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Tardigrades of the University of Central Arkansas Campus, Conway, AR
Marshalluna Land, Adam Musto, William R. Miller, David E. Starkey, and Jeffrey D. Miller

Southeastern Naturalist, Volume 11, Issue 3 (2012): 469–476

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2012 SOUTHEASTERN NATURALIST 11(3):469–476 Tardigrades of the University of Central Arkansas Campus, Conway, AR Marshalluna Land1, Adam Musto1, William R. Miller2, David E. Starkey1, and Jeffrey D. Miller1,3,* Abstract - Tardigrades were recovered from samples of moss and lichen growing on the bark of seven species of trees on the University of Central Arkansas (UCA) campus in Conway, AR. Of the 11 genera of tardigrades previously reported from the state, five were found in the UCA campus samples; of the 25 species previously reported, five were found in the UCA campus samples. Two species (Milnesium eurystomum, Macrobiotus polyopus) are new records for the state; one species of Echiniscus (arctomys group) could not be identified and may be new. Tardigrades were not uniformly distributed among available habitats (moss, lichen) or substrates (trees). Introduction Terrestrial tardigrades are small (0.5 mm) metazoans that typically inhabit mosses and lichens growing on trees, rocks, and the ground (McInnes 1994, Miller 1997). Little is known about their ecology, although other aspects of their biology are better documented (Kinchen 1994). Tardigrades are best known for their ability to survive conditions such as extreme cold and heat in a desiccated state called cryptobiosis (Miller 1997). Recently, tardigrades have become the first multi-celled animal to survive the vacuum, radiation, and temperature of outer space (Jonsson et al. 2008). The distributions of North American taxa are poorly known (McInnes 1994, Miller 1997). Multiple genera of tardigrades have been reported from the states contiguous to Arkansas (Louisiana: Hinton et al. 2010, Meyer and Domingue 2011; Mississippi: Hinton and Meyer 2009, Mitchell and Romano 2007; Missouri: Hidalgo and Combs 1985, Hohl et al. 2001, Lehmann et al. 2007; Oklahoma: Beasley 1978, Beasley and Pilato 1987, Lee and Woolever 1983; Texas: Hinton and Meyer 2007, Mehlen 1969, Miller and Mehlen 2007). To date, only three papers deal with tardigrades of Arkansas. Beasley and Pilato (1987) described a new species Doryphoribius gibber Beasley and Pilato based on specimens found in Benton County. Meyer (2001) reported 21 species from sites in Benton, Crawford, Franklin, Polk, and Washington counties. Meyer (2006) reported on the distribution and abundance of tardigrades in small samples in the Ouachita Mountains; he added two species to the state biodiversity list and extended the distribution of four others. 1Department of Biology, University of Central Arkansas, Conway, AR 72035. 2Department of Biology, Baker University, Baldwin City, KS 66006. 3Biological Research and Education Consultants, 446 Dearborn Avenue, Missoula, MT 59801. *Corresponding author - 470 Southeastern Naturalist Vol. 11, No.3 This report extends tardigrade distribution and diversity to Faulkner County in the central part of the state, and offers analyses for patterns of habitat associations. Materials and Methods The study area was the developed part of the University of Central Arkansas (UCA) campus, Conway, AR. Mosses and lichens were sampled to represent their occurrence on mature trees during December 2009 and March 2010. Each tree (substrate) was identified and located with a handheld GPS unit. Each habitat sample (approximately 5 x 5 cm) was scraped into a small paper bag and dried at room temperature. The dry samples were divided; half was stored as a herbarium sample and the other half was soaked in 25 ml of bottled water for 24 hours. Three 2-ml aliquots of the debris were extracted with a disposable pipette and examined at 20x magnification under a dissecting microscope. Specimens were mounted on a glass slide in PVA (polyvinyl alcohol) media with an Irwin loop. The cover slip was sealed with clear fingernail polish and the location of the specimen marked on the slide. Specimens were examined with an Olympus DX- 60 differential interference contrast (DIC or Nomarski) microscope. The keys found in Ramazzotti and Maucci (1983), Nelson and McInnes (2002), and Pilato and Binda (2010) were used for identification. Chi-square tests were used to