwintering carabid assemblages in ponds and streams, and therefore relatively rare farmland and adjacent semi-natural habitats has plants and insects that prefer grassland and marsh- been reported. Quantitative assemblage data of hi- land habitats were still extant (Kankyô-kagaku Co., bernating carabids and other insect predators in 2001). There were many arable and fallow rice and each farmland habitat is useful to create and man- vegetable fields at the study site. Fallow fields were age overwintering refuges for the predators. at various successional stages. These farmlands Carabid life-cycle patterns (breeding season and were surrounded by secondary forests composed hibernating developmental stage) vary across cli- mainly of the Japanese red pine Pinus densiflora matic regions and habitats (Murdoch, 1967; Paar- and the oak Quercus serrata. mann, 1979; Andersen, 1984). However, the life Overwintering ground beetles and other insect cycles of most carabid species excluding the tribe predators were sampled at the following eight plots Carabina are not well known in Japan (for Cara- which were within a 1 km2 area. Table 1 shows the bina see Sota, 1985). Collecting ground beetles in environmental conditions of sampling plots. Age winter helps to elucidate their life cycles, espe- after cultivation in each plot was estimated by con- cially their hibernating stages. Information on life sulting with farmers and based on vegetational suc- cycles of beneficial carabid species may be essen- cession. Vegetational succession advanced from A tial for proper land-management practices to aug- to C in rice fields, and from D to G in vegetable ment those already in use; In Europe, deep plough- fields. ing during autumn or winter is known to reduce the Methods. We arbitrarily set three quadrats numbers of overwintering carabid beetles and other (1.6 mϫ1.6 m) per plot on the ground except the predators (Kromp, 1999; Pfiffner and Luka, 2000). two plots (D: 2 quadrats and F: 1 quadrat), that This negative effect to carabids may be severe for were unfortunately ploughed while sampling. All hibernating larvae compared with overwintering the quadrats except the bank of an irrigation pond adults, since the larvae appear to be more vulnera- were set on relatively flat and horizontal ground. ble to physical disturbance than the adults. Ground inclination of three quadrats on the pond In the present study, we sampled overwintering bank was ca. 50°. We then dug up each quadrat to a carabid beetles and other insect predators in arable depth of 40 cm using hoes, and inspected the soil and fallow fields (rice and vegetables) with differ- thus obtained for ground beetles and other insect ent successional stages and a bank of adjacent irri- predators (see Yamazaki et al., 1999, 2002). The Overwintering Ground Beetles in Rice and Vegetable Fields 451

Fig. 1. Study site of the ground beetles and other insect predators overwintering in farmland habitats. A to H denote sampling plots.

Table 1. The environmental conditions of sampling plots

Years after Plots Land use Dominant plants abandonment

A Arable rice field — Astragalus sinicus (Leguminosae), grasses B Wet fallow rice field 1 Oenanthe javanica (Umbelliferae), Stellata sp. (Caryophyllaceae) C Dry fallow rice field 1 Erigeron canadensis (Asteraceae), A. sinicus

D Fallow vegetable field 1 0.5 Digitaria ciliaris (Poaceae), E. canadensis E Fallow potato field 1 D. ciliaris F Fallow vegetable field 2 1 Solidago altissima, Artemisia indica var. maximowiczii (Ateraceae) G Old fallow field Ͼ3 Miscanthus sinensis, Pleioblastus fortunei (Poaceae)

H Bank of irrigation pond — Mostly bare ground

sampling was conducted between December 1999 test was also used to clarify the difference. Plots D and March 2000 and in March 2001. As to ants, and F were excluded from these analyses due to the only queens were caught because of the difficulty lack of an adequate data set. The similarities and the labor intensity required for sampling work- among assemblages were compared using Ward’s ers. In the present study, we focused on epigaeic minimum-variance clustering method. Prior to the and soil macro-predators, but did not examine one-way ANOVA and cluster analysis, the no. of predators on plant surfaces such as lacewings and individuals was logarithmically transformed. Over- syrphids and other micro-predators. The collected wintering developmental stages and breeding sea- carabid larvae were identified according to the de- sons in carabids were compared among the plots. scriptions of Habu and Sadanaga (1961, 1963, Breeding seasons were determined on the basis of 1965, 1969, 1970a, b, 1971) and our collections the descriptions by Kurosa (1959), Habu and (Yamazaki et al., 1999, 2002). Sadanaga (1961, 1963, 1965, 1969, 1970a, b, The abundance and species richness of carabid 1971), Sota (1985) and Ishitani (1996). Chi-square beetles and other predators per quadrat were com- test was used to ascertain whether the percentage pared among the sampling plots. A one-way (no. of individuals) of larvae and autumn-breeders ANOVA model was used to compare the number of differed among the plots. species and abundance among the plots in carabid beetles and other predators, and Scheffé’s range 452 K. YAMAZAKI et al.

