Two new species of tardigrades &om Short

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1 Heterotardigrada Journal ofthe Linnean Socd~ (1996), 116: With 7 figures Tardigrade biology. Edited &y S. J. McInnes and D. B. Two new species of tardigrades &om Short Mountain, Tennessee, U.S.A. KAREN KENDALL-FITE Diuision of Pollution Prevmtion/Environmmtal Awareness, Tmnessee, Nashville, Tennessee, , USA. AND DIANE R. NELSON Department of Biological Sciences, East Tennessee State Universig, Johnson Cip, Tmnessee, 37614, U.S.A. Tardigrades were collected from three seepage spring sites at 549m on Short Mountain, Cannon County, Tennessee. Three terrestrial samples and three aquatic samples were taken monthly from each site. Terrestrial samples included mosses and lichens from rocks and fallen trees; one sample of leaf litter was also collected from two of the sites. Aquatic samples included sediment, decaying leaf litter, and aquatic plants. Specimens of tardigrades were mounted on individual slides in Hoyer s medium. Species were identified and photographed using phase and differential contrast microscopy. Twenty-eight species representing 13 genera were recorded Pseudechinism, Echinism, Doryphoribius, Ramazzothus, Hypsibius, Zsohypsibius, Diphascon, PlaticriSta, Ztaquascon, Murrayon, Macrobiotus, Minibwtus, and Milnesium. One of the Pseudechiniscus species and an Zsohypsibius species were new to science and are described in this paper The Linnean Society of Landon ADDITIONAL KEY WORDS: - Tardigrada - Zsohypsi6ius - Pseudechinircus ~ Eutardigrada - Echiniscidae - Hypsibiidae - Parachela. ~ CONTENTS Introduction Material and methods Taxonomic account Pseudechiniscus brevimontanus sp. nov Discussion Isohssibius kenodontis sp. nov Discussion References Correspondence to: Karen Kendd-Fite, 319 Hatfield Drive, Franklin, TN 37064, U.S.A /96/ $18.00/ The Linnean Society of London

2 206 K. KEND.%LL-FITE AND D. NEISON IhTRODUCTION Studies of tardigrades in Tennessee have been conducted primarily in East Tennessee by Nelson (1 975) and her graduate students (Howard, 1980; Williams, 1982; Kincer, 1989; McGlothlin, 1990). Additional reports include those by Riggin (1 962, 1964), Kathman & Nelson (1 987), and Maucci (1987). Only two surveys were previously conducted in Middle Tennessee (Barnes, 1974; Hunter, 1977). In Middle Tennessee, one of the highest points is Short Mountain, a unique geological structure located in Cannon County, with an elevation of 638 m (Wilson, 1968). An erosional remnant of the Cumberland Plateau, Short Mountain is capped by Pennsylvanian sandstone (Miller, 1974). During a year-long study of the tardigrades of Short Mountain (Kendall-Fite, 1993), 28 species in 13 genera were found, including one new species of Pseudechiniscus and one of Isohypsibius, which are described here. M;\TERI;\L KND METHODS From November 1990 through November 199 1, 13 monthly collections were made at three seepage spring sites on the southeastern face of Short Mountain at an elevation of approximately 549 m. Three samples of terrestrial mosses and lichens from rocks and fallen trees adjacent to each spring were taken monthly. In one collection a sample of terrestrial leaf litter was taken at two sites. During the study period, 1 17 terrestrial samples were collected. Aquatic samples of sediment, decaying leaf litter, and aquatic plants were also collected monthly from each spring site, for a total of 11 5 aquatic samples. In the laboratory, a portion of thc dried terrestrial sample was removed, placed in a jar, and covered with tap water. The following day an equal volume of 85% ethanol was added to the jar; the jar was capped, mixed, and allowed to stand for at least 30 minutes (Pennak, 1989). To process aquatic samples, an equal volume of 85% ethanol was added to each container and allowed to stand for at least 30 minutes. The contents of each jar were passed through a series of three sieves with pore sizes of 425pm, 250pm, and 45pm, respectively (Williams, 1982). The material collected on the 45 pm sieve was washed into watch glasses and examined for tardigrades with a dissecting microscope at 50 X. Each tardigrade was removed with an Irwin loop and mounted in Hoyer s medium on a microscope slide. Later the coverslip was ringed with clear epoxy cement. Individual tardigrades were examined using differential interference contrast and phase contrast microscopy with oil immersion. A calibrated ocular micrometer was used for measurements. Photographs were made with Kodak T-max 100 film. TASONOh*lIC ACCOUNT Class Heterotardigrada Marcus, 1927 Order Echiniscoidea Marcus, 1927 Family Echiniscidae Thulin, 1928 Genus Pseudechiniscus Thulin,

