Organisms Diversity & Evolution

, Volume 10, Issue 2, pp 123–133 | Cite as

Interglacial refugia and range shifts of the alpine grasshopper Stenobothrus cotticus (Orthoptera: Acrididae: Gomphocerinae)

  • Dirk BergerEmail author
  • Dragan P. Chobanov
  • Frieder Mayer
Original Article


A warming climate leads to shifts in distribution ranges to higher latitudes and altitudes. Consequently, cold-adapted alpine species can be trapped in interglacial Holocene refugia on high mountain summits if they fail to expand their ranges to the north. One example is the alpine grasshopper Stenobothrus cotticus. This species was assumed to be endemic to the southwestern Alps (France, Italy). However, we have found a second refugium in the Rila Mountains in southwestern Bulgaria. Analyses of the mitochondrial gene co1 and of phenotypic characters from morphology and behaviour did not reveal differences between the two geographically separated populations of S. cotticus studied. We suppose that S. cotticus had a wider distribution during colder periods, when its range was expanded to lower altitudes. This hypothesis is supported by the current distribution of the closely related montane S. rubicundulus.


Distribution Glacial expansion Interglacial refugia Stenobothrus cotticus Stenobothrus rubicundulus 



We thank A. Popov (NMNH, Sofia), B. Michajlova (MMNH, Skopje), A. Pulev (BHM, Blagoevgrad), L. Stefanov (Skopje), and O. von Helversen (Erlangen) for providing access to official and personal collections. We are very grateful to F. Willemse (Eygelshoven) for supplying inaccessible literature, and to W. Schulze (Erlangen) for technical advice. Furthermore we are indebted to W. Schulze (Erlangen), B. Gottsberger (Vienna), J. Ustinova (Karlsruhe), Klaus-Gerhard Heller (Magdeburg), and F. Willemse (Eygelshoven) for comments and fruitful discussions on the manuscript. This study was supported by the Deutsche Forschungsgemeinschaft (DFG) and the Staedtler-Stiftung.

Supplementary material

13127_2010_4_MOESM1_ESM.pdf (196 kb)
ESM 1 (PDF 195 kb)


