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.
Keywords
Body size Carabidae Contamination C-score Heavy metalsAbbreviations
- L
low contaminated localities
- H
high contaminated localities
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Acknowledgments
This study was supported by DS-3337/KEKiOP.
References
- 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
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.Google Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefGoogle Scholar
- Blick, R.A.J. and K.C Burns. 2011. Liana co-occurrence patterns in a temperate rainforest. J. Veg. Sci. 22:868–877.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Brandl R. and W. Topp. 1985. Size structure of Pterostichus spp. (Carabidae): aspects of competition. Oikos 44:234–238.Google Scholar
- 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
- Chase, J.M. and M.A. Leibold. 2003. Ecological Niches. Linking Classical and Contemporary Approaches. University of Chicago Press, Chicago, IL.CrossRefGoogle Scholar
- Clarke, K.R. 1993. Non-parametric multivariate analysis of changes in community structure. Aust. J. Ecol. 18:117–143.CrossRefGoogle Scholar
- Cody, M. L. and J. M. Diamond (eds). 1975. Ecology and Evolution of Communities. Harvard University Press, Cambridge., New York.Google Scholar
- 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
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Gadd, G. M. 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Gotelli, N.J. 2000. Null model analysis of species co-occurence patterns. Ecology 81:2606–2621.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Heino, J. 2009. Species co-occurence, nestedness and guild- environment relationships in stream macroinvertebrates. Freshw.Biol. 54:1947–1959.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Hurka, K. 1996. Carabidae of the Czech and Slowak Republics. Kabourek, Zlin.Google Scholar
- Koivula, M. 2011. Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys 100:287–317.CrossRefGoogle Scholar
- Magura, T, B. Tóthmérész and G. Lövei. 2006. Body size inequality of carabids along an urbanisation gradient. Basic Appl. Ecol. 7:472–482.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Niemelä, J. and D.J. Kotze. 2009. Carabid beetle assemblages along urban to rural gradients: A review. Landsc. Urban Plan. 92:65–71.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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.CrossRefGoogle Scholar
- Sota, T. 1987. Mortality pattern and age structure in two carabid populations with different seasonal life cycles. Res. Popul. Ecol. 29:237–254.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- StatSoft. 2012. STATISTICA (data analysis software system), version 12.0. http://www.statsoft.com.
- Stefanowicz, A.M., M. Niklińska and R. Laskowski. 2008. Metals affect soil bacterial and fungal functional diversity differently. Environ. Toxicol. Chem. 27:591–598.CrossRefPubMedPubMedCentralGoogle Scholar
- Stone, L. and A. Roberts. 1990. The checkerboard score and species distributions. Oecologia 85:74–79.CrossRefGoogle Scholar
- 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.CrossRefPubMedPubMedCentralGoogle Scholar
- Szafer, W. and K. Zarzycki. 1972. Szata roślinna Polski. Tom II, PWN, Warszawa.Google Scholar
- 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
- Thiele, H.U. 1977. Carabid Beetles in their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behavior. Springer, Stuttgart.CrossRefGoogle Scholar
- Ulrich, W. and H.J. Gotelli. 2007. Null model analysis of species nestedness patterns. Ecology 88:1824–1831.CrossRefPubMedPubMedCentralGoogle Scholar
- 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
- Żmudzki, S. and R. Laskowski. 2012. Biodiversity and structure of spider communities along a metal pollution gradient. Ecotoxicology 21:1523–1532.CrossRefPubMedPubMedCentralGoogle Scholar
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