species (66.0% of all the predator species) that RESULTS were collected. The collected carabid beetles con- Overview of predator assemblages sisted of 159 adults (37.2%) of 27 species and 268 In a total of eight plots, 605 individuals of cara- larvae (62.8%) of nine species (Table 2). In addi- bid beetles and other insect predators belonging to tion, one adult and 63 larvae (36.0% of all other at least 50 species were collected by the quadrat predators) of four click beetle species (Elateridae) sampling method. Among them, carabid beetles were sampled, and 47 larvae (26.4%) of several predominated in the assemblage, with 427 individ- soldier beetle species (Cantharidae) and 26 adults uals (70.6% of all the predators) belonging to 33 and four larvae (16.9%) of five rove beetle species

Table 2. Collected carabid beetles overwintering at eight plots of arable and fallow fields. Numbers without and in parentheses are adults and larvae, respectively. — denotes none found.

Plot Breeding Carabid species Rice fields Vegetable fields Pond Total seasona ABCDEFGH

Carabus yaconinus yaconinus Bates S — — — — — — — 1 1 Leptocarabus kumagaii Komiya et Kimura A — — (5) — — — — — (5) Scarites terricola pacificus Bates S — — — — — 3 — — 3 magnus (Motschulsky) S — — 1 — — — — — 1 Pterostichus sulcitarsis Morawitz S — — — — — 2 — — 2 P. haptoderoides japanensis Lutshnik A — — 10 3 — — — — 13 P. longinquus Bates S 1 23 — 1 — — — — 25 P. microcephalus (Motschulsky) S — — 2 — — — — — 2 Agonum chalcomus (Bates) ? 2 3 3 — — — — — 8 Colpodes japonicus (Motschulsky) ? 1 — — — — — — — 1 Dolichus halensis (Schaller) A — — (1) (6) (8) (1) — — (16) Amara congrua Morawitz S — — 15 — — 3 — — 18 Am. chalcites Dejean S — — 12 — — — 1 — 13 Anisodactylus signatus (Panzer) S — 1 1 2 13 — — — 17 An. puctatipennis Morawitz S — — — — — — 1 — 1 ?Harpalus vicarius Harold A — — — — — (18) — — (18) H. jureceki (Jedlicˇka) A — — — (3) (2) 2 — 1 3(5) H. griseus (Panzer) A — — — — (5) (2) — — (7) H. tridens Morawitz A — — — (13) (13) — — — (26) H. sinicus Hope A — — — (75) (14) 3 — — 3(89) H. niigatanus Schauberger A — — 1(2) (7) (92) — — — 1(101) H. chalcentus Bates S — — 5 — — 8 — — 13 Oxycentrus argutoroides (Bates) ? — — — — — — — 3 3 Trichotichnus congruus (Motschulsky) ? — — — — 1 — — — 1 T. noctuabundas Habu ? — — — — — — — 1 1 Bradycellus subditus (Lewis) ? — — 13 — — — — — 13 B. grandiceps (Bates) ? — — — — — 6 — — 6 inornatus Bates S — 1 — — — — — — 1 Stenolophus iridicolor Redtenbacher S — 5 — — — — — — 5 S. fulvicornis Bates S — — — — — — 1 — 1 Anoplogenius cyanescens (Hope) S — — — — — — 2 — 2 Chlaenius naeviger Morawitz S — — — — — — — 1 1 Carabidae Gen. sp. ? — (1) — — — — — — (1)

Total 4 33(1) 63(8) 6(104) 14(134) 27(21) 5 7 159(268)

a S: spring, A: autumn. Breeding seasons of each species were determined based on Kurosa (1959), Habu and Sadanaga (1961–1971), Sota (1985) and Ishitani (1996). Overwintering Ground Beetles in Rice and Vegetable Fields 453

Table 3. Collected insect predators except Carabidae at eight plots of arable and fallow fields. Numbers in and without parentheses are adults and larvae, respectively. — denotes none found.