3 SHORT MOUNTAIN TARDIGRADES 207 Pseudechiniscus brevimontanus Kendall-Fite & Nelson sp. nov. (Figs 1-3). Description HoloQpe, female (USNM #264088). Kendall-Fite (1993). Body length 165 pm. Eyespots present. Cephalic plate faceted. Fine cuticular granulation on cephalic and scapular plates; larger, heavy granulation on margins of segmental plates I1 and I11 and pseudosegmental plates, with central horizontal band of less prominent granulation. Median plates 1 and 2 divided; medium plate 3 undivided. Coarse granulation on median plates uniform (Figs 1, 2). Ventral cuticular granulation present with a dense patch between legs I1 and between legs 111; a mottled appearance on the rest of the ventral surface (Fig. 3). Cirri A short, 3 1.O pm; adjacent clavae well-formed, 4.5 pm; external (18.0 pm) and internal (15.0 pm) buccal cirri present and prominent. Cephalic papillae dome-shaped, 4.0 pm. Two triangular projections extending 6.5 pm from caudal margin of pseudosegmental plate (Figs 1, 2). Four single claws per leg; internal claws with thin, downward-curved ventral spurs. No dorsal leg spines; small, blunt papillae on legs IV. Collected from dried moss and lichen on fallen tree at site 2 on Short Mountain on 29 December Figure 1. Pseudechiniscus brevimontunus sp. nov. Habitus, dorsal view, scale bar = 10pm.

Purugpes. A total of five specimens; collected from dried moss and lichen from a fallen tree at site 2 on 29 December 1990.

4 Purugpes. A total of five specimens; collected from dried moss and lichen from a fallen tree at site 2 on 29 December One specimen deposited in the National Museum of Natural History (USNM #264089). One specimen deposited in Nelson collection, East Tennessee State University, Johnson City, Tennessee, U.S.A. Remaining three specimens deposited in Kendall-Fite collection, Nashville, Tennessee, U.S.A. Body length pm. Eyespots present. Dorsal and ventral cuticular granulation as in holotype. Cirri A pm; adjacent clavae well-formed. External and internal buccal cirri and cephalic papillae as in holotype. Two triangular projections extending from caudal margin of pseudosegmental plate. No dorsal leg spines. Claws and papillae on legs IV as in holotype. 7jpe locnlip. South-facing slope of South Mountain, Cannon County, Tennessee, U.S.A., at 549 m. Figures 2-3. PseudecLiniscus brevimontunus sp. nov. Fig. 2. Dorsal view, differential interference contrast. Fig. 3. Ventral Iiew; differential interference contrast. Scale bars = 10 pm.

