First Record of Riccardoella (Proriccardoella) Triodopsis (Acariformes: Trombidiformes: Ereynetidae) from Japan, with Additional Morphological Information

Species Diversity 24: 11–15 Published online 1 May 2019 DOI: 10.12782/specdiv.24.11

First Record of Riccardoella (Proriccardoella) triodopsis (Acariformes: Trombidiformes: Ereynetidae) from Japan, with Additional Morphological Information

Tsukasa Waki1,4, Satoshi Shimano2, and Takahiro Asami3 1 Meguro Parasitological Museum, 4-1-1 Shimomeguro, Meguro-ku, Tokyo 153-0064, Japan E-mail: [email protected] 2 Science Research Center, Hosei University, 2-17-1 Fujimi, Chiyoda-ku, Tokyo 102-8160, Japan 3 Department of Biology, Shinshu University, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan 4 Corresponding author (Received 2 May 2018; Accepted 16 November 2018)

The parasitic miteRiccardoella (Proriccardoella) triodopsis Fain and Klompen, 1990 was sampled from two localities in Chiba prefecture, Japan. The sampled mites were identified based on palps and leg chaetotaxy and structure of famulus on tibia I. This study is represented by the second record of R. triodopsis inhabiting the pulmonate snail and the first discovery in Japan. Key Words: Parasite, new record, Chiba Prefecture, mite.

Introduction Materials and Methods

At present, eight species are known in the genus Riccar- Host land snails, Acusta despecta sieboldtiana Sowerby, doella Berlese, 1923. Six out of the eight species were report- 1839 (Pulmonata: Camaenidae), were sampled from two ed from the lung and body surface of terrestrial gastropods, localities; Hegurishimo (35°05′20″N, 139°54′05″E) and Ohi and the remaining two species were found only from soils (35°05′20″N, 139°58′16″E), Minami-Bousou City, Chiba (Berlese 1923; Fain and van Goethem 1986; Fain and Klom- Prefecture, Japan in 21 April and 7 September 2014, respec- pen 1990; Fain and Barker 2003, 2004; André et al. 2004; tively. The land snails were transferred to the laboratory, and Waki et al. 2018a). The members of genus Riccardoella are mites were collected as follows. We held each of the sam- divided into two subgenera, Riccardoella Berlese, 1923 and pled snails by hands and observed its respiration holes and Proriccardoella Fain and van Goethem, 1986, based on the surface of the soft body once or twice a week for a month. morphology of setae and leg chaetotaxy. The subgenus Ric- When we found mites coming out from the respiration hole cardoella contains only one species, R. limacum Schrank, or walking around the mantle surface of the host, we col- 1776, which is the type species of the genus. The remaining lected specimens with a soft brush and then dropped into seven species belong to the subgenus Proriccardoella. 99% EtOH for fixation and preservation. For morphologi- In Japan, two species of the present genus were reported cal observation under a compound microscope, fixed mites from terrestrial gastropods. Riccardoella (Proriccardoella) were mounted, permeated, and sealed with Hoyer’s Medi- tokyoensis Waki and Shimano, 2018 was described from um on the slide. Body parts were measured with the cam- the lung of the clausiliid land snail, Tauphaedusa tau Boett- era control unit (DS-L3, Nikon) under the microscope. All ger, 1877, in a forest city park in Tokyo, Japan (Waki et al. measurements in the description are in micrometers (µm). 2018a). Riccardoella (Proriccardoella) reaumuri Fain and The mites were identified based on Waki et al. (2018a). Line van Goethem, 1986, which was described from the helicid drawings were prepared with a camera lucida attached to land snail, Arianta arbustorum Linnaeus, 1758, in France, the compound microscope (Eclipse Ni-U, Nikon). Morpho- was reported from three species of land snails on Okinawa- logical terminology followed André et al. (2004), Walter et jima-island (Waki et al. 2018b). In addition, Nakamura et al. al. (2009), and Waki et al. (2018a). (2006) reported Riccardoella sp., which was identified to the Mites sampled were identified by morphological observa- genus level, from soils in Shikoku, Japan. Here we report the tion under a compound microscope as follows with some occurrence of R. triodopsis Fain and Klompen, 1990 for the additional information. first time in Japan, since first taxonomically described from Alabama, USA. Additional morphological information is provided based on specimens newly collected.

