J. Acarol. Soc. Jpn., 26(1): 1-11. May 25, 2017 © The Acarological Society of Japan http://www.acarology-japan.org/ 1

Parasitism of water (: Hydrachnidiae) on Appasus japonicus in a paddy field in Sagamihara City, Kanagawa Prefecture, Japan

Hiroshi ABÉ1*, Yuri KOJIMA2, Mizuki IMURA2 and Yukino TANAKA2 1Biological laboratory, College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252-0880, Japan 2Tokyo Metropolitan Kokubunji High School, Shin-machi 3-2-5, Kokubunji, Tokyo 185-0004, Japan

(Received 31 December 2016; Accepted 23 February 2017)

ABSTRACT

The parasitic nature of water mites on aquatic heteropterans was investigated at a paddy field in Sagamihara City in August 2016. During the survey, three heteropteran species, Appasus japonicus, Aquarius paludum, and Ranatra chinensis, were collected. Among these species, water mites were found only on A. japonicus. The water mites were all in a post-larval resting stage and identified as the sp. The prevalence or intensity has no relation to the developmental stage or sex of A. japonicus. However, the host individuals infested with Hydrachna sp. were significantly larger than non-infested ones, and the mite intensity on each A. japonicus was apt to correlate with the host body size. Consequently, the Hydrachna sp. is opportunistically parasitic on larger A. japonicus individuals, regardless of the developmental stage or sex of the host. Though the Hydrachna sp. did not exhibit a preference for particular body parts of the juvenile A. japonicus, the mites preferred the forewing to the mesothorax, metathorax, foreleg, midleg, and hindleg of the adult one. The mites probably select large, inactive body parts rather than small, active parts for attachment on the adult host. Key words: Appasus japonicus, Hydrachnidiae, Hydrachna, parasitism, water mites

INTRODUCTION

In general, water mites, i.e., Hydrachnidiae, are temporarily parasitic on the body surface of several orders of aquatic in their life cycle (Smith and Oliver, 1986). Most of the studies on the host-parasite relationship between water mites and host insects have been executed mainly in Europe (Abé et al., 2015). The correspondence of the water mites to host taxa was especially well investigated. Smith and Oliver (1986) reviewed host insect taxa for larval water mites representing 70 genera in 28 families. In the 2000s, studies on water mite parasitism were * Corresponding author: e-mail: [email protected] DOI: 10.2300/acari.26.1 2 Hiroshi ABÉ et al. vigorously executed by Dr. Zawal in Poland (Zawal, 2002, 2003a, 2003b, 2004a, 2004b, 2006a, 2006b; Zawal and Dyatlova, 2006, 2008; Zawal and Jaskuła, 2008; Zawal and Szlauer- Łukaszewska, 2012; Zawal and Buczyński, 2013; Zawal et al., 2013, 2017). In Japan, studies on water mite parasitism on aquatic insects were started for the purpose of biological control against malaria by Yamada (1918). Recently, Abé and Ohba (2016) compiled information on water mite parasitism on aquatic organisms in Japan. According to their report, most of the studies on water mite parasitism in Japan treat dipteran hosts (Yamada, 1918; Miyazaki, 1933, 1935, 1936, 1945, 1947; Uchida and Miyazaki, 1935; Imamura, 1950a, 1951a, 1951b, 1952a; Hirabayashi and Fukunaga, 2007). On the other hand, studies on mite parasitism on other insect taxa, such as heteropterans (Masuda, 1934, 1942; Imamura, 1952b; Nagasawa et al., 2008; Morimoto, 2012; Abé et al., 2015), coleopterans (Masuda, 1934, 1935a, 1935b, 1942), odonates (Miyazaki, 1936; Imamura, 1950b, 1951c, 1951d; Imamura and Mitchell, 1967; Kobayashi and Toda, 2005), and plecopterans (Imamura, 1950c), are rather limited. In addition, most of the studies mentioned above are descriptive works on host-parasite correspondence between mite and host taxa. Detailed studies on the host-parasite relationship are scarce (Abé et al., 2015). Accordingly, this paper aims to obtain knowledge concerning the preference of water mites for species, developmental stages, sexes, body sizes, and body sites of heteropteran hosts collected in a paddy field in Sagamihara City in Japan.

