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Type: Article
Published: 2016-10-31
Page range: 495–529
Abstract views: 328
PDF downloaded: 248

Asian pheretimoid earthworms in North America north of Mexico: An illustrated key to the genera Amynthas, Metaphire, Pithemera, and Polypheretima (Clitellata: Megascolecidae)

Department of Earth and Planetary Sciences, Johns Hopkins University, 3400 N Charles St, Baltimore, MD 21218, USA
Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, KS 66502, USA Department of Biological and Environmental Sciences, Georgia College & State University, Campus Box 081, Milledgeville, GA 31061
Department of Earth and Planetary Sciences, Johns Hopkins University, 3400 N Charles St, Baltimore, MD 21218, USA
Annelida Pheretima complex invasive species Amynthas hilgendorfi Metaphire hilgendorfi Amynthas agrestis Amynthas tokioensis Oligochaeta

Abstract

The invasion of the pheretimoid earthworms in North America, especially the genera Amynthas and Metaphire, has raised increasing concerns among ecologists and land managers, in turn increasing the need for proper identification. However, the commonly used keys to this group are more than 30 years old with outdated taxonomic information and are based primarily on internal morphology. The requirement of significant amount of taxonomic expertise and dissection, even from the first entry of the key, has prevented broader use of these keys. As a result, many publications in the United States have used Amynthas spp. to represent the group without identifying the species. We present here a new key and diagnoses for the 16 pheretimoid earthworm species recorded in North America north of Mexico, including four genera: Amynthas (10), Metaphire (4), Pithemera (1), and Polypheretima (1). The descriptions were based on published records with modifications following inspection of specimens archived at the National Museum of Natural History, Smithsonian Institution, Washington, D.C. Photos of external and internal characters, including male pores, spermathecal pores, genital markings, spermathecae, prostate glands, and intestinal caeca, are presented to help identification. A summary of current knowledge about the ecology and historical context is provided for each species. We also highlight the previously overlooked and potentially common and widespread co-occurrence of three species—A. agrestis, A. tokioensis, and M. hilgendorfi—and point out that many recent claims of invasion of A. agrestis need to be re-evaluated for potential misidentification.

 

References

  1. Beddard, F.E. (1892a) On some species of the genus Perichaeta (sensu stricto). Proceedings of the Zoological Society of London, 1892, 153−172.

    Beddard, F.E. (1892b) On some Perichaetidae from Japan. Zoologische Jahrbücher. Abtheilung für Systematik, Geographie und Biologie der Thiere, 6, 755−766.

    Belliturk, K., Görres, J.H., Kunkle, J. & Melnichuk, R.D.S. (2015) Can commercial mulches be reservoirs of invasive earthworms? Promotion of ligninolytic enzyme activity and survival of Amynthas agrestis (Goto and Hatai, 1899). Applied Soil Ecology, 87, 27−31.
    http://dx.doi.org/10.1016/j.apsoil.2014.11.007

    Blakemore, R.J. (2003) Japanese earthworms (Annelida: Oligochaeta): a review and checklist of species. Organisms Diversity & Evolution, Electronic Supplement, 11, 1−43.
    http://dx.doi.org/10.1078/1439-6092-00082

    Blakemore, R.J. (2006) A series of searchable texts on earthworm biodiversity, ecology and systematics from various regions of the world. 2nd Edition. COE Soil Ecology Research Group, Yokohama National University, Yokohama. [CD-ROM]

    Blakemore, R.J. (2010a) Cosmopolitan earthworms – an eco-taxonomic guide to the peregrine species of the world. 4th Edition. VermEcology, Yokohama, 850 pp.

    Blakemore, R.J. (2010b) A new earthworm genus (Oligochaeta, Megadrili, Megascolecidae) from Japan. Bulletin of the National Museum of Nature and Science Series A-Zoology, 36, 95−100.

    Blakemore, R.J. (2012a) Amynthas carnosus (Goto & Hatai, 1899) redescribed on its neotype (Oligochaeta: Megadrilacea: Megascolecidae). Journal of Species Research, 1, 35−43.
    http://dx.doi.org/10.12651/JSR.2012.1.1.035

    Blakemore, R.J. (2012b) On opening a box of worms (Oligochaeta, Megascolecidae) – historical earthworm specimens transferred to Tokyo from the Saito Ho-on Kai Museum of Natural History in Sendai. Bulletin of the National Museum of Natural Science Series A, 38, 95−124.

