A review of the ecology and distribution of Protoribates (Oribatida, Oripodoidea, Haplozetidae) in Alberta, Canada, with the description of a new species
DAVID EVANS WALTER1,2 & SARAH LATONAS1
1Royal Alberta Museum 12845 102 Ave., Edmonton, AB, T5N OM6, Canada 2Corresponding author. E-mail: [email protected]
Abstract
The oribatid mite genus Protoribates Berlese (Haplozetidae) is reviewed for North America and the genus diagnosis is revised to account for the North American species, Protoribates robustior (Jacot, 1937) is redescribed and newly reported from western North America and a new species from Alberta is described. Protoribates haughlandae sp. n. is bisexual, heterotridactylous, and lives primarily in the peat soils of fens and bogs. Protoribates robustior is all-female, monodactylous, and occurs primarily in dry forests or in dry, treeless sites dominated by grasses, sedges, and shrubs. Both species feed on fungal hyphae and spores, but P. haughlandae also is an opportunistic predator and/or necrophage of small arthropods and P. robustior gut contents often include material that resembles plant cell walls. Examination of type specimens confirms that Protoribates prionotus (Woolley, 1968) is a junior synonym of the widespread Protoribateslophotrichus (Berlese, 1904). A key to differentiate Lagenobates from Protoribates and to identify the 7 species of the latter that are known or reported from North America is provided.
Until recently, Protoribates Berlese, 1908, has been a poorly known and taxonomically confusing genus variously treated as a member of the Haplozetidae or as the type genus of Protoribatidae. Weigmann et al. (1993) redescribed the type species (Oribates dentatus Berlese, 1883) and convincingly demonstrated that Xylobates Jacot, 1929, was a junior subjective synonym of Protoribates, as hypothesized by Grandjean in 1936. Miko et al. (1994), Weigmann and Miko (2002), and Weigmann and Monson (2004) further clarified generic concepts in the Haplozetidae for European species. However, many problematic taxa still exist, especially for species described under Xylobates. The purpose of this paper is to review the ecology, distribution, and systematics of Protoribates in North America and describe a new species from Alberta.
The Province of Alberta, Canada, covers about 661,000 km2 and stretches approximately 1,223 km from the Northwest Territories south to the state of Montana in the USA (49–60 N latitude) and 660 km from the Canadian province of Saskatchewan in the east (110th meridian) to the crest of the Rocky Mountains on the Alberta-British Columbia border (~120th meridian) in the west. The climate is continental in the south to subarctic in the north. Mixed grasslands cover south eastern Alberta, grading into aspen parkland in central Alberta and the foothills of the Rocky Mountains. Much of the northern two-thirds of the Province is covered by boreal forest (taiga), peatlands, and wetlands. About 330 species of oribatid mites are currently known to occur in Alberta (Walter et al.2012).
For the last five years (2007–2011), adult Oribatida have been used by the Alberta Biodiversity Monitoring Institute (2012) in their Province-wide assessment of the state of biological diversity. In total, 579 sites in Alberta have been sampled for oribatid mites. This survey presents a unique opportunity to assess the ecological and biogeographical distribution of oribatid mites within the Province.
Accepted by H. Schatz: 10 Jan. 2013; published: 7 Mar. 2013 483
Material and methods
Morphological terminology follows F. Grandjean as summarized by Norton & Behan-Pelletier (2009). This includes notation for prodorsal setae as follows [abbreviation (seta)]: ro (rostral), le (lamellar), in (interlamellar), ex (exobothridial), bo (bothridial seta or sensillus), and the unideficiency nomenclature for notogastral setae. Needle-like setae without obvious ornamentation are referred to as simple, those with small triangular spicules as barbed. Leg setation is presented as the number of setae (including the famulus on tarsus I) with solenidial counts in parentheses for each leg in the order: trochanter-femur-genu-tibia-tarsus. Dactyly is reported separately. Setae on the legs and palps are designated prime (e.g. a’) when on the anterior face of the segment (assuming the leg is perpendicular to the body) and double prime (e.g. a’’) when on the posterior face or by convention for setal pairs on the midline (e.g. ft’’, ft’). Epimeral setation is in sequence for fields I-II-III-IV. Lengths and widths are given as ranges in µm or as approximations for difficult measurements. Body length was measured along the midline from tip of rostrum to posterior edge of notogaster and body width at the greatest width of the hysterosoma (just posterior to the pteromorph) on specimens in cavity slides, except when noted. Summary statistics such as means and standard errors are avoided because when based on small sample sizes they give a misleading impression of precision and are difficult to interpret.
Collections with Alberta Biodiversity Monitoring Institute (ABMI) site numbers were obtained by field crews (often helicoptered to locations in Alberta with no road access) and are reported as digital GPS coordinates to within a 5.5 km radius of the site. Additional site and habitat data are available at the ABMI website (ABMI 2012). All ABMI collections are from organic soil layers (four 500 ml bulked cores per site) and were extracted into ethanol using Tullgren-modified Berlese funnels (Krantz & Walter 2009). The Moose Pasture Reference Site (MPRS) and some other collections are from a variety of litter, soil, and other organic substrates as noted.
