Eur. J. Entomol. 116: 309-319, 2019 | DOI: 10.14411/eje.2019.034

Altitudinal gradient in species richness and composition of dung beetles (Coleoptera: Scarabaeidae) in an eastern Euro-Mediterranean locality: Functional, seasonal and habitat influencesOriginal article

Yakup ªENYÜZ1, Jorge M. LOBO2,*, Kemal DINDAR1
1 Kütahya Dumlupinar University, Faculty of Art and Science, Department of Biology, Kütahya, Turkey; e-mails: yakupsenyuz@gmail.com, kemaldindar@gmail.com
2 Dep. Biogeography and Global Change, Museo Nacional de Ciencias Naturales, CSIC. c/ José Gutiérrez Abascal 2, 28006, Madrid, Spain; e-mail: Jorge.Lobo@mncn.csic.es

The altitudinal gradient in diversity of dung beetles (Scarabaeidae) was studied in a Mediterranean mountain chain located in Central Anatolia to (i) determine if there are altitudinal differences between the main taxonomic groups, (ii) describe the seasonal variations in these assemblages and (iii) assess whether closed habitats influence dung beetle diversity differentially at different altitudes. Beetles were collected throughout a year at 14 localities between 469 and 1810 m above sea level in three different types of habitats. Dung beetle assemblages at 400 to 1200 m did not vary greatly in species richness, abundance and biomass. However, they varied in composition, with the assemblages dominated by species of Scarabaeinae up to 900 m, whereas in the mid-mountain assemblages (from 900 m to 1600 m) the numbers of species of Aphodiinae was higher. The decline with increase in altitude in richness, abundance and biomass of both small and large species of Scarabaeinae up to 1500 m, together with the constancy of these parameters in the case of Aphodiinae, accounts for the changes in the composition from the lowland to mid-mountain localities. Unlike at other Mediterranean localities, the open/closed structure of the habitat only slightly influences these assemblages independently of altitude or season. The general seasonal pattern follows the classical Mediterranean bimodal pattern associated with summer drought, but the patterns are more complex when the seasonal responses of the different groups and at different localities are analysed separately. We propose that the interplay between local climatic conditions (mainly temperature) and evolutionary conserved species preferences accounts for both the current seasonal and altitudinal gradients and the changes in species composition in terms of Aphodiinae and Scarabaeinae.

Keywords: Coleoptera, Scarabaeidae, Scarabaeinae, Aphodiinae, dung beetles, species richness, historical factors, elevational turnover, seasonal variation, habitat, Anatolia

Received: June 24, 2019; Revised: September 11, 2019; Accepted: September 11, 2019; Published online: October 11, 2019  Show citation

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ªENYÜZ, Y., LOBO, J.M., & DINDAR, K. (2019). Altitudinal gradient in species richness and composition of dung beetles (Coleoptera: Scarabaeidae) in an eastern Euro-Mediterranean locality: Functional, seasonal and habitat influences. EJE116, Article 309-319. https://doi.org/10.14411/eje.2019.034
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References

