Ecologica Montenegrina 22: 90-96 (2019) This journal is available online at: www.biotaxa.org/em

https://zoobank.org/urn:lsid:zoobank.org:pub:D1A0E6C6-D3EA-49AB-A7D7-34EF1EA5D953

Oribatid mites (Acari: Oribatida) phoretic on passalid (Coleoptera: Passalidae), with description of a new species from Indonesia

SERGEY G. ERMILOV

Tyumen State University, Tyumen, Russia. E-mail: [email protected]

Received 13 July 2019 │ Accepted by V. Pešić: 1 August 2019 │ Published online 25 August 2019.

Abstract A new species of oribatid mites (Oribatida) phoretic on the , Macrolinus batesi (Coleoptera, Passalidae) is described from Sumatra, Indonesia. Graptoppia (Stenoppia) royi sp. nov. (Oppiidae) differs from G. (S.) italica by the smaller body size, the presence of thin transcostula and the absence of costulae. Data on oribatids phoretic on passalid beetles are summarized; nine identified oribatid species (from 19 beetle species) are listed.

Key words: phoresy, Graptoppia (Stenoppia), Insecta, systematics, morphology, Sumatra.

Introduction

The phoretic association of some groups of mites (Acari) with beetles (Insecta, Coleoptera) is widely known, however, the phoresy of oribatid mites (Oribatida) remains poorly studied, and therefore, each new case of their phoresy is important and interesting to science. Some oribatid species have morphological adaptations for attachment to the beetles (e.g., phoretic ptyctimous mites clasps the body setae of hosts between the rostrum of the aspis and the anterior portion of the genital plates; some Oppiidae and Scheloribatidae have modified leg claws allowing mites to be attached to the hosts) (see Norton 1980; Ermilov & Frolov 2019a,b). The majority of oribatid species have no morphological adaptations for phoresy, however the hosts have many unexposed body places on the ventral side (e.g., various grooves, ditches, poles) and under elytra, where a phoretic mite could ‗hide‘ and held on any surface that has some irregularity using the force of the leg claws (Ermilov & Frolov 2019a). During the taxonomic identification of phoretic oribatids1 on the passalid beetle, Macrolinus batesi (Passalidae) from Indonesia, I found one new species belonging to the genus Graptoppia Balogh, 1983, the subgenus Stenoppia Balogh, 1983 (family Oppiidae). This subgenus comprises seven species, which are distributed in the Ethiopian, Neotropical and Oriental regions, as well as the Mediterranean and Japan (Ermilov & Frolov 2019a). The main diagnostic characters of Graptoppia (Stenoppia) were summarized by Balogh (1983), Subías & Balogh (1989), and Balogh & Balogh (1992). An identification key to known

1 Specimens were kindly sent me by Prof. Dr. Roy A. Norton (State University of New York, Syracuse, U.S.A.) from the personal collection.

Ecologica Montenegrina, 22, 2019, 90-96

ERMILOV species is presented by Ermilov & Frolov (2019a). The main goal of this paper is to describe and illustrate the new species based on adults under the name Graptoppia (Stenoppia) royi sp. nov., and to summarize data on phoresy of Oribatida on Passalidae.

Material and methods

Specimens were mounted in lactic acid on temporary cavity slides for measurement and illustration. All body measurements are presented in micrometers. Drawings were made with a camera lucida using a Leica transmission light microscope ―Leica DM 2500‖. Morphological terminology used in this paper follows that of F. Grandjean: see Travé & Vachon (1975) for references, Norton (1977) for leg setal nomenclature, and Norton & Behan–Pelletier (2009), for overview.

Systematics

Family Oppiidae Subfamily Multioppiinae Genus Graptoppia Balogh, 1983 Subgenus Graptoppia (Stenoppia) Balogh, 1983