Slide-mounted specimens were cleared in lactic acid and mounted in a polyvinyl alcohol medium (Krantz and Walter 2009). Specimens for scanning electron microscopy were dried through absolute ethanol and acetone, mounted on Al-stubs with double sided sticky tape, and gold-coated in a Hummer sputter apparatus. SEMs of the new species are all from ABMI 910 SW (54.68661118, -115.556122) near Freeman Lake, 10 km W Swan Hills, 14.vi.2010; others are from the MPRS or as noted. Differential interference contrast images were obtained on a Leica DM 2500 microscope using a DFC 420 camera; images stacks were combined using the Combine ZP (2010) image stacking software when appropriate to achieve better depth of field.
Abbreviations used
ABMI Alberta Biodiversity Monitoring Institute http://www.abmi.ca/abmi/home/home.jsp.DEW D. E. Walter (author)CNC Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri-Food
Canada, Ottawa, Ontario, Canada.MPRS Moose Pasture Reference SiteUSNM National Museum of Natural History, Washington, DC, USA.PMAE.IZ Royal Alberta Museum, Invertebrate Zoology, 12845—102 Avenue, Edmonton, AB, T5N 0M6,
CanadaUSA United States of America
Systematics
Genus Protoribates Berlese, 1908
Type species: Oribata dentata Berlese, 1883: 1.
Diagnosis. Oripodoidea with pteromorphs subtriangular, hinged, movable, and associated with large muscle insertions on notogaster in region of Aa; discidium present as tectum, needle- to blade-like custodium usually present. Sensillus usually reclinate with sublanceolate head, rarely setiform or with erect club-like head. Lamella narrow; sublamella vestigial; prolamella absent; tutorium usually present as ridge; pedotecta I–II small, not visible
in dorsal view. Notogaster with octotaxic system composed of porose areas with distinct ring-like rims (in transmitted light), 10 pairs of short to vestigial notogastral setae. Epimeral setation 3-1-3-3; 5 pairs of genital setae; one pair of aggenital setae; 3 pairs of adanal setae. Chelicerae robust, chelate-dentate; palpal solenidion and eupathidium acm form double-horn on short to long apophysis. Tarsi usually monodactyl, less commonly heterotridactyl, rarely bidactyl.
Remarks. The genus Protoribates has had a long and confusing history and finding derived characters supporting this genus is difficult. As Grandjean (1936, 1954) pointed out, the genera of Haplozetidae seem best separated from other Oripodoidea by the desclerotization of the base of the pteromorph (partial in some species) to form a hinge and the development of a tectum near the insertion of legs IV, the discidium, which usually has a well developed cusp or custodium. The hinged pteromorphs can be pulled against the legs by a cluster of enlarged muscles inserted on the notogaster in the region of porose area Aa. Although possibly shared with the Parakalummidae (and apparently convergent with Galumnoidea and some Ceratozetoidea), the movable pteromorphs serve to separate Haplozetidae from other Oripodoidea. The discidium, although again apparently convergent with some distantly related groups (e.g. Oribatellidae), provides another derived character to support the Haplozetidae. Both Haplozetes and Protoribates share these characters states along with several characters of less clear polarity, e.g. usually 5 pairs of genital setae and 10 pairs of notogastral setae in the adult. The genus Haplozetes is differentiated from Protoribates by having the octotaxic system composed of invaginated saccules rather than flattened porose areas. Species of Peloribates are similarly sacculate, but have 13–14 pairs of well-developed notogastral setae. Species of Rostrozetes are similar, but have tubules instead of saccules and 10–11 pairs of notogastral setae.
Pérez-Iñigo (1992), mistakenly believing that Protoribates was an invalid name, proposed a new genus, Transoribates, with Protoribates latus Mihelčič, 1965, as the type species. This mite has movable pteromorphs, a discidium and notogastral porose areas, but also a sensillus with a short stalk and elongate, spiny club; four pairs of genital setae and a “nose-like” process on the rostrum. Except for the reduction in the number of genital setae and the clubbed sensillus, T. latus resembles Protoribates. The sensillus in the Haplozetidae often has a long stem, reflexed over the notogaster (i.e. reclinate) that may be setiform or end in a sublanceolate to fusiform head of varying lengths, e.g. many species of Haplozetes, Protoribates and Peloribates. However, other species in these genera, e.g. Peloribates juniperi (Ewing, 1913), Haplozetes cancellatus Beck, 1964, and Haplozetes clavatusBayartogtokh, 2000, have a short, clubbed sensillus and Haplozetes triungulatus Beck, 1964, has a seemingly intermediate sensillus with a short stem with an elongate, barbed head. The sensillus is also highly variable in species of Rostrozetes, including several with short-stemmed clubs (Beck 1965). Below we describe a new species with the diagnostic characters of Protoribates, but with a sensillus that has a short stem and obovate club. We do not attribute the new species to Transoribates because unlike that genus it has 5 pairs of genital setae and the difference in the form of the sensillus is within the normal range seen in other genera of Haplozetidae.