  1. Ander, K. (1949). Die boreo-alpinen Orthopteren Europas. Opuscula Entomologica, 14, 89–104.Google Scholar
  2. Baur, B., Baur, H., Roesti, C., & Roesti, D. (2006). Die Heuschrecken der Schweiz. Bern: Haupt.Google Scholar
  3. Bei-Bienko, G. Ya., & Mistshenko, L. L. (1951). Locusts and grasshoppers of the USSR and adjacent countries, I. Keys to the Fauna of the USSR, 38.Google Scholar
  4. Bellmann, H., & Luquet, G. C. (1995). Guide des sauterelles, grillons et criquets d’Europe occidentale. Lausanne: Delachaux et Niestle.Google Scholar
  5. Beniston, M., Diaz, H. F., & Bradley, R. S. (1997). Climatic change at high elevation sites: an overview. Climatic Change, 36, 233–251.CrossRefGoogle Scholar
  6. Berger, D. (2008). The evolution of complex courtship songs in the genus Stenobothrus Fischer, 1853 (Orthoptera, Caelifera, Gomphocerinae). Doct. dissertation, Erlangen-Nürnberg: Friedrich-Alexander-Universität.Google Scholar
  7. Bridle, J. R., & Butlin, R. K. (2002). Mating signal variation and bimodality in a mosaic hybrid zone between Chorthippus grasshopper species. Evolution, 56, 1184–1198.PubMedGoogle Scholar
  8. Bull, C. M. (1979). The function of complexity in the courtship of the grasshopper Myrmeleotettix maculatus. Behaviour, 69(3/4), 201–216.CrossRefGoogle Scholar
  9. Buresch, I., & Arndt, W. (1926). Die Glazialrelicte stellenden Tierarten Bulgariens und Mazedoniens. Zeitschrift für Morphologie und Ökologie der Tiere, 5(3), 381–405.CrossRefGoogle Scholar
  10. Butlin, R. K., & Hewitt, G. M. (1985). A hybrid zone between Chorthippus parallelus parallelus and C. p. erythropus (Orthoptera: Acrididae): behavioural characters. Biological Journal of the Linnean Society, 26, 287–299.CrossRefGoogle Scholar
  11. Comes, H. P., & Kadereit, J. W. (1998). The effect of Quaternary climatic changes on plant distribution and evolution. Trends in Plant Science, 3(11), 432–438.CrossRefGoogle Scholar
  12. Cooper, S. J., Ibrahim, K. M., & Hewitt, G. M. (1995). Postglacial expansion and genome subdivision in the European grasshopper Chorthippus parallelus. Molecular Ecology, 4, 49–60.CrossRefPubMedGoogle Scholar
  13. DeChaine, E. G., & Martin, A. P. (2004). Historic cycles of fragmentation and expansion in Parnassius smitheus (Papilionidae) inferred using mitochondrial DNA. Evolution, 58(1), 113–127.PubMedGoogle Scholar
  14. DeChaine, E. G., & Martin, A. P. (2005). Historical biogeography of two alpine butterflies in the Rocky Mountains: broad-scale concordance and local-scale discordance. Journal of Biogeography, 32, 1943–1956.CrossRefGoogle Scholar
  15. Drenowski, A. K. (1936). Beitrag zur Insektenfauna Bulgariens und Mazedoniens II (Lepidoptera, Hymenoptera, Diptera und Orthoptera). Mitteilungen der Bulgarischen Entomologischen Gesellschaft, 9, 237–256.Google Scholar
  16. Ebner, R. (1936). Eine boreoalpine Orthopterenart, Podisma frigida Boh., neu für die Balkanhalbinsel. Mitteilungen aus den Königlichen Naturwissenschaftlichen Instituten in Sofia, 9, 68.Google Scholar
  17. Ebner, R. (1937a). Orthopterologische Studien in Nordwest-Tirol. Konowia, 16(2), 28–40.Google Scholar
  18. Ebner, R. (1937b). Orthopterologische Studien in Nordwest-Tirol. Konowia, 16(2), 143–152.Google Scholar
  19. Ebner, R. (1951). Zur näheren Kenntnis einer boreoalpinen Orthopteren-Art (Aeropedellus variegatus F.-W.). Annalen des Naturhistorischen Museums in Wien, 58, 108–117.Google Scholar
  20. Elsner, N. (1968). Die neuromuskulären Grundlagen des Werbeverhaltens der Roten Keulenheuschrecke Gomphocerippus rufus (L.). Zeitschrift für Vergleichende. Physiologie, 60, 308–350.Google Scholar
  21. Elsner, N., & Wasser, G. (1995a). Leg and wing stridulation in various populations of the gomphocerine grasshopper Stenobothrus rubicundus (Germar, 1817). I. Sound patterns and singing movements. Zoology, 98, 179–190.Google Scholar
  22. Elsner, N., & Wasser, G. (1995b). The transition from leg to wing stridulation in two geographically distinct populations of the grasshopper Stenobothrus rubicundus. Naturwissenschaften, 82, 384–386.Google Scholar
  23. Fontana, P., Buzetti, F. M., Cogo, A., & Odé, B. (2002). Guida al riconoscimiento e allo studio di Cavallette, Grilli, Mantidi e insetti affini del Veneto. Guide natura, 1. Museo Naturalistico Archaeologico di Vicenza.Google Scholar
  24. Gaillard, M.-J. (2004). Ecosystem dynamics under changing climate—some illustrative cases from the past and their possible use in climate risk analysis. ESS Bulletin, 2(2), 44–56.Google Scholar
  25. Harz, K. (1957). Die Geradflügler Mitteleuropas. Jena: G. Fischer Verlag.Google Scholar
