(Acari, Oribatida) from Cuba - BioOne

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Mar 17, 2016 - An annotated checklist of the Cuban Oripodoidea (Acari, Oribatida) is provided. It includes 16 species from 10 genera and four families.

Systematic & Applied Acarology 21(4): 450–460 (2016) http://doi.org/10.11158/saa.21.4.6 Article

ISSN 1362-1971 (print) ISSN 2056-6069 (online)

http://zoobank.org/urn:lsid:zoobank.org:pub:EF2E5594-4518-408B-AE4D-C54408279F99

New species and records of oribatid mites of the superfamily Oripodoidea (Acari, Oribatida) from Cuba SERGEY G. ERMILOV Tyumen State University, Tyumen, Russia. E-mail: [email protected]

Abstract An annotated checklist of the Cuban Oripodoidea (Acari, Oribatida) is provided. It includes 16 species from 10 genera and four families. Of these, eight species, three genera and one family are recorded for the first time in Cuba. Two new species of the genus Protoribates (Haplozetidae) are described and illustrated on the basis of adult specimens. Protoribates tetrasetosus sp. nov. is morphologically most similar to P. mollicoma (Hammer, 1973), but differs from the latter by the short interlamellar, notogastral and ventral setae. Protoribates paramadagascarensis sp. nov. is morphologically most similar to P. madagascarensis (Balogh, 1960), but differs from the latter by the smaller body size, position of rostral and lamellar setae and notogastral setae lp, the absence of microgranulate cerotegument on the notogaster and anogenital region and the absence of a transverse ridge in the basal part of the prodorsum. Key words: oribatid mites, new species, morphology, systematics, Oripodoidea, Protoribates, new record, fauna, Cuba

Introduction This work is a part of our continuing study (Ermilov & Tolstikov 2015a; Niedbała & Ermilov 2015) on the Cuban fauna of oribatid mites (Acari, Oribatida), and includes the data on the superfamily Oripodoidea. Sixteen species of oripodoids (two new for science) were collected. The main goal of the paper is to present data on the localities, notes on records and overall known distribution of taxa and to describe new species under the names Protoribates tetrasetosus sp. nov. and P. paramadagascarensis sp. nov. (Haplozetidae). The genus Protoribates was proposed by Berlese (1908) with Oribata dentata Berlese, 1883 as type species. Currently it comprises about 80 species (Subías 2004, online version 2015; Ermilov & Tolstikov 2015b), which have a cosmopolitan distribution (Subías 2004, online version 2015). The main generic characters for the genus were summarized by Weigmann et al. (1993), Bayartogtokh (2010) and Walter & Latonas (2013). Identification keys for some species of Protoribates were presented by Balogh & Balogh (2002), Weigmann (2006), Bayartogtokh (2010), Walter & Latonas (2013) and Corpuz-Raros (2014).

Materials and methods Our results are based on collections from three localities in Cuba (unknown date and collector, mites were originally deposited in the Museum of Zoology of Tyumen State University, Russia): — Cuba 1: Parque Nacional Alejandro de Humboldt, 20°30'N, 74°40'W, leaf litter in forest.

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— Cuba 2: Valle de Viñales National Park, 22°40'56.8"N, 83°42'57.5"W, Ancon, leaf litter in forest. — Cuba 3: Cayo Santa Maria, 22°66'21'' N, 78°96'88'' W, leaf litter in forest. Specimens were mounted in lactic acid on temporary cavity slides for measurement and illustration. The body length was measured in lateral view, from the tip of the rostrum to the posterior edge of the ventral plate. Notogastral width refers to the maximum width in dorsal aspect. Lengths of body setae were measured in lateral aspect. All body measurements are presented in micrometers. Formulas for leg setation are given in parentheses according to the sequence trochanter–femur– genu–tibia–tarsus (famulus included). Formulas for leg solenidia are given in square brackets according to the sequence genu–tibia–tarsus. General terminology used in this paper follows that of Grandjean (summarized by Norton & Behan-Pelletier 2009). Drawings were made with a drawing tube using a Carl Zeiss transmission light microscope “Axioskop-2 Plus”.

