A Higher-Taxon Approach with Soil Invertebrates to Assessing Habitat Diversity in East Asian Rural Landscapes

  • S.-I. Tanabe
  • S.K. Kholin
  • Y.-B. Cho
  • S.-I. Hiramatsu
  • A. Ohwaki
  • S. Koji
  • A. Higuchi
  • S.Y. Storozhenko
  • S. Nishihara
  • K. Esaki
  • K. Kimura
  • K. Nakamura


Rural biodiversity in East Asia is at risk due to the loss of habitat diversity, and good indicators are needed to evaluate diverse habitats in rural landscapes. We examined whether the higher taxa (classes and orders) of soil invertebrates discriminated among several types of secondary forests such as broad-leaved deciduous forests, conifer forests and bamboo forests, primary forests, grasslands and/or wetlands, better than species assemblages of a well-established indicator, ground beetles (Coleoptera, Carabidae and/or Staphylinidae), in three East Asian regions (Japan, South Korea and the Russian Far East). We collected soil invertebrates with pitfall traps and used community composition and an ordination technique to test their performance as indicators. In Japan, the higher taxa of soil invertebrates discriminated finely among a wide range of habitats, and soil moisture seemed to be an important factor underlying habitat arrangement by these taxa along an ordination axis. While species assemblages of ground beetles detected large faunal differences among grasslands, wetlands and a composite group of three forest-type habitats (oak, conifer and bamboo forests), it failed to discriminate among any of the three forest-type habitats. When the analysis included only these types of forests, ground beetles were found to be able to discriminate finely among them, indicating limited performance in relation to the range of habitats covered. In the other two countries, the higher taxa of soil invertebrates showed a performance similar to that of species assemblages of ground beetles, possibly because of the narrow range of habitats analyzed. We conclude that the higher taxa of soil invertebrates are an effective tool for assessing the diversity of rural habitats across the East Asian region, where taxonomic knowledge at the species level is still insufficient. Our results may be applied broadly to other regions where agricultural intensification and land abandonment have caused quantitative and qualitative changes in rural landscapes.


Habitat Type Canonical Correspondence Analysis Detrended Correspondence Analysis Ground Beetle High Taxon 
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  1. Asteraki, E.J., Hanks, C.B., and Clements, R.O. (1995). The influence of different types of grassland field margin on carabid beetle (Coleoptera, Carabidae) communities. Agriculture, Ecosystems and Environment, 54, 195-202.CrossRefGoogle Scholar
  2. Baguette, M. (1993). Habitat selection of carabid beetle in deciduous woodlands of southern Belgium. Pedobiologia, 37, 365-378.Google Scholar
  3. Balmford, A., Green, M.J.B., and Murray, M.G. (1996). Using higher-taxon richness as a surrogate for species richness: I. regional tests. Proceedings of the Royal Society of London, Series B, 263, 1267-1274.CrossRefGoogle Scholar
  4. Balmford, A., Jayasuriya, A.H.M., and Green, M.J.B. (1996). Using higher-taxon richness as a surrogate for species richness: II. Local applications. Proceedings of the Royal Society of London, Series B, 263, 1571-1575.CrossRefGoogle Scholar
  5. Basset, Y., Mavoungou, J.F., Mikissa, J.B., Missa, O., Miller, S.E. and Kitching, R.L. (2004). Discriminatory power of different arthropod data sets for the biological monitoring of anthropogenic disturbance in tropical forests. Biodiversity and Conservation, 13, 709-732.CrossRefGoogle Scholar
  6. Bedford, S.E. and Usher, M.B. (1994). Distribution of arthropod species across the margins of farm woodlands. Agriculture, Ecosystems and Environment, 48, 295-305.CrossRefGoogle Scholar
  7. Benton, T.G., Vickery, J.A. and Wilson, J.D. (2003). Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology and Evolution, 18, 182-188.CrossRefGoogle Scholar
  8. Blake, S., McCracken, D.I., Eyre, M.D., Garside, A. and Foster, G.N. (2003). The relationship between the classification of Scottish ground beetle assemblages (Coleoptera, Carabidae) and the National Vegetation Classification of British plant communities. Ecography, 26, 602-616.CrossRefGoogle Scholar