Fig. 1. Idiosoma of Riccardoella (Proriccardoella) triodopsis (female, 21441A). A: Dorsal view, B: ventral view and coxae. Scale bar: 100 µm.

Family Ereynetidae Oudemans, 1931 [Japanese name: Yawasuji-dani-ka] Genus Riccardoella Berlese, 1923 [Japanese name: Katatsumuri-dani-zoku] Subgenus Proriccardoella Fain and van Goethem, 1986 [Japanese name: Fusage-katatsumuri-dani-azoku] Riccardoella (Proriccardoella) triodopsis Fain and Klompen, 1990 [New Japanese name: Nyumura-katatsumuri-dani] (Figs 1–5)

Riccardoella (Proriccardoella) triodopsis Fain and Klompen, 1990: 188–189, figs 1–5.

Material examined. Twenty mites were sampled in this study. The following description is based on five adult females and three adult males sampled from Acusta despecta sieboldtiana Sowerby, 1839 (Pulmonata: Camaenidae). These specimens examined are deposited in Meguro Para- sitological Museum, Tokyo, Japan with accession numbers 21441A–F (five females and one male) and 21442A, B (two males). Fig. 2. Gnathosoma of Riccardoella (Proriccardoella) triodopsis Description of adult female. Body (Figs 1, 4). Length (female, 21441B). Scale bar: 10 µm. 356–413. Color pale orange. Surface of idiosoma, gnathosoma, and legs with striated cuticle. Idiosoma (Figs 1, 4). Idiosoma oval. Idiosoma length with additional vi seta (Fig. 4D). 344–391 and width 237–288. Two pairs of lyrifissures (ia Ano-genital region (Fig. 1B). Two pairs of genital papil- and im) present (Figs 1A, 4A, B). Lyrifissures ip indistinct. lae. Females with eggs not observed. Genital area with ex- Lengths of setae on idiosoma: Dorsum: vi 24–30; ve 7–11; ternal row (aggenital setae (ag)) composed of 4 or 5 setae sci 49–77; sce 22–30; c1 20; c2 23–28; d1 18–21; e1 20–22; and internal row (genital setae (g)) composed of 4 or 5 setae. f1 20–21; f2 53–64; h1 18–21; h2 23–31. Venter: Length of Pair of lyrifissures (ih) present between h2 and ps2 (Figs 1B, setae 1a, 3a, and 4a: 6–9. All setae weakly barbed. Setae sci 4C). and f2 long and narrow (Fig. 4D). Other setae sub cylindri- Gnathosoma (Figs 1B, 2, 5A, B). Length 57–63 and width cal (Fig. 4D). Variation of setae: single specimen (21441D) 57–67. No eyespot. All setae not prolonged by filaments. Riccardoella (Proriccardoella) triodopsis from Japan 13

Fig. 3. Legs of Riccardoella (Proriccardoella) triodopsis (antiaxial face). A: Left leg I (female, 21441E). B–D: Left leg II and right legs III and IV: (female, 21441B). Scale bar: 50 µm.

Palptarsus with 4 barbed setae (3–5) with fine tip and sol- empodium. Claws, ca. 10 times longer than width, contain- enidion ω (3–4) (Fig. 5A, B), apically. ing inconspicuous dents. Legs (Figs 1B, 3, 5D–F). All legs cylindrical. Femur IV Description of male. Male smaller than female but divided into 2 segments. All setae on legs not prolonged by shape as in females. Body length (including gnathosoma) filaments. Setation on legs (I-II-III-IV, without solenidion, 313–357. eupathidion, and famulus included): tarsi I–IV 12-9-8-8; Idiosoma length (excluding gnathosoma) 290–321 and tibiae I–IV 5-3-3-3; genua I–IV 4-4-3-3; femora I–IV 6-4- width 167–221. Lengths of setae on idiosoma: dorsum: vi