  1. Akman Y. 1995: Türkiye orman vejetasyonu. [Forest Vegetation of Turkey.] Ankara Üniversitesi Fen Fakültesi, Ankara, 448 pp. [in Turkish].
  2. Akman Y. 1999: İklim ve Biyoiklim (Biyoiklim metodlari ve Türkiye iklimleri). [Climate and Bioclimate (Bioclimatic Methods and Turkey Climate).] Kariyer Matbaacilik, Ankara, 350 pp. [in Turkish].
  3. Anlaº S. 2011: Studies on the dung-inhabiting beetles (Insecta: Coleoptera) community of Western Anatolia, Turkey. - Ecol. Balkan. 3: 9-14.
  4. Baraud J. 1977: Coléoptères Scarabaeoidea: Faune de l'Europe occidentale: Belgique, France, Grande-Bretagne, Italie, Péninsule ibérique. Supplément à la Nouvelle Revue d'Entomologie, Vol. 7., Toulouse, 352 pp.
  5. Beck J., McCain C.M., Axmacher J.C., Ashton L.A., Bärtschi F. Brehm G., Choi S.-W., Cizek O., Colwell R.K. & Fiedler K. 2017: Elevational species richness gradients in a hyperdiverse insect taxon: a global meta-study on geometrid moths. - Global Ecol. Biogeogr. 26: 412-424. Go to original source...
  6. Birkett A.J., Blackburn G.A. & Menéndez R. 2018: Linking species thermal tolerance to elevational range shifts in upland dung beetles. - Ecography 41: 1510-1519. Go to original source...
  7. Brown J.H., Gillooly J.F., Allen A.P., Savage V.M. & West G.B. 2004: Toward a metabolic theory of ecology. - Ecology 85: 1771-1789. Go to original source...
  8. Cabrero-Sañudo F.J. & Lobo J.M. 2009: Biogeography of Aphodiinae dung beetles based on the regional composition and distribution patterns of genera. - J. Biogeogr. 36: 1474-1492. Go to original source...
  9. Cambefort Y. & Walter P. 1991: Dung beetles in tropical forests in Africa. In Hanski I. & Cambefort Y. (eds): Dung Beetle Ecology. Princeton University Press, Princeton, NJ, pp. 198-210. Go to original source...
  10. Chamberlain D., Tocco C., Longoni A., Mammola S., Palestrini C. & Rolando A. 2015: Nesting strategies affect altitudinal distribution and habitat use in Alpine dung beetle communities. - Ecol. Entomol. 40: 372-380. Go to original source...
  11. Chown S.L. & Nicolson S. 2004: Insect Physiological Ecology: Mechanisms and Patterns. Oxford University Press, Oxford, 243 pp. Go to original source...
  12. Clarke K.R. & Green R.H. 1988: Statistical design and analysis for a "biological effects" study. - Marine Ecol. Prog. Ser. 46: 213-226. Go to original source...
  13. Clarke K.R. & Gorley R.N. 2015: PRIMER v7: User Manual Tutorial. PRIMER-E, Plymouth, UK.
  14. Colwell R.K. & Lees D.C. 2000: The mid-domain effect: geometric constraints on the geography of species richness. - Trends Ecol. Evol. 15: 70-76. Go to original source...
  15. da Silva P.G., Lobo J.M., Carpintero Hensen M., Vaz-de-Mello F.Z. & Hernández M.I.M. 2018: Altitudinal gradient driving spatial and temporal β-diversity components: turnover and nestedness in subtropical dung beetle assemblages. - Divers. Distrib. 24: 1277-1290. Go to original source...
  16. Davis P.H. 1965: Flora of Turkey and East Aegean Islands. Vol. 1-9. Edinburgh University Press, Edinburgh.
  17. Davis A.L. & Scholtz C.H. 2001: Historical vs. ecological factors influencing global patterns of scarabaeine dung beetle diversity. - Divers. Distrib. 7: 161-174. Go to original source...
  18. Davis A.L., Scholtz C.H. & Chown S.L. 1999: Species turnover, community boundaries and biogeographical composition of dung beetle assemblages across an altitudinal gradient in South Africa. - J. Biogeogr. 26: 1039-1055. Go to original source...
  19. Errouissi F. & Jay-Robert P. 2019: Consequences of habitat change in euromediterranean landscapes on the composition and diversity of dung beetle assemblages (Coleoptera, Scarabaeoidea). - J. Insect Conserv. 23: 15-28. Go to original source...
  20. Escobar F., Lobo J.M. & Halffter G. 2006: Assessing the origin of Neotropical mountain dung beetle assemblages (Scarabaeidae: Scarabaeinae): the comparative influence of vertical and horizontal colonization. - J. Biogeogr. 33: 1793-1803. Go to original source...
  21. Espinoza V.R. & Noriega J.A. 2018: Diversity of the dung beetles (Coleoptera: Scarabaeinae) in an altitudinal gradient in the east slope of los Andes, Napo province, Ecuador. - Neotrop. Biodiver. 4: 144-150. Go to original source...
  22. Foord S.H. & Dippenaar-Schoeman A.S. 2016: The effect of elevation and time on mountain spider diversity: a view of two aspects in the Cederberg mountains of South Africa. - J. Biogeogr. 43: 2354-2365. Go to original source...
  23. Hanski I. 1980: The community of coprophagous beetles (Coleoptera, Scarabaeidae and Hydrophilidae) in northern Europe. - Ann. Entomol. Fenn. 46: 57-73.
