NORTH-WESTERN JOURNAL OF ZOOLOGY 7 (1): pp.132-137 ©NwjZ, Oradea, Romania, 2011 Article No.: 111115 www.herp-or.uv.ro/nwjz

Morphology of juvenile stages of Acrotritia ardua (Koch, 1841) (, , )

Sergey G. ERMILOV

Laboratory of Entomology, Phytosanitary Department, Nizhniy Novgorod Referral Сenter of the Federal service for Veterinary and Phytosanitary Inspection, Gagarin 97, 603107 Nizhniy Novgorod, Russia, E-mail: [email protected]

Received: 20. December 2009 / Accepted: 08. April 2011 / Available online: 01. May 2011

Abstract. The morphology of juvenile stages of the oribatid , Acrotritia ardua is described and illustrated. The body form of all juveniles were cylindrical, little extended, and not ptychoid. Prodorsal and gastronotic setae were of different lengths, setiform and smooth. Sensilli were absent. Bothridia present only as small ves- tiges. Formulas of body setation (larva to tritonymph): genital (0–1–4–7), aggenital (0–0–2–2), anal (0–0–0–3), adanal (0–0–3–3), gastronotic (12–14–14–14) and epimeral (3–1–2, 3–1–2–1, 3–1–3–2, 3–1–3–3). Palpal setation similar for all juvenile stages: 1–2–8(+1). Leg tarsi II–III without setae pv; tarsi IV without setae a; tarsi III without setae ft' or s. The larva of Acrotritia ardua is very similar to that of Acrotritia clavata sextiana; only slight differences were found in the following characters: sizes of body and length of some setae; setal formula of palps; number of setae on leg II tibia.

Key words: oribatid mite, Acrotritia ardua (Koch, 1841), morphology, juvenile stages, ontogeny.

Introduction cluded some traits in papers that were focused on specific body features. These include, for example: The ptychoid oribatid include more than 20 formulas of gastronotic, anal, adanal, genital, ag- genera and 1000 species that are collectively wide- genital and epimeral setae; formulas of solenidia spread (Subías 2004). Juvenile stages have been and setae of some segments of legs (Grandjean studied for a relatively few of the species, namely: 1933, 1934b, 1934c, 1949, 1964). Phthiracaridae (Phthiracarus anonymus Grandjean, Of the many species in Acrotritia Märkel & 1933, P. japonicus Aoki, 1958) (Grandjean 1934a, Meyer, 1959, the only juvenile that is well de- 1950, Soma 1990), Oribotritiidae ( megale scribed is the larva of Acrotritia clavata sextiana (Li- (Walker, 1965), Indotritia krakatauensis (Sellnick, ons, 1966). In the present paper we describe the ac- 1923) (=I. acanthophora Märkel, 1964), Paratritia ba- tive juvenile stages of Acrotritia ardua, and com- loghi Moritz, 1966, Sabacarus corneri Ramsay, pare the larvae of these two species. Sheals, 1969) (Walker 1965, Schubart 1967, Travé 1975), Euphthiracaridae (Acrotritia clavata sextiana Lions, 1966) (Lions 1966). For some genera and Material and methods families the juvenile stages remain poorly known, Most of the studied specimens of Acrotritia ardua were or not yet discovered. Adults are widespread in collected by the author in the Nizhniy Novgorod region forest soils, however juveniles are not numerous (European part of Russia) during the spring, summer and in samples. The reason they are not common in autumn of 2000–2002, 2007–2009. Juvenile stages were soil is that the juveniles (like those of all Ptyctima) found in the soil of pine (Volodarskiy district: 56º12'N, are burrowers in woody substrates. 43º22'E; Balakhninskiy district: 56º23'N, 43º36'E and The purpose of the present work is to describe 56º25'N, 43º36'E; Uren district: 57º27'N, 45º47'E) and mixed (Volodarskiy district: 56º15'N, 43º40'E; Se- and illustrate the morphology of all the juvenile menovskiy district: 57º03'N, 44º52'E) forests. The field- stages of the cosmopolitan species Acrotritia ardua collected materials include 35 juveniles of Acrotritia ardua: (Koch, 1841). The egg of Acrotritia ardua was de- 3 protonymphs, 14 deutonymphs, and 18 tritonymphs. scribed and illustrated earlier (Grandjean 1940, Moreover, additional specimens of juvenile stages were Baran & Ayyildiz 2000), as well as prelarva (Lions obtained from laboratory cultures (24 larvae, 18 proto- 1967). Adults of Acrotritia ardua were redescribed nymphs, 3 deutonymphs). Methods of cultivation were and illustrated by several authors (Märkel 1964, presented earlier (Ermilov & Lochynska 2008). All cul- tures began with adults. In the cultures all adult speci- Krivolutskiy 1975, Baran & Ayyildiz 2000, Weig- mens and juvenile stages feed semidecayed leaves of trees mann 2006). Grandjean (1967) noted that he stud- (Betula pendula, Quercus robur) and algae (Pleurococcus sp.). ied all the juvenile stages of Acrotritia ardua, but Terminology used in this paper follows Grandjean rather than describing them completely, he in- (see Travé & Vachon 1975 for references and Norton & Morphology of juvenile stages of Acrotritia ardua 133

