Contributions to the Turkish Oribatid Fauna (Acari: Oribatida) from Bolu Province

Turk J Zool 2011; 35(1): 63-70 © TÜBİTAK Research Article doi:10.3906/zoo-0905-1

Contributions to the Turkish oribatid fauna (Acari: Oribatida) from Bolu province

Ayşe TOLUK*, Nusret AYYILDIZ Erciyes University, Faculty of Science, Department of Biology, 38039 Kayseri - TURKEY

Received: 04.05.2009

Abstract: Four oribatid mites new to the Turkish fauna, namely Licneremaeus licnophorus (Michael, 1882), Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942), Lauroppia maritima acuminata (Strenzke, 1951), and Banksinoma lanceolata lanceolata (Michael, 1885), collected from Bolu province, Turkey, are given with their drawings and SEM photographs. On the basis of the collected samples, their morphological features and distributions in the world are also presented.

Key words: Acari, Oribatida, Licneremaeidae, Oppiidae, Thyrisomidae, taxonomy, new records, Bolu, Turkey

Bolu ilinden Türkiye oribatid faunasına katkılar (Acari: Oribatida)

Özet: Bolu ilinden toplanan ve Türkiye faunası için yeni olan dört oribatid akar türü; Licneremaeus licnophorus (Michael, 1882), Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942), Lauroppia maritima acuminata (Strenzke, 1951) ve Banksinoma lanceolata lanceolata (Michael, 1885) ışık mikroskobu çizimleri ve elektron mikroskobu fotoğrafları ile birlikte verilmiştir. Ayrıca, bu türlerin örneklerimiz üzerinden morfolojik özellikleri ile dünyadaki dağılışları hakkında da bilgiler sunulmuştur.

Anahtar sözcükler: Acari, Oribatida, Licneremaeidae, Oppiidae, Thyrisomidae, taksonomi, yeni kayıtlar, Bolu, Türkiye

Introduction Toluk and Ayyıldız, 2008a, 2008b, 2008c, 2009a, Oribatid mites play an important role in 2009b; Toluk et al., 2009). Works on the oribatid mites decomposition of plant litter, in nutrient cycling, in ofTurkeydonotmentionanydatafromBolu soil formation, and in distribution of fungal spores. province (Erman et al., 2007). They are probably the most numerous of the soil The taxa reported in this study belong to the mites, with about 10,000 species being listed in the oribatid mite families of Licneremaeidae Grandjean, latest version of the world mite catalogue (Subías, 1931; Oppiidae Sellnick, 1937; and Thyrisomidae 2009). Works on oribatid mites of Turkey have Grandjean, 1953. The family Licneremaeidae is gradually increased in the recent years (Baran and distinguished by the short and wide prodorsum, short Ayyıldız, 2007a, 2007b, 2009; Erman et al., 2007; parallel costulae, expanded leaf-like sensilla,

* E-mail: [email protected]