5 SHORT MOUNTAIN TARDIGRADES 209 EQmology. This species is named for the type locality, Short Mountain brevi-(l), short; -montan(l), mountain]. Discussion The family Echiniscidae was reviewed by Kristensen (1987). His cladogram of the 12 genera illustrates the divergence of the Pseudechiniscus from the Echiniscus line. The genera Pseudechiniscus and Echiniscus are cosmopolitan and comprise about 85% of the family (Kristensen, 1987). The genus Pseudechiniscus Thulin, 191 1, consists of approximately 30 species, including the type species Pseudechiniscus suillus (Ehrenberg, 1853). The genus is characterized by the presence of a pseudosegmental plate, internal and external buccal cirri, and filamentous cirri A. Median plates 1 and 2 are divided; median plate 3 is undivided. Kristensen (1987) distinguishes two groups: the suillus/conijir group without trunk cirri, and the victor group with trunk cirri or spines present. The new species belongs to the suillus/conijir group, and is characterized by two triangular projections on the caudal margin of the pseudosegmental plate and the granulation pattern on paired plates I1 and I11 and the pseudosegmental plate. Similar projections are found on Pseudechiniscus bartkei Weglarska, 1962, Pseudechiniscus bidenticulatus Bartos, 1963, Pseudechiniscus insolitus Maucci, 199 1, Pseudechiniscus islandicus (Richters, 1904), Pseudechiniscus novazeelandiae (Richters, 1908), Pseudechiniscus occultus Dastych, 1980, Pseudechiniscus ramazzottii Maucci, 1952 (Maucci, ; Ramazzotti & Maucci, 1983), and an undescribed species collected by McGlothlin (1990) on Roan Mountain. The Short Mountain species differs from P. bartkei by the absence of a tri-lobed median plate 1 and from P. bidenticulatus by the absence of circular projections on the posterior margins of paired plates I1 and I11 (Ramazzotti & Maucci, 1983). The presence of lateral projections at positions B, C, D and E, and dorsal projections on the paired and median plates distinguishes P. insolitus, P. islandicus, and P. occultus from our new species (Maucci, 1991; Ramazzotti & Maucci, 1983). The presence of lateral projections at positions B, C and D distinguishes P. nouazeelandiae and the Roan Mountain species from the Short Mountain species (McGlothlin, 1990; Ramazzotti & Maucci, 1983). In comparison to the cuticular pattern on P. breuimontanus, P. rammazzottii has coarse uniform granulation, absent only on the rostra1 margin of the scapular plate and the caudal margin of the paired plates (Ramazzotti & Maucci, 1983). In addition, P. ramazzottii has a robust spine on leg IV, whereas the papillae of P. breuimontanus are small and blunt. Class Eutardigrada Marcus, Order Parachela Schuster, Nelson, Grigarick, & Christenberry, 1980 Family Hypsibiidae Pilato, 1969 Genus Isobpsibius Thulin, 1928 Isohypsibius kenodontis Kendall-Fite & Nelson sp. nov. (Figs 4-7) Description Hologpe (USNM #264086). Kendall-Fite (1993). Body length 385 pm. Eyespots

6 210 4 K. KEhDALL-FITE AND D. NELSON Figure 4. Isohypsibius kenodmris sp. nov. A, habitus, ventral view; B, claws on legs 111; C, claws on legs IV: D, ventral buccal armature and crest; E, dorsal view of buccal-pharyngeal apparatus; F, granularion on dorsolaterd cuticle between legs 111 and IV. Scale bars, A = 100 prn, B-F = 10 pm.

