Co-occurrence pattern of ground beetle (Coleoptera, Carabidae) assemblages along pollution gradient in scotch pine forest

Abstract

Over the last 30 years there has been a great deal of interest in investigating patterns of species co-occurrence across space and time, which may be shaped by interspecific competition for shared resources. A good model of co-occurrence mechanisms is developed among predatory animals along a pollution gradient, where shared resources become more limited in more contaminated areas and the energy budget for detoxification is much higher. Community disassembly by heavy metal pollution may occur when the presence of toxic elements shifts patterns of species co-occurrence from structured to random. On the other hand, limited resources on a pollution gradient should lead to higher competition between dominant species. Disassembly may entail the loss of existing co-evolved interactions among species, which has ramifications for community dynamics and the quality of the functioning of polluted ecosystems. We expect an assemblage dominated by competitive species interactions to exhibit a significant segregation of taxa, whereas one dominated by mutualistic or syntrophic interactions would exhibit an aggregation of taxa. Responses of Carabidae co-occurrence patterns and changes in body size measures to heavy metal concentrations were investigated in a zinc contamination gradient in a Scots pine forest in the vicinity of Olkusz (southern Poland), at 12 study sites. The zinc concentration in the humus layer varied between 108 mg kg−1 dw to 6150 mg kg−1 dw. We used the C-score index, between all possible species pairs in a matrix. The ground beetle assemblages from the reference sites showed a significant segregation pattern. Community disassembly occurred only among assemblages in heavily polluted sites. The average value of skewness and kurtosis were significantly higher in the highly contaminated sites, indicating the greater proportion of small-bodied species in contaminated areas. The Gini coefficient was highest in the low contaminated sites, indicating the body-size inequality of carabid assemblages was greatest in the uncontaminated areas. Our data suggest that increased pollution contributes to the extinction of sensitive forest specialists with large body size and higher competitive abilities, leading to replacement by less sensitive generalists, with smaller body size and that the co-occurrence of species on heavily polluted sites is a result of unstable interactions between species in communities.

Abbreviations

L:

low contaminated localities

H:

high contaminated localities

References

  1. Aleksandrowicz, O.R. 2004. Biegaczowate (Carabidae). In: Bogdanowicz, W., E. Chudzińska, I. Pilipiuk, and E. Skibińska (eds.), Fauna Polski – charakterystyka i wykaz gatunków. Muzeum i Instytut Zoologii PAN. Warszawa. I: 28–42 [In Polish].

    Google Scholar 

  2. Azeria, E.T., J. Ibarzabal and C. Hébert. 2012. Effects of habitat characteristics and interspecific interactions on co-occurence patterns of saproxylic beetles breeding in tree boles after forest fire: null model analyses. Oecologia 168:1123–1135.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Banado, E.I., H.A. Regidor, H.A. Nú̉nez, R. Acosta and E. Gianoli. 2005. Species richness and structure of ants communities in a dynamic archipelago: effects of island area and age. J. Biogeogr. 32:221–227.

    Article  Google Scholar 

  4. Bayley, M., E. Baatrup, U. Heimbach and P. Bjerregaard. 1995. Elevated Cooper Levels during larval development cause altered locomotor behavior in the adult carabid beetle Pterostichus cupreus L. (Coleoptera: Carabidae). Ecotoxicol. Environ.Safety 32:166–170.

    CAS  Google Scholar 

  5. Bednarska, A.J., I. Portka, P.E. Kramarz and R. Laskowski. 2009. Combined effect of environmental pollutants (nickel, chlorpyrifos) and temperature on the ground beetle, Pterostichus oblongopunctatus (Coleoptera: Carabidae). Environ. Toxicol. Chem. 28:864–872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bednarska, A.J. and R. Laskowski. 2009. Environmental conditions enhance toxicant effects in larvae of the ground beetle Pterostichus oblongopunctatus (Coleoptera: Carabidae). Environ. Pollution 157:1597–1602.

    Article  CAS  Google Scholar 

  7. Blick, R.A.J. and K.C Burns. 2011. Liana co-occurrence patterns in a temperate rainforest. J. Veg. Sci. 22:868–877.

    Article  Google Scholar 

  8. Bonari, G., M. Migliorini, M. Landi, G. Protano, P.P. Fanciulli and C. Angiolini. 2017. Concordance between plant species, oribatid mites and soil in Mediterranean stone pine forest. Arthropod-Plant Interaction 11:61–69.

    Article  Google Scholar 

  9. Brandl R. and W. Topp. 1985. Size structure of Pterostichus spp. (Carabidae): aspects of competition. Oikos 44:234–238.

    Google Scholar 

  10. Butovsky, R.O. 2011. Heavy metals in carabids (Coleoptera, Carabidae). In: Kotze DJ, Assmann T, Noordijk J, Turin H, Vermeulen R (eds.), Carabid beetles as bioindicators: biogeographical, ecological and environmental studies. ZooKeys 100:215–222.