Checklist Specific localities for Oripodoidea, new records and overall known distribution1 are listed. Sixteen species (one not identified and two new to science) from 10 genera and four families were found. Eight species, three genera and one family are recorded for the first time in Cuba and of these two species are recorded for the first time in the Neotropical region (see checklist below). References on original descriptions for species are not presented in “References” section. Mochlozetidae — Unguizetes incertus (Balogh & Mahunka, 1969). Locality: Cuba 1, Cuba 3. Distribution: Neotropical region. First record of family, genus and species in Cuba. Haplozetidae — Haplozetes minutus (Tseng, 1984). Locality: Cuba 2, Cuba 3. Distribution: Taiwan and Brazil. First record of species in Cuba. — Lauritzenia (Magnobates) orghidani (Călugăr & Vasiliu, 1983). Locality: Cuba 2. Distribution: Cuba. — Protoribates antillensis (Mahunka, 1985). Locality: Cuba 2, Cuba 3. Distribution: Neotropical region. First record of species in Cuba. — Protoribates paracapucinus (Mahunka, 1988). Locality: Cuba 1, Cuba 2, Cuba 3. Distribution: Palaearctic, Oriental, Ethiopian and Neotropical regions. First record of species in Cuba. — Protoribates paramadagascarensis sp. nov. Locality: Cuba 2. — Protoribates tetrasetosus sp. nov. Locality: Cuba 2. — Trachyoribates (Rostrozetes) ovulum Berlese, 1908 sensu Beck (see 1965) as Rostrozetes foveolatus Sellnick, 1925. Locality: Cuba 1, Cuba 2, Cuba 3. Distribution: Cosmopolitan. Scheloribatidae — Fijibates dlouhyi (Mahunka, 1984). Locality: Cuba 1, Cuba 2, Cuba 3. Distribution: Neotropical region. First record of genus and species in Cuba. — Muliercula spora Coetzer, 1968. Locality: Cuba 1, Cuba 3. Distribution: South Africa. First record of genus in Cuba; first record of species in the Neotropical region.

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— Scheloribates (Scheloribates) acutirostris Călugăr & Vasiliu, 1983. Locality: Cuba 2. Distribution: Cuba. — Scheloribates (Scheloribates) praeincisus (Berlese, 1910). Locality: Cuba 1, Cuba 2, Cuba 3. Distribution: Tropics. — Scheloribates (Scheloribates) fimbriatus Thor, 1930. Locality: Cuba 3. Distribution: Cosmopolitan. First record of species in Cuba. — Perscheloribates sp. Locality: Cuba 1, Cuba 2, Cuba 3. Remarks. This species is morphologically similar to Scheloribates (S.) feideri Călugăr & Vasiliu, 1983. Călugăr & Vasiliu (1983) described this species from Cuba, including it in the genus Scheloribates, however, they did not note the number of leg claws in their paper. Hence, the study of the type material is necessary for final conclusion. Oripodidae — Benoibates borhidii Balogh & Mahunka, 1980. Locality: Cuba 2. Distribution: Neotropical region. — Benoibates juglans (Jacot, 1938). Locality: Cuba 1. Distribution: U.S.A. First record of species in the Neotropical region.