7 SHORT MOUNTAIN TARDIGRADES 21 1 present. Colourless cuticle, with an irregular polygonal network of partially fused granules on dorsal and lateral surfaces, not extending to the ventral surface, and on legs IV at the base of the claws (Figs 4F, 7). Indentations on the anterior margin of the small buccal ring may give the false appearance of short lamellae. Buccal armature without transverse crests or mucrones; however, there is a slight thickening at the top of the stylet sheath. Dorsal and ventral crests present on buccal tube for stylet muscle insertion. Buccal tube narrow, 4.0pm wide (external, at insertion of stylet supports) by 36.0 pm long; pt ratio = Length of buccal tube from top of stylet sheaths to insertion of stylet supports 27.5 pm. Pharyngeal bulb spherical, with two thin cuticular bars between apophyses and first macroplacoids. Large apophyses, triangular in lateral view; 2.5 pm in length. Three blunt rod-shaped macroplacoids; first 3.0pm long, second 2.5pm and third 3.5pm; first and second may appear partially connected, second and third clearly separate. Placoid row slightly curved; length 12.5 pm (Figs 4D & E, 5). No microplacoid or septulum. Isohypsibius-type claws, sequence (Figs 4B & C, 6). Primary branch and basal tract of external claw are longer and more slender than those of internal claw on legs I-IV, especially on legs IV. On leg IV posterior claw 2 1.O pm; anterior, 15.5 pm. On leg 111, external claw 17.5 pm; internal, pm. No lunules, but external claw has expanded base. Short accessory points, poorly developed, on primary branch of claws. No cuticular bars. Para&jes. Six adult paratypes with buccal apparatus and two in simplex; six exuvia with eggs. Six specimens deposited in the National Museum of Natural History (USNM #264087, # ). Five specimens deposited in Nelson collection, East Tennessee State University, Johnson City, Tennessee, U.S.A. Remaining specimens deposited in Kendall-Fite collection, Nashville, Tennessee, U.S.A. Body length pm. Cuticle as in holotype. Buccal tube pm wide by pm long. Distance from buccal ring to stylet support insertion pm. First macroplacoid pm; second macroplacoid pm; third macroplacoid pm. Smooth eggs, diameters of pm; 5-6 eggs deposited in exuvium. Qpe localip. South-facing slope of Short Mountain, Cannon County, Tennessee, U.S.A., 549m, dried moss on rock, site 2, 29 November 1991 (holotype and 13 paratypes), 17 July 1991 (1 paratype). Epmology. The name of this species in based on the absence of buccal armature Fenodontis (G) - toothless]. Discussion Isohypsibius hodontis is characterized by a granulated cuticle, three macroplacoids, no buccal armature, and no cuticular bars on the legs. Similar Isohypsibius species with granulations on the cuticle include Isohypsibius baldii Ramazzotti, 1945, Isohypsibius granulijir Thulin, 1928, Isohypsibius marii Bertolani 198 1, and Isohypsibius monoicus Bertolani 1981, all of which are typically aquatic (Bertolani, 1982; Ramazzotti & Maucci, 1983). Isohypsibius tetradacploides (Richters, 1907) has similar macroplacoids and also lacks cuticular bars, but the cuticle is smooth. The granulation pattern distinguishes the new species from others with sculptured

SHORT MOUNTAIN TARDIGRADES 213 cuticles. Isohypsibius kenodontis has an irregular polygonal network of partially fused granules on the dorsal and lateral, but not the ventral, cuticle.

