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Biodiversity Explosion: Collembola (Springtails) of Great Smoky Mountains National Park
Ernest C. Bernard and Kelly L. Felderhoff

Southeastern Naturalist, Volume 6, Special Issue 1 (2007): 175–182

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1Entomology and Plant Pathology Department, The University of Tennessee, 2431 Joe Johnson Drive, 205 Plant Sciences, Knoxville, TN 37996-4560. *Corresponding author - Biodiversity Explosion: Collembola (Springtails) of Great Smoky Mountains National Park Ernest C. Bernard1,* and Kelly L. Felderhoff 1 Abstract - Collembola are the most abundant hexapods, sometimes numbering 50,000 individuals/m2 in temperate deciduous forest. Prior to the All Taxa Biodiversity Inventory, 55 species had been reported from Great Smoky Mountains National Park (GSMNP), some of which were misidentifications. Currently, more than 200 species are recognized in GSMNP, including at least 60 species new to science and more than 100 new records. In addition, reexamination of type specimens in collections dating to the 1940s has validated a number of species that had been synonymized with other taxa, such as in the genus Morulina. One new genus has been collected, and three new species belonging to previously non-North American genera have been found (two South American, one Mediterranean). Several new records are major range extensions, such as Folsomia fimetaria, known previously from the Canadian Maritime provinces, and Hypogastrura tooliki, described from Alaska. Digital imaging and videography of live springtails is being used to more accurately render appearance and coloration and to document behaviors and interactions with other soil and litter biota. Molecular differentiation of Tomoceridae is underway in order to more reliably separate the many similar species of this common family. A Lucid-based online key for identification of southern Appalachian Collembola is under construction; where possible, this key will use characters visible with a dissecting microscope to distinguish species. Introduction Collembola (common name springtails) are the most abundant hexapods in most habitats, and among Arthropoda are second only to Acari (mites) in terms of densities in soil and plant litter. They derive their common name from a forked ventral appendage on the venter of the fourth abdominal segment, used like a lever to suddenly leap away from perceived danger. Springtails are found everywhere on every continent, and in temperate meadows and forests can reach densities of up to 50,000 individuals/m2 (Hopkin 1997). In winter and early spring, certain species (so-called snowfl eas) often are seen on patches of snow in huge aggregates of more than 100,000 individuals attracted to each other by pheromones (Verhoef et al. 1977). Springtails play essential roles in the detrital food web by consuming both primary materials and decay organisms. Larger species (>3 mm), such as species in the family Tomoceridae, directly comminute dead leaves and redeposit them in their frass. Most smaller species (<2 mm) are fungal, algal, or diatom The Great Smoky Mountains National Park All Taxa Biodiversity Inventory: A Search for Species in Our Own Backyard 2007 Southeastern Naturalist Special Issue 1:175–182 176 Southeastern Naturalist Special Issue 1 feeders, and there is evidence that many species have some selectivity in their diet (Bernard 2006b, Christiansen 1964, Poole 1959, Singh 1969, Thimm and Larink 1995). Nematodes may be important food sources for some species (Huhta et al. 1998), and opportunistic scavenging of dead invertebrates probably is common. Most species of Neanuridae and Odontellidae have stylet- like mouthparts that strongly suggest a liquid diet; one neanurid subfamily apparently specializes on slime molds (Greenslade et al. 2002). Some species appear to feed preferentially on soil nematodes (Lee and Widden 1996). A few species, such as Metisotoma grandiceps (Reuter), are specialized for predation on other small soil arthropods, and several species, most notably Sminthurus viridis L., are significant crop pests. Many surface-dwelling springtails may climb vegetation, where they consume fungal spores and pollen. Springtails also are among the most abundant canopy-dwelling hexapods and may be caught in large numbers in Malaise traps. Springtails form a significant proportion of the diets of ground-dwelling spiders, ground beetles (Carabidae), rove beetles (Staphylinidae), mesostigmatid mites, and other predacious arthropods. In the neotropics, certain small sphecid wasps even provision their nests with paralyzed springtails. Fountain and Hopkin (2005) have published an excellent review of all aspects of the widespread species Folsomia candida Willem. The taxonomic placement of Collembola has been controversial for many decades. Most entomologists consider them to be a separate class distantly allied to Protura, but this concept has been challenged in recent years with molecular data that seem to