  9. Bohac, J. (1999). Staphylinid beetles as bioindicators. Agriculture, Ecosystems and Environment, 74, 357-372.CrossRefGoogle Scholar
  10. Buckley, G.P. (1992). Ecology and Management of Coppice Woodlands. Chapman and Hall, London.Google Scholar
  11. Butterfield, J., Luff, M.L., Baines, M., and Eyre, M.D. (1995). Carabid beetle communities as indicators of conservation potential in upland forests. Forest Ecology and Management, 79, 63-77.CrossRefGoogle Scholar
  12. Coleman, D.C., Crossley, Jr. D.A., and Hendrix, P.F. (2004). Fundamental of Soil Ecology. Elsevier Inc., San Diego.Google Scholar
  13. Coll, M.T., Heneghan, L., and Bolger, T. (1995). Carabidae fauna in two Irish conifer stands: a comparison with those of some other European forests. Biology and Environment: Proceeding of the Royal Irish Academy, 95B, 171-177.Google Scholar
  14. Dennis, P., Young, M.R., Howard, C.L., and Gordon, I.J. (1997). The response of epigeal beetles (Col.: Carabidae, Staphylinidae) to varied grazing regimes on upland Nardus stricta grasslands. Journal of Applied Ecology, 34, 433-443.CrossRefGoogle Scholar
  15. du Bus de warnaffe, G., and Lebrun, P. (2004). Effects of forest management on carabid beetles in Belgium: implications for biodiversity conservation. Biological Conservation, 118, 219-234.CrossRefGoogle Scholar
  16. Fahy, O. and Gormally, M. (1998). A comparison of plant and carabid beetle communities in an Irish oak woodland with a nearby conifer plantation and clearfelled site. Forest Ecology and Management, 110, 263-273.CrossRefGoogle Scholar
  17. Fournier, E. and Loreau, M. (2001). Respective roles of recent hedges and forest patch remnants in the maintenance of ground-beetle (Coleoptera: Carabidae) diversity in an agricultural landscape. Landscape Ecology, 16, 17-32.CrossRefGoogle Scholar
  18. French, B.W. and Elliott, N.C. (1999). Temporal and spatial distribution of ground beetle (Coleoptera: Carabidae) assemblages in grasslands and adjacent wheat fields. Pedobiologia, 43, 73-84.Google Scholar
  19. Gardner, S.M. (1991). Ground beetle (Coleoptera: Carabidae) communities on upland heath and their association with heathland flora. Journal of Biogeography, 18, 281-289.CrossRefGoogle Scholar
  20. Gutiérrez, D., Menéndez, R. and Méndez, M. (2003). Habitat-based conservation priorities for carabid beetles within the Picos de Europa National Park, northern Spain. Biological Conservation, 115, 379-393.CrossRefGoogle Scholar
  21. Holmes, P.R., Fowles, A.P., Boyce, D.C. and Reed, D.K. (1993). The ground beetle (Coleoptera: Carabidae) fauna of Welsh peatland biotopes-species seemblages in relation to peatland habitats and management. Biological Conservation, 65, 61-67.CrossRefGoogle Scholar
  22. Hong, S.K. (1998). Changes in landscape patterns and vegetation process in the Far-Eastern cultural landscapes: human activity on pine-dominated secondary vegetation in Korea and Japan. Phytocoenologia, 28, 45-66.Google Scholar
  23. Howard, P.C., Viskanic, P., Davenport, T.R.B., Kigenyi, F.W., Baltzer, M., Dickinson, C.J. (1998). Complementarity and the use of indicator groups for reserve selection in Uganda. Nature, 394, 472-475.CrossRefGoogle Scholar
  24. Hughes, J.B., Daily, G.C. and Ehrlich, P.R. (2000). Conservation of insect diversity: a habitat approach. Conservation Biology, 14, 1788-1797.CrossRefGoogle Scholar
  25. Humphrey, J.W., Hawes, C., Peace, A.J., Ferris-Kaan, R. and Jukes, M.R. (1999). Relationships between insect diversity and habitat characteristics in plantation forests. Forest Ecology and Management, 113, 11-21.CrossRefGoogle Scholar
  26. Ings, T.C. and Hartley, S.E. (1999). The effect of habitat structure on carabid communities during the regeneration of a native Scottish forest. Forest Ecology and Management, 119, 123-136.CrossRefGoogle Scholar
  27. Jongman, R.H.G., ter Braak, C.J.F., and van Tongeren, O.F.R. (1995). Data Analysis in Community and Landscape Ecology. Cambridge University Press, Cambridge.Google Scholar
  28. Jukes, M.R., Peace, A.J., and Ferris, R. (2001). Carabid beetle communities associated with coniferous plantations in Britain: the influence of site, ground vegetation and stand structure. Forest Ecology and Management, 148, 271-286.CrossRefGoogle Scholar