9 SHORT MOUNTAIN TARDIGRADES 213 cuticles. Isohypsibius kenodontis has an irregular polygonal network of partially fused granules on the dorsal and lateral, but not the ventral, cuticle. In comparison, I. baldii has distinct tubercles, arranged dorsally in a reticular pattern. On I. granulijtt, the tubercles are smaller than on I. baldii and extend both dorsally and ventrally; also there is a short cuticular bar at the base of the claws on legs 1-111, and the buccal armature consists of a single row of rounded teeth. The cuticle of I. marii is reticulated; however, cuticular bars are present on legs 1-111, the buccal armature is similar to I. granul@r, and the rnicroplacoids are very narrow. The cuticle of I. monoicus is very similar to I. kenodontis, however the buccal armature of I. monoicus consists of 4-6 large points, more developed medially, on the ventral side, and a single large median arc on the dorsal side. In addition, the macroplacoids of I. monoicus are oval granules of similar dimensions and the claws are very large. Isohypsibius kenodontis was initially identified as a irhuliniu species based on the claw structure and the presence of what appeared to be short lamellae on the buccal ring. However, further comparison of type specimens of irhulinia with the new Isohypibius species in the laboratories of Drs R. Bertolani and H. Dastych, visited by the coauthor (Nelson), revealed that the indentations visible on the buccal ring in some Short Mountain specimens were not true lamellae. REFERENCES Barnes JA Tardigrades from Rutherford County, Tennessee. Unpublished Master's Thesis, Middle Tennessee State University, Murfreesboro. Bertolani R Tardigradi (Tardigrada). Guide per il Riconoscimento delle Specie Animali delle Acque Interne Italiane, 15. Verona, Italy: Consiglio Nazionale delle Ricerche. Howard CY Tardigrades from Rattlesnake Spring, Bradley County, Tennessee. Unpublished Master's Thesis, East Tennessee State University, Johnson City. Hunter ME A study of the Tardigrada from a farm in Montgomery County, Tennessee. Unpublished Master's Thesis, Austin Peay State University, Clarksville. Kathman RD, Nelson DR Population trends in the aquatic tardigrade Pseudobwhu augmti (Murray). In: Bertolani R, ed. Biology of Tardigrades. Selected Symposia and Monograph U.<.I., 1. Modena, Italy: Mucchi, Kendall-Fite M Tardigrades from Short Mountain, Cannon County, Tennessee. Unpublished Master's thesis, Middle Tennessee State University, Murfreesboro. Kincer CJ Effect of habitat disturbance on tardigrade populations from Brush Creek Tributary, Washington County, Tennessee. Unpublished Master's thesis, East Tennessee State University, Johnson City. Kristensen RM Generic revision of the Echiniscidae (Heterotardigrada) with a discussion of the origin of the family. In: Bertolani R, ed. Biology of Tardigrades. Selected Symposia and Monographs U.<.I., 1. Modena, Italy: Mucchi, Maucci W A contribution to the knowledge of the North American Tardigrada with emphasis on the fauna of Yellowstone National Park (Wyoming). In: Bertolani R, ed. Biology OfTardigradzs. Selected Symposia andmonographs UZI., 1. Modena, Italy: Mucchi, Maucci W Due move specie di Tardigradi muscicoli della Spagna. Bollettino del Mwco CiUico di StoriaNaNaturale di VETOW 15: McGlothlin KL Long-term stability in tardigrade populations on Roan Mountain, Tennessee. Unpublished Master's Thesis, East Tennessee State University, Johnson City. McInnes S Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal ofjvatural Histo? 28: Miller RA The geologic history of Tennessee. 'Tennessee Divisz'on of Geolo~ Bulletin 74: Nelson DR Ecological distribution of tardigrades on Roan Mountain, Tennessee-North Carolina. Memolie dell'lstituto Italian0 di Idrobwlogia 32 (Suppl): Pennak RW Tardigrada (Water Bears). Freshwater Inueltebrates ofthe United States, 3rd edn. New York John Wiley and Sons, Ramazzotti G, Maucci W I1 phylum Tardigrada. Memorie dell'istinatuta Italian0 di Idrobwhgia 41: Riggin GT Tardigrada of southwest Virginia: with the addition of a description of a new marine tardigrade species from Florida. Krginia Agruultural Expm'ment Station Technical Bulletin 152:

$21'4 K. KENDAI.I,-FITE t\nd D. NELSON Riggin GT. 1964. Tardigradeq from the Southern Appalachian Mountains. Transactions ojthr Amerian Microscopicd SJ&~ 83(3!: 277-282. Williams TC. 1982.$

10 21'4 K. KENDAI.I,-FITE t\nd D. NELSON Riggin GT Tardigradeq from the Southern Appalachian Mountains. Transactions ojthr Amerian Microscopicd SJ&~ 83(3!: Williams TC A study of tardigade populations from Brush Creek Tributary, Washington County, Tennessee. Unpublished Master's Thesis, East Tennessee State University, Johnson City. Wilson CWW Geological map and mineral resources of Short Mountain Quadrangle (GM 323-SW). Division of Geolog).. State of Tcrinessee and Washington D.C.: US. Geological Survey; 1:24,000; 57.5 X 47 cm. English.

REDESCRIPTION OF DORYPHORIBIUS VIETNAMENSIS (IHAROS, 1969) (TARDIGRADA) COMB. NOV. ON THE BASIS OF THE HOLOTYPE AND ADDITIONAL MATERIAL FROM CHINA

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