Plot

Predator species Rice fields Vegetable fields Pond Total

ABCDE FGH

Histeridae Atholus pirithous (Marseul) — — 1 — — — — — 1 Staphylinidae Olophrum arrowi Scheerpeltz — — — 1 — — — — 1 Paederus fuscipes (Curtis) — 17 — — — — — — 17 Lathrobium unicolor Kraatz — — — 1 — — — — 1 Tachyporus celatus Sharp — — 1 1 1 3 — — 6 Aleochara sp. — — 1 — — — — — 1 Staphylinidae Gen. sp. — — (2) — — (1) (1) — (4) Elateridae Agrypnus binodulus (Motschulsky) — — (23) — (35) — — — (58) Ampedus sp. — — — — — — (2) — (2) Melanotus cete Candeze — — — — — — 1 — 1 Melanotus sp. — — — — (1) — (2) — (3) Cantharidae Cantharidae Gen. spp. (1) (7) (6) — (28) (4) (1) — (47) Coccinellidae Coccinella septempunctata L. — — 3 — — — — — 3 Formicidae Crematogaster osakensis Forela — — 10 — 5 — — — 15 Vespidae Vespa tropica pulchra Buyssona ———————2 2 Reduviidae Peirates turpis Walker — — — — — 1 — — 1 Gryllotalpidae Gryllotalpa orientalis Burmeister 1 (2) (5) — — 1 — — 2(7) Anisolabididae Euborellia plebeja (Dohrn) — — 6 — — — — — 6

Total 1(1) 17(9) 22(36) 3 6(64) 5(5) 1(6) 2 57(121) No. of quadrats 3 3 3 1 3 2 3 3 21

a Queens.

(Staphylinidae) were also collected (Table 3). vegetable fields (plots D–G), there was a tendency for overwintering carabid beetles to decrease as Assemblage patterns according to vegetational succession proceeded: The no. of species was simi- succession lar among plots D–F, but plot G harbored a small The number of species and the no. of individuals number of carabid species (Fig. 2a). The no. of in- of carabids per quadrat were significantly different dividuals decreased according to vegetational suc- among the sampling plots (one-way ANOVA, cession (Fig. 2b). species number, dfϭ5, Fϭ6.24, pϽ0.01; no. of in- The number of species and the no. of individuals dividuals, dfϭ5, Fϭ17.73, pϽ0.0001) (Fig. 2). In of predators other than carabids per quadrat were rice fields (plots A–C), both the no. of species and also significantly different among the sampling individuals of carabids increased, from arable A to plots (one-way ANOVA, species number, dfϭ5, C (one year old fields), as the soil became dry and Fϭ4.96, pϽ0.05; No. of individuals, dfϭ5, succession proceeded. On the other hand, in fallow Fϭ7.20, pϽ0.01) (Fig. 3). In rice fields, both 454 K. YAMAZAKI et al.

Fig. 2. Carabid species number and abundance at eight plots of arable and fallow fields. (a) Species number per quadrat, (b) No. of individuals per quadrat. MeansϮ1SE. Different alphabetical letters above the bars indicate statistical difference at pϽ0.05 level of significance by Scheffé’s range test. Before analysis, no. of species and individuals were logarithmically transformed.

