Abstract
It has been proposed that communities change from r to K strategies during primary succession. However, because strong-flying organisms are expected to arrive first in newly created habitats and they show trait characteristics associated more often with K strategies, we hypothesized that the r to K trajectories would be more closely followed by flightless and poorly-flying organisms. Moreover, we expected that macroinvertebrate communities would converge in their functional composition due to deterministic forces while diverging as taxonomic assemblages due to stochastic drift and biotic interactions. However, we also expected that dispersal abilities of the organisms would affect these tendencies. To address these issues, macroinvertebrates were sampled from isolated manmade ponds of different ages (1–22 years old) constructed at reclaimed opencast coal mines. In accordance with our expectations, only flightless and poorly-flying organisms exhibited a slight shift from r to K strategies, the community taxonomically diverged along the primary succession gradient, and stochastic drift showed greater effects on strong-flying organisms. In contrast, the community did not converge in its functional composition. The weak differences observed among the macroinvertebrates from ponds of different ages suggested that limiting environmental conditions prevented the organisms from evolving to a more structured community.



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References
Arle, J. & F. Wagner, 2013. Effects of anthropogenic salinisation on the ecological status of macroinvertebrate assemblages in the Werra River (Thuringia, Germany). Hydrobiologia 701: 129–148.
Barnes, L., 1983. The colonization of ball-clay ponds by macroinvertebrates and macrophytes. Freshwater Biology 13: 561–578.
Bêche, L. A., E. P. Mcelravy & V. H. Resh, 2006. Long-term seasonal variation in the biological traits of benthic-macroinvertebrates in two Mediterranean-climate streams in California, U.S.A. Freshwater Biology 51: 56–75.
Belyea, L. R. & J. Lancaster, 1999. Assembly rules within a contingent ecology. Oikos 86: 402–416.
Bilton, D. T., J. R. Freeland & B. Okamura, 2001. Dispersal in freshwater invertebrates. Annual Review of Ecology and Systematics 32: 159–181.
Bloechl, A., S. Koenemann, B. Philippi & A. Melber, 2010. Abundance, diversity and succession of aquatic Coleoptera and Heteroptera in a cluster of artificial ponds in the North German Lowlands. Limnologica – Ecology and Management of Inland Waters 40: 215–225.
Boix, D., J. Sala, X. D. Quintana & R. Moreno-Amich, 2004. Succession of the animal community in a Mediterranean temporary pond. Journal of the North American Benthological Society 23: 29–49.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789.
Cañedo-Argüelles, M. & M. Rieradevall, 2011. Early succession of the macroinvertebrate community in a shallow lake: response to changes in the habitat condition. Limnologica – Ecology and Management of Inland Waters 41: 363–370.
Chase, J. M., 2003. Community assembly: when should history matter? Oecologia 136: 489–498.
Chevenet, F., S. Doledec & D. Chessel, 1994. A fuzzy coding approach for the analysis of long-term ecological data. Freshwater Biology 31: 295–309.
Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.
Clarke, K. R., & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. Plymouth, UK.
Clarke, K. R. & R. H. Green, 1988. Statistical design and analysis for a biological effects study. Marine Ecology: Progress Series 46: 213–226.
Clarke, K. & R. Warwick, 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Marine Ecology Progress Series 216: 265–278.
Clements, F. E., 1916. Plant Succession: An Analysis of the Development of Vegetation. Carnegie Institution of Washington, Washington.
Clements, W. H., 1994. Benthic invertebrate community responses to heavy metals in the upper Arkansas River Basin, Colorado. Journal of the North American Benthological Society 13: 30–44.
Cravotta, C., 2008. Dissolved metals and associated constituents in abandoned coal-mine discharges, Pennsylvania, USA. Part 1: constituent quantities and correlations. Applied Geochemistry 23: 166–202.
De Bie, T., L. De Meester, L. Brendonck, K. Martens, B. Goddeeris, D. Ercken, H. Hampel, L. Denys, L. Vanhecke, K. Van der Gucht, J. Van Wichelen, W. Vyverman & S. A. J. Declerck, 2012. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecology Letters 15: 740–747.
Diamond, J. M., 1975. Assembly of species communities. In Cody, M. L. & J. M. Diamond (eds), Ecology and Evolution of Communities. Harvard University Press, Cambridge: 342–444.
Drake, J. A., 1991. Community-assembly mechanics and the structure of an experimental species ensemble. The American Naturalist 137: 1–26.
Fairchild, G. W., A. M. Faulds & J. F. Matta, 2000. Beetle assemblages in ponds: effects of habitat and site age. Freshwater Biology 44: 523–534.
Florencio, M., C. Díaz-Paniagua, L. Serrano & D. T. Bilton, 2010. Spatio-temporal nested patterns in macroinvertebrate assemblages across a pond network with a wide hydroperiod range. Oecologia 166: 469–483.
Flory, E. A. & A. M. Milner, 2000. Macroinvertebrate community succession in Wolf Point Creek, Glacier Bay National Park, Alaska. Freshwater Biology 44: 465–480.
