, Volume 737, Issue 1, pp 245–264 | Cite as

The relevance of bryophytes in the macrophyte-based reference conditions in Portuguese rivers

  • Cristiana VieiraEmail author
  • Francisca C. Aguiar
  • Maria Teresa Ferreira


The identification of macrophyte reference communities represents a significant challenge in Mediterranean zones, where few aquatic taxa exist compared to other regions of the world. In the highly seasonal rivers of Portugal, we explored the contribution of bryophytes to enhance the compositional and ecological characterization of reference conditions. We performed partitioning, classification, and ordination analyses and obtained eight groups of bryophytic assemblages explained by water availability and quality. Groups A, B, and H assemblages are type-specific of the inland areas of the northern eco-region, reflecting the neutral minerotrophic currents with summer low currents. Groups C and D are type-specific of acidic oligotrophic shifting currents dependent of precipitation events in the mountainous streams of the North Atlantic eco-region. Groups E, F, and G are widespread in continental northern, central, and southern zones in neutral and highly mineralized watercourses with seasonal dryness. We propose bryophytes as a tool in the characterization of the reference conditions for two main reasons: (i) many of the recorded taxa are capable of withstanding the natural seasonal desiccation, and (ii) the type-specific bryophytes have perennial life-strategies and can be assessed at any time of year as a support for other type-specific macrophytes in compositional assessments of reference conditions.


Bryophytes Macrophytes Water Framework Directive Reference conditions Mediterranean region Portugal 



We thank Fundação para Ciência e a Tecnologia (FCT) for providing funding through post-doctoral grants to the first two authors (SFRH/BPD/63741/2009; SFRH/BPD/29333/2006). We also acknowledge the reviewers for their constructive comments regarding the earlier version of this manuscript. Also we thank Helena Hespanhol for assistance with Figs. 1 and 2 of this manuscript. We are grateful to Agência Portuguesa do Ambiente (APA) for the supply of biological and environmental data.

Supplementary material

10750_2013_1784_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)
10750_2013_1784_MOESM2_ESM.docx (37 kb)
Supplementary material 2 (DOCX 37 kb)
10750_2013_1784_MOESM3_ESM.docx (214 kb)
Supplementary material 3 (DOCX 215 kb)


  1. Aguiar, F. C., M. T. Ferreira, A. Albuquerque & I. Moreira, 2007. Alien and endemic flora at reference and non-reference sites in Mediterranean-type streams in Portugal. Aquatic Conservation: Marine and Freshwater Ecosystems 17: 335–347.CrossRefGoogle Scholar
  2. Aguiar, F. C., M. T. Ferreira, A. Albuquerque, P. Rodríguez-González & P. Segurado, 2009. Structural and functional responses of riparian vegetation to human disturbance: performance and spatial scale-dependence. Fundamental and Applied Limnology/Archiv für Hydrobiologie 175: 249–267.CrossRefGoogle Scholar
  3. Aguiar, F. C., M. J. Feio & M. T. Ferreira, 2011. Choosing the best method for stream bioassessment using macrophyte communities: Indices and predictive models. Ecological Indicators 11: 379–388.CrossRefGoogle Scholar
  4. Ah-Peng, C. & C. Raush de Traubenberg, 2004. Bryophytes aquatiques bioaccumulateurs de pollutants et indicateurs écophysiologiques de stress: synthèse bibliographique. Cryptogamie, Bryologie 25: 205–248.Google Scholar