Behan-Pelletier 2009, for overview). The illustrated specimens were permanently mounted and studied on flat microscope slides however, the measured specimens were temporarily mounted and studied on cavity micro- scope slides. All body measurements are presented in mi- crometers. All formulas of leg setation (see Table 2) are given, in order trochanter-femur-genu-tibia-tarsus (famulus in- cluded). All formulas of leg solenidia are given, in order genu-tibia-tarsus.

Results

Measurements and general form. Total length of: larva 164–217 (mean 189, n=14), protonymph 274– 295 (mean 285, n=13), deutonymph 381–398 (mean 391, n=10), tritonymph 481–564 (mean 515, n=15). Total width of: larva 82–94 (mean 87, n=12), protonymph 123–131 (mean 127, n=8), deuto- nymph 166–182 (mean 174, n=4), tritonymph 215–

265 (mean 236, n=4). The Bodies of all juveniles were longer than wide, approximately 2.2 times; Figures 1–3. Acrotritia ardua, larva: 1 – dorsal view, legs roughly cylindrical, little extended and not removed; 2 – ventral view, legs partly removed; 3 – lateral view, legs partly removed. Scale bar 50 μm. ptychoid.

Integument. General body cuticle weakly scle- rotized, colourless, smooth. Rutelli of subcapitu- lum and digits of chelicerae light brown. Prodorsum (Figs 1, 3, 10). Relatively short in all juveniles, about half-length of gastronotic region in lateral view. Outline roughly trapezoidal in dorsal view, rostrum widely rounded, with short sharp tip. Lateral parts of prodorsum with scle- rotized ribs. Rostral (ro), lamellar (le), interlamellar (in) setae long, setiform, smooth, with flagellate tips. Setae ro inserted on tip of rostrum. Setae le in- serted anteromedially to setae in. Setae in longest.

Setae ro longer than setae le in larvae and proto- nymphs, but shorter than le in deuto- and trito- Figures 4–6. Acrotritia ardua, larva: 4 – subcapitulum; 5 – palp; 6 – chelicera. Scale bar 20 μm. nymphs. Sensilli absent. Bothridia developed only as small but distinct vestigial opening (bo). Exobothridial setae (ex) very small, ventral to Gastronotic region (Figs 1-3, 10-13). Broadly bothridium. Comparison of prodorsal setae meas- oval. Rounded posteriorly. Larva with 10 pairs of urements of juvenile stages given in Table 1. gastronotic setae (c1–c3, cp, d1, d2, e1, e2, h1, h2).

Table 1. Prodorsal setae measurements of Acrotritia ardua during ontogeny.

Larva, Protonymph, Deutonymph, Tritonymph, Character mean (min-max) mean (min-max) mean (min-max) mean (min-max) n=9 n=7 n=7 n=10 Length ro 43 (41–45) 56 (49–61) 74 (69–77) 90 (82–98) Length le 29 (28–32) 46 (41–53) 76 (73–82) 98 (94–102) Length in 57 (53–65) 77 (73–82) 133 (123–139) 172 (155–180) Length ss Absent Absent Absent Absent Length ex 1 (1–2) 2 (2–4) 2 (2–4) 3 (2–4)

134 Ermilov, S.G.

of e-series (ar3), best seen in lateral view (Fig. 3).

Cupules ia, im, ip well visible in all stages laterally. Anogenital region (Figs 2, 3, 10-13). Ontogenetic genital, aggenital, adanal, anal formulas (larva to tritonymph): 0–1–4–7, 0–0–2–2, 0–0–3–3, 0–0–0–3 respectively. Genital and aggenital setae short, smooth; adanal and anal setae longer, setiform,

smooth (ad1=ad2>ad3; an1=an2>an3). Cupules ih, ips, iad and small opisthosomal gland opening (gla) well visible, appearing in normal ontogenetic pat- tern. Epimeral region (Figs 2, 3, 11). Nymphal epimera with paired, smooth plates having weakly defined borders. Setal formulas for epimera: larva 3–1–2; protonymph 3–1–2–1; deu- tonymph 3–1–3–2; tritonymph 3–1–3–3. Larval seta 1c scale-like, covering tip of retracted Cla-

