Phylogenetic clustering found in lichen but not in plant communities in European heathlands

Abstract

Species richness is a widespread measure to evaluate the effect of different management histories on plant communities and their biodiversity. However, analysing the phylogenetic structure of plant communities could provide new insights into the effects of different management methods on community assemblages and provide further guidance for conservation decisions. Heathlands require permanent management to ensure the existence of such a cultural landscape. While traditional management with grazing is time consuming, mechanical methods are often applied but their consequences on the phylogenetic community assemblages are still unclear. We sampled 60 vegetation plots in dry sandy heathlands (EU habitat type 2310) in northern Germany stratified by five different heathland management histories: fire, plaggen (turf cutting), mowing, deforestation and intensive grazing. Due to the distant relationship of vascular plants and lichens, we assembled two phylogenetic trees, one for vascular plants and one for lichens. We then calculated phylogenetic diversity (PD) and measures of phylogenetic community structure for vascular plant and lichen communities. Deforested areas supported significantly higher PD values for vascular plant communities. We found that PD was strongly correlated with species richness (SR) but the calculation of rarefied PD was uncorrelated to SR leading to a different ranking of management histories. We observed phylogenetic clustering in the lichen communities but not for vascular plants. Thus, management by mowing and intensive grazing promotes habitat filtering of lichens, while management histories that cause greater disturbance such as fire and plaggen do not seem to affect phylogenetic community structure. The set of management strategies fulfilled the goals of the managers in maintaining a healthy heathland community structure. However, management strategies that cause less disturbance can offer an additional range of habitat for other taxonomic groups such as lichen communities.

Abbreviations

PD:

Phylogenetic Diversity

VNP:

NGO Verein Naturschutzpark

rPD:

rarefied PD

SR:

Species Richness

MPD:

Mean Pairwise phylogenetic distance

NRI:

Net relatedness index

References

  1. Bailey, R.H. 1976. Ecological aspects of dispersal and establishment in lichens. In: Brown, D.H., Hawksworth, D.L. and Bailey , R.H. (eds), Lichenology: Progress and Problems. Academic Press, London. pp. 215–247.

    Google Scholar 

  2. Barclay-Estrup, P. and Gimingham, C.H. 1969. The description and interpretation of cyclical processes in a heath community: I. vegetational change in relation to the calluna cycle. J. Ecol. 57: 737–758.

    Google Scholar 

  3. Bossuyt, B., Honnay, O., Van Stichelen, K., Hermy, M. and Van Assche, J. 2001. The effect of a complex land use history on the restoration possibilities of heathland in central Belgium. Belg. J. Bot. 134: 29–40.

    Google Scholar 

  4. Cadotte, M.W., Cardinale, B.J. and Oakley, T.H. 2008. Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl. Acad. Sci. U.S.A. 105:17012–17017.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cadotte, M.W., Jonathan Davies, T., Regetz, J., Kembel, S.W., Cleland, E. and Oakley, T.H. 2010. Phylogenetic diversity metrics for ccological communities: integrating species richness, abundance and evolutionary history. Ecol. Lett. 13: 96–105.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cavender-Bares, J., Keen, A. and Miles, B. 2006. Phylogenetic structure of Floridian plant communities depends on taxonomic and spatial scale. Ecology 87: 109–122.

    Article  Google Scholar 

  7. Cavender-Bares, J., Kozak, K.H., Fine, P.V.A. and Kembel, S.W. 2009. The merging of community ecology and phylogenetic biology. Ecol. Lett. 12: 693–715.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Cooper, N., Rodríguez, J. and Purvis, A. 2008. A common tendency for phylogenetic overdispersion in mammalian assemblages. Proc. R. Soc. Lond. B Biol. Sci. 275: 2031–2037.

    Article  Google Scholar 

  9. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M., et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36: 465–469.

  10. Dinnage, R. 2009. Disturbance alters the phylogenetic composition and structure of plant communities in an old field system. PLoS ONE 4, e7071.

  11. Egorov, E., Prati, D., Durka, W., Michalski, S., Fischer, M., Schmitt, B., Blaser, S. and Brändle, M. 2014. Does land-use intensification decrease plant phylogenetic diversity in local grasslands? PLOS ONE 9, e103252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Faith, D.P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61: 1–10.