  5. Akiyama, H., 1995. Rheophytic mosses: their morphological, physiological, and ecological adaptations. Acta Phytotaxonomica et Geobotanica 46: 77–98.Google Scholar
  6. Baattrup-Pedersen, A., K. Szoszkiewicz, R. Nijboer, M. O’Hare & T. Ferreira, 2006. Macrophyte communities in unimpacted European streams: variability in assemblage patterns, abundance and diversity. Hydrobiologia 566: 179–196.CrossRefGoogle Scholar
  7. Bartram, J. & R. Ballance, 1996. Water Quality Monitoring. Chapman and Hall, London.Google Scholar
  8. Belbin, L. & C. McDonald, 1993. Comparing three classification strategies for use in ecology. Journal of Vegetation Science 4: 341–348.CrossRefGoogle Scholar
  9. Birk, S. & N. Willby, 2010. Towards harmonization of ecological quality classification: establishing common grounds in European macrophyte assessment for rivers. Hydrobiologia 652: 149–163.CrossRefGoogle Scholar
  10. Bowden, W. B., D. B. Arscott, D. Pappathanasi, J. C. Finlay, J. M. Glime, J. Lacroix, C. L. Liao, A. Hershey, T. Lampella, B. Peterson, W. Wollheim, K. Slavik, B. Shelley, M. B. Chesterton, J. A. Lachance, R. M. Leblanc, M. Steinman, A. M. Suren & S. B. Group, 1999. Roles of Bryophytes in stream ecosystems. Journal of the North American Benthological Society 18: 151–184.CrossRefGoogle Scholar
  11. Carvalho, R. C., C. Branquinho & J. M. Silva, 2011. Physiological consequences of desiccation in the aquatic bryophyte Fontinalis antipyretica. Planta 234: 195–205.PubMedCrossRefGoogle Scholar
  12. Casas, C., M. Brugués, R. M. Cros & C. Sérgio, 2006. Handbook Mossflora of the Iberian Peninsula and Balearic Islands. Institut d’estudis Catalans, Barcelona.Google Scholar
  13. Casas, C., M. Brugués, R. M. Cros & C. Sérgio, 2009. Handbook of Liverworts and Hornworts of the Iberian Peninsula and the Balearic Islands. Institut d’estudis Catalans, Barcelona.Google Scholar
  14. CEN, 2003. Water quality—guidance for the surveying of aquatic macrophytes in running waters EN14184:2003 Comité Européen de Normalization. 1–14.Google Scholar
  15. Ceschin, S., M. Aleffi, S. Bisceglie, V. Savo & V. Zuccarello, 2012. Aquatic bryophytes as ecological indicators of the water quality status in the Tiber River basin (Italy). Ecological Indicators 14: 74–81.CrossRefGoogle Scholar
  16. Clesceri, L. S., A. E. Greenberg & A. D. Eaton, 1999. Standard Methods for the Examination of Water & Wastewater, 20th ed. American Public Health Association, Washington.Google Scholar
  17. Cook, C. D. K., 1999. The number and kinds of embryo-bearing plants which have become aquatic: a survey. Perspectives in Plant Ecology, Evolution and Systematics 2: 79–102.CrossRefGoogle Scholar
  18. Crist, T. O., J. A. Veech, J. C. Gering & K. S. Summerville, 2003. Partitioning species diversity across landscape and regions: a hierarchical analysis of α, β and γ diversity. The American Naturalist 162: 734–743.PubMedCrossRefGoogle Scholar
  19. Demars, B. O. L. & A. C. Edwards, 2009. Distribution of aquatic macrophytes in contrasting river systems: A critique of compositional-based assessment of water quality. Science of the Total Environment 407: 975–990.PubMedCrossRefGoogle Scholar
  20. Demars, B. O. L. & D. M. Harper, 2005. Distribution of aquatic vascular plants in lowland rivers: separating the effects of local environmental conditions, longitudinal connectivity and river basin isolation. Freshwater Biology 50: 418–437.CrossRefGoogle Scholar