3-3; trochanters I–IV 1-1-1-0; coxae I–IV 2-1-2-1. Leg chae- 24–29; ve 7–13; sci 58–74; sce 22–27; c1 18–20; c2 19–24; totaxy eupathidiotaxy and solenidiotaxy given in Table 1. d1 18–20; e1 17–19; f1 18–20; f2 48–55; h1 14–18; h2 18–26. Tibia I with oval erenynetal organ φ (Fig. 3A). Erenynetal Venter: Length of setae 1a, 3a, and 4a: 6–9. Genital vestibule organ consisting from: famulus (k″) 11–12 long and guard of male with 3 pairs of eugenital setae (eug). Gnathosoma seta (l″) 13–17 long: famulus 65–82% of length of guard seta length 55–59 and width 55–59. Palptarsus with 4 setae l′, (Figs 3A, 5E, F). Famulus not forked apically. Solenidia on l″, v′, and v″ (3–5) and single solenidion (3–4). Erenynetal tarsi 1-1-0-0 (Figs 3A, B, 5C), no solenidia on tibiae, genua, organ with famulus (k″) 9–11 long and guard seta (l″) 14 femora, trochanters, or coxae. Solenidion ω in tarsi I and II long: famulus 67–79% of length of guard seta. Length of sol- subcylindrical, placed on dorsal position between setae ft′ζ enidia ω on tarsi I, II 5–6 and 4–6, respectively. and ft″ζ (Figs 3A, 5C). Length of solenidia ω on tarsi I 6–8 Habitat. This species inhabits the lung and body sur- and II 4–5. Eupathidion ζ on tarsi 7-1-0-0. Eupathidion with face of the terrestrial gastropod, A. despecta sieboldtiana long spine on tip (Fig. 5C, D). Pretarsus with two claws and Sowerby, 1839, living in litter layers and on short plants near 14 Tsukasa Waki et al.

the ground. Remarks. The mite sampled in the present study belongs to the genus Riccardoella by having the following morphological characteristics of the genus (Fain and van Goet- hem 1986; Fain and Barker 2003; André et al. 2004; Waki et al. 2018a): palp with 3 segments; tibia I with 5 setae; trochanter I with single seta; femur IV with 3 setae; idiosoma with lyrifissure im. The sampled mites belong to the subgenus Proriccardoella by having following morphological features: trochanter III with a seta; coxa I with 2 setae; tarsus I with famulus consisting more than 60% the length of its guard seta (l″); palptarsi and legs with setae not prolonged by a filament (see Fain and van Goethem 1986). The mites sampled were identified as R. triodopsis based on a combination of the following morphologies: tarsi II–IV with 9, 8, and 8 setae, respectively; tibia I with 5 setae; femur I with 6 setae; trochanters I and III with a seta; coxae I and III with 2 setae; palptarsus with 4 setae; famulus (k″) on tibia I not forked apically. Riccardoella triodopsis is similar to R. oudemansi Thor, 1932 in possession of morphological features: tarsi III and IV with 8 setae; tibia I with 5 setae; femora I and II with 6 and 4 setae, respectively. However, R. triodopsis is distin- Fig. 4. Lyrifissures and setae on idiosoma of Riccardoella (Proricca- guished from R. oudemansi in the presence of 2 setae in rdoella) triodopsis. A–C: Lyrifissures ia and im (female, 21441A) and coxa III and 4 setae on palptarsus whereas 3 setae present on ih (female, 21441C). D: Shapes of setae on idiosoma and additional setae vi (arrow) (female, 21441D). Scale bars: A–C, 5 µm; D, 10 µm. both parts in R. oudemansi. Moreover, famulus is not forked

Fig. 5. Setae on tarsus and palptarsus and solenidion of Riccardoella (Proriccardoella) triodopsis. A–B: Setae (v) and (l) and solenidion ω on palptarsus (female, 21441E). C: Solennidion ω and setae ft″ζ on tarsus I (female, 21441B). D: Eupathidion p′ζ on tarsus II (female, 21441D). E–F: Famulus k″ and its guard seta l″ on tibia I (female, 21441E). Scale bars: A–C, 10 µm; D–F, 5 µm.