    Article  Google Scholar 

  13. Faith, D.P., Reid, C.A.M. and Hunter, J. 2004. Integrating phylogenetic diversity, complementarity, and endemism for conservation assessment. Conserv. Biol. 18: 255–261.

    Article  Google Scholar 

  14. Fontaine, K.M., Ahti, T. and Piercey-Normore, M.D. 2010. Convergent evolution in Cladonia gracilis and allies. The Lichenologist 42: 323–338.

    Article  Google Scholar 

  15. Gerhold, P., Cahill Jr, J.F., Winter, M., Bartish, I.V. and Prinzing, A. 2015. Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Funct. Ecol. 29: 600–614.

    Article  Google Scholar 

  16. Giraudoux, P. 2009. pgirmess: Data analysis in ecology. R package version 1.5.9.

  17. Grafen, A. 1989. The phylogenetic regression. Philos. Trans. R. Soc. Lond. B Biol. Sci. 326: 119–157.

    Article  CAS  Google Scholar 

  18. Hall, T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.

    CAS  Google Scholar 

  19. Helms, G., Friedl, T. and Rambold, G. 2003. Phylogenetic relationships of the Physciaceae inferred from rDNA sequence data and selected phenotypic characters. Mycologia 95: 1078–1099.

    Article  CAS  Google Scholar 

  20. Helmus, M.R., Bland, T.J., Williams, C.K. and Ives, A.R. 2007. Phylogenetic measures of biodiversity. Am. Nat. 169: E68–E83.

    Article  Google Scholar 

  21. Hülsenbeck, J.P. and Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.

    Article  Google Scholar 

  22. Keienburg, T. and Prüter, J. 2006. Naturschutzgebiet Lüneburger Heide: Erhaltung und Entwicklung einer alten Kulturlandschaft. Mitteilungen Aus NNA 17, 65.

  23. Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D., Blomberg, S.P. and Webb, C.O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463–1464.

    Article  CAS  Google Scholar 

  24. Kuzmina, M. and Ivanova, N. 2011. Amplification for Plants and Fungi. Canadian Centre for DNA barcoding, Guelph, Canada.

    Google Scholar 

  25. Lake, S., Bullock, J.M. and Hartley, S. 2001. Impacts of livestock grazing on lowland heathland in the UK. Engl. Nat. Res. Rep. 422: 143.

    Google Scholar 

  26. Letten, A.D., Keith, D.A. and Tozer, M.G. 2014. Phylogenetic and functional dissimilarity does not increase during temporal heathland succession. Proc. R. Soc. Lond. B Biol. Sci. 281: 20142102.

    Article  Google Scholar 

  27. Londo, G. 1976. The decimal scale for releves of permanent quadrats. Vegetatio 33: 61–64.

    Article  Google Scholar 

  28. Lütkepohl, M. and Kaiser, T. 1997. Die Heidelandschaft. In: Naturschutzgebiet Lüneburger Heide: Geschichte, Ökologie, Naturschutz. Verlag H. M. Hausschild GmbH, Bremen. pp. 87–100.

    Google Scholar 

  29. Mallik, A.U. and Gimingham, C.H. 1985. Ecological effects of heather burning: II. Effects on seed germination and vegetative regeneration. J. Ecol. 73: 633–644.

    Google Scholar 

  30. Mayfield, M.M. and Levine, J.M. 2010. Opposing effects of competitive exclusion on the phylogenetic structure of communities: Phylogeny and coexistence. Ecol. Lett. 13: 1085–1093.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Mertz, P. 2002. Pflanzenwelt Mitteleuropas und der Alpen. Nikol Verlagsgesellschaft mbH & co.KG, Hamburg.

    Google Scholar 

  32. Moore, N.W. 1962. The heaths of dorset and their conservation. J. Ecol. 50: 369–391.

    Article  Google Scholar 

  33. Nipperess, D.A. and Matsen, F.A. 2013. The mean and variance of phylogenetic diversity under rarefaction. Methods Ecol. Evol. 4: 566–572.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Paradis, E., Claude, J. and Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Pienkowski, M.W., Watkinson, A.R., Kerby, G., Clarke, K.R. and Warwick, R.M. 1998. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35: 523–531.