Fukami, T. & D. A. Wardle, 2005. Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proceedings of the Royal Society B: Biological Sciences 272: 2105–2115.
Gleason, H. A., 1927. Further views on the succession-concept. Ecology 8: 299–326.
Gutiérrez, L. T. & W. R. Fey, 1980. Ecosystem Succession: A General Hypothesis and a Test Model of a Grassland. MIT Press, Cambridge, MA.
Harrison, S. S. C., & M. Dobson, 2008. Evolutionary drivers and the ecological traits of adult: aquatic insects In Lancaster, J. & R. A. Briers (eds), Aquatic Insects: Challenges to Populations. Proceedings of the Royal Entomological Society’s 24th Symposium. CABI International, Wallingford/Cambridge: 250–267.
Hassall, C., J. Hollinshead & A. Hull, 2012. Temporal dynamics of aquatic communities and implications for pond conservation. Biodiversity and Conservation 21: 829–852.
Jeffries, M., 1989. Measuring Tailing’s “element of chance in pond populations”. Freshwater Biology 20: 383–393.
Jeffries, M. J., 2002. Evidence for individualistic species assembly creating convergent predator:prey ratios among pond invertebrate communities. Journal of Animal Ecology 71: 173–184.
Jenkins, D. G., C. R. Brescacin, C. V. Duxbury, J. A. Elliott, J. A. Evans, K. R. Grablow, M. Hillegass, B. N. Lyon, G. A. Metzger, M. L. Olandese, D. Pepe, G. A. Silvers, H. N. Suresch, T. N. Thompson, C. M. Trexler, G. E. Williams, N. C. Williams & S. E. Williams, 2007. Does size matter for dispersal distance? Global Ecology and Biogeography 16: 415–425.
Jonsson, T., J. E. Cohen & S. R. Carpenter, 2005. Food webs, body size, and species abundance in ecological community description. In Caswell, H. (ed.), Advances in Ecological Research. Academic Press, San Diego: 1–84.
Lake, P. S., I. A. E. Bayly & D. W. Monton, 1989. The phenology of a temporary pond in western Victoria, Australia, with special reference to invertebrate succession. Archiv für Hydrobiologie 115: 171–202.
Lawrence, J. E., K. B. Lunde, R. D. Mazor, L. A. Bêche, E. P. McElravy & V. H. Resh, 2010. Long-term macroinvertebrate responses to climate change: implications for biological assessment in mediterranean-climate streams. Journal of the North American Benthological Society 29: 1424–1440.
MacArthur, R. H., & E. O. Wilson, 1967. Theory of Island Biogeography. Princeton University Press, Princeton.
Majer, J. D. & O. Nichols, 1998. Long-term recolonization patterns of ants in Western Australian rehabilitated bauxite mines with reference to their use as indicators of restoration success. Journal of Applied Ecology 35: 161–182.
Malmqvist, B., 2002. Aquatic invertebrates in riverine landscapes. Freshwater Biology 47: 679–694.
Margalef, R., 1968. Perspectives in Ecological Theory. University of Chicago Press, Chicago.
Masters, Z., I. Peteresen, A. G. Hildrew & S. J. Ormerod, 2007. Insect dispersal does not limit the biological recovery of streams from acidification. Aquatic Conservation: Marine and Freshwater Ecosystems 17: 375–383.
Mellado-Díaz, A., M. L. Suárez Alonso & M. R. Vidal-Abarca Gutiérrez, 2008. Biological traits of stream macroinvertebrates from a semi-arid catchment: patterns along complex environmental gradients. Freshwater Biology 53: 1–21.
Merricks, T. C., D. S. Cherry, C. E. Zipper, R. J. Currie & T. W. Valenti, 2007. Coal-mine hollow fill and settling pond influences on headwater streams in southern West Virginia, USA. Environmental Monitoring and Assessment 129: 359–378.
Nicola, G. G., A. Almodóvar & B. Elvira, 2010. Effects of environmental factors and predation on benthic communities in headwater streams. Aquatic Sciences 72: 419–429.
Noon, K. F., 1996. A model of created wetland primary succession. Landscape and Urban Planning 34: 97–123.
Odum, E. P., 1969. The strategy of ecosystem development. Science 164: 262–270.
Palmer, M., E. Bernhardt, W. Schlesinger, K. Eshleman, E. Foufoula-Georgiou, M. Hendryx, A. Lemly, G. Likens, O. Loucks, M. Power, P. White & P. Wilcock, 2010. Mountaintop mining consequences. Science 327: 148–149.
Poff, N. L., 1997. Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. Journal of the North American Benthological Society 16: 391–409.
Pond, G. J., M. E. Passmore, F. A. Borsuk, L. Reynolds & C. J. Rose, 2008. Downstream effects of mountaintop coal mining: comparing biological conditions using family- and genus-level macroinvertebrate bioassessment tools. Journal of the North American Benthological Society 27: 717–737.
Proctor, H. & A. Grigg, 2006. Aquatic invertebrates in final void water bodies at an open-cut coal mine in central Queensland. Australian Journal of Entomology 45: 107–121.