    Blakemore, R.J. (2013a) Jeju-do earthworms (Oligochaeta: Megadrilacea)-Quelpart Island revisited. Journal of Species Research, 2, 15−54.
    http://dx.doi.org/10.12651/JSR.2013.2.1.015

    Blakemore, R.J. (2013b) Ulleung-do earthworms—Dagelet Island revisited. Journal of Species Research, 2, 55−68.
    http://dx.doi.org/10.12651/JSR.2013.2.1.055

    Blakemore, R.J. (2013c) Megascolex (Perichaeta) diffringens Baird, 1869 and Pheretima pingi Stephenson, 1925 types compared to the Amynthas corticis (Kinberg, 1867) and A. carnosus (Goto & Hatai, 1899) species-groups (Oligochaeta: Megadrilacea: Megascolecidae). Journal of Species Research, 2, 99−126.
    http://dx.doi.org/10.12651/JSR.2013.2.2.099

    Blakemore, R.J. (2014) Miscellaneous earthworm types in the Natural History Museum, London (Annelida: Oligochaeta: Megadrilacea: Eudrilidae, Lumbricidae, Megascolecidae, Moniligastridae, Octochaetidae). Opuscula Zoologica (Budapest), 45, 119−155.

    Burtelow, A.E., Bohlen, P.J. & Groffman, P.M. (1998) Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. Applied Soil Ecology, 9, 197−202.
    http://dx.doi.org/10.1016/s0929-1393(98)00075-4

    Callaham, M.A., Hendrix, P.F. & Phillips, R.J. (2003) Occurrence of an exotic earthworm (Amynthas agrestis) in undisturbed soils of the southern Appalachian Mountains, USA. Pedobiologia, 47, 466−470.
    http://dx.doi.org/10.1078/0031-4056-00214

    Carrera-Martínez, R. & Snyder, B.A. (2016) First report of Amynthas carnosus (Oligochaeta, Megascolecidae) in the Western Hemisphere. Zootaxa, 4111 (3), 297−300.
    http://dx.doi.org/10.11646/zootaxa.4111.3.7

    Chang, C.-H. & Chen, J.-H. (2004) A new species of earthworm belonging to the genus Metaphire Sims and Easton 1972 (Oligochaeta: Megascolecidae) from southern Taiwan. Taiwania, 49, 219−224.

    Chang, C. H. & Chen, J. H. (2005) Three new species of octothecate pheretimoid earthworms from Taiwan, with discussion on the biogeography of related species. Journal of Natural History, 39, 1469−1482.
    http://dx.doi.org/10.1080/00222930400004586

    Chang, C.-H., Lin, S.-M. & Chen, J.-H. (2008) Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata, Megascolecidae). Molecular Phylogenetics and Evolution, 49, 958−968.
    http://dx.doi.org/10.1016/j.ympev.2008.08.025

    Chang, C.-H., Shen, H.-P. & Chen, J.-H. (2009a) Earthworm fauna of Taiwan. National Taiwan University Press, Taipei, 174 pp.

    Chang, C.-H., Rougerie, R. & Chen, J.-H. (2009b) Identifying earthworms through DNA barcodes: Pitfalls and promise. Pedobiologia, 52, 171−180.
    http://dx.doi.org/10.1016/j.pedobi.2008.08.002

    Chang, C.-H., Chuang, S.-C., Wu, J.-H. & Chen, J.-H. (2014) New species of earthworms belonging to the Metaphire formosae species group (Clitellata: Megascolecidae) in Taiwan. Zootaxa, 3774 (4), 324−332.
    http://dx.doi.org/10.11646/zootaxa.3774.4.2

    Chang, C.-H., Szlavecz, K., Filley, T., Buyer, J.S., Bernard, M.J. & Pitz, S.L. (2016a) Belowground competition among invading detritivores. Ecology, 97 (1), 160–170.

    Chang, C.-H., Szlavecz, K. & Buyer, J. (2016b) Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon. Soil Biology and Biochemistry, 100, 129–139.
    http://dx.doi.org/10.1016/j.soilbio.2016.06.004

    Cotrufo, M.F., Soong, J.L., Horton, A.J., Campbell, E.E., Haddix, M.L., Wall, D.H. & Parton, W.J. (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nature Geoscience, 8, 776−779.
    http://dx.doi.org/10.1038/ngeo2520

    Easton, E.G. (1979) A revision of the 'acaecate' earthworms of the Pheretima group (Megascolecidae: Oligochaeta): Archipheretima, Metapheretima, Planapheretima, Pleionogaster and Polypheretima. Bulletin of the British Museum (Natural History) Zoology, 35, 1−126.
    http://dx.doi.org/10.5962/bhl.part.20451

    Easton, E.G. (1981) Japanese earthworms: a synopsis of the megadrile species. Bulletin of the British Museum (Natural History) Zoology, 40, 33−65.