indicate that Crustacea and Collembola are sister groups. If we take the view that Collembola are Insecta sensu lato (and therefore an order, rather than a class) then the order Collembola is among the largest of the “minor” orders of insects. As of 1997, 6474 valid species had been described worldwide (Hopkin 1997). This number continues to rise steadily as numerous species new to science are described each year. The All Taxa Biodiversity Inventory (ATBI) in Great Smoky Mountains National Park (GSMNP) has as its goal the identification of all species of organisms living in GSMNP (Sharkey 2001). Previous to the ATBI, the only major survey of springtails in GSMNP was conducted by Wray et al. (1963), who identified 55 species from samples collected mostly along major Park roads. Many of the names used in that paper are no longer applicable to the North American fauna or are synonyms of other species. The Noland Creek drift sampling project conducted by C.R. Parker in the 1990s afforded a new look at GSMNP Collembola, with the results suggesting that the Park’s springtail fauna in reality was scarcely known. Since then, several intensive collecting efforts have been conducted to obtain a more complete understanding of GSMNP Collembola. The goals of this sampling and identification program are to characterize the springtail fauna of the Park, digitally image and video-record each species in life, describe species new to science, revise descriptions of known species, and present this sum of information in an electronic format for the world 2007 E.C. Bernard and K.L. Felderhoff 177 community. The goals of this paper are to summarize significant results to date, describe current springtail research in GSMNP, and indicate some possible research directions in the future. Materials and Methods For the past 14 years, springtails have been collected by various means throughout GSMNP, both in structured and unstructured sampling. The following trapping and collection methods have been used: drift-net collection, Tullgren funnels, pitfall traps, Lindgren funnels, and hand-collecting with an aspirator. Several areas of GSMNP have been sampled intensively yearround in several structured surveys, including: the Noland Creek headwaters drift collections; eleven biodiversity reference plots in the project “How to Conduct an All-taxa Biodiversity Inventory;” the Ravensford area survey (part of a land swap with the Eastern Band of Cherokee Indians); and the North Shore environmental impact survey (Table 1). In addition, many unstructured samples have been collected by GSMNP personnel, university and high school students, and other members of the public. Specimens typically have been preserved in 95% ethanol, but more recently have been preserved in absolute ethanol for possible DNA sequencing. Samples are sorted to morphospecies with the aid of a dissecting microscope. Digital images are made of each taxon before further processing, in order to have a visual record of color and pattern. Faithful images of species are needed as species in several large genera, such as Isotomurus Börner and Orchesella Templeton, are differentiated primarily by color and pattern. At least one specimen from each morphospecies of interest is cleared in Marc Andre I fl uid or 10% KOH (Christiansen and Bellinger 1980, 1998), then mounted in Hoyer’s medium (Bernard 2006a) for identification. Collection data are entered into the ATBI database and also maintained at the University of Tennessee. The David L. Wray collection of Collembola was borrowed from the North Carolina State University Entomology Museum and the North Carolina Department of Agriculture Insect Survey Collection. From the late 1930s until the 1970s, Wray collected extensively throughout the mountainous regions of the southern US and described numerous species. Most of his Table 1. Major Collembola collection efforts in Great Smoky Mountains National Park. Report or study CollectedA New records New species Wray et al. (1963) 55 35C 0 Ravensford (2000–2001) 123 25 15 USGS Pilot Project (2000–2003) 81 23 19 North Shore Survey (2004) 90 12 14 Noland Creek and miscellaneous (1993–present) -B 21 12 Totals 220 116 60 AAdds up to more than 220 due to many species being collected at more than one site. BNot calculated. COnly 35 of the 55 species listed in this survey are accepted in this paper as valid identifications. 