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Ground arthropod communities in paddy fields during the dry period: Comparison between different farming methods
Journal of Asia-Pacific Entomology 18 (2015) 413–419
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Short Communication
Ground arthropod communities in paddy fields during the dry period: Comparison between different farming methods Atsushi Ohwaki ⁎,1 Echigo-Matsunoyama Museum of Natural Science, 1712-2 Matsunoyama-matsukuchi, Tokamachi 942-1411, Japan
a r t i c l e
i n f o
Article history: Received 7 February 2015 Revised 30 April 2015 Accepted 1 May 2015 Available online 8 May 2015 Keywords: Agroecosystem Carabid beetle Management Predatory arthropods Spider Uncropped season
a b s t r a c t The ground arthropod communities in paddy fields during the dry period and the effects of different farming methods adopted during the cropping season on these communities were evaluated. Pitfall traps were used in six conventional, two herbicide-only, and four organic paddy fields in early November and early May at two sites in Niigata Prefecture, Japan. A total of 202 ground arthropods belonging to 18 taxa were collected, with eight taxa identified at the species level. The most abundant taxa were two predator groups, spiders and carabid beetles. Farming methods did not affect taxon richness, total abundance, abundance of individual taxa, or species composition, but the site marginally affected the abundance of some taxa. These results suggest that during the dry period paddy fields contained abundant predatory arthropods, and that the communities were not affected by the use of pesticides during the cultivation period. Because these predators are important natural enemies of rice pests, management strategies should be focused on both the cultivation period and the uncropped, dry period to enhance predator populations. © 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.
Introduction Paddy fields are representative agricultural lands in Asia, with 90% of paddy fields worldwide being located in this region (Yano, 2002). In Japan, the paddy field area was 24,700 km 2 in 2012 (MAFF, 2012), which represented more than half of the total farmland or 6% of the land surface of the nation. Despite this dominance, studies of organisms in these fields have been almost exclusively conducted in the flooded portion during the cultivation period to substitute for wetland habitats (Moriyama, 1997; Hidaka, 1998; Natuhara, 2013, but see Bambaradeniya et al., 2004; Stenert et al., 2009). Flooded fields are used as breeding and feeding habitats by fish (Saitoh et al., 1988; Nagayama et al., 2012), waterbirds (Lane and Fujioka, 1998; Toral et al., 2011), amphibians (Fujioka and Lane, 1997; Matsuhashi and Okuyama, 2002), aquatic insects (Hirai and Hidaka, 2002; Nishihara et al., 2006; Watanabe et al., 2013), and aquatic micro-organisms (Yamazaki et al., 2004a, 2004b). Other studies have focused on pest and/or predator populations in rice plants (Kajimura et al., 1993; Murata, 1995; Motobayashi et al., 2006). However, information on the faunal community of paddy
⁎ Tel.: +81 555 72 6186; fax: +81 555 72 6215. E-mail address: [email protected]. 1 Present address: Mount Fuji Research Institute (MFRI), Yamanashi Prefectural Government, Kenmarubi, Kamiyoshida, Fujiyoshida 403-0005, Japan.
fields during the dry period remains limited; few studies have been conducted on soil organisms (Bambaradeniya et al., 2004; Stenert et al., 2009) and carabid beetles (Yahiro et al., 1992). This is despite the fact that the dry period lasts for approximately half a year, from early autumn after harvest until spring before rice transplanting, due to the introduction of modern drainage systems since the 1950s and 1960s in Japan (Fujioka and Lane, 1997; Kiritani, 2004). The effects of agrochemicals on non-target organisms are an important issue for biodiversity conservation in agroecosystems (Kleijn et al., 2001, 2006; Hole et al., 2005). The negative effects of pesticides on nontarget aquatic organisms are known in paddy ecosystems (Relyea, 2005; Hayasaka et al., 2012a, 2012b), where pesticide residues can accumulate in soil for more than a year (Hayasaka et al., 2013). Pesticide residues in soil may have delayed effects on ground arthropods utilizing paddy fields during the dry season by direct contacts with residues or through the interactions with soil invertebrates that have absorbed agrochemicals. However, little is known regarding the effects of pesticide use during the cultivation period on the ground arthropod fauna during the dry period in these paddy fields. Paddy fields that are farmed in an environmentally friendly manner provide a good opportunity to examine the effects of pesticides on the ground fauna during the dry period, although these fields usually exist as small islands in a sea of conventionally farmed paddy fields. In this study, ground arthropod communities during the dry period in autumn (after harvest) and spring (before rice transplanting) were surveyed in paddy fields that were farmed in a conventional and
http://dx.doi.org/10.1016/j.aspen.2015.05.001 1226-8615/© 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
environmental friendly manner during the cropping season. The objective of this study was to determine (1) the ground arthropod fauna in paddy fields during the dry period, and (2) the effects of pesticide use during the cultivation period on ground arthropods in the dry period. I hypothesize that environmentally friendly farmed paddy fields have richer ground arthropod fauna than conventionally farmed paddy fields because pesticide residues in soil accumulated in conventionally farmed paddies may have adverse effects on ground arthropods.
Materials and methods Study area The study area was located in a region in Tokamachi City in temperate Japan (37°02′ N, 138°42′ E), which receives heavy snowfall continuously from late December to late March. Two sites, Araya and Kamiyama (elevation 220 and 380 m asl, respectively), in different terrace plains within the same river terrace system along the Shinano River, were established. The two sites were 2 km apart. Four organically farmed and four conventionally farmed paddy fields were selected in Araya, and two herbicide-only and two conventionally farmed paddy fields were selected in Kamiyama. The fields were referred to as organic, herbicide, and conventional paddy fields, as appropriate. Organic farming had been practiced in the organic paddy fields for five or six years before being sampled. Less information was available for the herbicide paddy fields, although the herbicide-only farming method had been practiced for at least a few years before sampling. The selected paddy fields in Araya were located 60–100 m apart from narrow secondary or riparian forest belts (20–40 m wide), whereas those in Kamiyama were adjacent to a 200 m-wide secondary forest belt on the slope between terrace plains. Organic and herbicide paddies are rare in this region; the studied fields were entirely surrounded by conventional paddies. The size of the studied paddies ranged from 0.1 ha to 0.39 ha (43 to 105 m long by 20 to 39 m wide). Fields were flooded beginning in early to mid-May, and drained in early September. Rice seedlings were transplanted in mid- to late May irrespective of farming methods. In the conventional paddy fields, insecticides were applied twice (fipronil or imidacloprid applied to rice seedlings in nursery boxes in mid-May, and dinotefuran in mid-August), herbicides were applied once about one week after rice transplanting (a mixture of indanofan, bensulfuron-methyl, and clomeprop in Araya, and a mixture of daimuron, bensulfuron-methyl, and fentrazamide in Kamiyama), fungicides were applied twice (probenazole in midJune, and basic copper sulfate in mid-July), and chemical fertilizers (nitrogen, phosphorus, potassium, and magnesium) were applied four times during the rice growing season. In the herbicide paddy fields, the same herbicides used in the conventional paddies in Araya were applied once about one week after rice transplanting and organic fertilizers were applied twice in mid May (before rice transplanting) and July, but insecticides and fungicides were not used. In the organic paddy fields, the same organic fertilizers used in the herbicide paddies were applied twice at the same timing as herbicide paddies. In all types of paddy fields, fertilizers (chemical fertilizers in conventional paddies and organic fertilizers in herbicide and organic paddies) were also applied twice during the dry period (mid-October, and early May at the timing of plowing). Midsummer drainage occurred for 10 days during July in the conventional and herbicide paddy fields only. All paddies were drained before harvest and left dry from mid-September to early May, although the paddies were covered with snow from late December to late March. The studied paddy fields had no vegetation with only bare soil during the sampling periods irrespective of farming methods and stubbles were plowed into soil before the autumn samplings in all paddies.