    Google Scholar 

  11. Chase, J.M. and M.A. Leibold. 2003. Ecological Niches. Linking Classical and Contemporary Approaches. University of Chicago Press, Chicago, IL.

    Book  Google Scholar 

  12. Clarke, K.R. 1993. Non-parametric multivariate analysis of changes in community structure. Aust. J. Ecol. 18:117–143.

    Article  Google Scholar 

  13. Cody, M. L. and J. M. Diamond (eds). 1975. Ecology and Evolution of Communities. Harvard University Press, Cambridge., New York.

  14. Diamond, J. M. 1975. Assembly of species communities. In: M. L. Cody and J. M. Diamond (eds), Ecology and Evolution of Communities. Harvard University Press, Cambridge, MA, USA, pp. 342–444.

    Google Scholar 

  15. Fountain, M.T. and S.P. Hopkins. 2004. A comparative study of the effects of metal contamination in Collembola in the field and in the laboratory. Ecotoxicology 13:573–587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gadd, G. M. 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gall J.E., R.S. Boyd and N. Rajakaruna. 2015. Transfer of heavy metals through terrestrial food webs: a review. Environ. Monit. Assess. 187:201–222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Gallagher, F., I. Pechmann, J.E. Bogden, J. Grabosky and P. Weis. 2008. Soil metal concentartions and productivity of Betula populifolia (gray birch) as measured by field spectometry and incremental annula growth in an abandoned urban Brownfield in New Jersey. Environ. Pollut. 156:699–706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gotelli, N.J. 2000. Null model analysis of species co-occurence patterns. Ecology 81:2606–2621.

    Article  Google Scholar 

  20. Grześ, I.M. 2010. Zinc tolerance in the ant species Myrmica rubra originating from a metal pollution gradient. Eur. J. Soil Biol. 46:87–90.

    Article  CAS  Google Scholar 

  21. Hammer, Ø., D.A.T Harper and P.D. Ryan. 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4:9.

    Google Scholar 

  22. Hedde, M., F. van Oort and I. Lamy 2012. Functional traits of soil invertebrates as indicators for exposure to soil disturbance. Environ. Pollut. 164:59–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Heino, J. 2009. Species co-occurence, nestedness and guild- environment relationships in stream macroinvertebrates. Freshw.Biol. 54:1947–1959.

    Article  Google Scholar 

  24. Holmstrup, M., A.M. Bindesbøl, G.J. Oostingh, A. Duschl, V. Scheil, H.R. Köhler, S. Loureiro, A.M. Soares, A.L. Ferreira, C. Kienle, A. Gerhardt, R. Laskowski, P. Kramarz, M. Bayley, C. Svendsen and D.J. Spurgeon. 2010. Interactions between effects of environmental chemicals and natural stressors: a review. Sci. Total Environ. 408(18):3746–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hurka, K. 1996. Carabidae of the Czech and Slowak Republics. Kabourek, Zlin.

  26. Koivula, M. 2011. Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys 100:287–317.

    Article  Google Scholar 

  27. Magura, T, B. Tóthmérész and G. Lövei. 2006. Body size inequality of carabids along an urbanisation gradient. Basic Appl. Ecol. 7:472–482.

    Article  Google Scholar 

  28. Maryański, M., P. Kramarz, R. Laskowski and M. Niklińska. 2002. Decreased energetic reserves, morphological changes and accumulation of metals in Carabid Beetles (Poecilus cupreus L.) exposed to Zinc- or Cadmium- contaminated Food. Ecotoxicology 11:127–139.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Migliorini, M., A. Petroli and F. Bernini. 2002. Comparative analysis of two edaphic zoocoenoses (Oribatid mites and Carabid Beetles) in five habitats of the ‘Pietraporciana’ and ‘Lucciolabella’ Nature Reserves (Orcia Valley, cenral Italy). Acta Oecol. 23:361–374.

    Article  Google Scholar 

  30. Migliorini, M., G. Pigino, T. Caruso, P.P. Fanciulli, C. Leonzio and F. Bernini. 2005. Soil communities (Acari Oribatida; Hexapoda Collembola) in a clay pigeon shooting range. Pedobiologia 49:1–13.

    Article  Google Scholar 

  31. Minor, M.A. 2011. Spatianl patterns and local diversity in soil oribatid mites (Acari: Oribatida) in three pine plantation forest. Eur. J. Soil Biol. 47:122–128.

    Article  Google Scholar 

  32. Możdżer, J.T., P. Kramarz, A. Piśkiewicz and M. Niklińska. 2003. Effects of cadmium and zinc on larval growth and survival in the ground beetle, Pterostichus oblongopunctatus. Environ. Int. 28:737–742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Niemelä, J. and D.J. Kotze. 2009. Carabid beetle assemblages along urban to rural gradients: A review. Landsc. Urban Plan. 92:65–71.

    Article  Google Scholar 

  34. Pitzalis, M., L. Luiselli and M.A. Bologna. 2010. Co-occurence analyses show that non-random community structure is disrupted by fire in two groups of soil arthropods (Isopoda Oniscidea and Collembola). Acta Oceol. 36:100–106.