    Gates, G.E. (1937) The genus Pheretima in North America. Bulletin of the Museum of Comparative Zoology, 80, 339−373.

    Gates, G.E. (1953) Further notes on the earthworms of the Arnold Arboretum, Boston. Breviora, 15, 1−9.

    Gates, G.E. (1954) Exotic earthworms of the United States. Bulletin of the Museum of Comparative Zoology at Harvard University, 111, 219−258.

    Gates, G.E. (1956) Reproductive organ polymorphism in earthworms of the oriental megascolecine genus Pheretima Kinberg, 1867. Evolution, 10, 213−227.
    http://dx.doi.org/10.2307/2405895

    Gates, G.E. (1958) On some species of the oriental earthworm genus Pheretima Kinberg, 1867, with a key to species reported from the Americas. American Museum Novitates, 1888, 1−33.

    Gates, G.E. (1963) Miscellanea Megadrilogica. VII. Greenhouse earthworms. Proceedings of the Biological Society of Washington, 76, 9−18.

    Gates, G.E. (1968) On a new anthropochorous species of earthworm genus Pheretima (Megascolecidae Oligochaeta). Journal of Natural History, 2, 253−261.
    http://dx.doi.org/10.1080/00222936800770911

    Gates, G.E. (1972) Burmese earthworms – Introduction to systematics and biology of megadrile oligochaetes with special reference to Southeast Asia. Transactions of the American Philosophical Society, 62, 5−324.
    http://dx.doi.org/10.2307/1006214

    Gates, G.E. (1982) Farewell to North American megadriles. Megadrilogica, 4, 12−77.

    Görres, J.H., Melnichuk, R.D.S. & Belliturk, K. (2014) Mortality pattern relative to size variation within Amynthas agrestis (Goto & Hatai 1899) (Oligochaeta: Megascolecidae) populations in the Champlain Valley of Vermont, USA. Megadrilogica, 16, 9−14.

    Goto, S. & Hatai, S. (1899) New or imperfectly known species of Earthworms, No. 2. Annotationes Zoologicae Japonenses, 3, 13−24.

    Greiner, H.G., Kashian, D.R. & Tiegs, S.D. (2012) Impacts of invasive Asian (Amynthas hilgendorfi) and European (Lumbricus rubellus) earthworms in a North American temperate deciduous forest. Biological Invasions, 14, 2017−2027.
    http://dx.doi.org/10.1007/s10530-012-0208-y

    Grube, E. (1879) Annelida. Philosophical Transactions of the Royal Society of London, 168, 554−556.
    http://dx.doi.org/10.1098/rstl.1879.0057

    Hong, Y. & James, S.W. (2011) New earthworm species of the genus Pheretima (Clitellata: Megascolecidae) from Mountain Province, Philippines. Journal of Natural History, 45, 1769−1788.
    http://dx.doi.org/10.1080/00222933.2011.560726

    Hong, Y. & James, S.W. (2013) Three new earthworm species of the genus Amynthas (Clitellata: Megascolecidae) from Mt. Chiak National Park, Korea. Zootaxa, 3646 (1), 75−81.
    http://dx.doi.org/10.11646/zootaxa.3646.1.6

    Horst, R. (1893) Earthworms from the Malay Archipelago. Zoologische Ergebnisse einer reise in Niederländisch Ost-Indien, 3, 28−77.

    Howell, C.D. (1939) The responses to light in the earthworm, Pheretima agrestis Goto and Hatai, with special reference to the function of the nervous system. Journal of Experimental Zoology, 81, 231−259.
    http://dx.doi.org/10.1002/jez.1400810205

    Ikeda, H., Callaham, M.A., Jr., O'Brien, J.J., Hornsby, B.S. & Wenk, E.S. (2015) Can the invasive earthworm, Amynthas agrestis, be controlled with prescribed fire? Soil Biology & Biochemistry, 82, 21−27.
    http://dx.doi.org/10.1016/j.soilbio.2014.12.011

    James, S.W. (2004) New genera and species of pheretimoid earthworms (Clitellata: Megascolecidae) from southern Luzon, Philippines. Systematics and Biodiversity, 2, 271−279.
    http://dx.doi.org/10.1017/S1477200004001446

    James, S.W. (2005) Preliminary molecular phylogeny in the Pheretima group of genera (Crassiclitellata: Megascolecidae) using Bayesian analysis. In: Pop, V.V. & Pop, A.A. (Eds.), Advances in Earthworm Taxonomy II (Annelida: Oligochaeta). Cluj University Press, Cluj-Napoca, pp. 129–142.