Table 1. Leg chaetotaxy, eupathidiotaxy, and solenidiotaxy of Riccardoella (Proriccardoella) triodopsis. Single and double prime marks: an- terior and posterior sides of the leg segment, respectively. Parentheses: a pair of setae.

Leg Coxa Trochanter Femur Genu Tibia Tarsus I 1b, 1c v′ d, (l), (v), bv″ d, l″, (v) d, (l), (v), k″, φ (ftζ), (tcζ), it′ζ, it″, (pζ), (u), (pv), ω II 2b v′ (l), v″, bv″ (l), (v) d, (v) (ft), (tc), p′, p″ζ, (u), pv′, ω III 3b, 3c v′ d, l′, v′ (l), v′ l″, (v) ft″, (tc), (p), (u), pv′ IV 4c — d, l″, v′ (l), v′ d, (v) ft″, (tc), (p), (u), pv′ Riccardoella (Proriccardoella) triodopsis from Japan 15 in its apical part in R. triodopsis but forked in R. oudemansi. pling bias? Journal of Cave and Karst Studies 66: 81–88. Baker, R. A. 1970. The food of Riccardoella limacum (Schrank)—Acari- Riccardoella triodopsis is also similar to R. reaumuri Fain Trombidiformes and its relationship with Pulmonate molluscs. and van Goethem, 1986 in the following morphological Journal of Natural History 4: 521–530. characters: tarsi III and IV with 8 setae; tibia I with 5 setae; Barker, G. M. and Ramsay, G. W. 1978. The slug mite Riccardoella li- femora I and II with 6 and 4 setae, respectively; coxa III macum (Acari: Ereynetidae) in New Zealand. New Zealand Ento- with 2 setae. However, these two species are clearly distin- mologist 6: 441–443. guished by the number of setae on palptarusus: 4 setae in R. Berlese, A. 1923. Centuria sesta di Acari nuovi. 1. Prostigmata. Redia triodopsis while 3 setae in R. reaumuri. Moreover, the apical 15: 242–246. part of famulus is not forked in R. triodopsis but forked in Fain, A. and Barker, G. M. 2003. A new genus and species of mite of the R. reaumuri. family Ereynetidae (Acari Prostigmata) from the pallial cavity of a New Zealand terrestrial gastropod (Athoracophoridae). Bulletin According to figures in the original description of R. tri- de la Société Royale Belge d’Entomologie 139: 233–238. odopsis by Fain and Klompen (1990), the famulus k″ is 83% Fain, A. and Barker, G. M. 2004. A new species of the genus Riccardoel- length of its guard l″ seta, although the authors described la Berlese, 1923 (Acari: Ereynetidae) occurring as a parasite in the that the famulus length is “almost as long as” its guard pallial cavity of Athoracophoridae (Gastropoda) in New Zealand. seta. In this study, the famulus of the Japanese specimens is Bulletin de la Société Royale Belge d’Entomologie 140: 43–48. shorter than in that original description. This difference in Fain, A. and van Goethem, J. L. 1986. Les acariens du genre Riccardoella length between the American and Japanese specimens may Berlese, 1923 parasites du poumon de mollusques gastéropodes represent geographic variation in this species. pulmonés terrestres. Acarologia 27: 125–140. So far, R. triodopsis has not been reported from anywhere Fain, A. and Klompen, J. S. H. 1990. Riccardoella (Proriccadoella) tri- else since its original description in 1990 from USA. Thus, odopsis nov. spec. (Acari: Ereynetidae) from the USA. Acarologia 31: 187–190. this is the second record of R. triodopsis and the first report Nakamura, Y., Ishikawa, K., Shiba, M., Fujikawa, T., Ono, H., Tamura from Japan. Chiba Prefecture is approximately 10,000 km far H., and Morikawa K. 2006. Soil animals of the 88 BUDDHIST from the type locality in Alabama, USA, suggesting