Depending on the definition used, Protoribates currently contains up to 60 described species with an overall semi-cosmopolitan distribution (Subías 2004). Weigmann et al. (1993) redescribed the type species of the genus, Oribates dentatus Berlese, 1883; considered Xylobates Jacot, 1929 a junior synonym; and redefined the genus based on four species: P. dentatus, P. capucinus Berlese, 1908; P. lophotrichus (Berlese, 1904), and P. oblongus(Ewing, 1909). The diagnosis herein largely follows their concept, but allows for an erect, as well as a reclinate, sensillus. Subías (2004) also lists Alloribates Banks, 1947; Propeschelobates Jacot, 1936; and Styloribates Jacot, 1929 as junior synonyms of Protoribates.
In their catalogue of North American oribatid mites, Marshall et al. (1987), prior to the clarification of its generic limit, recorded an undetermined species of Protoribates from New York and Qubec and Protoribates sp. nr. langenula (Berlese, 1904) from New Brunswick. They also considered a report of Protoribates monodactylus (Haller, 1884) by Michael (1898) unconfirmed and, based on the study of original specimens, recombined Oribata albida Ewing, 1908, and Scheloribates albidus (Ewing, 1909). Therefore, we do not follow Subías (2004) who considered this species a member of Protoribates. Marshall et al. (1987) additionally listed 8 species or subspecies of monodactyl Xylobates from North America. However, after examining type material, Norton and Kethley (1990) determined: (1) that Xylobates oblongus (Ewing, 1909) was distinct from capucinus; (2) that X. longus(Ewing, 1909) and X. longisetae Jacot, 1937, were junior synonyms of oblongus; (3) that X. singularis (Banks, 1947) and X. angustior Jacot, 1937, were junior synonyms of capucinus. They also raised X. capucinus robustior(Jacot, 1937) to the species level. If we include P. lophotrichus, P. imperfectus (Banks, 1906), P. prionotus
(Woolley, 1968), and P. dentatus (reported by Subías 2004 to be Holarctic), perhaps seven described species of Protoribates are known from or potentially occur in North America. Below we describe a new species, provide a new diagnosis for P. robustior, confirm the synonymy of P. prionotus with P. lophotrichus, and provide a key for the known species of the genus in North America.
Protoribates haughlandae sp. n.Figs 1–17, Map 1
Diagnosis. As for Protoribates (see above) and body length 470–570, colour reddish-brown, cuticle smooth; sensillus short (~58–65 long), sparsely barbed, ending in long, oboval club directed dorsally; sublamella short (~20), poorly defined; tutorial ridge long (~60) without cusp; notogastral setae very fine (~10–12 long); ventral shield with U-shaped submarginal furrow; discidium with subtriangular, knife-like custodium; femur II without distal ventral tooth; palptarsus double-horn on short, broad apophysis; heterotridactylous.
Description of female (N=22). Body length 460–470. Prodorsum (Figs 1, 3, 8–9). Smooth, rostrum blunt apically; lamella ~85 long, narrow (10–12), weakly striate longitudinally, without cusp; sublamella poorly defined, extending about one-third length of lamella; tutorial ridge (arrow in Fig 9) extending to level of le; sublamellar porose area Al (~21 diameter) near base of lamella above tutorial ridge; bo short (~58–65 long), sparsely barbed, ending in long, oboval club directed dorsally; ex minute (8), smooth; other prodorsal setae sparsely barbed, tapering, acuminate: ro (55–63); le (110–125), subparallel, directed anteriorly, inserted at tip of lamella, extending well past anterior of rostrum; in (115–120) passing anterior tip of lamella.
Notogaster (Figs 1, 3). Smooth, dorsal sejugal fissure distinct throughout; dorsophragmata well developed (15–20 long, ~18 wide), tongue-shaped, well separated (~50); pteromorph subtriangular with rounded tip, hinge (arrow in Fig 4) desclerotised over most of length, muscle insertions well developed between Aa and hinge; porose areas oval, surrounded by darker, ring-like rims: Aa largest (18–23 long), A1 (~10–15) inserted between lp and opisthonotal gland opening (gla), A2 (~12), A3 (~10); 10 pairs of short (10–12), fine notogastral setae.