Arthropod sampling and classification Four pitfall traps (500-mL plastic bottles, internal diameter 9 cm, height 11 cm) containing 150 ml 10% ethylene glycol solution were placed at the center of the paddy fields in a line at 5-m intervals, parallel to the long side of the rectangular paddy fields. The traps were opened for five days in late autumn (4–10 November, 2008) and for two days in mid-spring (1–3 May, 2009). The contents of the four traps were pooled as one sample. The collected arthropods were classified into ground (spiders, carabid beetles, staphylinids, weevils, ants, crickets, erythaeid mites, and amphipods) or non-ground arthropods (adults of Diptera, Lepidoptera, aphids, plant hoppers, pond skaters, parasitic wasps, small family-unidentified Coleoptera, and small unidentified insects). Although the majority of the non-ground arthropods were collected as two or less individuals and omitted from the analyses, dipteran adults (approximately 67% of total organisms collected; probably Sciaridae) and parasitic wasps (13 individuals) were included in the analyses because they were abundant and because small dipteran adults were important prey for paddy-dwelling wolf spiders (Ishijima et al. 2006) and parasitic wasps may use ground arthropods as hosts. Ground arthropods were classified into species (all carabid species, two weevil species and two spider species), genus (wolf spider: Alopecosa and Pirata), family (insects: unidentified weevil, Staphylinidae and Formicidae; mites: Erythraeidae), superfamily (cricket Grylloidea), and order (unidentified spiders and Amphipoda). Both ground and non-ground organisms collected in this study are listed in Appendix A. Data analysis In the following analyses, the pooled number of individuals from four traps per paddy was used to represent the abundances of each species for each paddy. In the four paddies where one or two traps were ruined in November, possibly by ravens, the arthropod abundances were corrected for the values per four traps (i.e., if one trap was ruined in a certain paddy, arthropod abundances of the remaining three traps were summed and multiplied by four over three, and these values were used as the arthropod abundances at the paddy). The biased sampling design (i.e., organic paddies in Araya only and herbicide paddies in Kamiyama only) made it impossible to compare the organic, herbicide, and conventional paddies as individual balanced factors in a single analysis. Therefore, I constructed two separate ANOVA models to test the effects of farming methods on species richness, total abundance and abundances of each taxon. In the first model, the data from the organic and herbicide paddies were combined because pesticides were not applied to either of these types of paddies. The effects of farming methods (organic/herbicide or conventional) and sites (Araya or Kamiyama) were used as the explanatory variables, and taxon richness, total arthropod abundance, and the abundance of species or taxa captured in more than three paddies were used as the response variables. In the second model, the effects of farming methods (organic or conventional) were tested using only the data from Araya to avoid the bias from lack of organic paddies in Kamiyama. In both ANOVA models, abundance data were transformed into square-root values. If a species or taxonomic group was observed in more than three paddies during both November and May, the statistical significance was tested for each date and the total for the two dates. To compare taxon composition of ground arthropods among the different farming methods and sites, the taxon composition was analyzed separately in the November and May samples using principal coordinate analysis (PCoA) based on a Bray–Curtis percentage dissimilarity matrix. PCoA ordinations were done separately for the two datasets, i.e., only ground arthropods or those plus dipteran adults and parasitic wasps. No transformation was performed for
A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
Pac. clercki* Unidentified spiders* Par. astrigera* Pla. magnus larva# Pte. haptoderoides# Pla. magnus adult# Alopecosa spp.* Erythraeidae Staphylinidae Ama. chalcites# Lis. oryzophilus Grylloidea Amphipoda Dol. halensis# Pirata spp.* Formicidae Tan. major Unidentified weevil
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Results and discussion Arthropod community in paddy fields during the dry period Collected in November Collected in May
0 10 20 30 40 50 60 70 Total number of individuals collected Fig. 1. Rank–abundance relationship of ground arthropods. The number of individuals collected in November and May are shown as black and white bars, respectively. The asterisks and hash signs represent spiders and carabid beetles, respectively.
the abundance of each taxon. PCoAs were performed using the “vegan” package (Oksanen et al., 2012) in R 2.15 (R Development Core Team, 2012).
A total of 202 ground arthropods belonging to 18 taxa were collected, plus 461 dipterans and 13 parasitic wasps. The samples collected in November included 129 ground arthropods belonging to 15 taxa, whereas the samples collected in May included 73 ground arthropods belonging to nine taxa. Spiders were the dominant ground arthropods collected, followed by carabid beetles. The only rice pest collected was the rice water weevil Lissorhoptrus oryzophilus, only three individuals were collected in November (Fig. 1). Spiders are strictly predacious, and although some carabid beetles were omnivorous or strictly phytophagous (Lövei and Sunderland, 1996; Kromp, 1999; Ikeda et al., 2010), all the species collected in this study have been reported to attack rice pest insects (Yano et al., 1995). Based on this, it appeared that ground arthropods present in paddy fields during the dry period were mainly predators. Pachygnatha clercki and wolf spiders are also dominant during the cultivation period. The former actively searches for prey on both the lower and upper parts of rice plants (Kobayashi et al., 2011), and the latter feeds on rice pests, such as planthoppers, leafhoppers (Ishijima et al., 2006) and young rice grasshopper larvae (personal observation). These spiders spend their entire lives in and around paddy fields and act as pest control agents (Lee et al., 1997; Chikuni 2008; Shinkai and Ogata 2014). Because paddy-dwelling wolf spiders feed on dipterous adults (Chironomidae) in mid-summer (Ishijima et al., 2006), the dipterous adults that were very abundant in both late November and early May, may be important prey for paddy-dwelling spiders in the dry period when other prey is not abundant.
Table 1 Abundance (mean ± s.d.) of species or taxa collected in at least four paddies and the statistical significances in relation to farming method and site. Araya Conventional
Kamiyama Organic
Conventional
Significance Herbicide
Ground arthropod Carabidae Pla. magnus adult
0.5 ± 1.0
2.0 ± 1.8
0.0 ± 0.0
0.0 ± 0.0
Pla. magnus larva
1.6 ± 1.7
1.0 ± 1.2
4.0 ± 0.0
1.5 ± 2.1
Pte. haptoderoides
0.3 ± 0.7
0.5 ± 1.0
1.0 ± 1.4
3.5 ± 3.5
Carabidae total
2.7 ± 3.1
4.5 ± 3.9
5.0 ± 1.4
5.5 ± 0.7
Staphylinidae
0.6 ± 0.7
0.5 ± 1.0
0.0 ± 0.0
0.0 ± 0.0
Spider Pac. clercki
7.1± 6.9
7.3± 8.2
3.5± 2.1
2.8± 0.2
Par. astrigera
4.3± 5.3
1.8± 2.1
0.5± 0.7
0.5± 0.7
Alopecosa spp.