63 Contributions to the Turkish oribatid fauna (Acari: Oribatida) from Bolu province

integument with a reticulate pattern or small granules, The terminology used in this paper follows 5 pairs of genital setae, 2 pairs of anal setae, the Grandjean (see Travé and Vachon, 1975), Balogh absence of aggenital setae, and tarsi with 3 claws. This (1983), and Subías and Balogh (1989). The specimens family includes 2 genera that are represented by 18 examined were deposited in the acarological species, and it is cosmopolitan (except Antarctica) in collection of the Zoological Museum of Erciyes distribution; formerly, none of them were known University, Kayseri, Turkey. from Turkey (Erman et al., 2007; Subías, 2009). The family Oppiidae is characterized by the Results presence and absence of costulae and cristae; highly varied sensilla; rostrum with 1 or 2 incisions, or entire Licneremaeidae Grandjean, 1931 and rounded; the presence and absence of setae ta; Licneremaeus Paoli, 1908 genital and anal plates of normal size, separated by a Type-species: Notaspis licnophorus Michael, 1882 distance usually equal to or greater than the length of Licneremaeus licnophorus the latter; 4-6 pairs of genital setae; and fused (Michael, 1882) (Figures 1 and 2.) epimeres III and IV. This family includes 129 genera and 36 subgenera, which are represented by 934 Measurements – Length: 208-220 μm, width: 120- species and 48 subspecies, and it is cosmopolitan in 128 μm (n = 9). distribution (Subías, 2009). Until now, 32 species and Prodorsum – Rostrum widely rounded. Rostral, 7 subspecies of the family Oppiidae were known from lamellar, and interlamellar setae smooth. Lamellae Turkey (Toluk and Ayyıldız, 2008a, 2008b, 2008c, well developed. Translamella straight and situated in 2009a, 2009b; Toluk et al., 2009). front of notogaster anterior margin. Sensilla The family Thyrisomidae is distinguished by flabelliform, anteriorly disciform. normal chelate and dentate chelicerae; long or short Notogaster – Surface of notogaster with large costulae, with a translamella; large genital and anal chitin laths. Anterior part of notogaster with a well plates, between them half the length of the latter or discernible chitinous lath longitudinally; its anterior less; 6 pairs of genital setae; and 2 pairs of anal setae. margins conspicuously narrowed; anterior margin This family includes a single genus, which is reaching to transversal lamella. A round lenticulus represented by 19 species and 5 subspecies, and it is present on its anterior part. Thirteen pairs of smooth cosmopolitan (except Ethiopia and Antarctica) in notogastral setae present. distribution; formerly, none of them were known from Turkey (Erman et al., 2007; Subías, 2009). In the present paper, the morphological features of 4 oribatid mite species that are new to the Turkish fauna are presented. The ventral drawings of Lauroppia maritima acuminata (Strenzke, 1951) and Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942) are given for the first time. The main goal of our research is to contribute to the knowledge of the Turkish oribatid fauna (Acari).

Materials and methods All material was collected in soil and litter samples from Bolu province, Turkey. The techniques used in A B the collecting, extraction, and preparation of the examined oribatid mites follow those proposed by Figure 1. Licneremaeus licnophorus (Michael, 1882): A) Dorsal Toluk et al. (2007). view, B) Ventral view (scale bar = 100 μm).

64 A. TOLUK, N. AYYILDIZ

100 µm A B

10 µm

100 µm 20 µm

C D

20 µm

Figure 2. Licneremaeus licnophorus (Michael, 1882): A) Dorsal view, B) Sensillum, C) Ventral view, D) Infracapitulum and epimeral regions, E) Genital and anal plates.

Ventral side – Ventralplatewithapolygonal Material examined – Turkey, Bolu province, sculpture. Epimeral borders distinctly visible and Gölcük lakeside, 40°39´37˝N, 31°37´38˝E, 1218 m, 10 strongly sclerotized. Epimeral setal formula 3-1-3-3. May 2008, grassy soil, 19 exs (2 of them were mounted Genito-anal region setal formula 5:0:2:2. Lyrifissures iad situated paraanally. Adanal setae ad1 in postanal, on aluminum stubs and gold-coated for scanning ad2 in paraanal, and ad3 in preanal position. electron microscopy).

65 Contributions to the Turkish oribatid fauna (Acari: Oribatida) from Bolu province

Distribution – Holarctic region (Subías, 2009). New record for Turkish fauna. Remarks – The body length is given as 200-210 μm by Pérez-Íñigo (1993) and 200-210 μm by Miko (2006). In this regard, the Turkish specimens (208- 220 × 120-128 μm) are in the range of the known dimensions of the species. This species is well characterized by the shape of sensilla, lamellae, and notogaster; ventral plate with a polygonal sculpture; and 13 pairs of smooth notogastral setae. In this regard, the Turkish specimens closely resemble the species in all features. Oppiidae Sellnick, 1937 Oppiellinae Seniczak, 1975