  29. Kato, M. (2001). ‘SATOYAMA’ and biodiversity conservation: ‘SATOYAMA’ as important insect habitats. Global Environmental Research, 5, 135-149.Google Scholar
  30. Koivula, M., Kukkonen, J. and Niemelä, J. (2002). Boreal carabid-beetle (Coleoptera: Carabidae) assemblages along the clear-cut originated succession gradient. Biodiversity and Conservation, 11, 1269-1288.CrossRefGoogle Scholar
  31. Koivula, M., Punttila, P., Haila, Y. and Niemelä, J. (1999). Leaf litter and the small-scale distribution of carabid beetles (Coleoptera: Carabidae) in the boreal forest. Ecography, 22, 424-435.CrossRefGoogle Scholar
  32. Krebs, J.R., Wilson, J.D., Bradbury, R.B., and Siriwardena, G.M. (1999). The second silent spring? Nature, 400, 611-612.CrossRefGoogle Scholar
  33. Kremen, C., Colwell, R.K., Erwin, T.L., Murphy, D.D., Noss, R.F. and Sanjayan, M.A. (1993). Terrestrial arthropod assemblages: their use in conservation planning. Conservation Biology, 7, 796-808.CrossRefGoogle Scholar
  34. Lensing, J.R., Todd, S., and Wise, D.H. (2005). The impact of altered precipitation on spatial stratification and activity-densities of springtails (Collembola) and spiders (Araneae). Ecological Entomology, 30, 194-200.CrossRefGoogle Scholar
  35. Lepš, J. and šmilauer, P. (2003). Multivariate Analysis of Ecological Data for CANOCO. Cambridge University Press, Cambridge.Google Scholar
  36. Luff, M.L. (1996). Use of carabids as environmental indicators in grasslands and cereals. Annales Zoologici Fennici, 33, 185-195.Google Scholar
  37. Luff, M.L., Eyre, M.D. and Rushton, S.P. (1989). Classification and ordination of habitats of ground beetles (Coleoptera, Carabidae) in north-east England. Journal of Biogeography, 16, 121-130.CrossRefGoogle Scholar
  38. Luff, M.L., Eyre, M.D. and Rushton, S.P. (1992). Classification and prediction of grassland habitats using ground beetles (Coleoptera, Carabidae). Journal of Environmental Management, 35, 301-315.Google Scholar
  39. Margules, C.R., and Pressey, R.L. (2000). Systematic conservation planning. Nature, 405, 243-253.PubMedCrossRefGoogle Scholar
  40. McCracken, D.I. (1994). A fuzzy classification of moorland ground beetle (Coleoptera: Carabidae) and plant communities. Pedobiologia, 38, 12-27.Google Scholar
  41. McGeoch, M. (1998). The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews, 73, 181-201.CrossRefGoogle Scholar
  42. Nakagoshi, N. and Hong, S.-K. (2001). Vegetation and landscape ecology of East Asian ‘SATOYAMA’. Global Environmental Research, 5, 171-181.Google Scholar
  43. Niemelä, J. (2001). Carabid beetles (Coleoptera, Carabidae) and habitat fragmentation: a review. European Journal of Entomology, 98, 127-132.Google Scholar
  44. Niemelä, J., Haila, Y., Halme, E., Lahti, T., Pajunen, T. and Punttila, P. (1988). The distribution of carabid beetles in fragments of old coniferous taiga and adjacent managed forests. Annales Zoologici Fennici, 25, 107-119.Google Scholar
  45. Niemelä, J., Haila, Y., Halme, E., Pajunen, T. and Punttila, P. (1992). Small-scale heterogeneity in the spatial distribution of carabid beetles in the southern Finnish taiga. Journal of Biogeography, 19, 173-181.CrossRefGoogle Scholar
  46. Niemelä, J., Haila, Y. and Punttila, P. (1996). The importance of small-scale heterogeneity in boreal forests: variation in diversity in forest-floor invertebrates across the succession gradient. Ecography, 19, 352-368.CrossRefGoogle Scholar
  47. Oliver, I. and Beattie, A.J. (1996). Invertebrate morphospecies as surrogates for species: a case study. Conservation Biology, 10, 99-109.CrossRefGoogle Scholar
  48. Oliver, I., Beattie, A.J. and York, A. (1998). Spatial fidelity of plant, vertebrate, and invertebrate assemblages in multiple-use forest in eastern Australia. Conservation Biology, 12, 822-835.CrossRefGoogle Scholar
  49. O’Neil, T.A., Steidl, R.J., Edge, W.D. and Csuti, B. (1995). Using wildlife communities to improve vegetation classification for conserving biodiversity. Conservation Biology, 9, 1482-1491.CrossRefGoogle Scholar
  50. Paoletti, M.G. and Bressan, M. (1996). Soil invertebrates as bioindicators of human disturbance. Critical Reviews in Plant Sciences, 15, 21-62.CrossRefGoogle Scholar