0.5± 0.6
0.8± 1.0
0.5± 0.7
1.0± 0.0
15.2± 6.7
12.8± 8.3
9.5± 0.7
6.7± 0.5
Erythraeidae
0.5± 1.0
0.8± 0.5
0.0± 0.0
0.0± 0.0
Non-ground arthropod Parasitic wasp
2.2± 3.1
1.5± 1.7
0.0± 0.0
0.0± 0.0
46.0± 27.7
51.0± 38.1
22.0± 4.2
27.8± 14.4
7.8± 2.6
8.8± 3.3
5.5± 2.1
6.5± 2.1
68.2± 22.6
72.8± 40.3
36.5± 4.9
40.0± 14.1
20.0± 8.6
20.3± 11.9
14.5± 0.7
12.2± 0.2
Spider total
Dipteran adult Taxon richness Total abundance Ground arthropod abundance a
a
Method (M)/site (S)
Method (only Araya)
M: F1,9 = 1.89, P = 0.202 S: F1,9 = 3.25, P = 0.105 M: F1,9 = 1.62, P = 0.236 S: F1,9 = 1.27, P = 0.288 M: F1,9 = 0.78, P = 0.400 S: F1,9 = 3.76, P = 0.084 M: F1,9 = 0.38, P = 0.555 S: F1,9 = 1.40, P = 0.267 M: F1,9 = 0.15, P = 0.710 S: F1,9 = 1.77, P = 0.216
F1,6 = 2.12, P = 0.196 F1,6 = 0.32, P = 0.591 –
M: F1,9 = 0.06, P = 0.815 S: F1,9 = 0.29, P = 0.603 M: F1,9 = 0.23, P = 0.642 S: F1,9 = 0.85, P = 0.381 M: F1,9 = 0.48, P = 0.507 S: F1,9 = 0.30, P = 0.597 M: F1,9 = 0.74, P = 0.411 S: F1,9 = 2.21, P = 0.172 M: F1,9 = 0.80, P = 0.394 S: F1,9 = 3.10, P = 0.112
F1,6 = 0.04, P = 0.858 F1,6 = 0.25, P = 0.632 F1,6 = 0.05, P = 0.829 F1,6 = 0.28, P = 0.617 F1,6 = 0.84, P = 0.395
M: F1,9 = 0.00, P = 1.000 S: F1,9 = 3.59, P = 0.091 M: F1,9 = 0.12, P = 0.742 S: F1,9 = 2.27, P = 0.166 M: F1,9 = 0.43, P = 0.527 S: F1,9 = 1.94, P = 0.197 M: F1,9 = 0.04, P = 0.852 S: F1,9 = 4.80, P = 0.056 M: F1,9 = 0.07, P = 0.792 S: F1,9 = 1.40, P = 0.267
F1,6 = 0.00, P = 0.999 F1,6 = 0.04, P = 0.854 F1,6 = 0.22, P = 0.653 F1,6 = 0.01, P = 0.918 F1,6 = 0.01, P = 0.936
This value is calculated as “[total abundance] − [non-ground arthropod (i.e., parasitic wasps and Dipterans) abundance]”.
F1,6 = 0.31, P = 0.601 –
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
It should be noted that Platynus magnus larvae were collected in November only (Fig. 1); all of the adults of this species collected in May were newly eclosed adults. Yahiro et al. (1992) surveyed carabid beetles in paddy fields and adjacent levees throughout the year in western Japan, and found that Pla. magnus occurred primarily during autumn, was abundant in the interior of paddy fields, but rare on the levees. This suggests that the species uses the interior of paddy fields during the dry period as a breeding habitat, and leaves the paddy fields after eclosion.
Effects of farming method and site on the arthropod community No significant differences were found between farming method and site in regard to taxon richness, total abundance, or abundance of particular species/taxa. Only marginal differences were found between sites for Pterostichus haptoderoides, parasitic wasps and total abundance (Table 1). When taxon richness and abundance at the November and May sampling dates were examined separately, very few significant or marginal differences were found: for total carabid abundance in May, organic/herbicide N conventional, F1,9 = 4.761, P = 0.057; for dipteran abundance in November, Araya N Kamiyama, F1,9 = 4.765, P = 0.057; and for taxon richness in November, Araya N Kamiyama, F1,9 = 7.840, P = 0.021. When the effects of farming method were tested using
only Araya samples, there were no significant differences in the abundance of any species/taxa or in taxon richness (Table 1). In addition, the PCoA ordinations using the data of ground arthropods, dipterans and parasitic wasps showed that there were no differences in the interactions of taxon composition with farming method or with site in either November or May (Fig. 2a, b). There was considerable overlap among the paddies with different farming methods or sites. The goodness of fit (GOF) was 0.968 in November and 0.976 in May, and the first and second axes explained 36.8% (eigenvalue: 0.419) and 23.2% (0.247) of the total variance in November, and 35.5% (1.01) and 25.4% (0.711) in May. Taxon composition of only ground arthropods did not differ in terms of farming method, but it slightly differed in terms of site in May; the paddies in Kamiyama plotted on the upper side of the diagram (Fig. 3b). In the PCoA ordinations using only ground arthropod data, the GOF was 0.962 in November and 0.973 in May, and the first and second axes explained 28.1% (eigenvalue: 0.798) and 19.2% (0.529) of the total variance in November, and 27.0% (1.08) and 21.8% (0.861) in May. The results indicated that environmentally friendly farming methods at the field scale during the cropping season did not improve ground-dwelling predator fauna during the dry period. Several possible explanations may account for these results, either alone
(a) 0.4
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Axis 2
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Axis 2
0.1
0.0
0.0
-0.2
-0.1 -0.2
-0.4 -0.2
-0.1
0.0
0.1
0.2
0.3
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0.0
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0.6
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Axis 1 Fig. 2. Principal coordinate analysis plots showing taxon composition (ground arthropods, dipteran adults, and parasitic wasps) of the studied paddy fields in (a) November and (b) May. ■: conventional paddies in Araya; □: organic paddies in Araya; ●: conventional paddies in Kamiyama; ○: herbicide paddies in Kamiyama.
-0.2
0.0
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0.4
0.6
Axis 1 Fig. 3. Principal coordinate analysis plots showing taxon composition (only ground arthropods) of the studied paddy fields in (a) November and (b) May. One conventional paddy in Araya was excluded from the analysis in May because no ground arthropods were obtained. ■: conventional paddies in Araya; □: organic paddies in Araya; ●: conventional paddies in Kamiyama; ○: herbicide paddies in Kamiyama.