Descriptions Protoribates tetrasetosus sp. nov. (Figs 1–10) Diagnosis Body size: 597–630 × 381–431. Body covered by microgranulate cerotegument. Rostral and lamellar setae of medium length, setiform, barbed. Interlamellar setae short, smooth. Bothridial setae with long, smooth stalks and heads short, dilated unilaterally, pointed apically and barbed. Notogastral setae minute. Four pairs of small, round porose areas. Subcapitular setae h shorter and thinner than a and m. Epimeral setal formula: 3-1-3-2. Pedotecta II bifurcate apically. Circumpedal carinae long, reaching anterior margin of ventral plate. Four pairs of genital setae present. Anogenital setae short, thin, smooth. Legs monodactylous. Description Measurements. Females larger than males. Body length: 597 (holotype: male), 614–630 (two paratypes: females), 581–597 (seven paratypes: males); notogaster width: 381 (holotype), 415–431 (two paratypes: females), 348–381 (seven paratypes: males). Integument. Body color brown to black-brown. Body surface smooth, covered by distinct, dense microgranulate cerotegument (diameter of granules up to 1). Prodorsum (Figs 1, 5, 6). Rostrum slightly protruding, narrowly rounded. Lamellae (lam) located dorso-laterally, half as long as prodorsum (measured in lateral view). Prolamellae absent. Sublamellae (slam) about one third the length of lamellae, poorly visible. Sublamellar porose areas (Al) oval (18–20 × 10–12), located near to sublamellae. Rostral setae (ro, 49–53) setiform, barbed, inserted laterally on prodorsum. Lamellar setae (le) similar in length and morphology to rostral setae, inserted on the lamellae ends. Interlamellar (in, 10–12) and exobothridial (ex, 8–12) setae short, thin, smooth. Bothridial setae (bs, 86–94) with long, simple, smooth stalks and and heads short, dilated unilaterally, pointed apically and barbed. Sejugal porose areas slightly visible only in dissected specimens, band-like. Tutoria (tu) lineate, strong, curving basally. Lateral carinae (car) well developed, reaching insertions of rostral setae. 452

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FIGURES 1–4. Protoribates tetrasetosus sp. nov., adult: 1 — dorsal view; 2 — ventral view (gnathosoma and legs not illustrated); 3 — subcapitulum, ventral view; 4 — right genital plate and part of epimeral region. Scale bar 100 μm (1, 2), 50 μm (3, 4).

Notogaster (Figs 1, 5). Anterior notogastral margin distinctly convex medially. Dorsophragmata (D) elongated, longitudinally oriented. Pteromorphs with distinct hinges (hin). Ten pairs of notogastral setae very short, thin, smooth; p1 (8) slightly longer than others (4–6). Four pairs of 2016