Graptoppia (Stenoppia) royi sp. nov. (Figs 1, 2) Diagnosis. Body size: 164–176 × 73–90. Rostrum rounded. Costulae absent. Transcostula poorly developed. Rostral, lamellar and interlamellar setae setiform, slightly barbed; le located on transcostula. Bothridial setae long, with unilaterally dilated, ciliate, rounded distally head. Anterior notogastral margin rounded. Notogastral setae c minute, needle-form, other setae of medium size, setiform, slightly barbed. Epimeral and anogenital setae setiform, slightly barbed. Epimeral border IV semi-oval. Description of adult. Measurements. Body length: 172 (holotype: female), 164–176 (13 paratypes: 10 females and 3 males); notogaster width: 73 (holotype), 73–90 (13 paratypes). No difference between females and males in body size. Integument (Fig. 1A). Body color light brownish. Body surface smooth, but region between transcostula and interlamellar setae microgranulate (diameter of granules less than 1), and lateral parts of body between bothridia and acetabula I–III sparsely tuberculate (diameter of tubercles up to 2). Prodorsum (Figs 1A, 1C). Rostrum rounded. Costulae absent. Transcostula (tcos) present, thin, poorly visible. Lateral semi-oval ridges not observed. Rostral (ro, 12–14), lamellar (le, 8–10) and interlamellar (in, 8–10) setae setiform, slightly barbed; le inserted on transcostula. Exobothridial setae (ex, 4) setiform, thin, smooth. Bothridial setae (bs, 30–32) with long stalk and shorter, unilaterally dilated and ciliated, rounded distally head (with 8-9 cilia). Interbothridial region with two pairs of clear muscle sigillae. Interbothridial tubercles absent. Postbothridial tubercles slightly developed. Longitudinal rows of muscle sigillae anteriad to bothridia present. Notogaster (Figs 1A, 1C, 1D). Anterior margin rounded. Ten pairs of notogastral setae; c (4) needle- form, others (la, lm, lp, h1–h3, p1–p3, 12–14) setiform, slightly barbed. Opisthonotal gland openings (gla) and all lyrifissures (ia, im, ip, ih, ips) distinct. Gnathosoma (Figs 2A–2C). Subcapitulum longer than wide (36–41 × 28–32). Subcapitular setae (a, m, h, 10–12) setiform, slightly barbed. Adoral setae (or1, or2, 4) setiform, thin, smooth. Palps (28–32) with typical setation 0-2-1-3-9(+ω). Postpalpal setae (4) thorn-like, smooth. Chelicerae (36–41) with two setiform, barbed setae (cha, 10–12; chb, 6–8). Trägårdh‘s organ (Tg) of chelicerae narrowly triangular. Epimeral and lateral podosomal regions (Figs 1B, 1C). With typical epimeral setal formula 3-1-3-3. Setae setiform, slightly barbed; 3c (12) longer than 1b, 3b, 4a, 4b, 4c (8) and 1a, 1c, 2a, 3a (6–8). Discidia triangular, rounded distally. Epimeral border IV distinct, semi-oval. Anogenital region (Figs 1B–D). Four pairs of genital (g1–g4, 6), one pair of aggenital (ag, 8), two pairs of anal (an1, an2, 8) and three pairs of adanal (ad1–ad3, 8) setae setiform, slightly barbed. Adanal lyrifissures (iad) located close and parallel to anal plates.

Ecologica Montenegrina, 22, 2019, 90-96 91

ORIBATID MITES PHORETIC ON PASSALID BEETLES

FIGURE 1. Graptoppia (Stenoppia) royi sp. nov., adult: A — dorsal view (legs not shown); B — ventral view (gnathosoma and legs not shown); C — anterior part of body (gnathosoma and legs not shown), lateral view; D — posterior part of body, lateral view. Scale bar 50 μm.

92

ERMILOV

FIGURE 2. Graptoppia (Stenoppia) royi sp. nov., adult: A — subcapitulum, ventral view; B — palp, right, antiaxial view; C — chelicera, right, antiaxial view; D — leg I, without trochanter, right, antiaxial view; E — femur and genu of leg II, left, dorsoantiaxial view; F — trochanter, femur and genu leg III, right, paraxial view; G — leg IV, left, antiaxial. Scale bar 10 μm (A; B; C; D–G).

Ecologica Montenegrina, 22, 2019, 90-96 93

ORIBATID MITES PHORETIC ON PASSALID BEETLES

Legs (Figs 1D–G). Claw on leg tarsi smooth. Porose area on femora and on trochanters III and IV not observed. Formulas of leg setation and solenidia: I (1-5-2-4-19) [1-2-2], II (1-5-2-4-16) [1-1-2], III (2-3- 1-3-15) [1-1-0], IV (1-2-2-3-12) [0-1-0]; homology of setae and solenidia indicated in Table 1. Setae p setiform on tarsi I, and very short, conical on tarsi II–IV. Famulus of tarsi I erect, blunt-ended, inserted posterior to solenidion ω1. Solenidia ω1 on tarsi I, ω1 and ω2 on tarsi II, φ on tibiae I–III and σ on genua III bacilliform, ω2 on tarsi I and φ2 on tibiae I slightly thickened, slightly blunt-ended, other solenidia setiform.