Fig. 3. Species number and abundance of insect predators other than carabid beetles at eight plots of arable and fallow fields. (a) Species number per quadrat, (b) No. of individuals per quadrat. MeansϮ1SE. Different alphabetical letters above the bars indi- cate statistical difference at pϽ0.05 level of significance by Scheffé’s range test. Before analysis, no. of species and individuals were logarithmically transformed. species richness and abundance of the other preda- Predator assemblages at eight plots tors increased with succession, similar to the case Predator assemblage patterns at each plot are of carabid beetles. In vegetable fields, although the briefly described as follows (Tables 2, 3): (A) The abundance of the other predators was high at plot E arable rice field harbored very small numbers (fallow potato field) (Fig. 3b), the no. of species of insect predators (Figs. 1, 2); (B) Wet fallow and abundance were similar among the other plots. rice field: A hygrophilous carabid, Pterostichus Among the eight plots, the average number of longiquus was the dominant species (23 individu- species of the other predators per quadrat was sig- als, 67.6% of carabid individuals), and Acupalpus nificantly correlated to that of carabids (Spear- inornatus, Stenolophus iridicolor and Paederus man’s correlation coefficient by rank test, Nϭ8, fuscipes were found only from this plot; (C) Dry rsϭ0.79, pϽ0.05) (Figs. 2a, 3a), although the aver- fallow rice field: Carabid (71 individuals of 12 age no. of individuals of other predators per species), staphylinid (four individuals of three quadrat was marginally correlated to that of cara- species) and elaterid beetles (23 Agrypnus binodu- bids (Spearman’s correlation coefficient by rank lus larvae) were relatively dominant, and Lepto- test, Nϭ8, rsϭ0.64, pϭ0.08) (Figs. 2b, 3b). This carabus kumagaii, Bradycellus subditus and the finding suggested that habitat preferences in cara- earwig Euborellia plebeja were specific to the plot. bids and other predators were similar. Two carabid species of the genus Amara were Overwintering Ground Beetles in Rice and Vegetable Fields 455

Fig. 4. Dendrograms showing the assemblage similarities of (a) carabid and (b) other insect predators hibernated at eight plots in arable and fallow fields. Ward’s minimum-variance clustering method was applied. Prior to clustering, no. of individuals was logarithmically transformed. A–C: rice fields, D–G: vegetable fields, H: pond bank. abundantly collected (27 individuals); (D) Fallow stages and breeding seasons in the collected cara- vegetable field 1: This plot was characterized by bid beetles at each plot. In rice fields (A–C), there the high abundance of Harpalus larvae (98 individ- was a tendency for the percentage of the no. of uals of four species). (E) Fallow potato field: Cara- species and individuals of larvae that overwintered bid (148 individuals of eight species), elaterid (36 to increase somewhat from arable (A) to fallow (B) individuals of two species) and cantharid beetles and (C). In vegetable fields (D–G), as to both no. (28 individuals) were abundant. Larvae of five of species and individuals however, the percentage Harpalus species occurred with high density simi- of larvae that hibernated decreased markedly and lar to plot D; (F) Fallow vegetable field 2: The the percentage of adults increased with vegeta- carabids Scarites terricola pacificus, P. sulcitarsis tional succession. Plots D and E had many over- and B. grandiceps were found only in this plot; (G) wintering Harpalus larvae (cf. Table 2). From the Old fallow field: The abundance of predators was pond bank (H), a small number of adults was very low (Figs. 2, 3), but two species of the carabid found. genus Stenolophus were only in this plot; (H) Bank With regard to breeding seasons, in the dry fal- of irrigation pond: Both species richness and abun- low rice field (C), autumn-breeders were found, dance of predators were very low (Figs. 2, 3). Sil- while in both the arable rice field (A) and wet fal- vicolous species, Carabus yaconinus yaconinus, low rice field (B), no autumn-breeders were col- Chlaenius naeviger and the hornet Vespa tropica lected. In fallow vegetable fields (D–G), with re- pulchra were sampled. gard to both the no. of species and individuals, the percentage of autumn-breeders decreased and the Similarities among assemblages percentage of spring-breeders tended to increase as Dendrograms of Fig. 4 show the similarities succession proceeded. A small number of adult among the assemblages of the plots in carabids and carabids collected at the pond bank (H) comprised other predators, respectively. For carabid assem- both spring- and autumn-breeders. blages, the fallow field plots D and E were similar, but three rice field plots (A–C), especially the dry DISCUSSION fallow rice field (C), were distinct from each other (Fig. 4a). For other predator assemblages, the Assemblage patterns according to vegetational arable rice field (A) and the bank of the pond (H) succession were similar, possibly due to the small number of In this study, we could not examine arable veg- predators sampled (Figs. 2, 3). The dry fallow rice etable fields and old rice fields, and our sampling field (C) bore a distinct assemblage of insect preda- was restricted to only eight plots. Therefore, the tors from other plots (Fig. 4a). findings presented in this paper are snapshots of overwintering predators in farmland. The present Overwintering developmental stages and breed- results may, however, reflect some important as- ing seasons in sampled carabids semblage patterns during vegetational succession Table 4 shows the overwintering developmental in farmlands. In rice fields (from A to C), overwin- 456 K. YAMAZAKI et al.