compare expected occurrence to the observed data (Zar 1999). The expected or null hypothesis is for uniformity of dispersion based on the assumptions that within a small area (the campus): (a) all species are distributed equally, (b) all substrates (trees) support all habitats (moss and lichen) equally, and (c) the occurrence of a tardigrade indicates that the conditions were within the survivable range of the species. Therefore, a statistical difference from the expected uniformity of occurrence of habitats and tardigrades provided evidence of habitat preference by the species. Results Sixty-nine samples (40 moss, 29 lichen) were collected from 14 trees of seven species (Table 1) on the UCA campus (35°04'52.5"N, 92°27'46.5"W) in Conway, AR. Two classes, three orders, three families, five genera, and eight species of tardigrades were recovered. The species identified were Echiniscus maucii Ramazzotti, Milnesium tardigradum Doyère, Milnesium eurystomum Maucci, Macrobiotus cf. hufelandi C.A.S. Schultze, Macrobiotus polyopus Marcus, Paramacrobiotus tonollii (Ramazzotti), Minibiotus intermedius (Plate), and an unidentifiable species of Echiniscus in the arctomys group that may be new. Seven specimens were classified as Macrobiotus cf. hufelandi, but without eggs the identification was considered tentative. One hundred and two tardigrades were recovered; 36 (35.3%) were found in lichen samples, and 66 (64.7%) were recovered from moss (Table 1). Moss and lichen habitats on two of six genera of trees (Quercus [oak], Liquidambar [sweet gum]) were home to all eight species and more than 81.4% of the specimens (Table 1). Two species, Minibiotus intermedius (n = 42) and 2012 M. Land, A. Musto, W.R. Miller , D.E. Starkey, and J.D. Miller 471 Table 1. Numbers of tardigrades recovered from habitats on substrates on the UCA campus. M. i. = Minibiotus intermedius, M. t. = Milnesium tardigradum, M. h. = Macrobiotus hufelandi, E. m. = Echiniscus mauccii, M. e. = Milnesium eurystomumm, P. t. = Paramacrobiotus tonollii, M. p. = Macrobiotus polyopus, and E.sp. 3. = Echiniscus sp. 3. # tardigrades Substrate Habitat recovered M. i. M. t. M. h. E. m. M. e. P. t. M. p. E. sp. 3 Quercus accutissima Carruthers Moss 15 12 1 2 (Sawtooth Oak) Lichen 7 5 2 Quercus phellos L. Moss 27 5 16 1 1 2 2 (Willow Oak) Lichen 11 2 5 2 1 1 Liquidambar styraciflua L. Moss 14 6 5 1 1 1 (Sweet Gum) Lichen 9 6 1 1 1 Magnolia grandiflora L. Moss 1 1 (Southern Magnolia) Lichen 3 1 2 Prunus serotina Ehrhart Moss 3 1 1 1 (Black Cherry) Lichen 2 2 Liriodendron tulipifera L. Moss 3 2 1 (Tulip Tree) Lichen 3 3 Catalpa speciosa (Warder ex Barney) Moss 3 3 Engelmann (Northern Catalpa) Lichen 1 1 Totals 102 42 37 7 6 4 3 1 2 % specimens by species 41.2 36.3 6.9 5.9 3.9 2.9 1.0 2.0 Substrates selected (n = 7) 6 3 3 6 3 2 1 1 Specimens per habitats (moss/lichen) 26/13 24/13 6/1 2/4 3/1 3/0 0/1 2/0 472 Southeastern Naturalist Vol. 11, No.3 Milnesium tardigradum (n = 37), comprised 77.5% of the specimens; the other six species contributed only 22.5% to the total (Table 1). Five tardigrade species occurred in both moss and lichen habitats, while two species (Paramacrobiotus tonollii, Echiniscus sp. 3), were found only in moss habitats, and one species (Macrobiotus polyopus) was only recovered from a lichen sample. The average number of tardigrades recovered per sample ranged from 7.5 to 0.25, with a mean of 1.48. Moss samples yielded a mean of 1.65 tardigrades per sample, while the lichen samples yielded a mean of 1.24. Moss and lichen habitats did not occur uniformly (χ2 = 8.64, df = 1, P < 0.05). Likewise, tardigrades were not distributed evenly on the substrates (χ2 = 199.14, df = 6, P < 0.05). Accepting the differential occurrence of the habitats, we altered the assumption of tardigrade occurrence to be proportional to the availability of moss (64.7%) and lichen (35.3%) habitats. Still, tardigrades were not distributed in proportion to the habitat (χ2 = 87.05, df = 13, P < 0.05; Table 2). Because chi-square of the total is a summation of the individual chi-squares for the parts, it is possible to evaluate the contribution of the parts to the total. Our individual calculated chi-square values ranged from 0.19 to 44.67, and three calculated values were significantly greater than the critical value (Table 2). The tardigrades from the moss and lichen habitats found on Magnolia grandiflora (Southern Magnolia) substrate exhibited a reversal