A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
or in combination. First, although residues of imidacloprid and fipronil likely remained in the soil of the conventional paddies (Hayasaka et al., 2012b, 2013), and pesticide applications negatively affect ground-dwelling wolf spiders in summer (Oyama and Kidokoro, 2003), these pesticides may not be absorbed by the ground predators through prey-predator interactions during the dry period. Second, because conventional paddies surrounded the sampled organic and herbicide paddies, these paddies may have been affected by the agrochemicals applied to the conventional paddies via leaching or aerial pesticide application (Reichenberger et al., 2007), preventing differences in agrochemical exposures within the arthropod communities. Third, paddy fields were tilled irrespective of farming methods, and tillage practices have harmful effects on ground spiders (Ishijima et al., 2006; Motobayashi et al., 2006). If tillage practices are more influential to ground arthropods than pesticide application, arthropod communities in paddy fields may not differ with respect to pesticide application. Finally, Pardosa astrigera, which was dominant in this study, is more common in upland fields or levees than paddy fields, and the wolf spiders that are common in paddy fields during the cropping season such as Par. pseudoannulata, Par. agrarian, and Pirata subpiraticus (Agriculture, Forestry and Fisheries Research Council, 2012) were rarely collected in this study. Although neither paddy interior during the cropping season nor surrounding levees were investigated, this study and the above report together suggested that ground arthropod fauna in paddy fields may shift from flooding to dry periods and that species invading from the surrounding dry areas such as levees are important components of the ground arthropod communities of the paddy fields during the dry season. Several studies reported the importance of arthropod invasion from surrounding field margins and setasides for constructing within-field ground arthropod communities (Schmidt et al., 2005; Schröter and Irmler, 2013). If invasion of ground arthropods from levees is very important for determining within-field communities during the dry season, ground arthropod communities may not differentiate between the organic and conventional paddies. In contrary, the effects of site were apparent in several of the taxa collected or taxon richness and abundance. The largest difference between the two sites was in landscape structure, i.e., the paddies in Araya were far from forest areas, whereas the paddies in Kamiyama were adjacent to forests. Although forest species were unlikely to contribute to this difference because they seldom move deeply into open vegetation (Roume et al., 2011; Ohwaki et al., 2015), some species may have preferred paddy fields adjacent to forests, or while others preferred fields far from forests. However, information on the habitat preferences of these species/taxa is lacking, i.e., it is unclear which open areas they prefer, open areas adjacent to forest or those far from the
417
forest. Another possible explanation is that the two sites differ in altitude by 160 m. Even an altitudinal difference by 150–200 m can affect the activities of some carabid beetles; their activity can continue one– two week later in the autumn and begin earlier in the spring in the sites at a lower elevation (Sota, 1985). Such phenological difference may have been responsible for a higher total abundance in Araya than in Kamiyama. Because the number of sampled paddies and sampling times were limited in this study, more intensive survey may find the reason for this difference, due to landscape structure or phenological difference. Conclusions Predatory arthropods play a vital role in controlling rice insect pests for integrated pest management (IPM). This study showed that many predatory arthropods inhabited paddy interior during the dry season and that some species such as Pac. astrigera invaded from the surrounding dry areas such as levees. Although most studies have exclusively focused on the non-crop habitats as sources of natural enemies of pests until now (Landis et al., 2000), this study also stressed the importance of within-field management as habitats of natural enemies given the dominance of predatory arthropods in paddy interior from autumn to spring. Further research is needed not only to evaluate the functional role of non-crop habitats as sources of natural enemies but also to clarify the effects of field managements such as spring and autumn tillage and agrochemical use on the predatory arthropod populations living in field interior during the dry season. It is also necessary to reveal the seasonal dynamics and habitat use of the predatory arthropods within and around the paddy fields to enhance pest control. Conflicts of interest The author have no conflicts of interest. Acknowledgments I am grateful to Mr. Nagumo and other land owners for allowing me to conduct this study, Mr. M. Yamagishi for his kind coordination, and Mr. H. Tokumoto for spider identification. I also thank Mr. S. Hattori and the Nakasato Eino Center of JA Tokamachi for teaching the farming schedule and the members of the EchigoMatsunoyama Museum of Natural Science for encouragement and support.
Appendix A. List of ground and non-ground organisms with the number of individuals corrected for per four traps at each site in November (left) and May (right)
Araya C1 Ground arthropods Insects Pla. magnus adult Pla. magnus larva Pte. haptoderouides Ama. chalcites Dol. halensis Staphylinidae Lis. oryzophilus Tan. major Unidentified weevil Ant Grylloidea
0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
Kamiyama C21
0/0 1.3/0 1.3/0 0/0 0/0 1.3/0 0/0 0/0 0/0 0/0 0/0
C3
0/0 1/0 0/0 0/0 0/0 1/0 0/0 0/0 0/0 0/1 2/0
C4
1/1 4/0 0/0 0/0 1/0 0/0 0/0 0/0 0/0 0/0 0/0
O1
1/2 2/0 0/0 0/4 0/0 0/4 0/0 1/0 0/0 0/0 0/0
O2
1/3 2/0 0/0 0/0 0/0 0/0 2/0 0/0 1/0 0/0 0/0
O3
0/0 0/0 0/0 0/0 0/0 0/0 1/0 0/0 0/0 0/0 0/0
O4
1/0 0/0 1/1 0/0 0/0 2/0 0/0 0/0 0/0 0/0 1/0
C52
0/0 3/0 0/2 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
C61
0/0 4/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
P11
0/0 0/0 0/6 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
P2
0/0 3/0 0/1 0/0 1/0 0/0 0/0 0/0 0/0 0/0 0/0
(continued on next page)
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(continued) Appendix A (continued) Araya C1 Spiders Pac. clercki Par. astrigera Alopecosa spp. Pirata spp. Unidentified spider Other arthropods Erythraeidae Amphipoda Non-ground organisms Insects Dipteran adult Parasitic wasp Moth adult Moth larva Microvelia spp. Aphid Plant hopper Unidentified insect Non-arthropods Slug
Kamiyama 1
C52
C61
P11
C2
C3
8/4 0/0 0/0 0/1 3/0
1.3/0 0/0 0/0 0/0 5.3/0
1/0 10/1 0/1 0/0 2/0
4/7 1/5 1/0 0/0 1/1
9/8 0/4 0/1 0/0 2/0
11/0 0/0 0/0 0/0 0/0
0/0 0/0 0/0 0/0 1/3
1/0 2/1 0/2 0/1 3/2
3/1 0/1 0/1 0/0 1.5/0
0/2 0/0 0/0 0/0 8/0
2.7/0 0/0 0/1 0/0 2.7/0
0/3 1/0 0/1 0/0 2/0
0/0 0/0
0/0 1.3/0
0/0 0/0
2/0 0/0
1/0 0/0
0/0 1/0
1/0 0/0
1/0 0/0
0/0 0/0
0/0 0/0
0/0 0/0
0/0 0/0
37/26 0/0 0/0 0/0 0/0 0/0 0/0 0/0
40/36 6.7/0 0/0 0/0 0/0 0/0 0/0 0/0
14/11 2/0 0/0 0/0 1/0 0/0 0/0 0/0
20/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
26/6 1/0 0/0 0/0 0/0 0/0 0/0 0/0
23/6 0/0 0/0 0/0 0/0 0/0 0/0 0/0
31/4 1/0 0/0 0/0 0/0 0/0 0/0 0/0
40/68 4/0 0/0 0/0 1/0 1/0 1/0 0/0
16.5/3 0/0 1.3/0 1/0 0/0 0/0 0/0 0/0
16/3 0/0 0/0 0/0 0/0 0/0 0/0 0/0
6.7/11 0/0 0/0 1/0 0/0 0/0 0/0 0/1
21/17 0/0 0/0 0/0 0/0 0/0 0/0 0/0
0/0
0/0
0/0
0/0
0/0
0/1
0/0
0/0
0/0
0/0
0/0
0/0
C4
O1
O2
O3
O4
P2
C1–4: Conventional paddies in Araya; O1–4: organic paddies in Araya, C5–6: conventional paddies in Kamiyama, P1–2: herbicide paddies in Kamiyama. 1: The number of individuals of each taxon in C2, C6 and P1 in November was corrected by multiplying four over three because one trap was ruined. 2: The number of individuals of each taxon in C5 in November was corrected by multiplying two because two traps were ruined.
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419 Schröter, L., Irmler, U., 2013. Organic cultivation reduces barrier effect of arable fields on species diversity. Agric. Ecosyst. Environ. 164, 176–180. Shinkai, E., Ogata, K., 2014. Organisms in paddy fields — Kumo. Nobunkyo, Tokyo (in Japanese). Sota, T., 1985. Life history patterns of carabid beetles belonging to the subtribe Carabina (Coleoptera, Carabidae) in the Kinki District, western Japan. Kontyu 53, 370–378. Stenert, C., Bacca, R.C., Maltchik, L., Rocha, O., 2009. Can hydrologic management practices of rice fields contribute to macroinvertebrate conservation in southern Brazil wetlands? Hydrobiologia 635, 339–350. Toral, G.M., Aragonés, D., Bustamante, J., Figuerola, J., 2011. Using landsat images to map habitat availabiligy for waterbirds in rice fields. Ibis 153, 684–694. Watanabe, K., Koji, S., Hidaka, K., Nakamura, K., 2013. Abundance, diversity, and seasonal population dynamics of aquatic Coleoptera and Heteroptera in rice fields: effects of direct seeding management. Environ. Entomol. 42, 841–850.