  21. Demars, B. O. L. & G. Thiébaut, 2008. Distribution of aquatic plants in the Northern Vosges rivers: implications for biomonitoring and conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 619–632.CrossRefGoogle Scholar
  22. Dierssen, K., 2001. Distribution, ecological amplitude and phytosociological characterization of European bryophytes, Vol. 56. J. Cramer, Berlin.Google Scholar
  23. Dodkins, I., F. Aguiar, R. Rivaes, A. Albuquerque, P. Rodríguez-González & M. T. Ferreira, 2012a. Measuring ecological change of aquatic macrophytes in Mediterranean rivers. Limnologica: Ecology and Management of Inland Waters 42: 95–107.CrossRefGoogle Scholar
  24. Dodkins, I. R., F. Aguiar & M. T. Ferreira, 2012b. Can Mediterranean river plants translate into quality assessment systems? Venturing into unexplored territories. In Boon, P. & P. Raven (eds), River Conservation and Management. Wiley, New York: 135–142.Google Scholar
  25. Englund, G., B. G. Jonsson & B. Malmqvist, 1997. Effects of flow regulation on bryophytes in North Swedish Rivers. Biological Conservation 79: 79–86.CrossRefGoogle Scholar
  26. Feio, M. J., F. C. Aguiar, S. F. P. Almeida & M. T. Ferreira, 2012. AQUAFLORA: A predictive model based on diatoms and macrophytes for streams water quality assessment. Ecological Indicators 18: 586–598.CrossRefGoogle Scholar
  27. Fernández Ordonez, M. C., T. E. Díaz González & M. A. Collado Prieto, 2003. Evaluación de la biodiversidad briopteridofítica de la cuenca del Río de Nueva (LLanes, Asturias, N Península Ibérica): bases pra su protección y conservación. Acta Botanica Barcelonensis 49: 191–208.Google Scholar
  28. Ferreira, M. T. & F. C. Aguiar, 2006. Riparian and aquatic vegetation in Mediterranean-type streams (western Iberia). Limnetica 25: 414–424.Google Scholar
  29. Ferreira, M. T., P. M. Rodríguez-González, F. C. Aguiar & A. Albuquerque, 2005. Assessing biotic integrity in Iberian rivers: development of a multimetric plant index. Ecological Indicators 5: 137–149.CrossRefGoogle Scholar
  30. Fritz, K. M., J. M. Glime, J. Hribljan & J. L. Greenwood, 2009. Can bryophytes be used to characterize hydrologic permanence in forested headwater streams? Ecological Indicators 9: 681–692.CrossRefGoogle Scholar
  31. Gauch, H. & R. H. Whittaker, 1981. Hierarchical classification of community data. Journal of Ecology 2: 573–597.Google Scholar
  32. Gecheva, G. & L. Yurukova, 2013. Water pollutant monitoring with aquatic bryophytes: a review. Environmental Chemistry Letters 72: 1–13.Google Scholar
  33. Goffinet, B., 2000. Origin and phylogenetic relationships of bryophytes. In Saw, A. J. & B. Goffinet (eds), Bryohyte Biology. Cambridge University Press, Cambridge: 124–149.CrossRefGoogle Scholar
  34. Hederson, P. A. & R. M. H. Seaby, 1999. Community Analysis Package 1.52 for Windows. Pisces Conservation Ltd, Lymington.Google Scholar
  35. Heino, J., R. Virtanen, K.-M. Vuori, J. Saastamoinen, A. Ohtonen & T. Muotka, 2005. Spring bryophytes in forested landscapes: land use effects on bryophyte species richness, community structure and persistence. Biological Conservation 124: 539–545.CrossRefGoogle Scholar
  36. Hill, M. O., R. G. H. Bince & M. W. Shaw, 1975. Indicator species analysis, a divisive polythetic method of classification, and its application to a survey of native pinewoods in Scotland. Journal of Ecology 63: 597–613.CrossRefGoogle Scholar