  26. Harz, K. (1975). Die Orthopteren Europas II. Series Entomologica, 11. The Hague: Dr. W Junk B.V.Google Scholar
  27. Heller, K.-G. (2006). Song evolution and speciation in bushcrickets. In S. Drosopoulos & M. F. Claridge (Eds.), Insect sounds and communication: Physiology, behaviour, ecology, and evolution (pp. 137–152). Boca Raton: CRC.Google Scholar
  28. Hewitt, G. M. (1975). A sex chromosome hybrid zone in the grasshopper Podisma pedestris (Orthoptera: Acrididae). Heredity, 35, 375–387.CrossRefPubMedGoogle Scholar
  29. Hewitt, G. M. (1996). Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247–276.Google Scholar
  30. Hewitt, G. M. (1999). Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87–112.CrossRefGoogle Scholar
  31. Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London, Series B, 359, 183–195.CrossRefGoogle Scholar
  32. Holdhaus, K. (1912). Kritisches Verzeichnis der boreoalpinen Tierformen (Glazialrelikte) der mittel- und südeuropäischen Hochgebirge. Annalen des Kaiserlich-Königlichen Naturhistorischen Hofmuseums, 26, 339–440.Google Scholar
  33. Holdhaus, K., & Lindroth, C. (1939). Die europäischen Koleopteren mit boreo-alpiner Verbreitung. Annalen des Naturhistorischen Museums in Wien, 50, 123–293.Google Scholar
  34. Holst, K. T. (1986). The Saltatoria (bush-crickets, crickets and grasshoppers) of northern Europe. Fauna Entomologica Scandinavica, 16.Google Scholar
  35. Ingrisch, S., & Pavićević, D. (1985). Zur Faunistik, Systematik und ökologischen Valenz der Orthopteren von Nordost-Griechenland. Mitteilungen der Münchner Entomologischen Gesellschaft, 75, 45–77.Google Scholar
  36. Jiggins, C. D., & Mallet, J. (2000). Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15(6), 250–255.CrossRefGoogle Scholar
  37. Kinzelbach, R. (2007). Der Treibhauseffekt und die Folgen für die Tierwelt. Klimawandel—ein Feigenblatt? Biologie in Unserer Zeit, 4(37), 250–259.CrossRefGoogle Scholar
  38. Knowles, L. L. (2000). Tests of Pleistocene speciation in montane grasshoppers (Genus Melanoplus) from the sky islands of western North America. Evolution, 54(4), 1337–1348.PubMedGoogle Scholar
  39. Knowles, L. L. (2001). Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology, 10, 691–701.CrossRefPubMedGoogle Scholar
  40. Kočárek, P., Holuša, J., & Vidlička, L. (2005). Blattaria, Mantodea, Orthoptera & Dermaptera of the Czech and Slovak Republics. Illustrated key 3. Zlín, Czech Republic: Kabourek Publ.Google Scholar
  41. Koschuh, A. (2008). Podismopsis styriaca nov. sp. (Orthoptera, Acridinae) ein Endemit im Ostalpenraum. Linzer Biologische Beiträge, 40(1), 627–638.Google Scholar
  42. Kropf, M., Kadereit, J. W., & Comes, H. P. (2002). Late Quaternary distributional stasis in the submediterranean mountain plant Anthyllis montana L. (Fabaceae) inferred from ITS sequences and amplified fragment polymorphism markers. Molecular Ecology, 11, 447–463.CrossRefPubMedGoogle Scholar
  43. Kropf, M., Kadereit, J. W., & Comes, H. P. (2003). Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Molecular Ecology, 12, 931–949.CrossRefPubMedGoogle Scholar
  44. Kruseman, C., & Jeekel, C. A. W. (1967). Stenobothrus (Stenobothrodes) cotticus nov. spec., a new grasshopper from the French Alps (Orthoptera, Acrididae). Entomologische Berichten, 27(1), 1–7.Google Scholar
  45. Lemonnier, M. (1999). Les peuplements d’Orthoptères (Insecta: Orthoptera) du Parc National du Mercantour (Alpes Maritimes, Alpes-de-Haute-Provence). Bulletin de la Société Entomologique de France, 104(2), 149–166.Google Scholar
  46. Lunt, D. H., Ibrahim, K. M., & Hewitt, G. M. (1998). mtDNA phylogeography and post-glacial patterns of subdivision in the meadow grasshopper Chorthippus parallelus. Heredity, 80(5), 633–641.CrossRefPubMedGoogle Scholar
  47. Marshall, J. A., & Haes, E. C. M. (1988). Grasshoppers and allied insects of Great Britain and Ireland. Colchester: Harley Books.Google Scholar
  48. Mendelson, T. C., & Shaw, K. L. (2005). Rapid speciation in an arthropod. Nature, 433, 375–376.CrossRefPubMedGoogle Scholar
  49. Müllenbach, R., Lagoda, P. J. L., & Welter, C. (1989). An efficient salt-chlorophorm extraction of DNA from blood and tissues. Trends in Genetics, 5, 391.PubMedGoogle Scholar
  50. Müller, U. C., Pross, J., & Bibus, E. (2003). Vegetation response to rapid climate change in Central Europe during the past 140,000 yr based on evidence from the Füramoos pollen record. Quaternary Research, 59, 235–245.CrossRefGoogle Scholar
  51. Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B. A. (Eds.). (2003). Alpine biodiversity in Europe. Ecological Studies, 167. Berlin: Springer.Google Scholar
