Abstract
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.
Similar content being viewed by others
References
Ander, K. (1949). Die boreo-alpinen Orthopteren Europas. Opuscula Entomologica, 14, 89–104.
Baur, B., Baur, H., Roesti, C., & Roesti, D. (2006). Die Heuschrecken der Schweiz. Bern: Haupt.
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.
Bellmann, H., & Luquet, G. C. (1995). Guide des sauterelles, grillons et criquets d’Europe occidentale. Lausanne: Delachaux et Niestle.
Beniston, M., Diaz, H. F., & Bradley, R. S. (1997). Climatic change at high elevation sites: an overview. Climatic Change, 36, 233–251.
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.
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.
Bull, C. M. (1979). The function of complexity in the courtship of the grasshopper Myrmeleotettix maculatus. Behaviour, 69(3/4), 201–216.
Buresch, I., & Arndt, W. (1926). Die Glazialrelicte stellenden Tierarten Bulgariens und Mazedoniens. Zeitschrift für Morphologie und Ökologie der Tiere, 5(3), 381–405.
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.
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.
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.
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.
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.
Drenowski, A. K. (1936). Beitrag zur Insektenfauna Bulgariens und Mazedoniens II (Lepidoptera, Hymenoptera, Diptera und Orthoptera). Mitteilungen der Bulgarischen Entomologischen Gesellschaft, 9, 237–256.
Ebner, R. (1936). Eine boreoalpine Orthopterenart, Podisma frigida Boh., neu für die Balkanhalbinsel. Mitteilungen aus den Königlichen Naturwissenschaftlichen Instituten in Sofia, 9, 68.
Ebner, R. (1937a). Orthopterologische Studien in Nordwest-Tirol. Konowia, 16(2), 28–40.
Ebner, R. (1937b). Orthopterologische Studien in Nordwest-Tirol. Konowia, 16(2), 143–152.
Ebner, R. (1951). Zur näheren Kenntnis einer boreoalpinen Orthopteren-Art (Aeropedellus variegatus F.-W.). Annalen des Naturhistorischen Museums in Wien, 58, 108–117.
Elsner, N. (1968). Die neuromuskulären Grundlagen des Werbeverhaltens der Roten Keulenheuschrecke Gomphocerippus rufus (L.). Zeitschrift für Vergleichende. Physiologie, 60, 308–350.
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.
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.
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.
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.
Harz, K. (1957). Die Geradflügler Mitteleuropas. Jena: G. Fischer Verlag.
Harz, K. (1975). Die Orthopteren Europas II. Series Entomologica, 11. The Hague: Dr. W Junk B.V.
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.
Hewitt, G. M. (1975). A sex chromosome hybrid zone in the grasshopper Podisma pedestris (Orthoptera: Acrididae). Heredity, 35, 375–387.
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.
Hewitt, G. M. (1999). Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87–112.
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.
Holdhaus, K. (1912). Kritisches Verzeichnis der boreoalpinen Tierformen (Glazialrelikte) der mittel- und südeuropäischen Hochgebirge. Annalen des Kaiserlich-Königlichen Naturhistorischen Hofmuseums, 26, 339–440.
Holdhaus, K., & Lindroth, C. (1939). Die europäischen Koleopteren mit boreo-alpiner Verbreitung. Annalen des Naturhistorischen Museums in Wien, 50, 123–293.
Holst, K. T. (1986). The Saltatoria (bush-crickets, crickets and grasshoppers) of northern Europe. Fauna Entomologica Scandinavica, 16.
Ingrisch, S., & Pavićević, D. (1985). Zur Faunistik, Systematik und ökologischen Valenz der Orthopteren von Nordost-Griechenland. Mitteilungen der Münchner Entomologischen Gesellschaft, 75, 45–77.
Jiggins, C. D., & Mallet, J. (2000). Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15(6), 250–255.
Kinzelbach, R. (2007). Der Treibhauseffekt und die Folgen für die Tierwelt. Klimawandel—ein Feigenblatt? Biologie in Unserer Zeit, 4(37), 250–259.
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.
Knowles, L. L. (2001). Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology, 10, 691–701.
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.
Koschuh, A. (2008). Podismopsis styriaca nov. sp. (Orthoptera, Acridinae) ein Endemit im Ostalpenraum. Linzer Biologische Beiträge, 40(1), 627–638.
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.
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.
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.
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.
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.
Marshall, J. A., & Haes, E. C. M. (1988). Grasshoppers and allied insects of Great Britain and Ireland. Colchester: Harley Books.
Mendelson, T. C., & Shaw, K. L. (2005). Rapid speciation in an arthropod. Nature, 433, 375–376.
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.
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.
Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B. A. (Eds.). (2003). Alpine biodiversity in Europe. Ecological Studies, 167. Berlin: Springer.
Obenberger, J. (1926). Orthoptères et Dermaptères de la République Tchécoslovaque. Fauna et flora Cechoslovenica, I. Praha: Académie Tchèque des Sciences et des Arts.
Otte, D. (1972). Simple versus elaborate behaviour in grasshoppers—an analysis of communication in the genus Syrbula. Behaviour, 17, 291–322.
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.
Pittioni, B. (1942). Die boreoalpinen Hummeln und Schmarotzerhummeln (Hymen., Apidae, Bombinae). I. Mitteilungen aus den Königlichen Naturwissenschaftlichen Instituten in Sofia, 15, 155–218.
Ragge, D. R., & Reynolds, W. J. (1998). The songs of the grasshoppers and crickets of western Europe. Colchester: Harley Books.
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.
Ritchie, M. G., & Garcia, C. M. (2005). Explosive speciation in a cricket. Heredity, 95, 5–6.
Schmitt, T. (2007). Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 11. doi:10.1186/1742-9994-4-11.
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.
Theurillat, J.-P., & Guisan, A. (2001). Potential impact of climate change on vegetation in the European Alps: a review. Climatic Change, 50, 77–109.
Thorens, P., & Nadig, A. (1997). Atlas de Distribution des Orthoptéres de Suisse. Documenta Faunistica Helvetica. Centre Suisse de Cartographie de la Faune.
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.
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.
Vargas, P. (2003). Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon, 52, 463–476.
Vedenina, V. Y., & von Helversen, O. (2003). Complex courtship in a bimodal grasshopper hybrid zone. Behavioral Ecology and Sociobiology, 54, 44–54.
Voisin, J. -F. (2003). Atlas des Orthoptères (Insecta: Orthoptera) et des Mantides (Insecta: Mantodea) de France. Patrimoines Naturels, 60.
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.
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.
von Helversen, O., & von Helversen, D. (1994). Forces driving coevolution of song and song recognition in grasshoppers. Fortschritte der Zoologie, 39, 253–284.
Warnecke, G. (1959). Verzeichnis der boreoalpinen Lepidopteren. Zeitschrift der Wiener Entomologischen Gesellschaft, 44(2), 17–26.
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.
Willemse, F. (1984). Catalogue of the Orthoptera of Greece. Fauna Graeciae, I. Athens.
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.
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 195 kb)
Rights and permissions
About this article
Cite this article
Berger, D., Chobanov, D.P. & Mayer, F. Interglacial refugia and range shifts of the alpine grasshopper Stenobothrus cotticus (Orthoptera: Acrididae: Gomphocerinae). Org Divers Evol 10, 123–133 (2010). https://doi.org/10.1007/s13127-010-0004-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-010-0004-4