    Article  Google Scholar 

  35. Ribera, I., S. Doledec, I.S. Downie and G.N. Foster. 2001. Effect of land disturbance and stress on species traits of ground beetles assemblages. Ecology 82:1112–1129.

    Article  Google Scholar 

  36. Sanders, N.J., N.J. Gotelli, N.E. Heller and D.M. Gordon. 2003. Community disassembly by an invasive species. Proc. Nat. Acad. Sci. USA 100:2474–2477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sanders, N.J., N.J., Gotelli, S.E. Wittman, J.S. Ratchford, A.M. Ellison and E.S. Jules. 2007. Assembly rules for ant communities across spatial scales and habitats. J. Biogeogr. 34:1632–1641.

    Article  Google Scholar 

  38. Šerić Jelaska L. and P. Durbesić. 2009. Comparison of the body size and wing form of carabid species (Coleoptera: Carabidae) between isolated and continuous forest habitats. Ann. soc. entomol. Fr. (n.s.). 45 (3):327–338.

    Article  Google Scholar 

  39. Skalski, T, D. Stone, P. Kramarz and R. Laskowski. 2010. Ground beetle community responses to heavy metal contamination. Baltic J. Coleopterol. 10(1):1 – 12.

    Google Scholar 

  40. Skalski, T, K. Gargasz and R. Laskowski. 2011. Does of mixed diffuse pollution degrease ground beetle diversity? Baltic J. Coleopterol. 11(1):1–15.

    Google Scholar 

  41. Skalski, T, R. Kędzior, D. Kolbe and S. Knutelski. 2015a. Ground beetles as indicators of heavy metal pollution in forests. Sylwan 159:905–911.

    Google Scholar 

  42. Skalski, T., R. Kędzior, D. Kolbe and S. Knutelski. 2015b. Different responses of epigeic beetles to heavy metal contamination depending on functional traits at the family level. Baltic J. Coleopterol. 15(2):81–90.

    Google Scholar 

  43. Skłodowski, J. 2014. Consequence of the transformation of a primeval forest into a managed forest for carabid beetles (Coleoptera: Carabidae) — a case study from Białowieża (Poland). Eur. J. Entomolo. 111(5):639–648.

    Article  Google Scholar 

  44. Sota, T. 1987. Mortality pattern and age structure in two carabid populations with different seasonal life cycles. Res. Popul. Ecol. 29:237–254.

    Article  Google Scholar 

  45. Spurgeon, D.J. and S.P. Hopkin. 1996. Effects of metal-contaminated soils on the growth, sexual development and early cocoon production of the earthworm Eisenia fetida with particular reference to zinc. Ecotoxicol. Environ. Safety 35:86–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. StatSoft. 2012. STATISTICA (data analysis software system), version 12.0. http://www.statsoft.com.

  47. Stefanowicz, A.M., M. Niklińska and R. Laskowski. 2008. Metals affect soil bacterial and fungal functional diversity differently. Environ. Toxicol. Chem. 27:591–598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stone, L. and A. Roberts. 1990. The checkerboard score and species distributions. Oecologia 85:74–79.

    Article  Google Scholar 

  49. Stone, D., P. Jepson, P. Kramarz and R. Laskowski. 2001. Time to death response in carabid beetles exposed to multiple stressors along a gradient of heavy metal pollution. Environ. Pollut. 113:239–244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Szafer, W. and K. Zarzycki. 1972. Szata roślinna Polski. Tom II, PWN, Warszawa.

    Google Scholar 

  51. Szyszko, J. 1983. Methods of macrofauna investigations. In: Szujecki A, Szyszko J, Mazur S, Perliński S (eds). The Process of Forest Soil Macrofauna Formation after Afforestation of Farmland. Warsaw Agricultural University Press, Warsaw. pp. 10–16.

    Google Scholar 

  52. Thiele, H.U. 1977. Carabid Beetles in their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behavior. Springer, Stuttgart.

    Book  Google Scholar 

  53. Ulrich, W. and H.J. Gotelli. 2007. Null model analysis of species nestedness patterns. Ecology 88:1824–1831.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Ulrich, W., K. Komosiński and M. Zalewski. 2008. Body size and biomass distributions of carrion visiting beetles: do cities host smaller species? Ecol. Res. 23:241–248.

    Google Scholar 

  55. Żmudzki, S. and R. Laskowski. 2012. Biodiversity and structure of spider communities along a metal pollution gradient. Ecotoxicology 21:1523–1532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by DS-3337/KEKiOP.

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Correspondence to R. Kędzior.

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Kędzior, R., Kosewska, A. & Skalski, T. Co-occurrence pattern of ground beetle (Coleoptera, Carabidae) assemblages along pollution gradient in scotch pine forest. COMMUNITY ECOLOGY 19, 148–155 (2018). https://doi.org/10.1556/168.2018.19.2.7

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Keywords

  • Body size
  • Carabidae
  • Contamination
  • C-score
  • Heavy metals