    James, S.W. (2009) Revision of the earthworm genus Archipheretima Michaelsen (Clitellata: Megascolecidae), with descriptions of new species from Luzon and Catanduanes Islands, Philippines. Organisms Diversity & Evolution, 9, 1–16. [244.e1–244.e16]
    http://dx.doi.org/10.1016/j.ode.2009.03.004

    Kinberg, J.G.H. (1867) Annulata nova. Öfversigt af Kongl Vetenskaps-Akademiens Förhandlingar Stockholm, 23, 97−103.

    Kobayashi, S. (1936) Distribution and some external characteristics of Pheretima (Ph.) carnosa (Goto et Hatai) from Korea. Science Report of the Tohoku Imperial University, 11 (1), 115−138.

    Michaelsen, W. (1892) Terricolen der Berliner Zoologischen Sammlung (II). Archiv für Naturgeschichte, Berlin, 58 (1), 209−261.
    http://dx.doi.org/10.5962/bhl.part.8321

    Michaelsen, W. (1895) Zur Kenntnis der Oligochaeten. Abhandlungen und Verhandlungen des Naturwissenschaftlichen Vereins, Hamburg, 13, 1−37.

    Perrier, E. (1872) Recherches pour servir à l'histoire des lombriciens terrestres. Archives du Museum National d'Histoire Naturelle (Paris), 8, 5−198.

    Perrier, E. (1875) Sur les Vers de terre des iles Philippines et de la Cochinchine. Comptes rendus hebdomadaires des séances de l'Académie des sciences, 81, 1043−1046.

    Redmond, C.T., Kesheimer, A. & Potter, D.A. (2014) Earthworm community composition, seasonal population structure, and casting activity on Kentucky golf courses. Applied Soil Ecology, 75, 116−123.
    http://dx.doi.org/10.1016/j.apsoil.2013.11.005

    Reynolds, J.W. (1978) The earthworms of Tennessee (Oligochaeta). IV. Megascolecidae, with notes on distribution, biology and a key to the species in the state. Megadrilogica, 3, 117−130.

    Reynolds, J.W. (2010) The earthworms (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae and Sparganophilidae) of Northeastern United States, revisited. Megadrilogica, 14, 101−157.

    Reynolds, J.W. (2011) The earthworms (Oligochaeta: Acanthodrilidae, Eudrilidae, Glossoscolecidae, Komarekionidae, Lumbricidae, Lutodrilidae, Megascolecidae, Ocnerodrilidae, Octochaetidae and Sparganophilidae) of Southeastern United States. Megadrilogica, 14, 175−320.

    Reynolds, J.W. (2014) A checklist by counties of earthworms (Oligochaeta: Lumbricidae, Megascolecidae and Sparganophilidae) in Ontario, Canada. Megadrilogica, 16, 111−135.

    Reynolds, J.W. & Wetzel, M.J. (2004) Terrestrial Oligochaeta (Annelida: Clitellata) in North America north of Mexico. Megadrilogica, 9, 71−98.

    Reynolds, J.W. & Wetzel, M.J. (2008) Terrestrial Oligochaeta (Annelida: Clitellata) in North America, including Mexico, Puerto Rico, Hawaii, and Bermuda. Megadrilogica, 12, 157−208.

    Richardson, D.R., Snyder, B.A. & Hendrix, P.F. (2009) Soil moisture and temperature tolerances and optima for a non-native earthworm species, Amynthas agrestis (Oligochaeta: Opisthopora: Megascolecidae). Southeastern Naturalist, 8, 325−334.
    http://dx.doi.org/10.1656/058.008.0211

    Rougerie, R., Decaens, T., Deharveng, L., Porco, D., James, S.W., Chang, C.-H., Richard, B., Potapov, M., Suhardjono, Y. & Hebert, P.D.N. (2009) DNA barcodes for soil animal taxonomy. Pesquisa Agropecuaria Brasileira, 44, 789−802.
    http://dx.doi.org/10.1590/s0100-204x2009000800002

    Shen, H.-P., Tsai, S.-C. & Tsai, C.-F. (2005) Occurrence of the earthworms Pontodrilus litoralis (Grube, 1855), Metaphire houlleti (Perrier, 1872), and Eiseniella tetraedra (Savigny, 1826) from Taiwan. Taiwania, 50, 11−21.