  37. Hill, M. O., N. Bell, M. A. Bruggeman-Nannenga, M. Brugués, M. J. Cano, J. Enroth, K. I. Flatberg, J.-P. Frahm, M. T. Gallego, R. Garilleti, J. Guerra, L. Hedenäs, D. T. Holoyak, J. Hyvönen, M. S. Ignatov, F. Lara, V. Mazimpaka, J. Muñoz & L. Söderström, 2006. Bryological Monograph. An annotated checklist of the mosses of Europe and Macaronesia. Journal of Bryology 28: 198–267.CrossRefGoogle Scholar
  38. Holmes, N. T. H., P. J. Boon & T. A. Rowell, 1998. A revised classification system for British rivers based on their aquatic plant communities. Aquatic Conservation: Marine and Freshwater Ecosystems 8: 555–578.CrossRefGoogle Scholar
  39. Holmes, N. T. H., J. R. Newman, S. Chadd, K. J. Rouen, L. Saint & F. H. Dawson, 1999. Mean trophic rank: a user’s manual. R&D Technical Report E38. Environmental Agency, Bristol.Google Scholar
  40. Hylander, K., M. Dynesius, B. G. Jonsson & C. Nilsson, 2005. Substrate form determines the fate of bryophytes in riparian buffer strips. Ecological Applications 15: 674–688.CrossRefGoogle Scholar
  41. INAG, I. P., 2008. Tipologia de rios em Portugal continental no Âmbito da Implementação da Directiva Quadro da Água. I—Caracterização abiótica. Ministério do Ambiente, Ordenamento do Território e do Desenvolvimento Regional, Instituto da Água IP.Google Scholar
  42. Kapfer, J., V. Audorff, C. Beierkuhnlein & E. Hertel, 2012. Do bryophytes show a stronger response than vascular plants to interannual changes in spring water quality? Freshwater Science 31: 625–635.CrossRefGoogle Scholar
  43. Lang, P. & K. J. Murphy, 2012. Environmental drivers, life strategies and bioindicator capacity of bryophyte communities in high-latitude headwater streams. Hydrobiologia 679: 1–17.CrossRefGoogle Scholar
  44. Lansdown, R. & S. Bosanquet, 2010. Riverine plants as biological indicators. In Hurford, C., M. Schneider & I. Cowx (eds), Conservation Monitoring in Freshwater Habitats: A Practical Guide and Case Studies. Springer, Dordrecht: 73–83.Google Scholar
  45. Legendre, P., 2013. Indicator species: computation. In Levin, S. A. (ed.) Encyclopedia of Biodiversity, Vol 4. Elsevier, Amsterdam: 264–268.Google Scholar
  46. Legendre, P., D. Borcard & P. R. Peres-Neto, 2005. Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological Monographs 75: 435–450.CrossRefGoogle Scholar
  47. Luís, L., S. J. Hughes & M. Sim–Sim, 2012. Bryofloristic evaluation of the ecological status of Madeiran streams: towards the implementation of the European Water Framework Directive in Macaronesia. Nova Hedwigia 96: 181–204.CrossRefGoogle Scholar
  48. Manolaki, P. & E. Papastergiadou, 2013. The impact of environmental factors on the distribution pattern of aquatic macrophytes in a middle-sized Mediterranean stream. Aquatic Botany 104: 34–46.CrossRefGoogle Scholar
  49. Nijboer, R. C., R. K. Johnson, P. F. M. Verdonschot, Sommerh, M. user & A. Buffagni, 2004. Establishing reference conditions for European streams. Hydrobiologia 516: 91–105.CrossRefGoogle Scholar
  50. Paavola, R., T. Muotka, R. Virtanen, J. Heino & P. Kreivi, 2003. Are biological classifications of headwater streams concordant across multiple taxonomic groups? Freshwater Biology 48: 1912–1923.CrossRefGoogle Scholar
  51. Pont, D., B. Hugueny, U. Beier, D. Goffaux, A. Melcher, R. Noble, C. Rogers, N. Roset & S. Schmutz, 2006. Assessing river biotic condition at a continental scale: a European approach using functional metrics and fish assemblages. Journal of Applied Ecology 43: 70–80.CrossRefGoogle Scholar
  52. Roleček, J., L. Tichý, D. Zelený & M. Chytrý, 2009. Modified TWINSPAN classification in which the hierarchy respects cluster heterogeneity. Journal of Vegetation Science 20: 596–602.CrossRefGoogle Scholar