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Short Communication
Ground arthropod communities in paddy fields during the dry period: Comparison between different farming methods Atsushi Ohwaki ⁎,1 Echigo-Matsunoyama Museum of Natural Science, 1712-2 Matsunoyama-matsukuchi, Tokamachi 942-1411, Japan
a r t i c l e
i n f o
Article history: Received 7 February 2015 Revised 30 April 2015 Accepted 1 May 2015 Available online 8 May 2015 Keywords: Agroecosystem Carabid beetle Management Predatory arthropods Spider Uncropped season
a b s t r a c t The ground arthropod communities in paddy fields during the dry period and the effects of different farming methods adopted during the cropping season on these communities were evaluated. Pitfall traps were used in six conventional, two herbicide-only, and four organic paddy fields in early November and early May at two sites in Niigata Prefecture, Japan. A total of 202 ground arthropods belonging to 18 taxa were collected, with eight taxa identified at the species level. The most abundant taxa were two predator groups, spiders and carabid beetles. Farming methods did not affect taxon richness, total abundance, abundance of individual taxa, or species composition, but the site marginally affected the abundance of some taxa. These results suggest that during the dry period paddy fields contained abundant predatory arthropods, and that the communities were not affected by the use of pesticides during the cultivation period. Because these predators are important natural enemies of rice pests, management strategies should be focused on both the cultivation period and the uncropped, dry period to enhance predator populations. © 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.
Introduction Paddy fields are representative agricultural lands in Asia, with 90% of paddy fields worldwide being located in this region (Yano, 2002). In Japan, the paddy field area was 24,700 km 2 in 2012 (MAFF, 2012), which represented more than half of the total farmland or 6% of the land surface of the nation. Despite this dominance, studies of organisms in these fields have been almost exclusively conducted in the flooded portion during the cultivation period to substitute for wetland habitats (Moriyama, 1997; Hidaka, 1998; Natuhara, 2013, but see Bambaradeniya et al., 2004; Stenert et al., 2009). Flooded fields are used as breeding and feeding habitats by fish (Saitoh et al., 1988; Nagayama et al., 2012), waterbirds (Lane and Fujioka, 1998; Toral et al., 2011), amphibians (Fujioka and Lane, 1997; Matsuhashi and Okuyama, 2002), aquatic insects (Hirai and Hidaka, 2002; Nishihara et al., 2006; Watanabe et al., 2013), and aquatic micro-organisms (Yamazaki et al., 2004a, 2004b). Other studies have focused on pest and/or predator populations in rice plants (Kajimura et al., 1993; Murata, 1995; Motobayashi et al., 2006). However, information on the faunal community of paddy
⁎ Tel.: +81 555 72 6186; fax: +81 555 72 6215. E-mail address: [email protected]. 1 Present address: Mount Fuji Research Institute (MFRI), Yamanashi Prefectural Government, Kenmarubi, Kamiyoshida, Fujiyoshida 403-0005, Japan.
fields during the dry period remains limited; few studies have been conducted on soil organisms (Bambaradeniya et al., 2004; Stenert et al., 2009) and carabid beetles (Yahiro et al., 1992). This is despite the fact that the dry period lasts for approximately half a year, from early autumn after harvest until spring before rice transplanting, due to the introduction of modern drainage systems since the 1950s and 1960s in Japan (Fujioka and Lane, 1997; Kiritani, 2004). The effects of agrochemicals on non-target organisms are an important issue for biodiversity conservation in agroecosystems (Kleijn et al., 2001, 2006; Hole et al., 2005). The negative effects of pesticides on nontarget aquatic organisms are known in paddy ecosystems (Relyea, 2005; Hayasaka et al., 2012a, 2012b), where pesticide residues can accumulate in soil for more than a year (Hayasaka et al., 2013). Pesticide residues in soil may have delayed effects on ground arthropods utilizing paddy fields during the dry season by direct contacts with residues or through the interactions with soil invertebrates that have absorbed agrochemicals. However, little is known regarding the effects of pesticide use during the cultivation period on the ground arthropod fauna during the dry period in these paddy fields. Paddy fields that are farmed in an environmentally friendly manner provide a good opportunity to examine the effects of pesticides on the ground fauna during the dry period, although these fields usually exist as small islands in a sea of conventionally farmed paddy fields. In this study, ground arthropod communities during the dry period in autumn (after harvest) and spring (before rice transplanting) were surveyed in paddy fields that were farmed in a conventional and
http://dx.doi.org/10.1016/j.aspen.2015.05.001 1226-8615/© 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
environmental friendly manner during the cropping season. The objective of this study was to determine (1) the ground arthropod fauna in paddy fields during the dry period, and (2) the effects of pesticide use during the cultivation period on ground arthropods in the dry period. I hypothesize that environmentally friendly farmed paddy fields have richer ground arthropod fauna than conventionally farmed paddy fields because pesticide residues in soil accumulated in conventionally farmed paddies may have adverse effects on ground arthropods.
Materials and methods Study area The study area was located in a region in Tokamachi City in temperate Japan (37°02′ N, 138°42′ E), which receives heavy snowfall continuously from late December to late March. Two sites, Araya and Kamiyama (elevation 220 and 380 m asl, respectively), in different terrace plains within the same river terrace system along the Shinano River, were established. The two sites were 2 km apart. Four organically farmed and four conventionally farmed paddy fields were selected in Araya, and two herbicide-only and two conventionally farmed paddy fields were selected in Kamiyama. The fields were referred to as organic, herbicide, and conventional paddy fields, as appropriate. Organic farming had been practiced in the organic paddy fields for five or six years before being sampled. Less information was available for the herbicide paddy fields, although the herbicide-only farming method had been practiced for at least a few years before sampling. The selected paddy fields in Araya were located 60–100 m apart from narrow secondary or riparian forest belts (20–40 m wide), whereas those in Kamiyama were adjacent to a 200 m-wide secondary forest belt on the slope between terrace plains. Organic and herbicide paddies are rare in this region; the studied fields were entirely surrounded by conventional paddies. The size of the studied paddies ranged from 0.1 ha to 0.39 ha (43 to 105 m long by 20 to 39 m wide). Fields were flooded beginning in early to mid-May, and drained in early September. Rice seedlings were transplanted in mid- to late May irrespective of farming methods. In the conventional paddy fields, insecticides were applied twice (fipronil or imidacloprid applied to rice seedlings in nursery boxes in mid-May, and dinotefuran in mid-August), herbicides were applied once about one week after rice transplanting (a mixture of indanofan, bensulfuron-methyl, and clomeprop in Araya, and a mixture of daimuron, bensulfuron-methyl, and fentrazamide in Kamiyama), fungicides were applied twice (probenazole in midJune, and basic copper sulfate in mid-July), and chemical fertilizers (nitrogen, phosphorus, potassium, and magnesium) were applied four times during the rice growing season. In the herbicide paddy fields, the same herbicides used in the conventional paddies in Araya were applied once about one week after rice transplanting and organic fertilizers were applied twice in mid May (before rice transplanting) and July, but insecticides and fungicides were not used. In the organic paddy fields, the same organic fertilizers used in the herbicide paddies were applied twice at the same timing as herbicide paddies. In all types of paddy fields, fertilizers (chemical fertilizers in conventional paddies and organic fertilizers in herbicide and organic paddies) were also applied twice during the dry period (mid-October, and early May at the timing of plowing). Midsummer drainage occurred for 10 days during July in the conventional and herbicide paddy fields only. All paddies were drained before harvest and left dry from mid-September to early May, although the paddies were covered with snow from late December to late March. The studied paddy fields had no vegetation with only bare soil during the sampling periods irrespective of farming methods and stubbles were plowed into soil before the autumn samplings in all paddies.