  24. Hanski I. 1983: Distributional ecology and abundance of dung and carrion feeding beetles Scarabaeidae in tropical rain forests in Sarawak, Borneo. - Acta Zool. Fenn. 167: 1-45.
  25. Hortal J., Diniz-Filho J.A.F., Bini L.M., Rodriguez M.A., Baselga A., Nogués-Bravo D., Rangel T.F., Hawkins B.A. & Lobo J.M. 2011: Ice age climate, evolutionary constraints and diversity patterns of European dung beetles. - Ecol. Lett. 14: 741-748. Go to original source...
  26. Hsieh T.C., Ma K.H. & Chao A. 2016: iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). - Meth. Ecol. Evol. 7: 1451-1456. Go to original source...
  27. Jay-Robert P., Lobo J.M. & Lumaret J.-P. 1997: Altitudinal turnover and species richness variation in European montane dung beetle assemblages. - Arctic Alpine Res. 29: 196-205. Go to original source...
  28. Jay-Robert P., Lumaret J.-P., Lobo J.M. & André J. 2003: The relationship between body size and population abundance in summer dung beetle communities of South-European mountains (Coleoptera: Scarabaeoidea). - Rev. Ecol. / Terre Vie 58: 307-320. Go to original source...
  29. Jay-Robert P., Lumaret J.-P. & Lebreton J.D. 2008: Spatial and temporal variation of mountain dung beetle assemblages and their relationships with environmental factors (Aphodiinae: Geotrupinae: Scarabaeinae). - Ann. Entomol. Soc. Am. 101: 58-69. Go to original source...
  30. Kadiri N., Lobo J.M. & Lumaret J.-P. 1997: Conséquences de l'interaction entre préférences pour l'habitat et quantité de ressources trophiques sur les communautés d'insectes coprophages (Coleoptera: Scarabaeoidea). - Acta Oecol. 18: 107-119. Go to original source...
  31. Laiolo P., Pato J. & Obeso J.R. 2018: Ecological and evolutionary drivers of the elevational gradient of diversity. - Ecol. Lett. 21: 1022-1032. Go to original source...
  32. Legendre P. & Gallagher E.D. 2001: Ecologically meaningful transformations for ordination of species data. - Oecologia 129: 271-280. Go to original source...
  33. Lobo J.M. 1993: Estimation of dung beetle biomass (Coleoptera: Scarabaeoidea). - Eur. J. Entomol. 90: 235-238.
  34. Lobo J.M. 1997: Influencias geográficas, históricas y filogenéticas sobre la diversidad de las comunidades locales: una revisión y algunos ejemplos utilizando Scarabaeoidea coprófagos (Coleoptera, Laparosticti). - Bol. Asoc. Esp. Entomol. 21: 15-31.
  35. Lobo J.M. 2000: Species diversity and composition of dung beetle (Coleoptera: Scarabaeoidea) assemblages in North America. - Can. Entomol. 132: 307-321. Go to original source...
  36. Lobo J.M. & Halffter G. 2000: Biogeographical and ecological factors affecting the altitudinal variation of mountainous communities of coprophagous beetles (Coleoptera: Scarabaeoidea): a comparative study. - Ann. Entomol. Soc. Am. 93: 115-126. Go to original source...
  37. Lobo J.M., Chehlarov E. & Guéorguiev B. 2007a: Dung beetle assemblage variation with altitude in the Bulgarian Rhodopes Mountains: a comparison. - Eur. J. Entomol. 104: 489-495. Go to original source...
  38. Lobo J.M., Guéorguiev B. & Chehlarov E. 2007b: Convergences and divergences between two European mountain dung beetle assemblages (Coleoptera, Scarabaeoidea). - Anim. Biodiv. Conserv. 30: 83-96. Go to original source...
  39. Lomolino M.V. 2001: Elevation gradients of species-density: historical and prospective views. - Global Ecol. Biogeogr. 10: 3-13. Go to original source...
  40. Lumaret J.-P. & Kirk A. 1987: Ecology of dung beetles in the French Mediterranean region (Coleoptera: Scarabaeidae). - Acta Zool. Mex. 24: 1-55. Go to original source...
  41. Lumaret J.-P. & Kirk A. 1991: South temperate dung beetles. In Hanski I. & Cambefort Y. (eds): Dung Beetle Ecology. Princeton University Press, Princeton, NJ, pp. 97-115. Go to original source...
  42. Lumaret J.-P. & Stiernet N. 1991: Montane dung beetles. In Hanski I. & Cambefort Y. (eds): Dung Beetle Ecology. Princeton University Press, Princeton, NJ, pp. 242-254. Go to original source...
  43. Lumaret J.-P. & Stiernet N. 1992: Biogeography of dung beetle communities in the Western and Central Alps (Coleoptera, Scarabaeoidea). - Biogeografia 16: 425-436. Go to original source...
  44. Lumaret J.-P. & Stiernet N. 1994: Adaptation and evolutive strategies of dung beetles in high mountains (Coleoptera, Scarabaeoidea). - Ecologie 25: 79-86.
  45. Mani M.S. 1968: Ecology and Biogeography of High Altitude Insects. Series Entomologica Vol. 4. Dr. V. Jung, The Hague, 528 pp. Go to original source...