Venter (Figs 2, 5, 14). Ventral setae mostly short (10–25), simple except g1 sparsely barbed; epimeral setae short (10–12 long), simple, 3a usually transverse, but aligned longitudinally in one specimen; epimeral fields with distinct borders and strong sigillar ornamentation; ap1 procurved, apsj (~65–70) ending in mushroom-like head at epimeral border near genital opening; ap3 (~32) extending about half distance to genital opening. Discidium (Figs 5, arrow 14) ~53 long x 20 high, custodium broadly tapering to point. Genital plates (65–73 long) with 3 pairs setae anterior, 2 pairs posterior, g1 (20) longest, others (~12–15) simple; genital papillae with broad (~11 long x 17 wide), rounded glans; ag (~12); ad1–3 subequal (20–27), ad3 inserted somewhat anterior to anal opening, ad1posterior to anal opening; iad adanal, parallel to large anal plates bearing 2 pairs of subequal (18–20) anal setae. Ventral shield with shallow, U-shaped submarginal furrow extending to about level of ag; circumpedal carina well developed; preanal organ normally developed.
Mouthparts (Figs 8–11). Subcapitulum diarthric, adoral setae (20–25) curved, tapering, barbed on one side. Rutellum broad, notched, with two teeth (Fig 10). Chelicerae large, robust (120 long x 55 high), movable digit (35–38) with 3 coarse teeth and distal hook; fixed digit with 2 teeth and hook; cheliceral setae coarsely barbed, tapering; Trägårdh organ small. Palpal setation 0-2-1-3-9(1); dorsal and lateral setae of femur, genu, tibia long, barbed; eupathid acm fused to solenidion to form double-horn on short, broad apophysis (Figs 10–11).
Legs (Figs 6, 8, 12–15). All tarsi heterotridactylous, median claws with sparse series of dorsal barbs; tarsi I–III short (60–75), laterally compressed, tarsus IV (65) more cylindrical, all with basal ventral porose areas; all tibiae with ventral porose areas, smallest (~15 long) on tibia IV; femora I–IV, trochanter IV with extensive porose areas on dorso-paraxial side, femora II–IV, trochanter IV with blade-like ventral keels. Leg setation (solenidia) of leg I: 1-5-3(1)-4(2)-20(2); II 1-5-2(1)-4(1)-15(2); III 2-3-1(1)-3(1)-15; IV 1-2-2-3(1)-12. Tarsus I (Figs 8, 12) excluding claws 65-70 long, famulus minute (4–5) blunt (Fig 6); solenidion ω2 (23) baculiform, ω1 (20) piliform; tibia I with strong apophysis bearing whiplike φ1 (130–150) and more or less ceratiform φ2 (65); genu I δ whiplike (~65). Tarsus II (Figs 8, 13) 60 long with 15 setae and two solenidia: 7 setal pairs (ft, tc, it, p, u, a, pv); seta s; solenidia ω1 (35), ω2 (32) baculiform; tibia II φ (~85), whiplike; genu II δ whiplike (~45); l” of genu II thick, spine-like (~25 long); femur II ventral keel lineate, running entire length of segment, rounded distally (Fig 13).
FIGURES 1–7. Protoribates haughlandae sp. n., Alberta, Canada. Adult. 1 dorsal habitus with left pteromorph extended (scale bar = 100 µm) 2 ventral habitus (scale bar = 50 µm) 3 lateral habitus (scale bar = 200 µm) 4 light micrograph of right pteromorph (scale bar = 100 µm, arrow points to hinge) 5 discidium (scale bar = 5 µm) 6 famulus of leg I (scale bar = 1 µm) 7arthropod cuticle in gut bolus (scale bar = 25 µm).
FIGURES 8–11. Protoribates haughlandae sp. n., Alberta, Canada. Adult. 8 lateral view of anterior with legs I–II withdrawn (scale bar = 50 µm) 9 dorso-lateral view of anterior with legs I–II extended to show tutorium (arrow) (scale bar = 30) 10 lateral view mouthparts (scale bar = 10 µm) 11 details of palpal tarsus (it’ not visible, scale bar = 1 µm).
Description of male (N=15). Similar to the female except generally smaller (470–520 long) and with spermapositor rather than ovipositor.
Description of deutonymph (N=1). Body (Figs 16–17) flattened, subrectangular, length 430, width 190. Prodorsal shield with uniform micropunctate ornamentation (interlamellar porose areas apparently not present) bearing 5 pairs of setae: bo (45 long) erect, terminating in drop-shape, sparsely spiculate club; in (65 long) thick (2), sparsely barbed; le broken off; ro (48) tapering-acuminate, sparsely barbed, extending well beyond tip of rostrum; ex minute (~3), smooth, erect. Gastronotic region smooth, white, with 15 pairs of sparsely barbed setae, each inserted eccentrically on a small porose sclerite; c3 in humeral position; h1-3 on posterior margin; p1-3ventral; many setae broken off but c1 (26), c2 (24), c3 (40), da (26), lm (26), lp (26), p2 (26), p3 (19). Coxal fields with microtuberculate ornamentation on posterior (I, II) and/or anterior (II, III, IV) margins; epimeral setation 3-1-2-2; genital valves with 2 pairs of setae; 1 ag; 3 ad; anal valves atrichous; 2 pairs of genital papillae. Tarsal claws sickle-shaped with dorsal line of sparse barbs; monodactyl, but claw on tarsus III bifurcate on left side (Fig 17 arrow); all femora with large porose areas on dorso-paraxial side; leg setation cannot be determined.
