Hidden diversity within the Nemastoma bidentatum Roewer, 1914 complex (Opiliones: Nemastomatidae) Part I: Morphological evidence
Abstract
Nemastoma bidentatum Roewer, 1914 is a complex of closely related litter-dwelling harvestmen, characterized by a penis glans with two pairs of lateral lancet-like spines, and a femur IV with a saw-like series of pointed tubercles. Here we a) revise the hitherto known taxa within the N. bidentatum complex, and b) analyze in detail the relations among the taxa in Slovenia. The study revealed that the N. bidentatum complex consists of four species: N. bidentatum Roewer, 1914 s. str., N. relictum Gruber & Martens, 1968 stat. nov., N. pluridentatum (Hadži, 1973) stat. nov. and N. kozari Novak, Kozel, Podlesnik & Raspotnig sp. nov. Moreover, N. bidentatum s. str. consists of six subspecies: N. bidentatum bidentatum Roewer, 1914, N. bidentatum sparsum Gruber & Martens, 1968, N. bidentatum gruberi Novak, Slana Novak, Kozel & Raspotnig ssp. nov., N. bidentatum martensi Novak, Slana Novak & Raspotnig ssp. nov., N. bidentatum schmidti Novak, Raspotnig & Slana Novak ssp. nov. and N. bidentatum sneznikensis Novak, Komposch, Slana Novak & Raspotnig ssp. nov. In Slovenia, the six subspecies of N. bidentatum form a parapatric complex around N. bidentatum schmidti. Hybrids occur in the contact zones between adjacent subspecies, but they are missing between distant subspecies. The taxonomic distinction of lineages / subspecies is congruent with their distribution patterns. With six of the nine taxa present, Slovenia is considered the center of the N. bidentatum complex speciation. At the time being, this complex is the most diversified harvestman group on a subspecific and young-species level and provides important details on speciation processes in Opiliones.
References
Babalean A.F. 2005. General overview of the opilionid fauna (Arachnida, Opiliones) in Romania. Scientific Annals of „Alexandru Ioan Cuza” University of Iasi. (New Series), Section 1. Animal Biology 51: 47−54.
Blick T. & Komposch C. 2004. Checkliste der Weberknechte Mittel- und Nordeuropas. Checklist of the harvestmen of Central and Northern Europe (Arachnida: Opiliones). Version 27. December 2004. Available from https://arages.de/fileadmin/Pdf/checklist2004_opiliones.pdf [accessed 25 Feb. 2021].
Braby M.F., Eastwood R. & Murray R. 2012. The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society 106: 699–716. https://doi.org/10.1111/j.1095-8312.2012.01909.x
Coleman D.C., Callaham Jr. M.A. & Crossley Jr. D.A. 2018. Fundamentals of Soil Ecology. 3rd Ed. Elsevier Academic Press.
Ćurčić B.P.M., Karaman I.M. & Tomić V.T. 1999. On some new and little known epigean harvestmen (Opiliones, Arachnida) from west Serbia, Yugoslavia. Arches of Biological Sciences, Belgrade 51 (4): 61–62.
De Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886. https://doi.org/10.1080/10635150701701083
Fernández R., Sharma P.P., Tourinho A.L. & Giribet G. 2017. The Opiliones tree of life: shedding light on harvestmen relationships through transcriptomics. Proceedings of the Royal Society B 284: e20162340. https://doi.org/10.1098/rspb.2016.2340
Giribet G. & Sharma P.P. 2015. Evolutionary biology of harvestmen (Arachnida, Opiliones). Annual Review in Entomology 60: 157–175. https://doi.org/10.1146/annurev-ento-010814-021028
Gruber J. 1976. Ergebnisse zoologischer Sammelreisen in der Türkei: Zwei neue Nemastomatidenarten mit Stridulationsorganen, nebst Anmerkungen zur systematischen Gliederung der Familie (Opiliones, Arachnida). Annalen des Naturhistorischen Museums in Wien 80: 781–801.
Gruber J. 2007. Dyspnoi – Historical systematic synopsis and family chapters. In: Pinto-da-Rocha R., Machado G. & Giribet G. (eds) Harvestmen: the Biology of Opiliones: 131−159. Harvard University Press, Cambridge MA.
Gruber J. & Martens J. 1968. Morphologie, Systematik und Ökologie der Gattung Nemastoma C.L. Koch (s. str.) (Opiliones, Nemastomatidae). Senckenbergiana Biologica 49 (2): 137−172.
Hadži J. 1927. Opilioni Schmidtove zbirke. Glasnik Muzejskega Društva za Slovenijo 7–8: 1−41 + VIII.