178 Southeastern Naturalist Special Issue 1 species require redescription according to current understanding of important morphological features, and these redescriptions are being incorporated into papers describing related species. For digital video of live springtails, specimens are extracted into a moist culture chamber with an activated charcoal-plaster of Paris substrate, and recorded through a digital video camera mounted on a trinocular stereo microscope. In many cases, these springtails are maintained in culture chambers with a small amount of yeast added for food, in an effort to establish living laboratory cultures for observation of behavior and population dynamics. In the case of scaled species of springtails (Lepidocyrtus Bourlet, Pseudosinella Schäffer, Tomoceridae), specimens can be maintained and fed until they molt so that pristine scale patterns and iridescences can be recorded. The loosely attached scales are usually partially abraded in field-caught specimens and readily detach in preservative. Recently, we have begun analyzing DNA sequences of southern Appalachian Collembola, under the guidance of J.K. Moulton, University of Tennessee. Molecular phylogenies currently are being used to help untangle species complexes in Tomoceridae, which contains a large number of synonyms and doubtful species (Table 2), and are being correlated with scale patterns, ground body color, and morphological features. Results To date, approximately 220 species of springtails have been identified from GSMNP (see for the species list, as well as images and phenologies for many of the species). In comparison, 812 species were listed by Christiansen and Bellinger (1998) for North America north of Mexico. Of the 220 species, 116 are new GSMNP records of species known elsewhere, and 60 are species new to science (Table 1). One of the undescribed species is in a genus also new to science. In three major structured studies, between 81 and 123 species were collected, with at least 12 new species in each study. Three non-North American genera have been collected: Arlea Womersley and Furculanurida Massoud (South America, Africa), and Stenognathellus Stach (Europe). The specimens in these genera all appear to be undescribed. Twelve of 18 Collembola families have been collected in GSMNP. Regular collecting year-round at Noland Creek revealed a previously unknown springtail fauna at high elevations (>1700 m) that was active in the winter and early spring but nearly disappeared in the summer (Fig. 1). Similarly, the deployment of Lindgren funnels in tree canopies in eleven biodiversity plots yielded a highly specialized arboreal springtail fauna, dominated by Hypogastrura packardi (Folsom), an undescribed Hypogastrura sp., Entomobrya assuta Folsom, E. clitellaria Guthrie, E. ligata Folsom, Vertagopus beta Christiansen and Bellinger, and at least one undescribed Uzelia sp. Uzelia Absolon is a genus of arboreal springtails typically reported in cold temperate zones, but not before known further south than Pennsylvania (Christiansen and Bellinger 1980). 2007 E.C. Bernard and K.L. Felderhoff 179 Many of the new records for GSMNP are significant range extensions for the species. For instance, Hypogastrura tooliki Fjellberg was described from Alaska (Fjellberg 1985) and has been collected in Idaho (J. Neufeld, University of Idaho, Moscow, ID. pers. comm.), but many specimens seemingly identical to this species were collected in the Ravensford survey. Similarly, Folsomia fimetaria (L.) previously was known in North America only from Nova Scotia (Christiansen and Bellinger 1980, 1998), but specimens apparently identical to this species have been collected at several locations in GSMNP. Live cultures have proven to be valuable for detecting behavioral differences and recognizing differences in population dynamics. An undescribed species of Arrhopalites (Sminthuridae) collected along Balsam Mountain Road and maintained in culture for more than two years in our laboratory is very similar to A. benitus (Folsom) in color and morphology. However, its behavior differs dramatically. The undescribed species leaps readily when the culture dish is open and runs rapidly, whereas A. benitus is much slower and more reluctant to jump. Another species from GSMNP, Folsomia nivalis (Packard), in culture continues to increase as long as the culture is fed, to the point that individuals are piled three or four deep, while F. candida ceases reproduction at high densities and thereafter declines in number. Living members of Tomoceridae are covered with scales similar to those of Lepidoptera. The scales themselves have little color, but they refract light to give distinct patterns of color and iridescence. This family has numerous nomenclatorial problems and poorly defined species due to the uniformity of morphological features and the presumed variability of body ground Figure 1. Population dynamics of Agrenia sp. collected 1992–1993 during drift-net sampling at Noland Creek, Great Smoky Mountains National Park. 180 Southeastern Naturalist Special Issue 1 color. Because the scales of tomocerids are dislodged when they are placed in preservative, scale patterns rarely have been reported. By maintaining numerous wild-caught individuals until they molt to reveal a pristine scale pattern, we have discriminated at least six putative species, several of which are likely to be undescribed. Scale patterns and DNA sequences for these taxa so far have proven to be congruent, strongly suggesting that scale patterns can be used to reliably identify species. Discussion The maturation of new techniques and diagnostic tools, as well as reappraisal of older taxonomic