The Rare Butterfly Tomares Nesimachus (Lycaenidae) as a Bioindicator for Pollination Services and Ecosystem Functioning in Northern Israel

in Israel Journal of Ecology and Evolution
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Evidence suggests that insects whose existence depends on fruit production may serve as good bioindicators, especially for pollination services. In this study we examined this hypothesis, focusing on one of Israel's rarest butterflies, Tomares nesimachus (Rhopalocera; Lycaenidae). The butterfly is affiliated with open grasslands in the north of Israel, where its sole host plant, Astragalus macrocarpus, occurs. In a two-year field study, we mapped the distribution of the butterfly in Israel and tried to evaluate the causes of its rarity and decline. We found that its abundance in habitat patches was correlated with several factors, including (a) fruit production of the host plants in each patch, (b) the number of other patches in the vicinity, (c) the characteristics of the "matrix" outside the patches within a distance of up to 2 km, (d) the richness of large bee species (the plant pollinators), and (e) the grazing management of the butterfly's habitat. The characteristics of the matrix further affected the richness of bees in the butterfly's habitat. Since butterfly abundance is correlated with species richness of pollinators, it can serve as an indicator of diverse, species-rich butterfly habitats (grasslands). We deduce that species that depend on fruit production and by themselves do not contribute to their host-plant pollination, may almost necessarily be affected by multiple ecological factors and therefore can indeed serve as good indicators. Our results further indicate that the butterfly's population dynamics are affected by large-scale processes, and hence its conservation requires the preservation of large open landscapes. Consequently, T. nesimachus may also serve as an umbrella species.

The Rare Butterfly Tomares Nesimachus (Lycaenidae) as a Bioindicator for Pollination Services and Ecosystem Functioning in Northern Israel

in Israel Journal of Ecology and Evolution

References

  • Cremene C. Groza G. Rakosy L. Schileyko A. A. Baur A. Erhardt A. Baur B. 2005. Alterations of steppe-like grasslands in Eastern Europe: a threat to regional biodiversity hotspots. Conservation Biology 19: 1606-1618.

  • Danin A. 2003. Database of the flora of Israel. OPTIMA Newsletter 37: 45-46.

  • Agerer-Kirchhoff C. 1976. Revision von Astragalus L. sect. Astragalus (Leguminosae). Boissiera 25: 1-197.

  • Ak�akaya H. R. Burgman M. A. Kindvall O. Wood C. C. Sj�gren-Gulve P. Hatfield J. McCarthy J. M. eds. 2004. Species conservation and management: case studies. Oxford University Press Oxford.

  • Allen-Wardell G. Bernhardt P. Bitner R. Burquez A. Buchmann S. Cane J. Cox P. A. Dalton V. Feinsinger P. Ingram M. Inouye D. Jones C. E. Kennedy K. Kevan P. Koopowitz H. Medellin R. Medellin-Morales S. Nabhan G. P. Pavlik B. Tepedino V. Torchio P. Walker S. 1998. The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conservation Biology 12: 8-17.

  • Andelman S. J. Fagan W. F. 2000. Umbrellas and flagships: efficient conservation surrogates or expensive mistakes. Proceedings of the National Academy of Science of the United States of America 97: 5954-5959.

  • Baur B. Joshi J. Schmid B. Haenggi A. Borcard D. Stary J. Pedroli-Christen A. Thommen G. H. Luka H. H-P. R. Oggier P. Ledergerber S. Erhardt A. 1996. Variation in species richness of plants and diverse groups of invertebrates in three calcareous grasslands of the Swiss Jura mountains. Revue Suisse de Zoologie 103: 801-833.

  • Baur B. Cremene C. Groza G. Rakosy L. Shileyko A. A. Baur A. Stoll P. Erhardt A. 2006. Effects of abandonment of subalpine hay meadows on plant and invertebrate diversity in Transylvania Romania. Biological Conservation 132: 261-273.

  • Benyamini D. 1990. A field guide to the butterflies of Israel including of Mt. Hermon and Sinai. Keter Publishing House Jerusalem.

  • Benyamini D. 1999. The biology and conservation of Iolana alfierii Witshire 1948: the Burning Bush blue (Lepidoptera: Lycaenidae). Linneana Belgica 17: 119-134.

  • Benyamini D. 2002. A field guide to the butterflies of Israel including of Mt. Hermon Sinai and Jordan (revised ed.). Keter Publishing House Jerusalem.

  • Betrus C. J. Fleishman E. Blair R. B. 2005. Cross-taxonomic potential and spatial transferabilityof an umbrella species index. Journal of Environmental Management 74: 79-87.

  • Biesmeijer J. C. Roberts S. P. M. Reemer M. Ohlm�ller R. Edwards M. Peeters T. Schaffers A. P. Potts S. G. Kleukers R. Thomas C. D. Settele J. Kunin W. E. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351-354.