  51. Pressey, R.L. (1994). Land classifications are necessary for conservation planning but what do they tell us about the fauna? In D. Lunney, S. Hand, P. Reed and D. Butcher (Eds.), Future of the Fauna of Western New South Wales (Vol. 246, pp. 31-41). Royal Zoological Society of New South Wales, N.S.W., Australia.Google Scholar
  52. Pykälä, J. (2000). Mitigating human effects on European biodiversity through traditional animal husbandry. Conservation Biology, 14, 705-712.CrossRefGoogle Scholar
  53. Rainio, J. and Niemelä J. (2003). Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodiversity and Conservation, 12, 487-506.CrossRefGoogle Scholar
  54. Rushton, S.P., Luff, M.L. and Eyre, M.D. (1991). Habitat characteristics of grassland Pterostichus species (Coleoptera, Carabidae). Ecological Entomology, 16, 91-104.CrossRefGoogle Scholar
  55. Rykken, J.J., Capen, D.E. and Mahabir, S.P. (1997). Ground beetles as indicators of land type diversity in the green mountains of Vermont. Conservation Biology, 11, 522-530.CrossRefGoogle Scholar
  56. Sanderson, R.A., Rushton, S.P., Cherrill, A.J. and Byrne, J.P. (1995). Soil, vegetation and space: an analysis of their effects on the invertebrate communities of a moorland in north-east England. Journal of Applied Ecology, 32, 506-518.CrossRefGoogle Scholar
  57. Scott, W. A. and Anderson, R. (2003). Temporal and spatial variation in carabid assemblages from the United Kingdom Environmental Change Network. Biological Conservation, 110, 197-210.CrossRefGoogle Scholar
  58. Similä, M., Kouki, J., M?nkk?nen, M. and Sippola, A.-L. (2002). Beetle species richness along the forest productivity gradient in northern Finland. Ecography, 25, 42-52.Google Scholar
  59. Storozhenko, S.Y., Sidorenko, V.S., Lafer, G.S. and Kholin, S.K. (2003). The International Biodiversity Observation Year (IBOY): insects of the forest ecosystems of the Primorye region. A. I. Kurentsov’s Annual Memorial Meetings, 13, 31-52. (In Russian).Google Scholar
  60. Su, J.C., Debinski, D.M., Jakubauskas, M.E. and Kindscher, K. (2004). Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conservation Biology, 18, 167-173.CrossRefGoogle Scholar
  61. Takeuchi, K., Brown, R.D., Washitani, I., Tsunekawa, A. and Yokohari, M. (2003). Satoyama: The Traditional Rural Landscape of Japan. Springer-Verlag, Tokyo.Google Scholar
  62. ter Braak, C.J.F., and šmilauer, P. (2002). CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, New York.Google Scholar
  63. Thiele, H.U. (1977). Carabid Beetles in Their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behavior. Springer-Verlag, Berlin.Google Scholar
  64. Turin, H., Alders, P.J., den Boer, P.J., van Essen, S., Hejierman, T., Laane, W. (1991). Ecological characterization of carabid species (Coleoptera, Carabidae) in the Nehterlands from thirty years of pitfall sampling. Tijdschrift voor Entomologie, 134, 279-304.Google Scholar
  65. Washitani, I. (2001). Traditional sustainable ecosystem ’SATOYAMA’ and biodiversity crisis in Japan: conservation ecological perspective. Global Environmental Research, 5, 119-133.Google Scholar
  66. Wilson, E.O. (1987). The little things that run the world (the importance and conservation of invertebrates). Conservation Biology, 1, 344-346.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • S.-I. Tanabe
    • 1
  • S.K. Kholin
    • 2
  • Y.-B. Cho
    • 3
  • S.-I. Hiramatsu
    • 4
  • A. Ohwaki
    • 5
  • S. Koji
    • 5
  • A. Higuchi
    • 6
  • S.Y. Storozhenko
    • 2
  • S. Nishihara
    • 7
  • K. Esaki
    • 8
  • K. Kimura
    • 1
  • K. Nakamura
    • 1
  1. 1.Institute of Nature and Environmental TechnologyKanazawa UniversityKanazawa 920-1192Japan
  2. 2.Institute of Biology and Soil Science Far Eastern Branch of the Russian Academy of SciencesRussia
  3. 3.Natural History MuseumHannam UniversityKorea
  4. 4.Shiramine Elementary SchoolJapan
  5. 5.Faculty of ScienceKanazawa UniversityJapan
  6. 6.Satoyama Nature School of KakumaKanazawa UniversityJapan
  7. 7.Graduate School of Agricultural and Life SciencesTokyo UniversityJapan
  8. 8.Ishikawa Forest Experiment StationJapan

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