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porose areas (Aa, A1, A2, A3) rounded, small, similar in diameter (16). Setae lp inserted posteriorly to A1. Setae h3 inserted far anteriorly to A2. Lyrifissures (ia, im, ip, ih, ips) and opisthonotal gland openings (gla) clearly visible. Gnathosoma. Morphology of subcapitulum, palps and chelicerae generally typical for Protoribates (see Weigmann et al. 1993; Ermilov & Anichkin 2011b; Ermilov et al. 2013). Subcapitulum longer than wide (114–118 × 90–94). Subcapitular setae setiform, barbed, a and m (both pairs 20) longer and thicker than h (12–16) (Fig. 3). Two pairs of adoral setae (or1, or2, 10–12) setiform, barbed. Palps (length 73–77) with setation 0-2-1-3-9(+ω). Solenidion of palptarsi attached to eupathidium, both located on dorsal tubercle. Chelicerae (length 139–143) with two barbed setae, cha (49) longer than chb (20–24). Trägårdh’s organ long, tapered. Epimeral and lateral podosomal regions (Figs 2, 4, 5). Apodemes 2 elongated, similar in length to apodemes 3. Sejugal apodemes (apo.sj) long, almost reaching genital aperture. Epimeral setal formula: 3-1-3-2. Setae (all 10–12) setiform, slightly barbed, 1a, 2a and 3a stronger barbed than others. Pedotecta I (Pd I) large, concave (in dorsal view) and lamina-like (in lateral view). Pedotecta II (Pd II) smaller, trapezoid, bifurcate apically (in ventral view) and lamina-like (in lateral view). Discidia (dis) triangular, broadly rounded. Circumpedal carinae (cp) very long, reaching anterior margin of ventral plate, connected to prodorsal lateral carinae. Anogenital region (Figs 2, 4). Four pairs of genital (g1, 12–14; g2–g4, 8–10), one pair of aggenital (ag, 6–10), two pairs of anal (an1, an2, 6–10) and three pairs of adanal (ad1–ad3, 12) setae setiform, thin, smooth. Setae ad3 inserted anterior to anterior margin of anal aperture. Adanal lyrifissures (iad) located close and parallel to anal plates. Ovipositor typical for Protoribates (see Ermilov & Anichkin 2011a, b), elongated (163 × 45), blades (73) shorter than length of distal section (beyond middle fold; 90). Each of three lobes with four straight, smooth setae; ψ1 ≈ τ1 (28) longer than ψ2 ≈ τa ≈ τb ≈ τc (12). Six coronal setae present, minute (4). Legs (Figs 7–10). Morphology of leg segments, setae and solenidia generally typical for Protoribates (see Weigmann et al. 1993; Miko et al. 1994; Ermilov & Anichkin 2011b). Monodactylous, claw of each leg strong, smooth. Ventro-basal parts of tibiae I and II with well developed teeth (t). Ventro-anterior parts of femora rounded. Porose areas on all femora and trochanters III, IV well visible. Formulas of leg setation and solenidia: I (1-5-3-4-20) [1-2-2], II (15-2-4-16) [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. Famulus (ɛ) short, thin, straight, indistinctly dilated distally. Genua and tibiae without thick setae. Solenidia ω1 on tarsus I, ω1 and ω2 on tarsus II and σ on genua III thickened, blunt-ended, other solenidia thinner, setiform. Material examined Holotype (male) and nine paratypes (two females and seven males): locality Cuba-2 (see “Material and methods” section). Type deposition The holotype is deposited in the collection of the Senckenberg Museum, Görlitz, Germany; nine paratypes are deposited in the collection of the Tyumen State University Museum of Zoology, Tyumen, Russia. Etymology The specific name “tetrasetosus” refers to the four pairs of genital setae.

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FIGURES 5–10. Protoribates tetrasetosus sp. nov., adult: 5 — lateral view of anterior part of body (legs not illustrated); 6 — medio-distal part of bothridial seta; 7 — femur, genu and basal part of tibia of leg I, left, paraxial view; 8 — femur, genu and tibia of leg II, right, antiaxial view; 9 — trochanter, femur and genu of leg III, right, antiaxial view; 10 — leg IV, left, antiaxial view. Scale bar 100 μm (5), 50 μm (6–10).

Remarks Protoribates tetrasetosus sp. nov. is morphologically most similar to P. mollicoma (Hammer, 1973) from Polynesia and India (see Hammer, 1973) in having body of medium size, monodactylous legs, four pairs of genital setae and bothridial setae with long stalks and heads short, dilated unilaterally, pointed apically and barbed. However, the new species differs from the latter by the short interlamellar (vs. long), notogastral and ventral (vs. all medium length) setae. 2016

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TABLE 1. Leg setation and solenidia of adult Protoribates tetrasetosus sp. nov. (same data for P. paramadagascarensis sp. nov.) Leg I II III IV

Tr v' v' l', v' v'

Fe d, (l), bv'', v'' d, (l), bv'', v'' d, l', ev' d, ev'

Ge (l), v', σ (l), v'*, σ l', σ d, l'

Ti (l), (v), φ1, φ2 (l), (v), φ l', (v), φ l', (v), φ

Ta (ft), (tc), (it), (p), (u), (a), s, (pv), v', (pl), l'', ɛ, ω1, ω2 (ft), (tc), (it), (p), (u), (a), s, (pv), l'*, ω1, ω2 (ft), (tc), (it), (p), (u), (a), s, (pv) ft'', (tc), (p), (u), (a), s, (pv)

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. Tr — trochanter, Fe — femur, Ge — genu, Ti — Tibia, Ta — tarsus. * — seta v' on genu II absent and seta l' on tarsus II present only in Protoribates tetrasetosus sp. nov.