  • Binzenh�fer B. Schr�der B. Strauss B. Biedermann R. Settele J. 2005. Habitat models and habitat connectivity analysis for butterflies and burnet moths—the example of Zygaena carniolica and Coenonympha arcania.Biological Conservation 126: 247-259.

  • Brown J. K. S. Freitas A. V. L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32: 934-956.

  • B�chs W. 2003. Biotic indicators for biodiversity and sustainable agriculture. Agriculture Eco-systems and Environment 98: 1-16.

  • Burnham K. P. Anderson D. R. 2002. Model selection and multimodel inference a practical information-theoretic approach. Springer New York.

  • Caro T. M. O'Doherty G. 1999. On the use of surrogate species in conservation biology. Conservation Biology 13: 805-814.

  • Conradt L. Bodsworth E. J. Roper T. J. Thomas C. D. 2000. Non-random dispersal in the butterfly Maniola jurtina: implications for metapopulation models. Proceedings of the Royal Society of London B 267: 1505-1510.

  • Conradt L. Roper T. J. Thomas C. D. 2001. Dispersal behaviour of individuals in metapopulations of two British butterflies. Oikos 95: 416-424.

  • Dolev A. Perevolotsky A. 2004. The Red Book of vertebrates in Israel. Israel Nature and National Parks Protection Authority and Society for the Protection of Nature in Israel Press Jerusalem.

  • Fleishman E. Murphy D. D. Brussard P. E. 2000. A new method for selection of umbrella species for conservation planning. Ecological Applications 10: 569-579.

  • Fleishman E. Blair R. B. Murphy D. D. 2001. Empirical validation of a method for umbrella species selection. Ecological Applications 11: 1489-1501.

  • Hadar L. Noy-Meir I. Perevolotsky A. 1999. The effect of shrub clearing and grazing on the composition of a Mediterranean plant community: functional groups versus species. Journal of Vegetation Science 10: 673-682.

  • Hambler C. Speight M. R. 2004. Extinction rates and butterflies. Science 305: 1563.

  • Hanski I. 2001. Population dynamic consequences of dispersal in local populations and in meta-populations. In: Clobert J. Danchin E. Dhondt A. A. Nichols J. D. eds. Dispersal. Oxford University Press Oxford pp. 283-298.

  • Hanski I. Gilpin M. E. 1997. Metapopulation biology: ecology genetics & evolution. Academic Press London.

  • Harrison S. 1989. Long-distance dispersal and colonization in the bay checkerspot butterfly Euphydryas editha bayensis.Ecology 70: 1236-1243.

  • Kerr J. T. Sugar A. Packer L. 2000. Indicator taxa rapid biodiversity assessment and nestedness in an endangered ecosystem. Conservation Biology 14: 1726-1734.

  • Klein A.-M. Vaissiere B. E. Cane J. H. Steffan-Dewenter I. Cunningham S. A. Kremen C. Tscharntke T. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B 274: 303-313.

  • Kremen C. Williams N. M. Thorp R. W. 2002. Crop pollination from native bees at risk from agricultural intensifications. Proceedings of the National Academy of Science of the United States of America 99: 16812-16816.

  • Larsen T. B. Nakamura I. 1983. The butterflies of East Jordan. Entomologist Gazette 34: 135-208.

  • Launer A. E. Murphy D. D. 1994. Umbrella species and the conservation of habitat fragments: a case of a threatened butterfly and a vanishing grassland ecosystem. Biological Conservation 69: 145-153.

  • Li Q. Mayzlish E. Shamir I. Pen-Mouratov S. Sternberg M. Steinberger Y. 2005. Impact of grazing on soil biota in a Mediterranean grassland. Land Degradation & Development 16: 581-592.

  • Mac Nally R. Fleishman E. 2004. A successful predictive model of species richness based on indicator species. Conservation Biology 18: 646-654.

  • Meffe G. K. Carrol C. R. 1997. Principles of conservation biology. Sinauer Associates Sunderland Massachusetts.

  • Ne'eman G. 2003. To be or not to be—the effect of nature conservation management on flowering of Paeonia mascula (L.) Miller in Israel. Biological Conservation 109: 103-109.

  • New T. R. 1997. Butterfly conservation. Oxford University Press Oxford.

  • Nowicki P. Settele J. Thomas J. A. Woyciechowski M. 2005. A review of population structure of Maculinea butterflies. In: Settele J. K�hn E. Thomas J. A. eds. Studies on the ecology and conservation of butterflies in Europe Vol. 2 Species ecology along a European gradient: Maculinea butterflies as a model. Pensoft Sofia/Moscow pp. 144-149.

  • Oostermeijer J. G. B. Van Swaay C. A. M. 1998. The relationship between butterflies and environmental indicator values: a tool for conservation in a changing landscape. Biological Conservation 86: 271-280.

  • Osem Y. Perevolotsky A. Kigel J. 2004. Site productivity and plant size explain the response of annual species to grazing exclusion in a Mediterranean semi-arid rangeland. Journal of Ecology 92: 297-309.