FIGURES 12–15. Protoribates haughlandae sp. n., Alberta, Canada. Adult legs in lateral views (scale bars = 10 µm). 12tarsus and tibia I 13 leg II 14 leg III (arrow points to tip of discidium) 15 leg IV.
Type material. Holotype ♀ (slide) and 38 paratypes: 8 ♀, 8 ♂ (slides), 6 adults (SEM), 15 adults (alcohol), 1 deutonymph (slide), ex organic layer in rich fen, with mostly small black spruce, tamarack, dwarf birch, willow, sedges and grasses, near Freeman Lake 10 km W Swan Hills (ABMI 910 SW 54.68661118, -115.556122), 14.vi.2010; holotype in PMAE.IZ, paratypes in PMAE.IZ, CNC, USNM. Additional paratypes: male, ABMI 13 NE (59.8699646, -112.579437) 10 km SW unnamed road, Wood Buffalo National Park, 12.vi.2009, mature mesic upland black spruce forest with Labrador tea, feathermoss; 2 adults, ABMI 63 SW (59.41637802, -111.659508) 6 km W unnamed road, Wood Buffalo National Park, 26.v.2011, rich fen dominated by tall shrubs, dwarf birch, willow with sedges and grasses; ♀, ♂, ABMI 484 SE (57.29631805, -119.8769) 30 km SE Miligan Hills Provincial
Park, 4.vi.2007, rich fen with shrubs, dwarf birch, willow, sedges, and grasses; 6 adults, ABMI 391 SW (57.26052475, -110.455292) 80 km NNE Fort McMurray, 31.v.2011, poor fen with shrubs, Labrador tea, sphagnum, sedges; 1 adult, ABMI 392 SW (57.1747551, -110.14296) 90 km NE Fort McMurray, 31.v.2011, poor fen with mostly small black spruce, tamarack and Labrador tea, sphagnum, sedges; 4 ♀, 2 ♂, ABMI 515 SW (57.12088013, -119.900093) 25 km W Chinchaga Wildland, 16.vi.2007, bog with black spruce, tamarack, Labrador tea, sphagnum, lichen; ♀, ABMI 472 NW (56.99316788, -113.571747) 10 km NNE Chipewyan Lake, 28.v.2008, rich fen, with mostly small black spruce, tamarack, dwarf birch, willow, sedges and grasses; ♀, 6 ♂, ABMI BOG6 SW (56.50244, -111.3064) 2 km S jct Routes 63 and 881, 28.vi.2007, untreed area with human disturbance; ♀, ABMI 569 NE (56.32915115, -112.424896) 20 km S Grand Rapids Wildland, 27.v.2009, rich fen, with mostly small black spruce, tamarack, dwarf birch, willow, sedges and grasses; 3 adults, ABMI 604 NW, SE (56.03934479, -111.209465) 20 km W Rout 881, Wood Buffalo National Park, 12.vi.2011, poor fen with mostly small black spruce and tamarack, Labrador tea, sphagnum, sedges; 2 adults, ABMI 608 SE (55.91720963, -110.027626) 3 km NE Graham Lake, 11.vi.2011, rich fen with dwarf birch, willow, sedges, grass; 2 adults, ABMI 608 NE (55.91720963, -110.027626) 3 km NE Graham Lake, 11.vi.2011, poor fen, with shrub cover with Labrador tea, sphagnum, sedges; ♀, ♂, ABMI BOG1 SW (55.3271, -112.47242) 200 m E Route 63, 12 km SE of McMillian Lake, 13.vi.2008, rich fen dominated by shrubs, dwarf birch, willow, sedges and grasses; ♀, ABMI BOG2 SW (55.30589, -112.48525) 200 m E Route 63, 15 km SE of McMillian Lake, 13.vi.2008, rich fen dominated by shrubs, dwarf birch, willow, sedges and grasses; ♂, ABMI UPL5 SE (55.15843, -113.0178) 1 km E Range Road 203A, SE Calling Lake Provincial Park, 17.vi.2007, bog with Labrador tea, sphagnum, sedges, grasses, and herbs; 2 adults, ABMI A761-4 SE (55.15634537, -111.656158) 5 km NE Buffalo Lake, 8.vi.2011, bog with mostly small black spruce and tamarack, Labrador tea, sphagnum, lichen; ♂, ABMI 881 SW (54.70869064, -114.23317) W Hwy 44 18 km N Hybert Lake Wildland, 26.v.2009, poor fen, with shrub cover, Labrador tea, sphagnum, sedges; ♂, ABMI 883 SE (54.6693573, -113.595978) 6 km E Bleak Lake along RR 244, 2.vi.2009, rich fen with mostly small black spruce, tamarack, dwarf birch, willow, sedges and grasses; ♀, ABMI 916 SW (54.49138641, -113.665222) near Bolloque Lake, 31.v.2009, mature moist upland balsam poplar mixed woodland with horsetail, dogwood, rose, willow; ♂, ABMI 974 NW (54.32911682, -116.306122) N Hwy 43 35 km E Fox Creek, 30.v.2008, bog with mature black spruce and tamarack, Labrador tea, sphagnum, lichen; 3 adults, ABMI 1071 SW (53.88096619, -117.342422) along Willow Creek Road, Yellowhead County, 27.v.2011, mature rich upland balsam poplar mixed forest with dogwood, ferns, feathermoss; ♂, 1170 NE (53.34415054, -117.076775) NE