Moritzoppia Subías and Rodriguez, 1988 AB Type-species: Oppia keilbachi Moritz, 1969 Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942) (Figures 3 and 4.) Figure 3. Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942): A) Dorsal view, B) Ventral view (scale bar = 100 μm). Measurements – Length: 212-232 μm, width: 90- 100 μm (n = 10). Prodorsum – Rostrum tridentate; separated by 2 aluminum stubs and gold-coated for scanning deep incisions; the lobes sharped, rostral setae ciliated, electron microscopy). arising on the dorsal surface of rostrum, curved Distribution – Sweden, Austria (Miko, 2006). inwards. Lamellar setae smooth, arising at the distal New record for Turkish fauna. end of the costulae, situated closer to interlamellar Remarks – setae than to rostral setae. Costulae present. The body length for the type specimen is given as 200 μm by Forsslund (1942). In this regard, Interlamellar setae (in) smooth. Sensilla (ss) globular, the Turkish specimens (212-232 μm) are longer than with several distinct barbs. the type specimens. These differences in dimensions Notogaster – Elongate oval-shaped, with anterior are considered within the variation limits. This species margin convex. Ten pairs of thin and smooth is well characterized by divided rostrum, the shape of notogastral setae. Setae c2 longer than other setae. sensilla, and costulae. Except for the body size, the Ventral side – Epimeral borders distinctly visible Turkish specimens closely resemble the type species and strongly sclerotized. Epimeral setal formula 3-1- in all features. 3-3. Genital plates 22 μm in length, 24 μm in width, Lauroppia Subías and Minguez, 1986 with 4 pairs of setae, with longest anteriorly and all of Type-species: Dameosoma fallax Paoli, 1908 them smooth. Anal plates 26 μm in length, 28 μm in Lauroppia maritima acuminata (Strenzke, 1951) width, with 2 pairs of setae, all of them equal in length (Figures 5 and 6.) and smooth. Posterior border of epimera IV undulate. Lyrifissures iad situated paraanally. Adanal setae ad1 Measurements – Length: 232-248 μm, width: 118- in postanal, ad2 in paraanal, and ad3 in preanal 126 μm (n = 10). position. Prodorsum – Rostrum tridentates; separated by 2 Material examined – Turkey, Bolu province, deep incisions; the median lobes sharped and prolonged anteriorly, the lateral lobes rounded. Gölcük lakeside, 40°39´38˝N, 31°37´60˝E, 1225 m, 10 Rostral setae smooth, arising on the dorsal surface of May 2008, litter, 44 exs (2 of them were mounted on

66 A. TOLUK, N. AYYILDIZ

10µm 100 µm

C D

20 µm 10µm

E F

100 µm 20 µm

Figure 4. Moritzoppia (Moritzoppia) tridentata (Forsslund, 1942): A) Rostrum and rostral setae, B) Dorsal view, C) Prodorsum, D) Sensillum, E) Ventral view, F) Genital plate.

rostrum, curved inwards. Lamellar setae (le) smooth, Notogaster – Notogaster oval, straight anteriorly, arising at the distal end of the costulae, situated closer without 1 pair of prominent humeral processes; 10 to interlamellar setae than to rostral setae. Costulae pairs of smooth notogastral setae present. in ss present. Interlamellar setae ( ) smooth. Sensilla ( ) Ventral side – Epimeral borders distinctly visible fusiform. and strongly sclerotized. Epimeral setal formula 3-1-