Hadži J. 1928. Beitrag zur Kenntnis der Opilioniden-Fauna von Slowenien (Jugoslawien). Zoologischer Anzeiger 77 (1−2): 5−19.
Hadži J. 1931. Opilioni Triglavskoga masiva. Prirodoslovne razprave 1: 107−154.
Hadži J. 1973a. Novi taksoni suhih južin (Opilionidea) v Jugoslaviji. Razprave SAZU, IV. razred 16 (1): 1−120.
Hadži J. 1973b. Opilionidea. In: Hadži J., Lorković Z., Horvatić S., Bole J. & Martinčič A. (Consilium JAZU, eds) Catalogus Faunae Jugoslaviae III/4: 1–24. SAZU, Ljubljana.
Haig M., Beever E.A., Chambers S.M., Draheuim H.M., Dugger B.D., Dunham S., Elliot-Smith E., Fontaine J.B., Kesler D.C., Knaus B.J., Lopes I.F., Loschl P., Mullins T.D. & Sheffield L.M. 2006. Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conservation Biology 20 (6): 1584–1594. https://doi.org/10.1111/j.1523-1739.2006.00530.x
Halse S. 2018. Research in calcretes and other deep subterranean habitats outside caves. In: Moldovan O.T., Kováč L. & Halse S. (eds) Cave Ecology: 415–434. Springer, Cham. https://doi.org/10.1007/978-3-319-98852-8
ICZN, International Commission on Zoological Nomenclature 1999. International Code of Zoological Nomenclature (fourth edition).The International Trust for Zoological Nomenclature, c/o The Natural History Museum, London.
Irwin D.E. 2012. A novel approach for finding ring species: look for barriers rather than rings. BMC Biology 10: 21. https://doi.org/10.1186/1741-7007-10-21
Isaac N.J.B., Mallet J. & Mace G.M. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology and Evolution 19: 464–469. https://doi.org/10.1016/j.tree.2004.06.004
Klimeš L. 2000. Checklist of harvestmen (Opiliones) of Czechia and Slovakia. Ekológia Bratislava 19, Suppl. 3: 125–128.
Koch C.L. 1836. Die Arachniden getreu nach der Natur abgebildet und beschrieben. Vol. 3. C.H. Zeh’sche Buchhandlung, Nürnberg.
Komposch C. 1999. Rote Liste der Weberknechte Kärntens (Arachnida: Opiliones). In: Rottenburg T., Wieser Ch., Mildner P. & Holzinger W.E. (eds): Rote Listen gefährdeter Tiere Kärntens. Naturschutz in Kärnten 15: 547–565. Amt der Kärntner Landesregierung, Abt. 20, Landesplanung, Klagenfurt.
Komposch C. 2002. The harvestmen fauna of Hungary (Arachnida, Opiliones). In: Samu F. & Szinetár Cs. (eds) Proceedings of the 20th European Colloquium of Arachnology: 227–242. Szombathely.
Komposch C. 2009. Opiliones (Weberknechte). In: Rabitsch W. & Essl F. (eds) Endemiten – Kostbarkeiten in Österreichs Pflanzen- und Tierwelt: 476−500. Naturwissenschaftlicher Verein für Kärnten & Umweltbundesamt.
Komposch C. 2011. Endemic harvestmen and spiders of Austria (Arachnida: Opiliones, Araneae). Arachnologische Mitteilungen 40: 65–79. https://doi.org/10.5431/aramit4008
Komposch C. & Gruber J. 2004. Die Weberknechte Österreichs (Arachnida, Opiliones). Denisia 12, zugleich Kataloge der Österreichishen Landesmuseen Neue Serie 14: 485–534.
Kovač I. 1997. Suhe južine (Opiliones) v različnih habitatih v Prekmurju. (Harvestmen (Opiliones) in various habitats in Prekmurje.) Diploma work, Department of Biology, Faculty of Education, University of Maribor.
Kurt K. 2014. Updated checklist of harvestmen (Arachnida, Opiliones) in Turkey. Archives of Biological Sciences 66 (4): 1617−1631. https://doi.org/10.2298/ABS1404617K
Loksa I. 1962. Beiträge zur Kenntnis der Weberknecht-Fauna Ungarns, I. Zoologischer Anzeiger 168: 256–269.