Figures 7–9. Acrotritia ardua, larva: legs I–III, parède’s organ (Cl; organ extended between bases respectively. Scale bar 50 μm. of legs I and II in figures), inserted in distinct al- veolus. Epimeral setae setiform, smooth; setae 1b, Nymphs with 14 pairs of gastronotic setae (setae 3c, 4c longest, with flagellate tips. h3, p1–p3 appeared). Gastronotic setae long, seti- Gnathosoma (Figs 4–6). Subcapitulum sten- form, smooth; some setae with flagellate tips. Se- arthric. Hypostomal setae a, m, h setiform, smooth; tae of f-row absent; vestigial alveoli of f1 well or setae m little shorter. Lateral lips with 3 pairs of weakly visible, alveoli of setae f2 weakly visible or setiform, barbed adoral setae (or). Palps with 3 not visible. Relative lengths of gastronotic setae in segments; total length: larva 32–36 (mean 34, n=4), larva: setae e1 longest, setae e2 slightly shorter; protonymph 41 (n=4), deutonymph 53–61 (mean other setae much shorter; in nymphs: setae e1, h1 57, n=4), tritonymph 73–82 (mean 75, n=4). Palpal longest, other setae much shorter. Distinct simple setation similar for all juvenile stages: 1–2–8(+1ω). transverse linear groove present posterior to setae Seta v' in first segments thin, smooth. Setae d and

Figures 10–13. Acrotritia ardua, nymphs: 10 – protonymph, lateral view, legs partly removed; 11 – protonymph, ventral view, legs partly removed; 12 – deutonymph, hysterosoma, lat- eral view, legs III, IV partly removed. Scale bars 10–12 100 μm, 13 200 μm.

Morphology of juvenile stages of Acrotritia ardua 135

Figures 14–15. Acrotritia ardua, tarsi of legs: 14 – tarsus Figures 16–19. Acrotritia ardua, tritonymph: legs I– I of protonymph, 15 – tarsus I of deutonymph. IV, respectively. Scale bar 50 μm. Scale bar 20 μm.

v' in second segment setiform, barbed. Tarsi with Table 2. Setal and solenidial counts on legs of Acrotritia ardua during ontogeny. following setae: cm, (it), acm, (ul), sul, v1''. Seta cm thorn-like, smooth; setae it setiform, barbed; seta Formula of Formula of vl'' thorn-like, barbed; others setae more or less setae solenidia rod-like, straight, smooth. Palpal solenidion very Leg I long, longer than tarsus, blunt-ended. Fixed and Larva 0–2–2–4–14 2–1–1 Protonymph 0–2–2–4–14 2–1–2 movable digits of chelicerae each with 4–5 blunt Deutonymph 1–2–2–4–14 2–1–2 teeth. Cheliceral setae (cha, chb) short, smooth, Tritonymph 1–2(3)–2–5–16 2–1–3 slightly blunt-ended. Length of chelicerae: larva Leg II 73–82 (mean 77, n=5), protonymph 86–94 (mean Larva 0–2–2–4–11 1–1–1 90, n=3), deutonymph 114–127 (mean 118, n=4), Protonymph 0–2–2–4–11 1–1–1 tritonymph 123–143 (mean 130, n=6). Deutonymph 1–2–2–4–11 1–1–2 Legs (Figs 7–9, 14–19). Tarsi with 1 simple Tritonymph 1–2(3)–2–4–13 1–1–2 claw. Setae long, setiform. Most setae with minute Leg III barbs (visible only under high magnification). Larva 0–2–1–3–9 1–1–0 Tarsi II–III without setae pv; tarsi IV without setae Protonymph 0–2–1–3–9 1–1–0 Deutonymph 1–2–1–3–9 1–1–0 a; tarsi III without setae ft' and s. Seta ft' of tarsi I, Tritonymph 2–2–1–3–11 1–1–0 II anterolateral to solenidion ω1 in larva and Leg IV protonymph (Fig. 14), but posterolateral to ω1 (Fig. Protonymph 0–0–0–0–7 0–0–0 15) in deuto- and tritonymph. Solenidia ω1 (on Deutonymph 1–1–1–2–10 0–1–0 tarsi I) and ω1, ω2 (on tarsi II) long, thick, blunt- Tritonymph 2–1–1–2–10 0–1–0 ended. Genua I with coupled small seta l' and so- lenidion σ'. Seta d of nymphal genua I-III ex- pressed only as vesitigal alveolus (especially well Discussion visible in tritonymphs; see also Grandjean 1942). Deuto- and tritonymphal femur IV with only one The larva of Acrotritia ardua is very similar in body seta, ev'; seta d appears in adults only. Ontogeny structure to that of Acrotritia clavata sextiana, which of leg setae and solenidia given in Tables 2 and 3. is the only juvenile of Euphthiracaridae described