67 Contributions to the Turkish oribatid fauna (Acari: Oribatida) from Bolu province

3-3. Genital plates 24 μm in length, 30 μm in width, with 5 pairs of setae, all of them smooth and with longest anteriorly. Anal plates 36 μm in length, 34 μm in width, with 2 pairs of setae, all of them equal in length and smooth. Posterior border of epimera IV undulate. Lyrifissures iad situated paraanally. Adanal setae ad1 in postanal, ad2 in paraanal, and ad3 in preanal position. Material examined – Turkey, Bolu province, Gölcük lakeside, 40°39´20˝N, 31°37´38˝E, 1080 m, 10 May 2008, litter in decaying wood, 40 exs (2 of them were mounted on aluminum stubs and gold-coated for scanning electron microscopy). Distribution – Holarctic region (Subías, 2009). A B New record for Turkish fauna. Remarks – The dimensions of the type specimen Lauroppia maritima acuminata are given as 227-244 / 115-132 μm by Strenzke (1951). Figure 5. (Strenzke, 1951): A) Dorsal view, B) Ventral view (scale bar = 100 μm). The Turkish specimens (232-248 μm) are in the range of the dimensions of the type specimen. This species

100 µm 30 µm

10 µm CD

10 µm

Figure 6. Lauroppia maritima acuminata (Strenzke, 1951): A) Dorsal view, B) Prodorsum, C) Rostrum, D) Sensillum.

68 A. TOLUK, N. AYYILDIZ

is well characterized by tridentate rostrum and the shape of sensilla. In this regard, the Turkish specimens closely resemble the type species in all features. Thyrisomidae Grandjean, 1953 Banksinoma Oudemans, 1930 Type-species: Banksinoma lanceolata oudemansi Fujikawa, 1979 Banksinoma lanceolata lanceolata (Michael, 1885) (Figure 7.) Measurements – Length: 296 μm, width: 154 μm (n = 1). Prodorsum – Rostrum with pointed apex. Rostral setae smooth, near each other, arising on the dorsal surface of rostrum, 154 μm in length. Lamellar setae A B smooth, very long, about 58 μm in length, extending beyond rostrum, arising at the distal end of the Figure 7. Banksinoma lanceolata lanceolata (Michael, 1885): A) costulae, situated closer to interlamellar setae than to Dorsal view, B) Ventral view (scale bar = 100 μm). rostral setae. Interlamellar setae (in) smooth, 16 μm ss in length. Costulae convergent. Sensilla ( ) fusiform- Material examined – Turkey, Bolu province, lanceolate, pointed at apex. Gölcük lakeside, 40°39´38˝N, 31°37´598˝E, 1225 m, Notogaster – Notogaster oval; 11 pairs of smooth 10 May 2008, litter, 1 ex. notogastral setae present. Distribution – Palearctic and Hawaii (Subías, Ventral side – Epimeral borders distinctly visible 2009). New record for Turkish fauna. and strongly sclerotized. Epimeral setal formula 3-1- Remarks – The body length is given as 375 μm by 3-3. Genital and anal plates large, near each other, not Pérez-Íñigo (1971), 350 μm by Bulanova-Zachvatkina touching. Genital plates 52 μm in length, 72 μm in (1975), and 300-360 μm by Miko (2006). In terms of width, with 6 pairs of setae, all of them equal in length the body length, the Turkish specimen (296 μm) is in and smooth. Anal plates 54 μm in length, 58 μm in the range of the known measurements of the species. width, with 2 pairs of setae, all of them equal in length This species is well characterized by acute rostrum, and smooth. Lyrifissures iad situated paraanally. the shape of sensilla and costulae, and the long setae Adanal setae ad1 in postanal, ad2 in paraanal, and ro and la. In this regard, the Turkish specimen closely ad3 in preanal position. resembles the species in all features.