  • Pe'er G. Benyamini D. 2008. A template for publishing the "conservation chain" from problem identification to practical action exemplified through the campaign for butterfly protection in Israel. Israel Journal of Ecology and Evolution 54: 19-39 this issue.

  • Pe'er G. Settele J. 2008. Butterflies in and for conservation: trends and prospects. Israel Journal of Ecology and Evolution 54: 7-17 this issue.

  • Pfeifer M. A. Andrick U. R. Frey W. Settele J. 2000. On the ethology and ecology of a small and isolated population of the Dusky Large Blue Butterfly Glaucopsyche (Maculinea) nausithous (Bergstraesser 1779)(Lep. Lycaenidae). Nota Lepidopterologica 23: 147-172.

  • Pollard E. Yates T. J. 1993. Monitoring butterflies for ecology and conservation. Chapman & Hall London.

  • Roberge J.-M. Angelstam P. 2004. Usefulness of the umbrella species concept as a conservation tool. Conservation Biology 18: 76-85.

  • Schultz C. B. 2000. Using invertebrates to assess sustainable farming review of Paoletti M. G. et al. 1999. Invertebrate biodiversity as bioindicators of sustainable landscapes. Conservation Biology 14: 1929-1930.

  • Settele J. Henle K. 2003. Grazing and cutting regimes for old grassland in temperate zones in biodiversity conservation and habitat management. In: Gherardi F. Corti C. Gualtieri M. eds. Encyclopedia of life support systems (EOLSS). Eolss Publishers [http://www.eolss.net chapter E1-67-03-02 Internet-version 11 pp.]. http://www.eolss.net

  • Settele J. Reinhardt R. 2000. �kologie der Tagfalter Deutschlands: Grundlagen und Schutzaspekte. In: Settele J. Feldmann R. Reinhardt R. eds. Die Tagfalter Deutschlands. Ulmer Stuttgart pp. 60-123.

  • Settele J. Hammen V. Hulme P. Karlson U. Klotz S. Kotarac M. Kunin W. Marion G. O'Connor M. Petanidou T. Peterson K. Potts S. Pritchard H. Pysek P. Rounsevell M. Spangenberg J. Steffan-Dewenter I. Sykes M. Vighi M. Zobel M. K�hn I. 2005a. ALARM—Assessing LArge-scale environmental Risks for biodiversity with tested Methods. GAIA—Ecological Perspectives for Science and Society 14: 69-72.

  • Settele J. K�hn E. Thomas J. A. 2005b. Studies on the ecology and conservation of butterflies in Europe Vol. 2. Species ecology along a European gradient: Maculinea butterflies as a model. Pensoft Sofia/Moscow.

  • Sternberg M. Gutman M. Perevolotsky A. Ungar E. D. Kigel J. 2000. Vegetation response to grazing management in a Mediterranean herbaceous community: a functional group approach. Journal of Applied Ecology 37: 224-237.

  • Thomas J. A. 2005. Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 339-357.

  • Thomas J. A. Clarke R. T. 2004. Extinction rates and butterflies—Response. Science 305: 1563-1565.

  • Thomas J. A. Morris M. G. 1994. Patterns mechanisms and rates of decline among UK invertebrates. Philosophical Transactions of the Royal Society of London B 344: 47-54.

  • Thomas J. A. Settele J. 2004. Evolutionary biology: butterfly mimics of ants. Nature 432: 283-284.

  • Thomas J. A. Telfer M. G. Roy D. B. Preston C. D. Greenwood J. J. D. Asher J. Fox R. Clarke R. T. Lawton J. H. 2004. Comparative losses of British butterflies birds and plants and the global extinction crisis. Science 303: 1879-1881.

  • Thomas J. A. R. T. C. Randle Z. Simcox D. J. Schoenrogge K. Elmes G. W. Wardlaw J. C. Settele J. 2005. Maculinea and myrmecophiles as sensitive indicators of grassland butterflies (umbrella species) ants (keystone species) and other invertebrates. I. In: Settele J. K�hn E. Thomas J. A. eds. Studies on the ecology and conservation of butterflies in Europe Vol. 2. Species ecology along a European gradient: Maculinea butterflies as a model. Pensoft Sofia/Moscow pp. 28-31.

  • van Swaay C. Warren M. 1999. Red data book of European butterflies (Rhopalocera). Council of Europe Publishing Strasbourg (Nature and Environment Series No. 99).

  • Vessby K. Soederstroem B. Glimskaer A. Svensson B. 2002. Species-richness correlations of six different taxa in Swedish seminatural grasslands. Conservation Biology 16: 430-439.

  • Wilcox B. A. 1984. In situ conservation of genetic resources: determinants of minimum area requirements. In: McNeely J. A. Miller K. R. eds. National parks conservation and development: the role of protected areas in sustaining society. Smithsonian Institution Press Washington DC pp. 639-647.

  • Zar J. H. 1999. Biostatistical analysis. Prentice-Hall Upper Saddle River NJ.

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