Mallet J. 2013. Subspecies, semispecies, superspecies. In: Levin A.S. (ed.) Encyclopedia of Biodiversity 7: 46−48. Elsevier, Academic Press, San Diego. http://doi.org/10.1016/B978-0-12-384719-5.00138-6
Mammola S., Giachino P.M., Piano E., Jones A., Barberis M., Badino G. & Isaia M. 2016. Ecology and sampling techniques of an understudied subterranean habitat: the Milieu Souterrain Superficiel (MSS). The Science of Nature 103: e88. https://doi.org/10.1007/s00114-016-1413-9
Marcellino I. 1973. Notizie su Opilioni (Arachnida) italiani e dell´Alto Isonzo. Annali del Museo Civico di Storia Naturale di Genova 79: 192–205.
Martens J. 1978. Spinnentiere, Arachnida: Weberknechte, Opiliones. In: Senglaub F., Hannemann H. & Schumann H. (eds) Die Tierwelt Deutschlands 64: 1–464. Fischer Verlag, Jena.
Martens J. 2006. Weberknechte aus dem Kaukasus (Arachnida, Opiliones, Nemastomatidae). Senckenbergiana Biologica 86 (2): 145–210.
Miralles A., Vasconcelos R., Perela A., Harris D.J. & Carranza S. 2010. An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). Zoologica Scripta 10: 1–29. https://doi.org/10.1111/j.1463-6409.2010.00453.x
Monahan W.B., Pereira R.J. & Wake D.B. 2012. Ring distributions leading to species formation: a global topographic analysis of geographic barriers associated with ring species. BMC Biology 10: e20. https://doi.org/10.1186/1741-7007-10-20
Mučalica M. 1988. A contribution to the study of harvestmen (Opiliones, Arachnida) on the mountains Avala and Fruska gora (Serbia, Yugoslavia). Glasnik Prirodnjačkog muzeja srpske zemlje. Serija B, Biološke nauke 43/44: 193−198.
Murphree C.S. 1988. Morphology of the dorsal integument of ten opilionid species. Journal of Arachnology 16 (2): 237–252.
Novak T. 2004a. Harvestmen of the Museo Friulano di Storia Naturale in Udine (Arachnida: Opiliones). Part 1. Gortania 26: 211−241.
Novak T. 2004b. An overview of harvestmen (Arachnida: Opiliones) in Croatia. Natura Croatica 13: 231−296.
Novak T. 2005a. An overview of harvestmen (Arachnida: Opiliones) in Bosnia and Herzegovina. Natura Croatica 14: 301−350.
Novak T. 2005b. The harvestmen fauna (Arachnida: Opiliones) from the Sub Mediterranean region of Slovenia − II. Annales, Series historiae naturalis 15: 103−114.
Novak T. 2005c. Terrestrial fauna from cavities in Northern and Central Slovenia, and a review of systematically ecologically investigated cavities. Acta Carsologica 34: 169−210. https://doi.org/10.3986/ac.v34i1.285
Novak T. & Gruber J. 2000. Remarks on published data on harvestmen (Arachnida: Opiliones) from Slovenia. Annales, Series historiae naturalis 10: 281−308.
Novak T., Gruber J. & Slana L. 1984. Remarks on Opiliones from cavities in Slovenia (Yugoslavia). Mémoires de Biospéologie 11: 185–197.
Novak T., Gruber J. & Slana L. 1995. A contribution to the knowledge of the harvestmen (Opiliones) from the submediterranean region of Slovenia. Annales, Series historiae naturalis 5: 181−192.
Novak T., Gruber J. & Slana L. 1996. Weberknechte (Opiliones) des Zentral-Europäischen zoogeographischen Gebietes Sloweniens. Znanstvena revija, Maribor 7: 47−60.
Novak T., Slana L., Červek N., Mlakar M., Žmaher N. & Gruber J. 2002. Harvestmen (Opiliones) in human settlements of Slovenia. Acta Entomologica Slovenica 10: 131−154.