MATERIAL AND METHODS

Study area and study period This study was conducted at a paddy field in Sagamihara City in Kanagawa Prefecture in Japan (Fig. 1). The study was carried out on August 4 and 26, 2016, when the paddy field was filled with water. Seasonal fluctuations of the host-parasite community structure on water mite parasitism were repeatedly reported (Davids, 1973; Harris and Harrison, 1974; Smith, 1988; Ihle and McCreadie, 2003; Zawal, 2006a, 2006b; Zawal and Buczyński, 2013; Zawal et al., 2013). Zawal (2006b) and Zawal and Buczyński (2013) suggested that the occurrence of water mite larvae synchronizes with that of the host insects throughout the year. Accordingly, the study period was established in summer, with a high abundance of water mites and aquatic insects in the study area. Sample collection and measuring Aquatic heteropterans were collected by hand with a scoop net like that used in Abé et al. (2015). For each heteropteran insect collected at the study area, the specific name, developmental stage, sex, body size, and presence or absence of water mites were recorded. Heteropterans were identified by species, referring to Tsuzuki et al. (2003). The developmental stage was determined based on the growth condition of the wings and the body length. Sex was determined based on the morphology of the subgenital plate (Tsuzuki et al., 2003). As a criterion of host body size, total body length was measured using a vernier caliper. Measurements, in millimeters, were expressed as the mean ± standard deviation. If water mites were discovered on a host body, the number of mites on each part of the body (Fig. 2), the head, pronotum, scutellum, forewing, prothorax, mesothorax, metathorax, abdomen, foreleg, midleg, hindleg, and respiratory siphon (if Parasitism of water mites on Appasus japonicus in Sagamihara City 3

Fig. 1. Map showing the provenance of materials in Japan.

applicable), was recorded. The ratio of the number of infested host individuals (or certain body parts) to the total number of host individuals (or total number of body parts) was indicated as “prevalence.” The number of mites observed on a certain host individual was given as “intensity” and indicated as a range in some cases. The number of mites estimated per host individual (or certain body part) was expressed as “average intensity” (Abé et al., 2015). The prevalence and intensity of mites were examined for the juvenile and adult hosts or the female and male hosts. To perform a taxonomic examination of water mites on a host body, seven host individuals infested with mites in the post-larval resting stage were incubated in a laboratory for about three weeks until an active nymph emerged from the resting stage. Then taxonomic investigations of water mites were performed based on the morphological characteristics referred to by Tuzovskij (1987, 1990). Statistics A two-way contingency table analysis using the χ2 test was performed for examining the dependence or independence between (1) the host developmental stage (adult or juvenile) and the mite infestation (infested or non-infested), and (2) the host sex (male or female) and the mite infestation. A Mann-Whitney U test was performed to examine the differences in (1) the host body size between developmental stages, host sexes, or infested and non-infested hosts and (2) the mite intensity between host developmental stages or host sexes. Multiple pairwise comparisons of the prevalence on each body part of a host were performed using the Tukey WSD test. Multiple pairwise comparisons of the mite intensity on each body part were performed using the Tukey-Kramer HSD test. The relationship between the mite intensity and host body size was 4 Hiroshi ABÉ et al.

Fig. 2. Schematic diagram of each body part of A. japonicus.

examined using Spearman’s rank correlation (ρ). The statistical analyses were conducted using JMP ver. 4.0 (SAS Institute, Inc.) and Excel Statistics ver.7.0 (Esumi Co., Ltd.).

RESULTS

Occurrence of water mites on host heteropterans Parasitic water mites collected in the present survey were all in the resting stage (nymphochrysalis), and emerged active nymphs belonged to a single species in the genus Hydrachna (Acari: Hydrachnidiae). Unfortunately, obtained nymphs (Fig. 3A, B) could not be identified by species. Therefore, the mites are referred to as the Hydrachna sp. in the present paper. The morphological features of the Hydrachna sp. accorded well with those of the Hydrachna sp.2 recorded in Abé et al. (2015). Hydrachna sp.2 was also found on A. japonicas specimens collected in Kanagawa and Yamanashi prefectures in Japan (Abé et al., 2015). The Hydrachna sp. in the present study and the formerly recorded Hydrachna sp.2 in Abé et al. (2015) must belong to the same species. Parasitism of water mites on Appasus japonicus in Sagamihara City 5

Fig. 3. Emerged nymph of the Hydrachna sp. from nymphochrysalis on A. japonicus: A. dorsal aspect; B. ventral aspect. Scale bars: 100 μm