Table 4. Overwintering developmental stages and breeding seasons of carabid beetles collected at eight plots of arable and fallow fields

Plot

Rice fields Vegetable fields Pond Total

ABCDEFG H

Overwintering stages No. of species Adults 3 583274 524 Larvae0 125630 0 6 Adults/larvae 0 010000 0 3 Total 3 6 11 8 8 10 4 5 33 Larvae (%) 0.0 16.7 18.2 62.5 75.0 30.0 0.0 0.0 18.2 No. of individuals Adults 4 33 63 6 14 27 5 7 159 Larvae 0 1 8 104 134 21 0 0 268 Total 4 34 71 110 148 48 5 7 427 Larvae (%)a 0.0 ab 2.9 a 11.3 a 94.5 c 90.1 c 43.8 b 0.0 ab 0 ab 62.8 Breeding seasons No. of species Spring 1 462144 216 Autumn 0 046150 1 9 Unknown 2 220610 2 8 Autumn (%) 0.0 0.0 33.3 75.0 12.5 50.0 0.0 20.0 27.3 No. of individuals Spring 1 30 36 3 13 16 5 2 106 Autumn 0 0 19 107 134 26 0 1 287 Unknown 3 4 160160 434 Total 4 34 71 110 148 48 5 7 427 Autumn (%)b 0.0 abc 0.0 a 26.8 b 97.3 d 90.5 d 54.2 c 0.0 abc 14.3 abc 67.2