Arthropod sampling and classification Four pitfall traps (500-mL plastic bottles, internal diameter 9 cm, height 11 cm) containing 150 ml 10% ethylene glycol solution were placed at the center of the paddy fields in a line at 5-m intervals, parallel to the long side of the rectangular paddy fields. The traps were opened for five days in late autumn (4–10 November, 2008) and for two days in mid-spring (1–3 May, 2009). The contents of the four traps were pooled as one sample. The collected arthropods were classified into ground (spiders, carabid beetles, staphylinids, weevils, ants, crickets, erythaeid mites, and amphipods) or non-ground arthropods (adults of Diptera, Lepidoptera, aphids, plant hoppers, pond skaters, parasitic wasps, small family-unidentified Coleoptera, and small unidentified insects). Although the majority of the non-ground arthropods were collected as two or less individuals and omitted from the analyses, dipteran adults (approximately 67% of total organisms collected; probably Sciaridae) and parasitic wasps (13 individuals) were included in the analyses because they were abundant and because small dipteran adults were important prey for paddy-dwelling wolf spiders (Ishijima et al. 2006) and parasitic wasps may use ground arthropods as hosts. Ground arthropods were classified into species (all carabid species, two weevil species and two spider species), genus (wolf spider: Alopecosa and Pirata), family (insects: unidentified weevil, Staphylinidae and Formicidae; mites: Erythraeidae), superfamily (cricket Grylloidea), and order (unidentified spiders and Amphipoda). Both ground and non-ground organisms collected in this study are listed in Appendix A. Data analysis In the following analyses, the pooled number of individuals from four traps per paddy was used to represent the abundances of each species for each paddy. In the four paddies where one or two traps were ruined in November, possibly by ravens, the arthropod abundances were corrected for the values per four traps (i.e., if one trap was ruined in a certain paddy, arthropod abundances of the remaining three traps were summed and multiplied by four over three, and these values were used as the arthropod abundances at the paddy). The biased sampling design (i.e., organic paddies in Araya only and herbicide paddies in Kamiyama only) made it impossible to compare the organic, herbicide, and conventional paddies as individual balanced factors in a single analysis. Therefore, I constructed two separate ANOVA models to test the effects of farming methods on species richness, total abundance and abundances of each taxon. In the first model, the data from the organic and herbicide paddies were combined because pesticides were not applied to either of these types of paddies. The effects of farming methods (organic/herbicide or conventional) and sites (Araya or Kamiyama) were used as the explanatory variables, and taxon richness, total arthropod abundance, and the abundance of species or taxa captured in more than three paddies were used as the response variables. In the second model, the effects of farming methods (organic or conventional) were tested using only the data from Araya to avoid the bias from lack of organic paddies in Kamiyama. In both ANOVA models, abundance data were transformed into square-root values. If a species or taxonomic group was observed in more than three paddies during both November and May, the statistical significance was tested for each date and the total for the two dates. To compare taxon composition of ground arthropods among the different farming methods and sites, the taxon composition was analyzed separately in the November and May samples using principal coordinate analysis (PCoA) based on a Bray–Curtis percentage dissimilarity matrix. PCoA ordinations were done separately for the two datasets, i.e., only ground arthropods or those plus dipteran adults and parasitic wasps. No transformation was performed for
A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
Pac. clercki* Unidentified spiders* Par. astrigera* Pla. magnus larva# Pte. haptoderoides# Pla. magnus adult# Alopecosa spp.* Erythraeidae Staphylinidae Ama. chalcites# Lis. oryzophilus Grylloidea Amphipoda Dol. halensis# Pirata spp.* Formicidae Tan. major Unidentified weevil
415
Results and discussion Arthropod community in paddy fields during the dry period Collected in November Collected in May
0 10 20 30 40 50 60 70 Total number of individuals collected Fig. 1. Rank–abundance relationship of ground arthropods. The number of individuals collected in November and May are shown as black and white bars, respectively. The asterisks and hash signs represent spiders and carabid beetles, respectively.
the abundance of each taxon. PCoAs were performed using the “vegan” package (Oksanen et al., 2012) in R 2.15 (R Development Core Team, 2012).
A total of 202 ground arthropods belonging to 18 taxa were collected, plus 461 dipterans and 13 parasitic wasps. The samples collected in November included 129 ground arthropods belonging to 15 taxa, whereas the samples collected in May included 73 ground arthropods belonging to nine taxa. Spiders were the dominant ground arthropods collected, followed by carabid beetles. The only rice pest collected was the rice water weevil Lissorhoptrus oryzophilus, only three individuals were collected in November (Fig. 1). Spiders are strictly predacious, and although some carabid beetles were omnivorous or strictly phytophagous (Lövei and Sunderland, 1996; Kromp, 1999; Ikeda et al., 2010), all the species collected in this study have been reported to attack rice pest insects (Yano et al., 1995). Based on this, it appeared that ground arthropods present in paddy fields during the dry period were mainly predators. Pachygnatha clercki and wolf spiders are also dominant during the cultivation period. The former actively searches for prey on both the lower and upper parts of rice plants (Kobayashi et al., 2011), and the latter feeds on rice pests, such as planthoppers, leafhoppers (Ishijima et al., 2006) and young rice grasshopper larvae (personal observation). These spiders spend their entire lives in and around paddy fields and act as pest control agents (Lee et al., 1997; Chikuni 2008; Shinkai and Ogata 2014). Because paddy-dwelling wolf spiders feed on dipterous adults (Chironomidae) in mid-summer (Ishijima et al., 2006), the dipterous adults that were very abundant in both late November and early May, may be important prey for paddy-dwelling spiders in the dry period when other prey is not abundant.
Table 1 Abundance (mean ± s.d.) of species or taxa collected in at least four paddies and the statistical significances in relation to farming method and site. Araya Conventional
Kamiyama Organic
Conventional
Significance Herbicide
Ground arthropod Carabidae Pla. magnus adult
0.5 ± 1.0
2.0 ± 1.8
0.0 ± 0.0
0.0 ± 0.0
Pla. magnus larva
1.6 ± 1.7
1.0 ± 1.2
4.0 ± 0.0
1.5 ± 2.1
Pte. haptoderoides
0.3 ± 0.7
0.5 ± 1.0
1.0 ± 1.4
3.5 ± 3.5
Carabidae total
2.7 ± 3.1
4.5 ± 3.9
5.0 ± 1.4
5.5 ± 0.7
Staphylinidae
0.6 ± 0.7
0.5 ± 1.0
0.0 ± 0.0
0.0 ± 0.0
Spider Pac. clercki
7.1± 6.9
7.3± 8.2
3.5± 2.1
2.8± 0.2
Par. astrigera
4.3± 5.3
1.8± 2.1
0.5± 0.7
0.5± 0.7
Alopecosa spp.