of the expected ratios, resulting in significant values for chi-square (moss: χ2 = 24.36, lichen: χ2 = 44.67, df = 1, P < 0.05). The lichen samples from Liriodendron tulipifera (Tulip Tree) Table 2. Chi-squared analysis of the occurrence of tardigrades recovered from moss and lichen samples on trees of the University of Central Arkansas campus. Trees = # of trees sampled, tard./ substrate = # of tardigrades recovered per substrate, % tard. = % tardigrades, χ2 = calculated χ2 with df = 1, tard./habitat = # of tardigrades recovered per habitat, % spec. = % specimens. Tard./ % # Tard./ % Substrate trees substrate tard. χ2 Habitat samples habitat spec. χ2 Quercus accutissima 1 22 21.6 30.32A Moss 2 15 68.2 0.19 (Sawtooth Oak) Lichen 2 7 31.8 0.34 Quercus phellos 5 38 37.3 130.77A Moss 16 27 71.1 0.62 (Willow Oak) Lichen 10 11 28.9 1.14 Liquidambar styraciflua 4 23 22.5 34.54A Moss 10 14 60.9 0.23 (Sweet Gum) Lichen 8 9 39.1 0.42 Magnolia grandiflora 1 4 3.9 1.35 Moss 4 1 25.0 24.36A (Southern Magnolia) Lichen 2 3 75.0 44.67A Prunus serotina 1 5 4.9 0.63 Moss 2 3 60.0 0.34 (Black Cherry) Lichen 3 2 40.0 0.63 Liriodendron tulipifera 1 6 5.9 0.18 Moss 3 3 50.0 3.34 (Tulip Tree) Lichen 2 3 50.0 6.13A Catalpa speciosa 1 4 3.9 1.35 Moss 3 3 75.0 1.64 (Northern Catalpa) Lichen 2 1 25.0 3.00 df = 6 df = 13 Totals 14 102 199.14B 69 102 87.05C Asignificant (χ2 [0.05] = 3.84, df = 1) Bsignificant (χ2 [0.05] = 12.59, df = 6) Csignificant (χ2 [0.05] = 22.36, df = 13) 2012 M. Land, A. Musto, W.R. Miller , D.E. Starkey, and J.D. Miller 473 contained significantly more tardigrades than expected (lichen: χ2 = 6.12, df = 1, P < 0.05; Table 2.) Discussion The taxonomy and distribution of tardigrades in Arkansas are poorly described. Only three papers have dealt with tardigrades in the western and northwestern portions of the state (Table 3). We have reduced the list of species found by Meyer (2001) by one. Echiniscus banus Caskey, 1971 is not a described species (Degma et al. 2011a). It should be, but its description has never been published. It was reported in a 1971 unpublished Master’s thesis titled “The Tardigrades of Texas” by D.S. Caskey at Lamar University. We have imbedded the reference here and listed the animals as Echiniscus sp. 2 in Table 3. Table 3. Tardigrades of Arkansas. Key: 1= Beasley and Pilato 1987; 2 = Meyer 2001; 3 = Meyer 2006; 4 = this report. Counties: B = Benton, C = Crawford, Fa = Faulkner, Fr = Franklin, P = Polk, and W = Washington. Genus species B C Fa Fr P W Heterotardigrada Echiniscus mauccii Ramazzotti, 1956 4 2 E. virginicus Riggin, 1962 3 2 Echiniscus sp. 1 2 2 2 2 Echiniscus sp. 2 (E. banus Caskey, 1971) 2 Echiniscus sp. 3 4 Pseudechiniscus brevimontanus Kendall-Fite 2 and Nelson, 1996 P. novaezelandiae (Richters, 1908) 2 2 P. suillus (Ehrenberg, 1853) 2 2 2 Eutardigrada Milnesium tardigradum Doyère, 1840 2 2 4 2 2, 3 2 M. eurystomum Maucci, 1991 4 Astatumen trinacriae (Arcidiacono, 1962) 2 Diphascon (Diphascon) alpinum Murray, 1906 2 Hypsibius calcaratus Bartoš, 1935 2 2 H. convergens (Urbanowicz, 1925) 2 Ramazzottius baumanni (Ramazzotti, 1962) 3 R. oberhaeuseri (Doyère, 1840) 2 3 2 Doryphoribius gibber Beasley and Pilato, 1987 1 Macrobiotus echinogenitus Richters, 1904 2 2 2 2 2 M. cf. harmsworthi (Murry, 1907) 2 3 M. cf. hufelandi C.A.S. Schultze, 1833 4 2 M. islandicus Richters, 1904 2 M. occidentalis Murray, 1910 2 2 M. polyopus Marcus, 1928 4 Macrobiotus sp. 1 2 2 2 2, 3 2 Macrobiotus sp. 2 2 2 2 2 Paramacrobiotus tonollii (Ramazzotti, 1956) 4 3 P. areolatus (Murray, 1907) 2 Minibiotus furcatus (Ehrenberg, 1859) 2 M. intermedius (Plate, 1888) 2 2 4 2 2, 3 2, 3 474 Southeastern Naturalist Vol. 11, No.3 The samples collected on the UCA campus contained 5 of the 11 genera previously found in Arkansas and 5 of the 25 known species. Two species (Milnesium eurystomum, Macrobiotus polyopus) are new records for the state; Echiniscus sp. 3 could not be identified to species and may be a new record for the state because Meyer (2001) reported two unidentified species for the genus but did not describe them sufficiently to allow comparison. On a larger scale, three tardigrade species (Milnesium tardigradum, Minibiotus intermedius, Macrobiotus cf. hufelandi) are cosmopolitan in distribution (McInnes 1994) and are likely to be widespread in Arkansas. Two other species (Macrobiotus tonolli, Echiniscus maucci) are restricted to North America and have known distributions