that R. temples in Shikoku Islands. Memoirs of the Faculty of Agriculture, triodopsis may have a worldwide distribution. In this study, Ehime University 51: 25–48. R. triodopsis was collected from the land snail A. despecta Oudemans, A. C. 1931. Acarologische Aanteekeningen CVIII. Ento- sieboldtiana the member of Camaenidae Pilsbry, 1895, mologische Berichten 8: 251–263. whereas the type host Triodopsis obstricta Say, 1821 belongs Schüpbach, H. U. and Baur, B. 2008a. Experimental evidence for a new to Polygyridae Pilsbry, 1895. This suggests that R. triodop- transmission route in a parasitic mite and its mucus-dependent sis probably show a wide host range. Similarly, Riccardoella orientation towards the host snail. Parasitology 135: 1679–1684. Schüpbach, H. U. and Baur, B. 2008b. Parasitic mites influence fitness limacum Schrank, 1776, R. oudemansi, and R. reaumuri components of their host, the land snail Arianta arbustorum. In- have been found each from three to four families of terres- vertebrate Biology 127: 350–356. trial mollusks and thus have worldwide distributions (Turk Stojnić, B., Vidović, B., Jokić, G., Vukša, M., Blažić T., and Đedović, S. and Phillips 1946; Baker 1970; Barker and Ramsay 1978; 2016. First record of two slug mite species of the genus Riccardoel- Fain and van Gorthem 1986; Ueckermann and Tiedt 2003; la Berlese (Acari: Ereynetidae) in Serbia. Pesticidi i Fitomedicina Schüpbach and Baur 2008a, b; Zabludovskaya and Badanin 31: 145–150. 2010; Stojnić et al. 2016; Waki et al. 2018a). Thus, it may Turk, F. A. and Phillips, S. 1946. A Monograph of the slug mite—Riccar- be a common feature for the mites of Riccardoella to have a doella limacum (Schrank.). Journal of Zoology 115: 448–472. wide range of hosts and distribution. Ueckermann, E. A. and Tiedt, L. R. 2003. First record of Riccardoella limacum (Schrank, 1776) and Riccardoella oudemansi Thor, 1932 The Japanese name newly established for the species re- (Acari: Ereynetidae) from South Africa. African Plant Protection fers to Mr. Nobuhiro Nyumura, who sampled the specimens 9: 23–26. examined in this study. Waki, T., Hiruta, S. F., and Shimano, S. 2018a. A new species of the genus Riccardoella (Acari: Prostigmata: Ereynetidae) from the land snail Tauphaedusa tau (Gastropoda: Clausliidae) in Japan. Acknowledgments Zootaxa 4402: 163–174. Waki, T., Shimano, S., Asami, T., Miyai, T., and Sasaki, T. 2018b. Ricca- We thank Mr. Nobuhiro Nyumura for providing mite rdoella reaumuri Fain & van Goethem, 1986 (Acariformes: Trom- samples. This work was supported by JSPS KAKENHI Grant bidiformes: Ereynetidae) from terrestrial mollusks in Okinawa- jima Island, as first record from Japan. The Biological Magazine Numbers JP15K07201 and JP18K06392 to S. S., and “LNest Okinawa 56: 27–31. Grant Natural History Award” to T. W. Walter, D. E., Lindquist, E. E., Smith, I. M., Cook, D. R., and Krantz, G. W. 2009. Order Trombidiformes. Chapter 13. Pp. 233–420. In: Krantz, G. W. and Walter, D. E. (Eds) A Manual of Acarology. References Texas Tech University Press, Lubbock. Zabludovskaya, S. and Badanin, I. 2010. The slug mite Riccardoella André, H. M., Ducarme, X., and Lebrun, P. 2004. New ereynetid mites (Proriccardoella) oudemansi (Prostigmata, Ereynetidae) from (Acari: Tydeoidea) from karstic areas: True association or sam- Ukraine. Vestnik Zoologii 44: 163–166.