    Shen, H.-P., Chang, C.-H., Li, C.-L., Chih, W.-J. & Chen, J.-H. (2013) Four new earthworm species of the genus Amynthas (Oligochaeta: Megascolecidae) from Kinmen, Taiwan. Zootaxa, 3599 (5), 471−482.
    http://dx.doi.org/10.11646/zootaxa.3599.5.4

    Shen, H.-P., Chang, C.-H. & Chih, W.-J. (2014) Five new earthworm species of the genera Amynthas and Metaphire (Megascolecidae: Oligochaeta) from Matsu, Taiwan. Journal of Natural History, 48, 495−522.
    http://dx.doi.org/10.1080/00222933.2013.826742

    Sims, R.W. & Easton, E.G. (1972) A numerical revision of the earthworm genus Pheretima auct. (Megascolecidae: Oligochaeta) with the recognition of new genera and an appendix on the earthworms collected by the Royal Society North Borneo Expedition. Biological Journal of the Linnean Society, 4, 169−268.
    http://dx.doi.org/10.1111/j.1095-8312.1972.tb00694.x

    Snyder, B.A., Boots, B. & Hendrix, P.F. (2009) Competition between invasive earthworms (Amynthas corticis, Megascolecidae) and native North American millipedes (Pseudopolydesmus erasus, Polydesmidae): Effects on carbon cycling and soil structure. Soil Biology & Biochemistry, 41, 1442−1449.
    http://dx.doi.org/10.1016/j.soilbio.2009.03.023

    Snyder, B.A., Callaham, M.A. Jr. & Hendrix, P.F. (2011) Spatial variability of an invasive earthworm (Amynthas agrestis) population and potential impacts on soil characteristics and millipedes in the Great Smoky Mountains National Park, USA. Biological Invasions, 13, 349−358.
    http://dx.doi.org/10.1007/s10530-010-9826-4

    Snyder, B.A., Callaham, M.A. Jr., Lowe, C.N. & Hendrix, P.F. (2013) Earthworm invasion in North America: Food resource competition affects native millipede survival and invasive earthworm reproduction. Soil Biology & Biochemistry, 57, 212−216.
    http://dx.doi.org/10.1016/j.soilbio.2012.08.022

    Szlavecz, K., Chang, C.-H., Burgess, J.L. & Csuzdi, C. (2014) Earthworms (Annelida: Clitellata) of Plummers Island, Maryland, U.S.A., with description of a new species. Proceedings of the Biological Society of Washington, 126, 312−322.
    http://dx.doi.org/10.2988/0006-324X-126.4.312

    Tsai, C.-F. (1964) On some earthworms belonging to the genus Pheretina Kinberg collected from Taipei area in North Taiwan. Quarterly Journal of the Taiwan Museum, 17, 1−35.

    Tsai, C.-F., Shen, H.-P. & Tsai, S.-C. (2010) Four new species of Amynthas earthworms (Oligochaeta: Megascolecidae) from the Central Mountain Range of southern Taiwan. Journal of Natural History, 44, 1251−1267.
    http://dx.doi.org/10.1080/00222931003624788

    Tsai, C.-F., Shen, H.-P., Tsai, S.-C., Lin, K.-J., Hsieh, H.-L. & Yo, S.-P. (2009) A checklist of oligochaetes (Annelida) from Taiwan and its adjacent islands. Zootaxa, 2133, 33−48.

    Vaillant, L. (1868) Note sur l'anatomie de deux éspèces du genre Perichaeta, et essai de classification des Annélides lombriciens. Mémoires de la Section des Sciences Académie des Sciences et Lettres de Montpellier, 7, 143−173.

    Zhang, W., Hendrix, P.F., Snyder, B.A., Molina, M., Li, J., Rao, X., Siemann, E. & Fu, S. (2010) Dietary flexibility aids Asian earthworm invasion in North American forests. Ecology, 91, 2070−2079.
    http://dx.doi.org/10.1890/09-0979.1

    Zhang, W., Hendrix, P.F., Dame, L.E., Burke, R.A., Wu, J., Neher, D.A., Li, J., Shao, Y. & Fu, S. (2013) Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization. Nature Communications, 4, 2576.
    http://dx.doi.org/10.1038/ncomms3576