References Balogh, J. 1983. A partial revision of the Oppiidae Grandjean, 1954 Baran, Ş. and Ayyıldız, N. 2009. Quadroppia (Coronoquadroppia) (Acari: Oribatei). Acta Zool. Acad. Sci. Hung. 29: 1-79. sezeki sp. n. (Acari, Oribatida), a new soil mite from Turkey. Biologia 64: 113-115. Baran, Ş. and Ayyıldız, N. 2007a. Two new species of soil mites (Acari, Oribatida, Oppiidae and Machuellidae) from Turkey. Zootaxa Bulanova-Zachvatkina, E.M. 1975. Families Caleremaeidae and 1445: 57-64. Thyrisomidae. In: Claves de identification de acaros edaficos. Sarcoptiformes (eds. M.S. Ghilarov and D.A. Krivolutsky), Baran, Ş. and Ayyıldız, N. 2007b. A new species of the family Nauka, Moscow, pp. 193-196. Quadroppiidae (Acari, Oribatida) from Turkey. J. Acarol. Soc. Jpn. 16: 1-4. Erman, O., Özkan, M., Ayyıldız, N. and Doğan, S. 2007. Checklist of the mites (Arachnida: Acari) of Turkey. Second supplement. Zootaxa 1522: 1-21.

69 Contributions to the Turkish oribatid fauna (Acari: Oribatida) from Bolu province

Forsslund, K. H. 1942. Schwedische Oribatei (Acari). I. Arkiv. Zool. Toluk, A. and Ayyıldız, N. 2008a. Two new species of the genus 34: 1-11. Rhinoppia Balogh, 1983 (Acari: Oribatida) from Turkey. Ent. News 119: 263-270. Miko, L. 2006. Oppiidae Grandjean, 1951. In: Hornmilben (Oribatida). Die Tierwelt Deutschland, Begründet 1925 von Toluk, A. and Ayyıldız, N. 2008b. New and unrecorded oppioid mites Friedrich Dahl, 76. Teil. Goecke & Evers, Keltern, pp. 263-296. (Acari: Oribatida) from Yozgat Pine Grove National Park, Turkey. Acarologia 48: 209-223. Pérez-Íñigo, C. 1971. Ácaros Oribátidos de Suelos de España Peninsular e Islas Baleares (Acari, Oribatei) Parte III. Eos 46: Toluk, A. and Ayyıldız, N. 2008c. A study on the oribatid mites (Acari: 263-349. Oribatida) known and new to the Turkish fauna. Türk. Entomol. Derg. 33: 31-39. Pérez-Íñigo, C. 1993. Acari, Oribatei, Poronota . In: Fauna Ibérica, vol. 3 (eds. M.A. Ramos et al.), Museo Nacional de Ciencias Toluk, A. and Ayyıldız, N. 2009a. New records of the oppioid mites Naturales, CSIC, Madrid. (Acari: Oribatida) for the Turkish fauna from Artvin Province. Turk. J. Zool. 33: 13-21. Subías, L.S. 2009. Listado sistematico, sinonimico y biogeografico de los acaros oribatidos (Acariformes: Oribatida) del Mundo Toluk, A. and Ayyıldız, N. 2009b. Three new species of Oppiidae from (Excepto fosiles). Graellsia 60: 3-305. http://www.ucm.es Turkey (Acari: Oribatida). Zootaxa 1988: 33-47. /info/zoo/Artropodos/Catalogo.pdf (accessed 10.11.2009). Toluk, A., Ayyıldız, N. and Subías, L.S. 2007. Two new species of Subías, L.S. and Balogh, P. 1989. Identification keys to the genera of oppioid mites from Turkey (Acari: Oribatida). Zootaxa 1551: Oppiidae Grandjean, 1951 (Acari: Oribatei). Acta Zool. Hung. 61-68. 35: 355-412. Toluk, A., Ayyıldız, N. and Subías, L.S. 2009. Three new species of the Strenzke, K. 1951. Some new Central European moss-mites. Ann. family Oppiidae (Acari: Oribatida) from Turkey. Acta Zool. Mag. Nat. Hist. 12: 719-726. Acad. Sci. Hung. 55: 23-35. Travé, J. and Vachon, M. 1975. François Grandjean 1882-1975 (notice biographique). Acarologia 17: 1-19.