Hwy 47, Yellowhead County, 11.vi.2010, rich fen with mostly small black spruce, tamarack, dwarf birch, willow, sedges and grasses; ♂, 1171 SW (53.28146744, -116.769356) SW Hwy 47, Yellowhead County, 12.vi.2010, mature mesic upland pine forest, with Labrador tea and feathermoss; ♀, OG-1210-2 SW (52.93924713, -114.774429) S of Buck Lake, 11.vi.2010, treeless, human disturbed site with grasses, sedges; 3 adults, 1238 SE (52.8145256, -115.467941) 25 km NE Aurora Natural Area, 13.vi.2011, mature mesic upland forest with Labrador tea and feathermoss; 1 adult, OG-1160-1 SW (52.78925323, -110.302109) SE of Porter Lake, 31.v.2011, treeless, human disturbed site with lichens and bryophytes; 4 adults, 1379 SW (51.84659195, -114.763763) along Twp Road 334 N of Sundre, 31.v.2008, rich fen with mostly small black spruce, tamarack, dwarf birch, willow, with sedges and grasses; female, 1379 SE (51.84659195, -114.763763) along Twp Road 334 N of Sundre, 31.v.2008, rich fen with mostly small black spruce, tamarack, dwarf birch, willow, with sedges and grasses; 2 adults, 1439 SW (51.02621841, -111.178215) S jct Rts 561 and 884, 10.vi.2011, treeless, human disturbed site with grasses, sedges, herbs, ferns; 6 adults, 1439 NE, SE, SW (51.02621841, -111.178215) S of Cabin Lake, 10.vi.2011, treeless, human disturbed site with grasses, sedges, herbs, ferns. In PMAE.IZ.
Ecology and distribution. Protoribates haughlandae sp. n. is found primarily in open peatland habitats including rich and poor fens (alkaline to neutral wetlands fed by ground water) and bogs (acidic wetlands formed from rainwater) and extends into some of the more mesic forests (Table 1). Males were commonly collected and all populations appear to be bisexual. The gravid female can carry up to 6 eggs. Gut boluses were composed primarily of pigmented and unpigmented fungal hyphae and spores, often mixed with small particles of unknown organic matter. Two females had gut boluses with limbs and setae of soft-bodied arthropods indicating opportunistic predation (Fig 7). One female also contained numerous fragments of possible moss spores. The single deutonymph (tentatively assigned to the new species based on its size, sensillus, shape of genital papillae (Fig 17) and the absence of any other Oripodoidea in the sample), has a few fungal spores in the anal region of the gut.
TABLE 1. Habitat distribution of Protoribates species in Alberta: the number of sites where each species has been collected.
Remarks. The most distinctive character of the new species is the relatively short and erect sensillus (Figs 3, 8–9), otherwise not reported in the genus, and the heterotridactylous tarsal claws. In these characters the new species resembles some Haplozetes, but possesses the notogastral porose areas typical of other species of Protoribates, rather than saccules (see Weigmann 2010).
Because the new species tends to die with its legs retracted into a defensive position, the discidium is difficult to observe but unlike many Protoribates, that of the new species is not drawn out into a long, needle-like tip as is commonly seen in the genus (e.g. Fig 24), but is short and more knife-like, than needle-like. The apophysis bearing the palptarsal double-horn in species of Protoribates is often well developed, forming a strongly hook-like process (see Fig 20), but is short and broad in the new species (Figs 10–11), similar to that of P. dentatus (Weigmann et al.1993, Fig VI 5).
The legs of Protoribates species have been illustrated by Weigmann et al. (1993), Miko et al. (1994), and Ermilov and Anichkin (2011), and the latter have presented a hypothesis of setal homologies. The leg setation of the new species appears to be the same as P. heterodactylus Ermilov and Anichkin (2011) from Vietnam, including
the 15 setae on tarsus II (v’ and l’’ apparently absent). Both P. dentatus (Weigmann et al. 1993) and P. lophotrichus(Miko et al. 1994) have 17 setae on tarsus II. Similar interspecific variation in the setation of tarsus II is known in Haplozetes (Beck, 1964).