0.5± 0.6
0.8± 1.0
0.5± 0.7
1.0± 0.0
15.2± 6.7
12.8± 8.3
9.5± 0.7
6.7± 0.5
Erythraeidae
0.5± 1.0
0.8± 0.5
0.0± 0.0
0.0± 0.0
Non-ground arthropod Parasitic wasp
2.2± 3.1
1.5± 1.7
0.0± 0.0
0.0± 0.0
46.0± 27.7
51.0± 38.1
22.0± 4.2
27.8± 14.4
7.8± 2.6
8.8± 3.3
5.5± 2.1
6.5± 2.1
68.2± 22.6
72.8± 40.3
36.5± 4.9
40.0± 14.1
20.0± 8.6
20.3± 11.9
14.5± 0.7
12.2± 0.2
Spider total
Dipteran adult Taxon richness Total abundance Ground arthropod abundance a
a
Method (M)/site (S)
Method (only Araya)
M: F1,9 = 1.89, P = 0.202 S: F1,9 = 3.25, P = 0.105 M: F1,9 = 1.62, P = 0.236 S: F1,9 = 1.27, P = 0.288 M: F1,9 = 0.78, P = 0.400 S: F1,9 = 3.76, P = 0.084 M: F1,9 = 0.38, P = 0.555 S: F1,9 = 1.40, P = 0.267 M: F1,9 = 0.15, P = 0.710 S: F1,9 = 1.77, P = 0.216
F1,6 = 2.12, P = 0.196 F1,6 = 0.32, P = 0.591 –
M: F1,9 = 0.06, P = 0.815 S: F1,9 = 0.29, P = 0.603 M: F1,9 = 0.23, P = 0.642 S: F1,9 = 0.85, P = 0.381 M: F1,9 = 0.48, P = 0.507 S: F1,9 = 0.30, P = 0.597 M: F1,9 = 0.74, P = 0.411 S: F1,9 = 2.21, P = 0.172 M: F1,9 = 0.80, P = 0.394 S: F1,9 = 3.10, P = 0.112
F1,6 = 0.04, P = 0.858 F1,6 = 0.25, P = 0.632 F1,6 = 0.05, P = 0.829 F1,6 = 0.28, P = 0.617 F1,6 = 0.84, P = 0.395
M: F1,9 = 0.00, P = 1.000 S: F1,9 = 3.59, P = 0.091 M: F1,9 = 0.12, P = 0.742 S: F1,9 = 2.27, P = 0.166 M: F1,9 = 0.43, P = 0.527 S: F1,9 = 1.94, P = 0.197 M: F1,9 = 0.04, P = 0.852 S: F1,9 = 4.80, P = 0.056 M: F1,9 = 0.07, P = 0.792 S: F1,9 = 1.40, P = 0.267
F1,6 = 0.00, P = 0.999 F1,6 = 0.04, P = 0.854 F1,6 = 0.22, P = 0.653 F1,6 = 0.01, P = 0.918 F1,6 = 0.01, P = 0.936
This value is calculated as “[total abundance] − [non-ground arthropod (i.e., parasitic wasps and Dipterans) abundance]”.
F1,6 = 0.31, P = 0.601 –
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
It should be noted that Platynus magnus larvae were collected in November only (Fig. 1); all of the adults of this species collected in May were newly eclosed adults. Yahiro et al. (1992) surveyed carabid beetles in paddy fields and adjacent levees throughout the year in western Japan, and found that Pla. magnus occurred primarily during autumn, was abundant in the interior of paddy fields, but rare on the levees. This suggests that the species uses the interior of paddy fields during the dry period as a breeding habitat, and leaves the paddy fields after eclosion.
Effects of farming method and site on the arthropod community No significant differences were found between farming method and site in regard to taxon richness, total abundance, or abundance of particular species/taxa. Only marginal differences were found between sites for Pterostichus haptoderoides, parasitic wasps and total abundance (Table 1). When taxon richness and abundance at the November and May sampling dates were examined separately, very few significant or marginal differences were found: for total carabid abundance in May, organic/herbicide N conventional, F1,9 = 4.761, P = 0.057; for dipteran abundance in November, Araya N Kamiyama, F1,9 = 4.765, P = 0.057; and for taxon richness in November, Araya N Kamiyama, F1,9 = 7.840, P = 0.021. When the effects of farming method were tested using
only Araya samples, there were no significant differences in the abundance of any species/taxa or in taxon richness (Table 1). In addition, the PCoA ordinations using the data of ground arthropods, dipterans and parasitic wasps showed that there were no differences in the interactions of taxon composition with farming method or with site in either November or May (Fig. 2a, b). There was considerable overlap among the paddies with different farming methods or sites. The goodness of fit (GOF) was 0.968 in November and 0.976 in May, and the first and second axes explained 36.8% (eigenvalue: 0.419) and 23.2% (0.247) of the total variance in November, and 35.5% (1.01) and 25.4% (0.711) in May. Taxon composition of only ground arthropods did not differ in terms of farming method, but it slightly differed in terms of site in May; the paddies in Kamiyama plotted on the upper side of the diagram (Fig. 3b). In the PCoA ordinations using only ground arthropod data, the GOF was 0.962 in November and 0.973 in May, and the first and second axes explained 28.1% (eigenvalue: 0.798) and 19.2% (0.529) of the total variance in November, and 27.0% (1.08) and 21.8% (0.861) in May. The results indicated that environmentally friendly farming methods at the field scale during the cropping season did not improve ground-dwelling predator fauna during the dry period. Several possible explanations may account for these results, either alone
(a) 0.4
(a) 0.2
Axis 2
0.2
Axis 2
0.1
0.0
0.0
-0.2
-0.1 -0.2
-0.4 -0.2
-0.1
0.0
0.1
0.2
0.3
-0.2
0.0
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(b) (b)
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-0.4 -0.6
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0.4
Axis 1 Fig. 2. Principal coordinate analysis plots showing taxon composition (ground arthropods, dipteran adults, and parasitic wasps) of the studied paddy fields in (a) November and (b) May. ■: conventional paddies in Araya; □: organic paddies in Araya; ●: conventional paddies in Kamiyama; ○: herbicide paddies in Kamiyama.
-0.2
0.0
0.2
0.4
0.6
Axis 1 Fig. 3. Principal coordinate analysis plots showing taxon composition (only ground arthropods) of the studied paddy fields in (a) November and (b) May. One conventional paddy in Araya was excluded from the analysis in May because no ground arthropods were obtained. ■: conventional paddies in Araya; □: organic paddies in Araya; ●: conventional paddies in Kamiyama; ○: herbicide paddies in Kamiyama.