Protoribates paramadagascarensis sp. nov. (Figs 11–20) Diagnosis Body size: 481–547 × 298–332. Body indistinctly microfoveolate. Rostral, lamellar and interlamellar setae setiform, barbed; ro shortest, in longest. Bothridial setae with long, barbed stalks and heads short, dilated unilaterally, pointed apically and barbed. Notogastral setae minute. Four pairs of porose areas rounded, A1–A3 very small. Subcapitular setae m shorter and thinner than a and h. Epimeral setal formula: 3-1-3-2. Pedotecta II bifurcate apically. Circumpedal carinae of medium length, reaching level of discidia. Anogenital setae setiform, thin, smooth except long adanal setae ad1 and ad2. Legs tridactylous. Description Measurements. Body length: 514 (holotype: female), 481–547 (seven paratypes: all females); notogaster width: 315 (holotype), 298–332 (seven paratypes). Integument. Body color brown to black-brown. Body surface microfoveolate, but foveolae (their diameter less than 1) visible under high magnification in dissected specimens. Microgranulate cerotegument (diameter of granules up to 1) presented only on lateral sides of prodorsum. Prodorsum (Figs 11, 15, 16). Rostrum slightly protruding, narrowly rounded. Lamellae located dorso-laterally, half as long as prodorsum (measured in lateral view). Prolamellae absent. Sublamellae about one third the length of lamellae, poorly visible. Sublamellar porose areas oval (14–16 × 8–10), located near to sublamellae. Rostral (36–45), lamellar (57–65) and interlamellar (110–118) setae setiform, barbed. Rostral setae inserted dorso-laterally on prodorsum. Lamellar setae inserted on the prodorsum surface, medially to the lamellae ends. Exobothridial setae (8) thin, smooth. Bothridial setae (94–102) with long, barbed stalks and heads short, dilated unilaterally, pointed apically and barbed. Sejugal porose areas slightly visible only in dissected specimens, bandlike. Tutoria lineate. Lateral carinae well developed, not reaching insertions of rostral setae. Notogaster (Figs 11, 15). Anterior notogastral margin almost straight, slightly convex medially. Dorsophragmata elongated, longitudinally oriented. Pteromorphs with distinct hinges. Ten pairs of notogastral setae minute (4). Four pairs of porose areas rounded, Aa (6–8) larger than A1, A2 and A3 (2–4). Setae lp inserted posterior to A1. Setae h3 inserted anterior to A2. Lyrifissures and opisthonotal gland openings clearly visible. Gnathosoma. Morphology of subcapitulum, palps and chelicerae generally typical for Protoribates (see Weigmann et al. 1993; Ermilov & Anichkin 2011b; Ermilov et al. 2013). Subcapitulum longer than wide (114–118 × 90–94). Subcapitular setae setiform, barbed (except smooth or indistinctly barbed a), a (26–28) and h (32–36) longer and thicker than m (14–16) (Fig. 13). Two pairs of adoral setae (16) setiform, barbed. Palps (length 69–73) with setation 0-2-1-3456

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9(+ω). Solenidion of palptarsi attached to eupathidium, both located on dorsal tubercle. Chelicerae (length 135–139) with two barbed setae, cha (49) longer than chb (24–28). Trägårdh’s organ long, tapered.

FIGURES 11–14. Protoribates paramadagascarensis sp. nov., adult: 11 — dorsal view; 12 — ventral view (gnathosoma and legs not illustrated); 13 — subcapitulum, ventral view; 14 — right genital plate and part of epimeral region. Scale bar 100 μm (11, 12), 50 μm (13, 14). 2016

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FIGURES 15–20. Protoribates paramadagascarensis sp. nov., adult: 15 — lateral view of anterior part of body (legs not illustrated); 16 — medio-distal part of bothridial seta; 17 — femur and genu of leg I, left, antiaxial view; 18 — trochanter, femur and genu of leg II, left, antiaxial view; 19 — trochanter, femur and genu of leg III, right, antiaxial view; 20 — leg IV, right, antiaxial view. Scale bar 100 μm (15), 50 μm (16–20).