TABLE 1. Leg setation and solenidia of adult Graptoppia (Stenoppia) royi sp. nov. Leg Tr Fe Ge Ti Ta (ft), (tc), (it), (p), (u), (a), s, (pv), v’, (pl), I v’ d, (l), bv”, v” (l), σ (l), (v), φ1, φ2 ɛ, ω1, ω2 II v’ d, (l), bv”, v” (l), σ (l), (v), φ (ft), (tc), (it), (p), (u), (a), s, (pv), l”, ω1, ω2 III l’, v’ d, l’, ev’ l’, σ l’, (v), φ (ft), (tc), (it), (p), (u), (a), s, (pv) IV v’ d, ev’ d, l’ l’, (v), φ ft”, (tc), (p), (u), (a), s, (pv)

Note: Tr, Fe, Ge, Ti, Ta – leg trochanter, femur, genu, tibia, tarsus, respectively. Roman letters refer to normal setae, Greek letters to solenidia (except ɛ = famulus). Single prime (’) marks setae on anterior and double prime (”) setae on posterior side of the given leg segment. Parentheses refer to a pair of setae.

Material examined. Holotype (female) and 13 paratypes (10 females and 3 males): Indonesia, Sumatra, Batang Makat Forest, in various ventral grooves on pro- and mesothorax (morphological adaptations for attachment are absent in mites) of passalid beetle, Macrolinus batesi Kuwert, 1898, [collection date is unknown] in the year of 1937 (Coll. C.T. & B.B. Brues). Type deposition. The holotype and two paratypes are deposited in the collection of the Smithsonian Institution, Museum of Natural History, Washington, D.C., U.S.A.; 11 paratypes are deposited in the collection of the Tyumen State University Museum of Zoology, Tyumen, Russia. All type specimens are in ethanol with a drop of glycerol. Etymology. The species name is dedicated to the well-known acarologist, Prof. Dr. Roy A. Norton (State University of New York, Syracuse, U.S.A.) for his extensive contributions to our knowledge of mites. Differential diagnosis. Graptoppia (Stenoppia) royi sp. nov. is morphologically most similar to Graptoppia (Stenoppia) italica (Bernini, 1973) from the Mediterranean in having transcostula, rounded rostrum, ciliate bothridial setae, short exobothridial setae, rounded anterior margin of notogaster and barbed notogastral setae, but differs from the latter by the smaller body size (164–176 × 73–90 versus 207 × 105), the presence of thin transcostula and the absence of costulae (versus costulae and transcostulae thick, forming trapezoid structure).

General remarks

As it was noted earlier (Norton 1980; Ermilov & Frolov 2019a), beetles of the family Passalidae are one of the representatives of Coleoptera which are actively used by oribatid mites for phoresy. Norton (1980) presented data on unidentified Mesoplophora, Malaconothrus, Oppia, Protoribates, Scheloribates and Metaleius spp. phoretic on 19 identified and one unidentified species of Passalidae ( interruptus, P. interstitialis, P. morio, P. punctiger, Passalus sp., Popilius disjunctus, Proculus goryi, Verres longicornis, Ptichopus angulatus, Labienus compergus, L. inaequalis, L. ptox, Macrolinus batesi, M. latipennis, Aceraius grandis, A. helferi, A. laevicollis, A. pilifer, Erionomus planiceps, E. platypleura), which were collected from the different regions of the world. Later, Niedbała (1985, 2000) identified many Mesoplophora spp. from these materials, having recorded: Mesoplophora (Mesoplophora) permodica Niedbała, 1985 phoretic on Popilius disjunctus (U.S.A.); Mesoplophora (Parplophora) flavida Niedbała, 1985 on Aceraius helferi (Thailand), A. laevicollis (Indonesia), A. pilifer (Philippines), and Macrolinus latipennis (Indonesia); M. (P.) polita Niedbała, 1985 on Labienus inaequalis, and L. ptox (both New Guinea); M. (P.) subtilis Niedbała, 1981 on Aceraius laevicollis (Indonesia), Labienus inaequalis, L. ptox (both New Guinea), Passalus interruptus (Surinam), P. interstitialis (Honduras), P. punctiger (Brazil, Honduras), and P. sp. (Panama). Franklin & Woas (1992) described Neoamerioppia phoretica (Franklin & Woas, 1992) phoretic on unknown passalid beetle from Brazil.