A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
or in combination. First, although residues of imidacloprid and fipronil likely remained in the soil of the conventional paddies (Hayasaka et al., 2012b, 2013), and pesticide applications negatively affect ground-dwelling wolf spiders in summer (Oyama and Kidokoro, 2003), these pesticides may not be absorbed by the ground predators through prey-predator interactions during the dry period. Second, because conventional paddies surrounded the sampled organic and herbicide paddies, these paddies may have been affected by the agrochemicals applied to the conventional paddies via leaching or aerial pesticide application (Reichenberger et al., 2007), preventing differences in agrochemical exposures within the arthropod communities. Third, paddy fields were tilled irrespective of farming methods, and tillage practices have harmful effects on ground spiders (Ishijima et al., 2006; Motobayashi et al., 2006). If tillage practices are more influential to ground arthropods than pesticide application, arthropod communities in paddy fields may not differ with respect to pesticide application. Finally, Pardosa astrigera, which was dominant in this study, is more common in upland fields or levees than paddy fields, and the wolf spiders that are common in paddy fields during the cropping season such as Par. pseudoannulata, Par. agrarian, and Pirata subpiraticus (Agriculture, Forestry and Fisheries Research Council, 2012) were rarely collected in this study. Although neither paddy interior during the cropping season nor surrounding levees were investigated, this study and the above report together suggested that ground arthropod fauna in paddy fields may shift from flooding to dry periods and that species invading from the surrounding dry areas such as levees are important components of the ground arthropod communities of the paddy fields during the dry season. Several studies reported the importance of arthropod invasion from surrounding field margins and setasides for constructing within-field ground arthropod communities (Schmidt et al., 2005; Schröter and Irmler, 2013). If invasion of ground arthropods from levees is very important for determining within-field communities during the dry season, ground arthropod communities may not differentiate between the organic and conventional paddies. In contrary, the effects of site were apparent in several of the taxa collected or taxon richness and abundance. The largest difference between the two sites was in landscape structure, i.e., the paddies in Araya were far from forest areas, whereas the paddies in Kamiyama were adjacent to forests. Although forest species were unlikely to contribute to this difference because they seldom move deeply into open vegetation (Roume et al., 2011; Ohwaki et al., 2015), some species may have preferred paddy fields adjacent to forests, or while others preferred fields far from forests. However, information on the habitat preferences of these species/taxa is lacking, i.e., it is unclear which open areas they prefer, open areas adjacent to forest or those far from the
417
forest. Another possible explanation is that the two sites differ in altitude by 160 m. Even an altitudinal difference by 150–200 m can affect the activities of some carabid beetles; their activity can continue one– two week later in the autumn and begin earlier in the spring in the sites at a lower elevation (Sota, 1985). Such phenological difference may have been responsible for a higher total abundance in Araya than in Kamiyama. Because the number of sampled paddies and sampling times were limited in this study, more intensive survey may find the reason for this difference, due to landscape structure or phenological difference. Conclusions Predatory arthropods play a vital role in controlling rice insect pests for integrated pest management (IPM). This study showed that many predatory arthropods inhabited paddy interior during the dry season and that some species such as Pac. astrigera invaded from the surrounding dry areas such as levees. Although most studies have exclusively focused on the non-crop habitats as sources of natural enemies of pests until now (Landis et al., 2000), this study also stressed the importance of within-field management as habitats of natural enemies given the dominance of predatory arthropods in paddy interior from autumn to spring. Further research is needed not only to evaluate the functional role of non-crop habitats as sources of natural enemies but also to clarify the effects of field managements such as spring and autumn tillage and agrochemical use on the predatory arthropod populations living in field interior during the dry season. It is also necessary to reveal the seasonal dynamics and habitat use of the predatory arthropods within and around the paddy fields to enhance pest control. Conflicts of interest The author have no conflicts of interest. Acknowledgments I am grateful to Mr. Nagumo and other land owners for allowing me to conduct this study, Mr. M. Yamagishi for his kind coordination, and Mr. H. Tokumoto for spider identification. I also thank Mr. S. Hattori and the Nakasato Eino Center of JA Tokamachi for teaching the farming schedule and the members of the EchigoMatsunoyama Museum of Natural Science for encouragement and support.
Appendix A. List of ground and non-ground organisms with the number of individuals corrected for per four traps at each site in November (left) and May (right)
Araya C1 Ground arthropods Insects Pla. magnus adult Pla. magnus larva Pte. haptoderouides Ama. chalcites Dol. halensis Staphylinidae Lis. oryzophilus Tan. major Unidentified weevil Ant Grylloidea
0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
Kamiyama C21
0/0 1.3/0 1.3/0 0/0 0/0 1.3/0 0/0 0/0 0/0 0/0 0/0
C3
0/0 1/0 0/0 0/0 0/0 1/0 0/0 0/0 0/0 0/1 2/0
C4
1/1 4/0 0/0 0/0 1/0 0/0 0/0 0/0 0/0 0/0 0/0
O1
1/2 2/0 0/0 0/4 0/0 0/4 0/0 1/0 0/0 0/0 0/0
O2
1/3 2/0 0/0 0/0 0/0 0/0 2/0 0/0 1/0 0/0 0/0
O3
0/0 0/0 0/0 0/0 0/0 0/0 1/0 0/0 0/0 0/0 0/0
O4
1/0 0/0 1/1 0/0 0/0 2/0 0/0 0/0 0/0 0/0 1/0
C52
0/0 3/0 0/2 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
C61
0/0 4/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
P11
0/0 0/0 0/6 0/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
P2
0/0 3/0 0/1 0/0 1/0 0/0 0/0 0/0 0/0 0/0 0/0
(continued on next page)
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A. Ohwaki / Journal of Asia-Pacific Entomology 18 (2015) 413–419
(continued) Appendix A (continued) Araya C1 Spiders Pac. clercki Par. astrigera Alopecosa spp. Pirata spp. Unidentified spider Other arthropods Erythraeidae Amphipoda Non-ground organisms Insects Dipteran adult Parasitic wasp Moth adult Moth larva Microvelia spp. Aphid Plant hopper Unidentified insect Non-arthropods Slug
Kamiyama 1
C52
C61
P11
C2
C3
8/4 0/0 0/0 0/1 3/0
1.3/0 0/0 0/0 0/0 5.3/0
1/0 10/1 0/1 0/0 2/0
4/7 1/5 1/0 0/0 1/1
9/8 0/4 0/1 0/0 2/0
11/0 0/0 0/0 0/0 0/0
0/0 0/0 0/0 0/0 1/3
1/0 2/1 0/2 0/1 3/2
3/1 0/1 0/1 0/0 1.5/0
0/2 0/0 0/0 0/0 8/0
2.7/0 0/0 0/1 0/0 2.7/0
0/3 1/0 0/1 0/0 2/0
0/0 0/0
0/0 1.3/0
0/0 0/0
2/0 0/0
1/0 0/0
0/0 1/0
1/0 0/0
1/0 0/0
0/0 0/0
0/0 0/0
0/0 0/0
0/0 0/0
37/26 0/0 0/0 0/0 0/0 0/0 0/0 0/0
40/36 6.7/0 0/0 0/0 0/0 0/0 0/0 0/0
14/11 2/0 0/0 0/0 1/0 0/0 0/0 0/0
20/0 0/0 0/0 0/0 0/0 0/0 0/0 0/0
26/6 1/0 0/0 0/0 0/0 0/0 0/0 0/0
23/6 0/0 0/0 0/0 0/0 0/0 0/0 0/0
31/4 1/0 0/0 0/0 0/0 0/0 0/0 0/0
40/68 4/0 0/0 0/0 1/0 1/0 1/0 0/0
16.5/3 0/0 1.3/0 1/0 0/0 0/0 0/0 0/0
16/3 0/0 0/0 0/0 0/0 0/0 0/0 0/0
6.7/11 0/0 0/0 1/0 0/0 0/0 0/0 0/1
21/17 0/0 0/0 0/0 0/0 0/0 0/0 0/0
0/0
0/0
0/0
0/0
0/0
0/1
0/0
0/0
0/0
0/0
0/0
0/0
C4
O1
O2
O3
O4
P2
C1–4: Conventional paddies in Araya; O1–4: organic paddies in Araya, C5–6: conventional paddies in Kamiyama, P1–2: herbicide paddies in Kamiyama. 1: The number of individuals of each taxon in C2, C6 and P1 in November was corrected by multiplying four over three because one trap was ruined. 2: The number of individuals of each taxon in C5 in November was corrected by multiplying two because two traps were ruined.
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