  52. Obenberger, J. (1926). Orthoptères et Dermaptères de la République Tchécoslovaque. Fauna et flora Cechoslovenica, I. Praha: Académie Tchèque des Sciences et des Arts.Google Scholar
  53. Otte, D. (1972). Simple versus elaborate behaviour in grasshoppers—an analysis of communication in the genus Syrbula. Behaviour, 17, 291–322.CrossRefGoogle Scholar
  54. Pauls, S. U., Lumbsch, H. T., & Haase, P. (2007). Phylogeography of the montane caddisfly Drusus discolor: evidence for multiple refugia and periglacial survival. Molecular Ecology, 15, 2153–2169.CrossRefGoogle Scholar
  55. Pittioni, B. (1942). Die boreoalpinen Hummeln und Schmarotzerhummeln (Hymen., Apidae, Bombinae). I. Mitteilungen aus den Königlichen Naturwissenschaftlichen Instituten in Sofia, 15, 155–218.Google Scholar
  56. Ragge, D. R., & Reynolds, W. J. (1998). The songs of the grasshoppers and crickets of western Europe. Colchester: Harley Books.Google Scholar
  57. Ramme, W. (1951). Zur Systematik, Faunistik und Biologie der Orthopteren von Südost-Europa und Vorderasien. Mitteilungen aus dem Zoologischen Museum in Berlin, 27, 1–431.Google Scholar
  58. Ritchie, M. G., & Garcia, C. M. (2005). Explosive speciation in a cricket. Heredity, 95, 5–6.CrossRefPubMedGoogle Scholar
  59. Schmitt, T. (2007). Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 11. doi: 10.1186/1742-9994-4-11.CrossRefPubMedGoogle Scholar
  60. Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G., & Cosson, J.-F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453–464.CrossRefPubMedGoogle Scholar
  61. Theurillat, J.-P., & Guisan, A. (2001). Potential impact of climate change on vegetation in the European Alps: a review. Climatic Change, 50, 77–109.CrossRefGoogle Scholar
  62. Thorens, P., & Nadig, A. (1997). Atlas de Distribution des Orthoptéres de Suisse. Documenta Faunistica Helvetica. Centre Suisse de Cartographie de la Faune.Google Scholar
  63. Tonkov, S., & Marinova, E. (2005). Pollen and plant macrofossil analyses of radiocarbon dated mid-Holocene profiles from two subalpine lakes in the Rila Mountains, Bulgaria. The Holocene, 15(5), 663–671.CrossRefGoogle Scholar
  64. Varga, Z. S., & Schmitt, T. (2008). Types of oreal and oreotundral disjunctions in the western Palearctic. Biological Journal of the Linnean Society, 93, 415–430.CrossRefGoogle Scholar
  65. Vargas, P. (2003). Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon, 52, 463–476.CrossRefGoogle Scholar
  66. Vedenina, V. Y., & von Helversen, O. (2003). Complex courtship in a bimodal grasshopper hybrid zone. Behavioral Ecology and Sociobiology, 54, 44–54.CrossRefGoogle Scholar
  67. Voisin, J. -F. (2003). Atlas des Orthoptères (Insecta: Orthoptera) et des Mantides (Insecta: Mantodea) de France. Patrimoines Naturels, 60.Google Scholar
  68. von Helversen, O. (1986). Gesang und Balz bei Feldheuschrecken der Chorthippus albomarginatus-Gruppe (Orthoptera: Acrididae). Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere, 113, 319–342.Google Scholar
  69. von Helversen, O., & Elsner, N. (1977). The stridulatory movements of acridid grasshoppers recorded with an opto-electronic device. Journal of Comparative Physiology, 122, 53–64.CrossRefGoogle Scholar
  70. von Helversen, O., & von Helversen, D. (1994). Forces driving coevolution of song and song recognition in grasshoppers. Fortschritte der Zoologie, 39, 253–284.Google Scholar
  71. Warnecke, G. (1959). Verzeichnis der boreoalpinen Lepidopteren. Zeitschrift der Wiener Entomologischen Gesellschaft, 44(2), 17–26.Google Scholar
  72. Webb, T., & Bartlein, P. G. (1992). Global changes during the last 3 million years: climatic controls and biotic responses. Annual Reviews of Ecology and Systematics, 23, 141–173.CrossRefGoogle Scholar
  73. Willemse, F. (1984). Catalogue of the Orthoptera of Greece. Fauna Graeciae, I. Athens.Google Scholar
  74. Zhang, L.-B., Comes, H. P., & Kadereit, J. W. (2001). Phylogeny and Quaternary history of the European montane/alpine endemic Soldanella (Primulaceae) based on ITS and AFLP variation. American Journal of Botany, 88(12), 2331–2345.CrossRefGoogle Scholar

Copyright information

© Gesellschaft fuer Biologische Systematik 2010

Authors and Affiliations

  • Dirk Berger
    • 1
    • 2
    Email author
  • Dragan P. Chobanov
    • 3
  • Frieder Mayer
    • 1
    • 4
  1. 1.Institut für BiologieUniversität Erlangen-NürnbergErlangenGermany
  2. 2.Senckenberg Naturhistorische Sammlungen DresdenMuseum für TierkundeDresdenGermany
  3. 3.Institute of ZoologyBulgarian Academy of SciencesSofiaBulgaria
  4. 4.Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu BerlinBerlinGermany

Personalised recommendations