    Article  Google Scholar 

  36. Piessens, K., Honnay, O. and Hermy, M. 2005. The role of fragment area and isolation in the conservation of heathland species. Biol. Conserv. 122: 61–69.

    Article  Google Scholar 

  37. Pino-Bodas, R., Martín, M.P., Burgaz, A.R. and Lumbsch, H.T. 2013. Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Mol. Ecol. Resour. 13: 1058–1068.

    CAS  PubMed  Google Scholar 

  38. Poczai, P. and Hyvönen, J. 2010. Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects. Mol. Biol. Rep. 37: 1897–1912.

    Article  CAS  Google Scholar 

  39. Prieto, M. and Wedin, M. 2013. Dating the diversification of the major lineages of Ascomycota (Fungi). PLoS ONE 8, e65576.

  40. R Core Team 2014. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

  41. Rodrigues, A.S.L., Brooks, T.M. and Gaston, K.J. 2005. Integrating phylogenetic diversity in the selection of priority areas for conservation: Does it make a difference? In: Purvis, A., Gittleman, J.L. and T. Brooks. (eds.), Phylogeny and Conservation. Cambridge University Press, New York. pp. 101–119.

    Google Scholar 

  42. Rohwer, J.G., Li, J., Rudolph, B., Schmidt, S.A., Werff, H. van der and Li, H. 2009. Is Persea (Lauraceae) monophyletic? Evidence from nuclear ribosomal ITS sequences. Taxon 58: 1153–1167.

    Article  Google Scholar 

  43. Rohwer, J.G., Moraes, P.L.R.D., Rudolph, B. and Werff, H.V.D. 2014. A phylogenetic analysis of the Cryptocarya group (Lauraceae) and relationships of Dahlgrenodendron, Sinopora, Triadodaphne, and Yasunia. Phytotaxa 158: 111–132.

    Article  Google Scholar 

  44. Ronquist, F. and Hülsenbeck, J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schmull, M., Miadlikowska, J., Pelzer, M., Stocker-Wörgötter, E., Hofstetter, V., Fraker, E., Hodkinson, B.P., Reeb, V., Kukwa, M., Lumbsch, H.T., et al. 2011. Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103: 983–1003.

  46. Stenroos, S. 2002. Phylogeny of the genus Cladonia s.lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18: 237–278.

    Google Scholar 

  47. Stevens, P.F. 2001. Angiosperm phylogeny website. Version 13, October 2014.

  48. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Vamosi, S.M., Heard, S.B., Vamosi, J.C. and Webb, C.O. 2009. Emerging patterns in the comparative analysis of phylogenetic community structure. Mol. Ecol. 18: 572–592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Verdú, M. and Pausas, J.G. 2007. Fire drives phylogenetic clustering in Mediterranean Basin woody plant communities. J. Ecol. 95: 1316–1323.

    Article  Google Scholar 

  51. Webb, C.O. 2000. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am. Nat. 156: 145–155.

    Article  Google Scholar 

  52. Webb, N.R. 1998. The traditional management of European heathlands. J. Appl. Ecol. 35: 987–990.

    Article  Google Scholar 

  53. Webb, N.R. and Vermaat, A.H. 1990. Changes in vegetational diversity on remnant heathland fragments. Biol. Conserv. 53: 253–264.

    Article  Google Scholar 

  54. Webb, C.O., Ackerly, D.D., McPeek, M.A. and Donoghue, M.J. 2002. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33: 475–505.

    Article  Google Scholar 

  55. Webb, C.O., Ackerly, D.D. and Kembel, S.W. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098–2100.

    Article  CAS  Google Scholar 

  56. Winter, M., Devictor, V. and Schweiger, O. 2013. Phylogenetic diversity and nature conservation: where are we? Trends Ecol. Evol. 28: 199–204.

    Google Scholar 

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Correspondence to I. Geedicke.

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Geedicke, I., Schultz, M., Rudolph, B. et al. Phylogenetic clustering found in lichen but not in plant communities in European heathlands. COMMUNITY ECOLOGY 17, 216–224 (2016). https://doi.org/10.1556/168.2016.17.2.10

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Keywords

  • Heathland
  • Historical land use
  • Lüneburger Heide
  • Lichen
  • MPD
  • Phylogenetic community structure
  • Phylogenetic diversity
  • Rarefaction
  • Species richness