Etymology. The new species is named in honour of Dr. Diane Haughland, an ecologist and lichenologist, who during her PhD studies first brought this mite to our attention.
Protoribates lophotrichus (Berlese, 1904)
Oribates lophothrichus Berlese, 1904: 27.Protoribates lophothrichus (Berlese, 1904)—Sellnick 1928: 15.Protoribates lophotrichus (Berlese, 1904)—Willmann 1931:160 (emendation for grammar—see Marshall et al. 1987); Miko et
Material examined. Holotype ♀ Xylobates prionota Woolley, 1968: USA, Michigan: Label (in faint pencil): Livingston Co, Mich; E.S. George Reserve; 27 Nov – 1949; K. Bohnsack; 215A; in USNM. Paratypes 3 ♀ same data as holotype; 2 ♀ same data except Dec. 10, 1949, in Field Museum of Natural History.
Remarks. Subías (2004) lists P. prionotus as a junior synonym of P. lophotrichus, a species most easily characterized by its setiform sensillus. Examination of the holotype of Xylobates prionota Woolley, 1968, shows that the Subías (2004) synonymy appears to be correct. As shown in the redescription of P. lophotrichus by Miko et al. (1994), P. prionotus has the same distinctive sensillus, the same leg chaetotaxy, a tutorium expressed as a tectum, and 5 pairs of genital setae (erroneously given as 4 pairs in Woolley (1968)). The palps are not clearly visible in the holotype, but in one paratype they have the same distinctive, short and broad apophysis bearing the double-horn (see Fig IV 3 in Miko et al. (1994)).
Xylobates capucinus robustior Jacot, 1937: 244; Marshall et al. (1987): 267.Xylobates robustior Jacot, 1937—Norton and Kethley (1990): 490 (new status).
Diagnosis. Female ventral length 470–530, males unknown, body yellow-brown to brown in colour, cuticle smooth. Prodorsum (Figs 18, 21, 22) with narrow lamellae, poorly developed sublamella, short (~40) tutorial ridge, rostrum (Figs 18, 20) slightly raised medially, margin smooth, rounded; bo (~80) reflexed over notogaster, head narrowly expanded, acuminate distally, ciliate on anterior margin (Fig 21); ex minute (~2); other prodorsal setae, barbed, tapering, acuminate: in (~90–95), le (~40); ro (40). Notogaster with alveoli for 10 pairs of setae and 4 pairs of well developed porose areas each surrounded by a ring-like region (Fig 23), Aa (12–13) largest, A1 (5) with lpinserted on medial margin of ring; A2 (5), A3 (5); pteromorphs movable with hinge and well developed muscles (Fig 23); dorsophragmata relatively short (25), widely separated (55). Discidium (~55 long) with long, needle-like custodial tip (Fig 24); ad1 (30–40) somewhat longer than ad2 (25–27), both with short barbs, ad3 (~12–13) about half as long as ad2. Tarsus I (62–65 long, excluding apotele) with 17 setae (Figs 25–26): 7 setal pairs (ft, tc, it, p, u, a, pv) setae s, v’ (l’’ and setal pair pl absent), famulus (5–7) peg-like; solenidion ω1 (30–32) narrow and tapering, but with rounded tip, ω2 (30–35) baculiform; seta a’ (22–25), thick, with 3–5 pectines. Tarsus II (52–55 long) with s (20–23) very thick, with 4–7 pectines; a’ (23–26) similar, but with more pectines; pv’’ (~38 long) somewhat thickened (shaft ~2 wide) with numerous ventral pectines; solenidia ω1–2 (20–22) both baculiform. Tibia I–II each with strong to weak basal-ventral tooth; femora II–IV each with ventral blade-like keel, prolonged into strong distal lobe on femur II; ventral porose areas apparently absent from tarsi and tibiae; monodactyl, each claw with dorsal series of short barbs. Palpal tarsal double-horn hook-like, on well developed apophysis.
FIGURES 27–29 Protoribates capucinus Berlese, 1908, Nova Scotia. Adult. 27 Dorsosejugal region (arrow points to a dorsophragma). Protoribates imperfectus (Banks, 1906), Florida, USA. Adult. 28 alar region showing elongate, sinuate porose area Aa and setae lm, la. Protoribates oblongus (Ewing, 1909), Missouri, USA. Adult. 29 lateral view of tarsus and tibia I.