Epimeral and lateral podosomal regions (Figs 12, 14, 15). Apodemes 2 clearly shorter than apodemes 3. Sejugal apodemes long, almost reaching genital aperture. Epimeral setal formula: 3-13-2. Setae 3c (20) longer than others (12–14), all setiform, slightly barbed. Pedotecta I large, concave (in dorsal view) and lamina-like (in lateral view). Pedotecta II smaller, trapezoid, bifurcate apically 458

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(in ventral view) and lamina-like (in lateral view). Discidia triangular, broadly rounded. Circumpedal carinae of medium length, reaching level of discidia. Anogenital region (Figs 12, 14). Five pairs of genital (g1, 12–16; g2–g5, 8–12), one pair of aggenital (10–12), two pairs of anal (26–28) and three pairs of adanal (ad1, 53–61; ad2, 45–49; ad3, 10–12) setae setiform, smooth. Setae ad3 inserted posteriorly to anterior margin of anal aperture. Adanal lyrifissures located close and parallel to anal plates. Ovipositor typical for Protoribates (see Ermilov & Anichkin 2011a, b), elongated (205 × 36), blades (82) shorter than length of distal section (beyond middle fold; 123). Each of three lobes with four straight, smooth setae; ψ1 ≈ τ1 (28–30) longer than ψ2 ≈ τa ≈ τb ≈ τc (14). Six coronal setae present, minute (4). Legs (Figs 17–20). Morphology of leg segments, setae and solenidia generally typical for Protoribates (see Weigmann et al. 1993; Miko et al. 1994; Ermilov & Anichkin 2011b). Tridactylous, median claw thicker than laterals, all serrate dorsally. Ventro-basal parts of tibiae I and II with slightly developed teeth. Ventro-anterior parts of femora rounded. Porose areas on all femora and trochanters III, IV well visible. Formulas of leg setation and solenidia: I (1-5-3-4-20) [1-2-2], II (1-5-3-4-15) [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. Famulus short, thin, straight, indistinctly dilated distally. Genua and tibiae without thick setae. Solenidia ω1 on tarsus I, ω1 and ω2 on tarsus II and σ on genua III thickened, blunt-ended, other solenidia thinner, setiform. Material examined Holotype (female) and seven paratypes (all females): locality Cuba-2 (see “Material and methods” section). Type deposition The holotype is deposited in the in the collection of the Senckenberg Museum, Görlitz, Germany; seven paratypes are deposited in the collection of the Tyumen State University Museum of Zoology, Tyumen, Russia. Etymology The specific name “paramadagascarensis” refers to the similarity of the new species to Protoribates madagascarensis (Balogh, 1960). Remarks Protoribates paramadagascarensis sp. nov. is morphologically most similar to P. madagascarensis (Balogh, 1960) from the Ethiopian region (see Balogh 1960; Mahunka 1986) in having tridactylous legs, bothridial setae with long stalks and heads short, dilated unilaterally, pointed apically and barbed, short notogastral setae and long, thin and smooth adanal setae ad1 and ad2. However, the new species differs from the latter by the smaller body size (481–547 × 298–332 vs. 760–845 × 533–505); rostral setae inserted dorso-laterally (vs. laterally); lamellar setae inserted on prodorsum surface, medially to the lamellae ends (vs. on the lamellae ends); notogastral setae lp inserted posteriorly to A1 (vs. medially to A1); microgranulate cerotegument absent on notogaster and anogenital region (vs. cerotegument well visible); transverse ridge absent in basal part of prodorsum (vs. ridge present). Acknowledgements The author cordially thanks Dr. Elizabeth A. Hugo-Coetzee (National Museum, Bloemfontein, South Africa), two anonymous reviewers for their valuable comments and Dr. Dania Prieto (University of Havana, Havana, Cuba) for collaboration. The study was supported by the Russian Science Foundation (project 14-14-01134). 2016

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