94

ERMILOV

Corpuz-Raros (1992) noted some species of oribatid mites on unknown passalids from the Philippines, however, these mites were located loosely on beetles (pers. com. Dr. L.A. Corpuz-Raros), therefore, it is premature to consider them active phoretic species. Ermilov & Frolov (2019) registered five species (Mesoplophora (Parplophora) flavida, M. (P.) polita, Graptoppia (Stenoppia) luisi Ermilov & Frolov, 2009, Ramusella (Sabahoppia) blattarum (Oudemans, 1911), and Perscheloribates kontumensis Ermilov & Frolov, 2009) phoretic on A. grandis from Vietnam. Hence, 19 identified beetle species of Passalidae, which were used by oribatid mites as hosts for active phoresy, are known; and only nine identified oribatid species (and also some not identified species) phoretic on these passalids are registered. Thus, the phoresy of oribatids on beetles (first of all on Passalidae) remains a poorly studied aspect of acarology, and requires further detailed faunistic and ecological researches for understanding of relationship between Oribatida and Insecta.

Acknowledgements

I cordially thank Prof. Dr. Roy A. Norton (State University of New York, Syracuse, U.S.A.), who kindly presented specimens of the new oppiid species for my study; and two anonymous reviewers for valuable comments.

References

Balogh, J. (1983) A partial revision of the Oppiidae Grandjean, 1954 (Acari: Oribatei). Acta Zoologica Academiae Scientiarum Hungaricae, 29 (1–3), 1–79. Balogh, J. & Balogh, P. (1992) The oribatid mites genera of the World. Vol. 1. Hungarian National Museum Press, Budapest, 263 p. Bernini, F. (1973) Notulae oribatologicae VII. Gli Oribatei (Acarida) dell‘isolotto di Basiluzzo (Isole Eolie). Lavori Della Societa Italiana di Biogeografia, Nuova Serie, 3, 355–480. Corpuz-Raros, L. (1992) Oribatid mites (Acari: Oribatida) from the Visayas and Palawan, Philippines. Asia Life and Sciences, 1 (1–2), 75–109. Ermilov, S.G. & Frolov, A.V. (2019a) New and interesting oribatid mites (Acari, Oribatida) phoretic on Aceraius grandis (Coleoptera, Passalidae) from Vietnam. Systematic and Applied Acarology, 24 (5), 945–961. Ermilov, S.G. & Frolov, A.V. (2019b) Ramusella (Dosangoppia) bochkovi (Acari, Oribatida, Oppiidae), a new subgenus and species of oribatid mites phoretic on Ceratophyus polyceros (Pallas, 1771) (Coleoptera, Geotrupidae) from Russia. Systematic and Applied Acarology, 24(2), 209–221. Franklin, E. & Woas, S. (1992) Some oribatid mites of the family Oppiidae (Acari, Oribatei) from Amazonia. Andrias, 9, 5–56. Kuwert, A. (1898) Die Passaliden Dichotomisch Bearbeitet. Novitates Zoologicae, 5, 137–205. Niedbała, W. (1981) Mesoplophora subtilis sp. n. de Pérou (Acari, Oribatida, Mesoplophoridae). Polskie Pismo Entomologiczne, 51, 511–517. Niedbała, W. (1985) Essai critique sur Mesoplophora (Acari, Oribatida, Mesoplophoridae). Annales Zoologici, 39 (4), 93–117. Niedbała, W. (2000) The ptyctimous mites fauna of the Oriental and Australian regions and their centers of origin (Acari: Oribatida). Genus (Supplement), 1–493. Norton, R.A. (1977) A review of F. Grandjean's system of leg chaetotaxy in the Oribatei (Acari) and its application to the family Damaeidae. In: Dindal, D.L. (Editor), Biology of oribatid mites. SUNY College of Environmental Science and Forestry, Syracuse, pp. 33–61. Norton, R.A. (1980) Observations on phoresy by oribatid mites (Acari: Oribatei). International Journal of Acarology, 6 (2), 121–130. Norton, R.A. & Behan-Pelletier, V.M. (2009) Oribatida. Chapter 15. In: Krantz, G.W. & Walter, D.E. (Editors), A Manual of Acarology. Texas Tech University Press, Lubbock, pp. 430–564. Oudemans, A.C. (1911) Acarologische Aanteekeningen XXXVII. Entomologische Berichten, 61 (3), 165–

Ecologica Montenegrina, 22, 2019, 90-96 95

ORIBATID MITES PHORETIC ON PASSALID BEETLES

175. Subías, L.S. & Balogh, P. (1989) Identification keys to the genera of Oppiidae Grandjean, 1951 (Acari: Oribatei). Acta Zoologica Hungarica, 35 (3–4), 355–412. Travé, J. & Vachon, M. (1975) François Grandjean. 1882–1975 (Notice biographique et bibliographique). Acarologia, 17 (1), 1–19.

96