in contiguous states, Missouri and Tennessee (McInnes 1994). As such, their occurrence in Arkansas was not unexpected. Two species (Milnesium eurystomum, Macrobiotus polyopus) are new records for the state. One species (Macrobiotus polyopus) has previously been reported only from South America and Southeast Asia; the extension of its range to North America is unusual but not unexpected because tardigrades are believed to be wind dispersed (Miller 1997). Isolated records of species known previously only from other continents may also be the product of passive transport by the global movement of ornamental plant products or other human actions (Kinchin 1994). This global transport might make a tardigrade species invasive, and with their documented ability to be a vector for plant pathogenic bacteria (Krantz et al. 1999), might elevate them to an economically important level. The differences in the number of tardigrades recovered from the habitat samples collected from a single substrate species when compared to the number collected from any of the other single substrate species indicates that the habitat/ substrate combination likely impacts the suitability of the habitat for tardigrades. Therefore, a species that exhibits an unequal distribution may be expressing habitat selection. The total number of tardigrades recovered from moss and lichen provides an indication of the suitability of the habitats to support tardigrades. In general, moss supported more tardigrades numerically and taxonomically than lichen (Table 1). Two species (Minibiotus intermedius, Milnesium tardigradum) were recovered in higher numbers from almost every habitat from each substrate where they occurred with other species (Table 1). The exceptions to their ubiquitous distribution include the lack of these species from moss growing on Southern Magnolia, and lichen on Prunus serotina (Black Cherry) and Tulip Trees, and both habitats on Catalpa speciosa (Northern Catalpa) (Table 1). On average, 64.7% of the specimens were recovered from moss samples regardless of the substrate on which the moss grew (Table 1). The exception to the general pattern occurred on Southern Magnolia. On this tree, the ratio of tardigrades recovered from moss and lichen samples was reversed (Table 2). In addition, the number of tardigrades was higher than expected on the Tulip Tree. Although the numbers of specimens are low, the reversal in the expected pattern in these two substrates indicates further collection and analysis are warranted. 2012 M. Land, A. Musto, W.R. Miller , D.E. Starkey, and J.D. Miller 475 The difference in the distribution of moss and lichen, perhaps as a consequence of the characteristics of the substrate (tree), may be a major contributing factor to distribution of tardigrades. The more frequent occurrence of tardigrades in moss on oak trees than on the Southern Magnolia tree may reflect the difference in the bark structure and water dynamics. Oak trees have a much rougher bark than Southern Magnolia trees, which may affect the ability of the moss to adhere and grow on the substrate. Although raising the issue of subtle aspects of tardigrade ecology, the results of the present study are descriptive rather than predictive. The number of tardigrades and the species composition found in a sample vary considerably over a short distance (Degma et al. 2011b, Meyer 2006, Miller et al. 1994). At the present time, cataloging species and reporting relative abundance in samples is important to assembling a clearer picture of the diversity and distribution of tardigrades on local, regional, and continental scales. Acknowledgments We wish to acknowledge the support of the study by the Department of Biology of the University of Central Arkansas. W.R. Miller was supported by the Department of Biology of Baker University and NSF Grant DEB 0640847. Literature Cited Beasley, C.W. 1978. The tardigrades of Oklahoma. American Midland Naturalist 99(1):128–141. Beasley, C.W., and G. Pilato. 1987. Two new species of Doryphoribius (Eutardigrada, Hypsibiidae) from North America. Animalia 14(1/3):99–105. Degma, P., R. Bertolani, and R. Guidetti. 2011a. Actual checklist of Tardigrada species (2009–2011, Ver. 18: 27-04-2011). Available online at http://www.tardigrada.modena. checklist of Tardigrada.pdf. Accessed on 30 April 2011. Degma, P., S. Katina, and L. Sabatovicova. 2011b. 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