During the survey, 135 individuals of the following three heteropteran species were collected from a paddy field in Sagamihara City (Table 1): Appasus japonicus (n = 86), Aquarius paludum (n = 48), and Ranatra chinensis (n = 1). Among these host species, the Hydrachna sp. was found exclusively on A. japonicus and the mites lodged on 18 out of 86 host individuals. The prevalence was 20.93% and the average intensity was 0.73. Preference of water mites for host stage A total of 22 adults and 64 juveniles of A. japonicus were collected. The body length of the adult (n = 22, 19.82 ± 0.96) was significantly larger than that of the juvenile (n = 64, 12.54 ± 2.20) (p < 0.0001, Mann-Whitney U test). The mites were detected on 6 out of 22 adult hosts (prevalence 27.3%) and 12 out of 64 juvenile hosts (prevalence 18.8%) (Table 2). The prevalence was not varied with the host developmental stage (p = 0.406, χ2 test). The average intensity was 1.18 in adult hosts and 0.58 in juvenile hosts (Table 2). The intensity was not significantly different between adult and juvenile hosts (p = 0.337, Mann-Whitney U test). Preference of water mites for host sex A total of 8 males and 14 females of the adult A. japonicus were collected. The body length of the female (n = 14, 20.33 ± 0.59) was significantly larger than that of the male (n = 8, 18.91±0.80) (p = 0.0015, Mann-Whitney U test). The mites were parasitic on 2 out of 8 male hosts (prevalence 25.0%) and 4 out of 14 female hosts (prevalence 28.6%) (Table 2). The prevalence was not affected by the host sex (p = 0.856, χ2 test). The average intensity of the Hydrachna sp. on each sex of the adult A. japonicus (n = 22) was 0.50 in the male and 1.57 in the female (Table 2). The intensity was not significantly different between host sexes (p = 0.828, Mann-Whitney U test). Preference of water mites for host body size 6 Table 1. Parasitic nature of the Hydrachna sp. on aquatic heteropterans in Sagamihara City.

Table 2. Prevalence and intensity of the Hydrachna sp. on A. japonicus. Hiroshi A BÉ etal.

Table 3. Prevalence and average intensity of the Hydrachna sp. on 11 body parts of 64 juveniles and 22 adults of A. japonicus. Parasitism of water mites on Appasus japonicus in Sagamihara City 7

Fig. 4. Scatter plot between mite intensity and host body length (n = 86, ρ = 0.237, p = 0.052).

The body length of the infested host (n = 18, 15.86±3.20) was significantly different from that of the non-infested one (n = 68, 14.01±3.80) (p = 0.038, Mann-Whitney U test). Furthermore, the number of mites on each host individual tended to increase with the host body size (ρ = 0.237, p = 0.052) (Fig. 4). Preference of water mites for host body part The prevalence of the Hydrachna sp. on host body parts varies with the developmental stages of A. japonicus (p = 0.022, χ2 test). The prevalence was not different among the head, pronotum, scutellum, forewing, prothorax, mesothorax, metathorax, abdomen, foreleg, midleg, and hindleg in juvenile hosts (p < 0.05, Tukey WSD test) (Table 3). However, the prevalence on the forewing was significantly larger than that on the mesothorax, metathorax, foreleg, midleg, and hindleg in adult hosts (p < 0.05, Tukey WSD test) (Table 3). According to the results of the multiple comparisons of mite intensity on each body part mentioned above, the intensity was not different among the body parts for all combinations in the juvenile or adult host (p < 0.05, Tukey-Kramer HSD test) (Table 3).