R Core Team, 2012. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
Roff, D. A., 1990. The evolution of flightlessness in insects. Ecological Monographs 60: 389–421.
Ruhí, A., D. Boix, J. Sala, S. Gascón & X. D. Quintana, 2009. Spatial and temporal patterns of pioneer macrofauna in recently created ponds: taxonomic and functional approaches. Hydrobiologia 634: 137–151.
Ruhí, A., J. Herrmann, S. Gascón, J. Sala, J. Geijer & D. Boix, 2012. Change in biological traits and community structure of macroinvertebrates through primary succession in a man-made Swedish wetland. Freshwater Science 31: 22–37.
Ruhí, A., D. Boix, S. Gascón, J. Sala & X. D. Quintana, 2013. Nestedness and successional trajectories of macroinvertebrate assemblages in man-made wetlands. Oecologia 171: 545–556.
Saglam, I. K., D. A. Roff & D. J. Fairbairn, 2008. Male sand crickets trade-off flight capability for reproductive potential. Journal of Evolutionary Biology 21: 997–1004.
Samuels, C. L. & J. A. Drake, 1997. Divergent perspectives on community convergence. Trends in Ecology & Evolution 12: 427–432.
Schneider, D. W. & T. M. Frost, 1996. Habitat duration and community structure in temporary ponds. Journal of the North American Benthological Society 15: 64.
Sim, L. L., J. A. Davis, K. Strehlow, M. McGuire, K. M. Trayler, S. Wild, P. J. Papas & J. O’Connor, 2013. The influence of changing hydroregime on the invertebrate communities of temporary seasonal wetlands. Freshwater Science 32: 327–342.
Southwood, T. R. E., 1977. Habitat, the templet for ecological strategies? Journal of Animal Ecology 46: 337–365.
Statzner, B., S. Dolédec & B. Hugueny, 2004. Biological trait composition of European stream invertebrate communities: assessing the effects of various trait filter types. Ecography 27: 470–488.
Tachet, H., P. Richoux, M. Bournaud & P. Usseglio-Polatera, 2000. Invertébrés d’eau douce: Systématique, Biologie, Écologie. CNRS Editions, Paris.
Tischendorf, L., D. J. Bender & L. Fahrig, 2003. Evaluation of patch isolation metrics in mosaic landscapes for specialist vs. generalist dispersers. Landscape Ecology 18: 41–50.
Townsend, C. R. & A. G. Hildrew, 1994. Species traits in relation to a habitat templet for river systems. Freshwater Biology 31: 265–275.
Townsend, C., S. Dolédec & M. Scarsbrook, 1997. Species traits in relation to temporal and spatial heterogeneity in streams: a test of habitat templet theory. Freshwater Biology 37: 367–387.
Velasco, J., A. Millán & L. Ramírez Díaz, 1993. Colonización y sucesión de nuevos medios acuáticos. I. Composición y estructura de las comunidades de insectos. Limnetica 9: 73–86.
Verberk, W. C. E. P., H. Siepel & H. Esselink, 2008. Life-history strategies in freshwater macroinvertebrates. Freshwater Biology 53: 1722–1738.
Walker, L. R., D. A. Wardle, R. D. Bardgett & B. D. Clarkson, 2010. The use of chronosequences in studies of ecological succession and soil development. Journal of Ecology 98: 725–736.
Warton, D. I., S. T. Wright & Y. Wang, 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3: 89–101.
Weiher, E., G. D. P. Clarke & P. A. Keddy, 1998. Community assembly rules, morphological dispersion, and the coexistence of plant species. Oikos 81: 309–322.
Wellborn, G. A., D. K. Skelly & E. E. Werner, 1996. Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics 27: 337–363.
Woodward, G. & A. G. Hildrew, 2002. Body-size determinants of niche overlap and intraguild predation within a complex food web. Journal of Animal Ecology 71: 1063–1074.
Young, T. P., J. M. Chase & R. T. Huddleston, 2001. Community succession and assembly comparing, contrasting and combining paradigms in the context of ecological restoration. Ecological Restoration 19: 5–18.
Zedler, J. B. & J. C. Callaway, 1999. Tracking wetland restoration: do mitigation sites follow desired trajectories? Restoration Ecology 7: 69–73.
Acknowledgments
This work was supported by a research and assistance agreement between Endesa S.A and the Pyrenean Institute of Ecology-CSIC. The first author was the recipient of a Ph.D. grant from the Government of Aragón (Spain). The authors are grateful to the people working at the Endesa mines of Teruel, and to our fieldwork assistants. Finally, the authors would like to thank to Dr. Jeffries, and the other anonymous reviewer for their helpful comments on a previous version of this manuscript.
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Miguel-Chinchilla, L., Boix, D., Gascón, S. et al. Taxonomic and functional successional patterns in macroinvertebrates related to flying dispersal abilities: a case study from isolated manmade ponds at reclaimed opencast coal mines. Hydrobiologia 732, 111–122 (2014). https://doi.org/10.1007/s10750-014-1851-3
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DOI: https://doi.org/10.1007/s10750-014-1851-3