Novak T., Lipovšek Delakorda S. & Slana L. 2006. A review of harvestmen (Arachnida: Opiliones) in Slovenia. Zootaxa 1325 (1): 267−276. https://doi.org/10.11646/zootaxa.1325.1.17
Novak T., Janžekovič F., Rak M., Ivajnšič D., Kozel P., Slana Novak L. & Škornik S. 2017. Can highland habitat type distributions replace mapping of harvestman species? Journal of Insect Conservation 21 (2): 331−343. https://doi.org/10.1007/s10841-017-9979-x
Oatley G., Bowie R.C.K. & Crowe T.M. 2011. The use of subspecies in the systematics of southern African white-eyes: historical entities or eco-geographic variants. Journal of Zoology 284: 21–30. https://doi.org/10.1111/j.1469-7998.2010.00772.x
Patten M.A. & Unitt P. 2002. Diagnosability versus mean differences of sage sparrow subspecies. The Auk 119 (1): 26–35. https://doi.org/10.1093/auk/119.1.26
Raspotnig G., Leutgeb V., Schaider M. & Komposch C. 2010. Naphthoquinones and anthraquinones from scent glands of a dyspnoid harvestman, Paranemastoma quadripunctatum. Journal of Chemical Ecology 36: 158–162. https://doi.org/10.1007/s10886-010-9745-y
Raspotnig G., Bodner M., Schäffer S., Koblmüller S., Schönhofer A. & Karaman I. 2014. Chemosystematics in the Opiliones (Arachnida): a comment on the evolutionary history of alkylphenols and benzoquinones in the scent gland secretions of Laniatores. Cladistics 30: 1–8. https://doi.org/10.1111/cla.12079
Raspotnig G., Schaider M., Föttinger P. & Schönhofer A. 2017. A model for phylogenetic chemosystematics: Evolutionary history of quinones in the scent gland secretions of harvestmen. Frontiers in Ecology and Evolution 5: 139. https://doi.org/10.3389/fevo.2017.00139
Roewer C.F. 1914. Die Familien der Ischyropsalidae und Nemastomatidae der Opiliones−Palpatores. Archives für Naturgeschichte 80 A (3): 99−169.
Roewer C.F. 1917. Über Nemastomatiden und ihre Verbreitung. Archives für Naturgeschichte 83 A (2): 140–160.
Roewer C.F. 1923. Die Weberknechte der Erde. Gustav Fischer, Jena.
Roewer C.F. 1951. Über Nemastomatiden. Weitere Weberknechte XVI. Senckenbergiana 32: 95–153.
Sangster G. 2009. Number of bird species result from taxonomic progress, not taxonomic inflation. Proceedings of the Royal Society B 276 (1670): 3185–3191. https://doi.org/10.1098/rspb.2009.0582
Schaider M., Novak T., Komposch C., Leis H.-J. & Raspotnig G. 2018. Methyl-ketones in the scent glands of Opiliones: a chemical trait of cyphophthalmi retrieved in the dyspnoan Nemastoma triste. Chemoecology 28: 61–67. https://doi.org/10.1007/s00049-018-0257-5
Schönhofer A.L. 2013. A taxonomic catalogue of the Dyspnoi Hansen and Sørensen, 1904 (Arachnida: Opiliones). Zootaxa 3679 (1): 1–68. https://doi.org/10.11646/zootaxa.3679.1.1
Schönhofer A.L. & Holle T. 2007. Nemastoma bidentatum (Arachnida: Opiliones: Nemastomatidae): neu für Deutschland und die Tschechische Republik. Arachnologische Mitteilungen 33: 25–30. https://doi.org/10.5431/aramit3306
Schulz J.W. & Pinto-da-Rocha R. 2007. Morphology and functional anatomy. In: Pinto-da-Rocha R., Machado G. & Giribet G. (eds) Harvestmen: the Biology of Opiliones: 14–61. Harvard University Press, Cambridge MA.
Staręga W. 1976. Weberknechte (Opiliones, excl. Sironidae) Bulgariens. Annales Zoologici 33(18): 287−433.
Šilhavý V. 1956. Sekáči – Opilionidea. In: Fauna ČSR 7. Nakladatelství Československé akademie věd, Praha.
Torstrom S.M., Pangle K.L. & Swanson B.J. 2014. Shedding subspecies: The influence of genetics on reptile subspecies taxonomy. Molecular Phylogenetics and Evolution 76: 134–143. https://doi.org/10.1016/j.ympev.2014.03.011
Willemart R.H., Farine J.-P. & Gnaspini P. 2009. Sensory biology of Phalangida harvestmen (Arachnida, Opiliones): a review, with new morphological data on 18 species. Acta Zoologica 90: 209–227. https://doi.org/10.1111/j.1463-6395.2008.00341.x
Wolff J.O., García-Hernández S. & Gorb S.N. 2016. Adhesive secretions in harvestmen (Arachnida: Opiliones). In: Smith A.M. (ed.) Biological Adhesives: 281–301. Springer. https://doi.org/10.1007/978-3-319-46082-6
Zink R.M. 2004. The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society London B 271: 561–564. https://doi.org/10.1098/rspb.2003.2617
Copyright (c) 2021 Tone Novak, Ljuba Slana Novak, Peter Kozel, Miriam Gudrun Schaider, Christian Komposch, Saška Lipovšek, Jan Podlesnik, Igor Paušič, Günther Raspotnig
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.