DISCUSSION

Appasus japonicus in is known thus far to be a host of some Hydrachna species in Japan (Masuda, 1934, 1942; Nagasawa et al., 2008; Abé et al., 2015). Abé et al. (2015) examined the prevalence and intensity of the Hydrachna sp. (Hydrachna sp.2 in their paper) in the developmental stages of the host insect A. japonicus and found that the Hydrachna sp. had a clear host preference for A. japonicus among some aquatic heteropteran species. Considering that the Hydrachna sp. was exclusively parasitic on A. japonicus in the present study, the Hydrachna sp. clearly has a preference for A. japonicus. Abé et al. (2015) reported that although the prevalence of the Hydrachna sp. was not affected by the host developmental stages of A. japonicus, the intensity was significantly different 8 Hiroshi ABÉ et al. between juvenile and adult hosts, and more mites are parasitic on a juvenile host. In the present study, however, there were no significant differences in prevalence or intensity between the host developmental stages. The inconsistency between the prevalence and intensity needed to be explained by a possible hypothesis (Abé et al., 2015), in that the mites attach initially to the nymph host and, thereafter, some of them come off the host body as the host stage advances with moltings. Alternatively, the adult was collected just after the final molting, so the exposure period to mites was shorter than that of the nymph. In these cases, the nymph host will be exposed to higher probabilities of infestation than the adult. On the other hand, the present result can be simply explained by the fact that every host individual is exposed to the same chance of encounter and parasitic load with mites, irrespective of its developmental stage. The body size of the adult A. japonicus was significantly larger than that of the juvenile, and the body size of the female was larger than that of the male. There were no significant differences in mite prevalence or intensity between the sexes or developmental stages of A. japonicus. However, the host individuals infested with Hydrachna sp. were significantly larger than non- infested ones. Thus, the mite intensity on each A. japonicus individual was apt to be correlated with the host body size. As the host body size becomes larger, the number of mites is likely to increase. If every host individual is exposed to the same chance of encounter with mites, irrespective of its developmental stage and sex, the larger host will be infested with more mites. Therefore, it is probable that the Hydrachna sp. is opportunistically parasitic on larger A. japonicus individuals regardless of the host developmental stage and sex. The Hydrachna sp. did not exhibit a preference for particular body parts of the juvenile A. japonicus. On the other hand, the mites preferred the forewing to the mesothorax, metathorax, foreleg, midleg, and hindleg of the adult host. Although A. japonicus frequently swims around in the water, its flight tendency is known to be quite weak regardless of sex (Tsuzuki et al., 2003), so that migration among distant habitats is only occasionally observed (Ohba et al., 2010). Considering the small body size of the juvenile A. japonicus, it is possible that the mites cannot afford to select a preferable site for lodging on the tiny body of the juvenile host. By contrast, the mites can allow themselves to select a preferable site on the large body of the adult host, and they will be parasitic on the large, inactive body parts, e.g., the forewing, rather than on the small, active parts, such as the leg and thorax, in order to escape physical disturbances due to the daily swimming and cleaning actions of the host.

ACKNOWLEDGEMENTS

The authors thank Hiroyuki Yaguchi and Hiroshi Ichi-ishi of Tokyo Metropolitan Kokubunji High School for giving us an opportunity of studying water mite parasitism.

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摘要 神奈川県相模原市の水田におけるコオイムシへのミズダニの寄生 安倍 弘（日本大学）・小島優里・井村 美月・田中 雪乃（東京都立国分寺高校） 2016 年の 8 月に神奈川県相模原市の水田で水生カメムシ類の採集を行い，それらへのミ ズダニの寄生状況を調べた．調査期間中にミズカマキリ 1 個体，アメンボ 48 個体，コオイ ムシ 86 個体が採集され，その中でコオイムシ 18 個体にダニが寄生していた．ダニはすべて 第 1 蛹の段階だったが，若虫まで飼育して分類群の同定を行った結果，全てのダニがオオミ ズダニの一種であることが明らかになった．オオミズダニの一種はコオイムシのみに寄生し ていたことから，コオイムシに対する宿主選好性があると考えられるが，宿主であるコオイ ムシへのダニの寄生率ならびに寄生数と，宿主の発育段階（成体・幼体）ならびに性との関 連は見られなかった．一方，寄生されていたコオイムシの体サイズは寄生されていなかった コオイムシの体サイズより有意に大きかった．また，ダニの寄生数はコオイムシの体サイズ と正の相関がみられる傾向があった．これらのことから，オオミズダニの一種がコオイムシ と出会う機会はコオイムシの発育段階や性が異なっていても同じであると思われ，体サイズ が比較的大きい個体に日和見的に寄生する傾向があると考えられる．また，コオイムシの幼 体は成体と比べて体がかなり小さく，体の各部位へのダニの寄生率には差がなかったが，成 体では胸や肢に比べて前翅に寄生する傾向があった．コオイムシは飛翔傾向が弱く，成体の 前翅は他の部位に比べて大きく動きが少ないことから，前翅への寄生率が高かった可能性が ある．