136 Ermilov, S.G.

Table 3. Development of leg setation of Acrotritia ardua*

Trochanter Femur Genu Tibia Tarsus Leg I

Larva – d, bv'' (l), σ, σ' d, l', (v), φ (ft), (tc), (p), (u), (a), s, (pv), e, ω1

Protonymph – – – – ω2 Deutonymph v' – – – –

Tritonymph – l'' (20%) – l'' (it), ω3 Leg II

Larva – d, bv'' (l), σ d, l', (v), φ (ft), (tc), (p), (u), (a), s, ω1 Protonymph – – – – –

Deutonymph v' – – – ω2 Tritonymph – l'' (20%) – – (it) Leg III Larva – d, ev’ l', σ d, l', v', φ ft'', (tc), (p), (u), (a) Protonymph – – – – – Deutonymph v' – – – – Tritonymph l' – – – (it) Leg IV Protonymph – – – – ft'', (p), (u), (pv) Deutonymph v' ev' d d, v', φ (tc), s Tritonymph l' – – – –

*Roman letters refer to normal setae, Greek letters refer to solenidia, e - famulus. One apostrophe (') marks setae on ante- rior and double apostrophe (") setae on posterior side of the given leg segment. Parentheses refer to a pair of setae. Setae are listed only for the stage in which they first appear.

(Lions 1966). Only slight differences between them cuse, NY, USA, for his consultations and help with col- can be found using literature data, but other dif- lecting literature, for his thorough review of this manu- ferences are found during direct comparison of script and many valuable suggestions. specimens.

1) Larvae of Acrotritia ardua are slightly smaller: length 189, width 87 in Acrotritia ardua; References 212, 104, respectively in Acrotritia clavata sextiana. Baran, S., Ayyildiz, N. (2000): Systematic studies on 2) Length of le: 29 in A. ardua; 20 in A. clavata ardua (C.L. Koch) (Acari, Oribatida) in Erzincan and Erzurum sextiana. Plains. Turkish Journal of Zoology 24: 231-236. 3) Length of in: 57 in A. ardua; 66 in A. clavata Ermilov, S.G., Lochynska, M. (2008): The influence of temperature on the development time of three oribatid mite species (Acari, sextiana. Oribatida). North-Western Journal of Zoology 4: 274-281. 4) Formula of palps: 1–2–8+1 in A. ardua; 1–2– Grandjean, F. (1933): Étude sur le développement des Oribates. 7+1 in A. clavata sextiana. Bulletin de la Société zoologique de France 58: 30-61. Grandjean, F. (1934a): Phthiracarus anonymum n. sp. Revue française 5) Tibia of legs II: with 4 setae in A. ardua; with d’Entomologie 1: 51-58. 3 setae in A. clavata sextiana. Grandjean, F. (1934b): Observations sur les Oribates (6e série). Larvae of Acrotritia ardua and Acrotritia clavata Bulletin de Muséum 6: 353-360. Grandjean, F. (1934c): Les poils des épimières chez les Oribates sextiana are similar in many other characters, for (Acariens). Bulletin de Muséum 6: 504-512. example: form of body; type of body setae; in > ro Grandjean, F. (1940): Observations sur les Oribates (15e série). > le; absence of sensilli; bothridia not developed; Bulletin de Muséum 12: 332-339. Grandjean, F. (1942): La chaetotaxie comparée des pattes chez les identical setations on gastronotum, epimera and Oribates (2e série). Bulletin de la Société zoologique de France legs (except tibia II); arrangement of body setae, 67: 40-53. cupules, gla; presence of linear groove (ar3). Grandjean, F. (1949): Formules anales, gastronotiques, génitales et aggénitales du développement numérique des poils chez les Descriptions of juvenile stages of ptychoid Oribates. Bulletin de la Société zoologique de France 74: 201-225. mites are scarce and often incomplete, therefore, a Grandjean, F. (1950): Observations sur les Oribates (20e série). meaningful comparison of genera or families is Bulletin de Muséum 22: 73-80. Grandjean, F. (1964): La solénidiotaxie des Oribates. Acarologia 6: currently not feasible. 529-556. Grandjean, F. (1967): Nouvelles observations sur les Oribates (5e série). Acarologia 9: 242-272. Krivolutskiy, D.A. (1975): Family Euphthiracaridae Jacot, 1931. pp. Acknowledgements. The author cordially thanks Prof. 374-377. In: Ghilyarov, M.S. (ed.), Key to soil inhabiting mites. . Nauka, Moscow. Dr. Roy A. Norton, State University of New York, Syra-

Morphology of juvenile stages of Acrotritia ardua 137

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