  46. Martín-Piera F. & Lobo J.M. 1996: A comparative discussion of trophic preferences in dung beetle communities. - Anim. Biodiv. Conserv. 19: 13-31.
  47. Martín-Piera F., Veiga C.M. & Lobo J.M. 1992: Ecology and biogeography of dung-beetle communities (Coleoptera, Scarabaeoidea) in an Iberian mountain range. - J. Biogeogr. 19: 677-691. Go to original source...
  48. McCoy E.D. 1990: The distribution of insects along elevational gradients. - Oikos 58: 313-322. Go to original source...
  49. Menéndez R. & Gutiérrez D. 1996: Altitudinal effects on habitat selection of dung beetles (Scarabaeoidea Aphodiidae) in the northern Iberian peninsula. - Ecography 19: 313-317. Go to original source...
  50. Menéndez R., González-Megías A., Jay-Robert P. & Marquéz-Ferrando R. 2014: Climate change and elevational range shifts of dung beetles. - Global Ecol. Biogeogr. 23: 646-657. Go to original source...
  51. Merckx V.S., Hendriks K.P., Beentjes K.K., Mennes C.B., Becking L.E., Peijnenburg K.T., Afendy A., Arumugam N., de Boer H. & Biun A. 2015: Evolution of endemism on a young tropical mountain. - Nature 524: 347-350. Go to original source...
  52. Mongyeh E.T., Philips T.K., Kimbi H.K. & Fokam E.B. 2018: Elevational and possible bushmeat exploitation effects on dung beetle (Scarabaeidae: Scarabaeinae) communities on Mount Cameroon, West Central Africa. - Environ. Entomol. 47: 1072-1082. Go to original source...
  53. Monteith G.B. 1985: Altitudinal transect studies at Cape Tribulation, North Queensland VII. Coleoptera and Hemiptera (Insecta). - Queensl. Nat. 26: 70-80.
  54. Numa C., Lobo J.M. & Verdú J.R. 2012: Scaling local abundance determinants in Mediterranean dung beetles. - Insect Conserv. Diver. 5: 106-117. Go to original source...
  55. Nunes C.A., Braga R.F., Figueira J.E.C., de Siqueira Neves F. & Fernandes G.W. 2016: Dung beetles along a tropical altitudinal gradient: environmental filtering on taxonomic and functional diversity. - PLoS ONE 11: e0157442, 16 pp. Go to original source...
  56. Oommen M.A. & Shanker K. 2005: Elevational species richness patterns emerge from multiple local mechanisms in Himalayan woody plants. - Ecology 86: 3039-3047. Go to original source...
  57. Radtke M.G., da Fonseca C.R.V. & Williamson G.B. 2010: Dung beetle communities: a Neotropical-North Temperate comparison. - Neotrop. Entomol. 39: 19-27. Go to original source...
  58. Ricklefs R.E. 2006: Evolutionary diversification and the origin of the diversity-environment relationship. - Ecology 87: S3-S13. Go to original source...
  59. Romero-Alcaraz E. & Ávila J.M. 2000: Effect of elevation and type of habitat on the abundance and diversity of Scarabaeoid dung beetle (Scarabaeoidea) assemblages in a Mediterranean area from Southern Iberian Peninsula. - Zool. Stud. 39: 351-359.
  60. Rosenzweig M.L. 1995: Species Diversity in Space and Time. Cambridge University Press, New York, 436 pp. Go to original source...
  61. Sinclair B.J., Ferguson L.V., Salehipour-Shirazi G. & MacMillan H.A. 2013: Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. - Integr. Comp. Biol. 53: 545-556. Go to original source...
  62. Sole C.L. & Scholtz C.H. 2010: Did dung beetles arise in Africa? A phylogenetic hypothesis based on five gene regions. - Mol. Phylogenet. Evol. 56: 631-641. Go to original source...
  63. Strömberg C.A. 2011: Evolution of grasses and grassland ecosystems. - Annu. Rev. Earth Planet. Sci. 39: 517-544. Go to original source...
  64. Szewczyk T. & McCain C.M. 2016: A systematic review of global drivers of ant elevational diversity. - PLoS ONE 11: e0155404, 16 pp. Go to original source...
  65. Veiga C.M., Lobo J.M. & Martín-Piera F. 1989: Las trampas pitfall con cebo, sus posibilidades en el estudio de las comunidades coprófagas de Scarabaeoidea (Col.). II. Análisis de efectividad. - Rev. Ecol. Biol. Sol 26: 91-109.
  66. Verdú J.R., Arellano L. & Numa C. 2006: Thermoregulation in endothermic dung beetles (Coleoptera: Scarabaeidae): Effect of body size and ecophysiological constraints in flight. - J. Insect Physiol. 52: 854-860. Go to original source...
  67. Wiens J.J. & Graham C.H. 2005: Niche conservatism: integrating evolution, ecology, and conservation biology. - Annu. Rev. Ecol. Evol. Syst. 36: 519-539. Go to original source...
  68. Zamora J., Verdú J.R. & Galante E. 2007: Species richness in Mediterranean agroecosystems: spatial and temporal analysis for biodiversity conservation. - Biol. Conserv. 134: 113-121. Go to original source...

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