characters, is resulting in a more coherent understanding of springtail diversity. Colors and patterns of many species are variable; this variability has resulted, rightly so, in the reluctance of collembologists to place much weight on pigmentation within genera. However, in some genera, color patterns may be as reliable as morphological structures for separating species. Wallace (1973) resolved problems with the biogeography of S. viridis by determining that this taxon was a three-species complex that could be separated by pattern. Another species, Isotomurus palustris (Müller), has been reported from most areas of the world, and has an extensive list of synonyms (Table 2). The reported variability of this species obscures the differentiation of other Isotomurus spp. and has retarded progress on the taxonomy of this genus. However, in an analysis of color patterns coupled with a molecular analysis, 14 southern European Isotomurus spp. were differentiated, suggesting that I. palustris populations reported around the world are likely to be separate species (Carapelli et al. 1995, 2001). Likewise, the study of Tomoceridae in North America has been slowed by the difficulty in separating species, especially Pogonognathellus fl avescens (Tullberg) (Table 2) and P. dubius (Christiansen). Maintenance of Tomoceridae in culture at the University of Tennessee is allowing us to develop a unique congruence of ephemeral morphological features, traditional morphology, and DNA sequencing. Our Table 2. Published subspecies, forms, synonyms, and mistaken identities for two widespread species of Collembola.A Isotomurus palustris (Müller) Pogonognathellus fl avescens (Tullberg) I. p. aquatilis (Müller) P. f. americanus (Schött) I. p. balteatus (Reuter) P. f. arcticus (Schött) I. p. bimaculatus (Ågren) P. f. separatus (Folsom) I. p. cincta (Krausbauer) Pogonognathus beckeri Börner I. p. fucicola (Reuter) Tomocerus alba (Packard) I. p. fusca (Nicolet) T. crassicauda (Denis) I. p. maculata (Schäffer) T. niger Axelson I. p. pallida (Schäffer) T. pallidus (Packard) I. p. prasina (Reuter) T. plumbeus L. I. p. rubromaculata (Parfitt) I. p. texensis Folsom I. p. trifasciata (Bourlet) I. p. unifasciata (Börner) ACompiled from Christiansen and Bellinger (1998), Salmon (1964), and Stach (1947). 2007 E.C. Bernard and K.L. Felderhoff 181 studies suggest that the southern Appalachian region harbors a large number of morphologically similar species that can be differentiated by scale pattern, body ground color, and DNA analysis. Finally, the enormous range disjunctions observed for some species, e.g., H. tooliki, raise questions regarding their conspecificity that can only be answered with further study. Reliable separation of species allows for deeper exploration of the life histories of these species. For instance, three species of Morulina Börner occur sympatrically in GSMNP. This neanurid genus consists of large (2–5 mm), bulky, dark blue litter-dwelling springtails with non-chewing mouthparts. These species can be separated easily by the shape of the buccal cone and mandible, among other characters (Bernard 2006b), but also can be separated by intestinal contents. Two species with more substantial mandibles can ingest fungal hyphae; one species ingests larger hyphal pieces, the other consumes thinner hyphae. The third species, with small, slender mandibles, apparently does not ingest solid food items. The maturation of digital imaging technology allows for the full development of online identification materials. In the near future, it will be possible to identify many southern Appalachian springtail species by accessing an interactive Lucid key on the internet and using no more than a stereo microscope to note the relevant identifying features. Such a program could be expanded without great difficulty to cover the Collembola of North America as an accessible on-line resource, a goal first achieved in black-and-white print form by Christiansen and Bellinger (1980, 1998). Acknowledgements We thank the personnel of Great Smoky Mountains National Park, US Geological Survey, and Discover Life in America for their interest and indispensable assistance in collecting the springtail fauna of GSMNP, especially Charles R. Parker, Keith Langdon, Rebecca Nichols, and Jeanie Hilten. Ian and Stephanie Stocks were of immense assistance while employed at the University of Tennessee. We thank Pennie J. Long, Adriean Mayor, and Tracy Goodrich for collecting assistance during the various structured surveys. Collembola research in GSMNP has been generously supported by the Cherokee Central School District, US Geological Survey, Discover Life in America, US National Park Service, and the Tennessee Agricultural Experiment Station. Literature Cited Bernard, E.C. 2006a. Redescription of Cosberella conatoa Wray (Collembola: Hypogastruridae) and description of C. lamaralexanderi n. sp. Proceedings of the Biological Society of Washington 119:269–278. Bernard, E.C. 2006b. 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