a The percentages of larval stage differed among plots (chi-square test, dfϭ7, c 2ϭ263.4, pϽ0.0001). b The percentages of autumn breeders differed among plots (chi-square test, dfϭ7, c 2ϭ23.51, pϽ0.0001). a, b The values with different alphabetical letters are significantly different (sequential Bonferroni test (Rice, 1989), aϭ0.05). tering carabid beetles increased as the soil became mocks for overwintering. In Europe, high densities dry and vegetational succession proceeded, while of overwintering carabids and other predators have in fallow vegetable fields (from D to G) carabids been found in dense vegetation (Sotherton, 1984; decreased according to succession (Fig. 2). These Thomas et al., 1991; Pfiffner and Luka, 2000). trends also applied more or less to other insect Dense vegetation such as tussock-forming grasses predators (Fig. 3). The increase in carabids in the provides less variable temperature environments dry fallow rice field may be attributed to the loss of (Bossenbroek et al., 1977). Such temperature water content in the soil and vegetational develop- buffering properties of dense vegetation may favor ment. In the dry fallow rice field, the carabids P. overwintering carabids. In addition, vegetation fos- haptoderoides japanensis, two Amara species and ters many prey species for carabid predators. B. subditus were abundantly found (Table 2). Since Thomas et al. (1992) found that a carabid, Deme- these carabid species are known to inhabit rela- trias atricapillus fed on prey even in winter, and tively dry fields and orchards (Habu and Sadanaga, that D. atricapillus abundantly overwintered at 1961, 1963; Ishitani and Yano, 1994; Ishitani, dense vegetation areas, but that no significant rela- 1996), these xerophilous species appeared to over- tionships were found between the no. of D. atri- winter where they were active during the warm capillus and their potential prey among habitats. season. Moreover, the low water content in the soil In fallow vegetable fields, carabid abundance of may be advantageous for carabids to hibernate. larval stage and autumn-breeders decreased from D Främbs (1994) reported that even hygrophilous to G, according to vegetational succession (Table species living in peat bogs migrated to drier hum- 4). This was because many carabid larvae of the Overwintering Ground Beetles in Rice and Vegetable Fields 457 genus Harpalus were found from the one-year-old Among other insect predators, Agrypnus binodu- fallow fields D and E but no Harpalus was found lus (Elateridae) larvae and cantharid larvae were from the more than three-year-old fallow field G abundantly found, especially in the dry fallow rice (Table 2). All the sampled Harpalus species except field C and fallow potato field E. A. binodulus larva H. chalcentus are known as autumn-breeders and is known to be predacious (Kurosa, 1959; Ôhira, overwinter as adults and larvae (Habu and 1968), but its feeding preferences are not known. Sadanaga, 1961, 1965, 1970a). Many Harpalus In Europe, cantharid larvae are voracious predators species larvae feed on the seeds of Poaceae, Polyg- feeding on earthworms, aphids and other inverte- onaceae, Asteraceae and so on (Kirk, 1972; Jor- brates (Langenstück et al., 1998) and have high gensen and Toft, 1997; Kromp, 1999; Tooley and dispersal ability in farmlands (Traugott, 2002). In Brust, 2002). Since at plots D and E, D. ciliaris Japan, however, although the taxonomy of adult densely covered the ground, the Harpalus larvae cantharid species has been progressively devel- sampled appeared to feed on the seeds of D. cil- oped, its larval biology remains little known iaris and hibernated at the sites. Yamazaki et al. (Imasaka, 1998). Bionomics of these elaterid and (1999) reported that Harpalus larvae (especially H. cantharid species should be clarified to use these capito and H. sinicus) overwintered with high den- potentially beneficial predators for pest control. sities in marshy ground along a river where grasses In conclusion, the findings of the present study vegetated. As vegetational succession proceeded, suggest that, in farmland management, in order to D. ciliaris and other grasses declined, possibly re- increase the numbers of many carabids and other sulting in the loss of Harpalus larvae in plot G. predators, the rice fields and vegetable fields Luff (2002) compared dominant carabid genera should be maintained in a considerably dry state among world farmlands and stated that Harpalus (but, to sustain regional biodiversity, some rice species were particularly predominant in the Japa- fields should maintain permanent waters; e.g. Hi- nese agricultural fauna. daka, 1998). Furthermore, because the old (more than three-year-old) fallow fields harbored only a Habitat preferences in beneficial species and small number of carabid and other predators, it is farmland management recommended to maintain fallow fields at an early Although these Harpalus larvae are not preda- successional stage. In addition, ploughing fallow tors but seed-feeders of weeds, some of those fields in winter may reduce the predators, espe- adults have omnivorous feeding habits, sometimes cially carabid, elaterid and cantharid larvae, since feeding on insects (Ishitani, 1996). Furthermore, larvae appear to be more vulnerable to physical certain Harpalus species can be used for biological disturbances than adult stages. To validate these control of injurious weeds (Brust, 1994; Kromp, farmland management practices in Japan, further 1999; Tooley and Brust, 2002). Therefore, aug- field data on predatory insects overwintering in mentation of Harpalus species in fallow fields ap- farmlands of various districts and experimental pears to be beneficial for farmland management. studies that manipulate management practices are Ploughing fallow fields in winter may reduce the required. populations of these Harpalus larvae, since larval stage appears to be more vulnerable than adult ACKNOWLEDGEMENTS stage due to the fragility of larval integuments. We thank the farmers for permitting us to conduct the pres- Dolichus halensis is a beneficial predacious ent study and two anonymous reviewers for improving the carabid attacking larvae of the diamondback moth manuscript. Thanks are also due to Dr. Y. Hayashi (Kawanishi Plutella xylostella and other lepidopteran and City, Hyogo Prefecture) for identifying staphilinid beetles. planthopper pests (Habu and Sadanaga, 1963; REFERENCES Wakisaka et al., 1991), and in the present study the plots D and E harbored this species with relatively Andersen, J. (1984) A re-analysis of the relationship between high densities (Table 2). This carabid is an autumn- life cycle patterns and the geographical distribution of Fennoscandian carabid beetles. J. Biogeogr. 11: 479– breeder and overwinters as larvae, so ploughing 489. fallow fields in winter may negatively affect this Best, R. L. and C. C. Beegle (1977) Food preferences of five species. species of carabids commonly found in Iowa cornfields. 458 K. YAMAZAKI et al.

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