Material examined. USA: Cotypes: 37 females on slide 34F21-1 (with one Scheloribates lanceoliger (Berlese)), USNM; “from surface of soil (beneath the litter) of a 70 year old, mixed woodland, laboratory grounds, Bent Creek Experimental Forest, Buncombe Co., N. Car.; taken January 7th 1935, slide 34F21-1 (Jacot 1937); 5 females ex litter in second growth maple, beech, birch forest, Heiberg Memorial Forest (42.739, -76.077833), NY, 21.ix.2011, R.A. Norton. Alberta: 3 adults, Moose Pasture (53.656667, 112.759444), 2009; 4 ♀ MacTaggart Park, Edmonton, 1 June 2012; ♀, ABMI 892 NE (54.36624146, -110.994919), 31.v.2010; ♀, ABMI 452 NW (56.85694885, -110.307251), 10.vi.2011; 3 ♀, ABMI 330 NE, SW (57.66861725, -110.962219), 14.vi.2007; ♀ (545 SE (56.26429367, -110.207954), 1.vi.2007; 8♀ , ABMI 151 SW (58.76856232, -111.240944), 27.v.2010; ♀, ABMI 359 NE (57.45488358, -111.054222), 15.vi.2007; 2 adults (SEM) Onoway (53.77N, 114.06W), 13.iii.2008; 2 ♀, ABMI 64 NW (59.31958008, -111.284081), 27.v.2011; ♀, ABMI 1477 SW (50.88052368, -112.734695),
MAP 1 Collections of Protoribates robustior Jacot, 1937 (filled circles) and Protoribates haughlandae sp. n. (open circles), in Alberta, Canada. Stars mark major cities.
24.vi.2008; ♀, ABMI 1601 NE (49.73745728, -113.825783), 12.vi.2007; 3 ♀, ABMI 1602 NW (49.6853714, -113.608124), 13.vi.2007; ♀, ABMI 1602 SE (49.6853714, -113.608124), 13.vi.2007; 1adult (SEM), ABMI 1618 SW (49.56171417, -113.921532), 11.vi.2008; F, 2 ♀, ABMI 1567 SE (50.08177185, -113.789474), 29.v.2009; 10 adults (3 SEM) , ABMI OG-1218-1 NW (52.67760086, -112.46682), 28.v.2011; 1 adult , ABMI 1092 NE (53.23706055, -111.039818), 27.v.2011; 1 adult , ABMI 1461 NE (50.90753174, -111.286209), 15.vi.2011; ♀, ABMI 1434 NW (51.23065567, -112.634445), 12.vi.2008. All in PMAE.IZ. For habitat data see below and Table 1.
Ecology and distribution. Of the 30 specimens sexed, all were females. Other species of Xylobates are suspected thelytokous parthenogens (Norton and Kethley 1990) and that may be true of this species as well. Gravid females carry 2–3 large eggs. Of the Alberta collections on hand, 11 are from dry, treeless sites with grasses and sedges, 5 from dry upland forest mostly dominated by pine, and 3 from aspen woodlands (Table 1). The gut contents are difficult to interpret. Most gut boluses contain some fungal material, both dark and hyaline hyphae and the occasional spore. However, most boluses are composed mostly of coarse or sheet-like particulate matter, possible plant cell fragments, and a rare pollen grain. Hartenstein (1962) reported that P. lophotrichus fed primarily on the parenchyma of leaves and xylem fragments undergoing microbial decomposition and probably derived most of their nutrition from the microbes.
Remarks. Protoribates robustior appears to be widely distributed in eastern North America and can be distinguished from other species in this and similar genera by the characters in the key below. As far as we have been able to determine, this is the only species of Protoribates in North America where the setation of tarsus I is reduced by the loss of three fundamental setae and the absence of l’’ is usually easy to discern (Figs 25 vs 29).
Key to the species of Protoribates of North America (adults)
Although the two Albertan species of Protoribates occur primarily in the upper organic soil layers on open sites and tolerate human disturbance (Table 1), P. robustior occurs primarily on dry sites (grasslands, pine forests) and P.
haughlandae sp. n. primarily in wet sites (fens, bogs). Protoribates robustior has been collected from across the length of eastern Alberta, from the Canadian Shield in the far north east to the foothills and grasslands of the southeast (Map 1). Protoribates haughlandae sp. n., however, primarily inhabits the boreal forest and foothills (Map 1), probably reflecting the distribution of open peatlands.
The monodactyl species of Protoribates with reclinate sensilli tend to be very similar in appearance and many can be differentiated only with difficulty by variable characters such as the presence of spurs on leg segments, relative lengths of the adanal setae and the position of seta lp in relation to porose area A1 (see Weigmann et al.1993). All also probably reproduce by thelytokous parthenogenesis (Norton and Kethley 1990). It may be that these “species” are related clonal lineages that would be better subsumed under the oldest species name, but further study, especially of genetic similarity, is needed before this can be determined. In addition to Protoribates, at least two species similar to Lagenobates lagenula (Berlese, 1904) occur in eastern Canada and merit further study.
Acknowledgements
We would like to acknowledge the useful and constructive comments made by two anonymous referees, Roy Norton, Gerd Weigmann and Valerie Behan-Pelletier on earlier drafts of this manuscript and we would especially like to thank Valerie and Roy for providing specimens of species of Protoribates from eastern North America.
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