  53. Ros, R. M., V. Mazimpaka, U. Abou-Salama, M. Aleffi, T. L. Blockeel, M. Brugués, M. J. Cano, R. M. Cros, M. G. Dia, G. M. Dirkse, W. E. Saadawi, A. Erda, A. Ganeva, J. M. González-Mancebo, I. Herrnstadt, K. Khalil, H. Kürschner, E. Lanfranco, A. Losada-Lima, M. S. Refai, S. Rodríguez-Nuñez, M. Sabovljevi, C. Sérgio, H. Shabbara, M. Sim–Sim & L. Söderström, 2007. Hepatics and Anthocerotes of the Mediterranean, an annotated checklist. Cryptogamie, Bryologie 28: 351–437.Google Scholar
  54. Scarlett, P. & M. O’Hare, 2006. Community structure of in-stream bryophytes in English and Welsh rivers. Hydrobiologia 553: 142–152.CrossRefGoogle Scholar
  55. Schumacker, R., A. Lecointe, J. Touffet, P. D. Zuttere, L. Leclercq & R. Fabri, 1981. Hyocomium armoricum (Brid.) Wijk. & Marg. en Belgique et dans Nord-Ouest de la France (Ardenne, Bretagne, Normandie). Étude chorologique, écologique et phytosociologique. Cryptogamie, Bryologie 2: 277–321.Google Scholar
  56. Sérgio, C. & S. Carvalho, 2003. Annotated catalogue of Portuguese bryophytes. Portugaliae Acta Biologica 21: 5–230.Google Scholar
  57. Sérgio, C., M. Brugés, R. M. Cros, C. Casas & C. Garcia, 2006. The 2006 Red List and updated checklist of bryophytes of the Iberian Peninsula (Portugal, Spain and Andorra). Lindbergia 31: 109–125.Google Scholar
  58. Slack, N. G. & J. M. Glime, 1985. Niche relationships of mountain stream bryophytes. The Bryologist 88: 7–18.CrossRefGoogle Scholar
  59. SPSS, 2006. SPSS 15.0 for Windows. SPSS Inc., Chicago, USA.Google Scholar
  60. Suren, A. M., 1996. Bryophyte distribution patterns in relation to macro-, meso, and micro-scale variables in South Island, New Zealand streams. New Zealand Journal of Marine and Freshwater Research 30: 501–523.CrossRefGoogle Scholar
  61. Suren, A. M. & M. J. Duncan, 1999. Rolling stones and mosses: effect of substrate stability on bryophyte communities in streams. Journal of the North American Benthological Society 18: 457–467.CrossRefGoogle Scholar
  62. Suren, A. M. & S. J. Ormerod, 1998. Aquatic bryophytes in Hymalayan streams: testing a distribution model in a highly heterogeneous environment. Freshwater Biology 40: 697–716.CrossRefGoogle Scholar
  63. Szoszkiewicz, K., T. Ferreira, T. Korte, A. Baattrup-Pedersen, J. Davy-Bowker & M. O’Hare, 2006. European river plant communities: the importance of organic pollution and the usefulness of existing macrophyte metrics. In Furse, M., D. Hering, K. Brabec, A. Buffagni, L. Sandin & P. M. Verdonschot (eds), The Ecological Status of European Rivers: Evaluation and Intercalibration of Assessment Methods. Developments in Hydrobiology, Vol. 188. Springer, Dordrech: 211–234.Google Scholar
  64. ter Braak, C. J. F. & P. Šmilauer, 2003. Canoco 4.52 for Windows. Biometris. Plant Research International, Wageningen.Google Scholar
  65. Tremp, H., D. Kampmann & R. Schulz, 2012. Factors shaping submerged bryophyte communities: a conceptual model for small mountain streams in Germany. Limnologica: Ecology and Management of Inland Waters 42: 242–250.CrossRefGoogle Scholar
  66. Vanderpoorten, A., 1999. Aquatic bryophytes for a spatio-temporal monitoring of the water pollution of the rivers Meuse and Sambre (Belgium). Environmental Pollution 104: 401–410.CrossRefGoogle Scholar
  67. Vanderpoorten, A., 2002. Hydrochemical determinism, ecological polymorphism, and indicator values of aquatic bryophytes for water quality. In Ambasht, R. S. & N. K. Ambasht (eds), Applied Aquatic Ecology Modern Trends in Ecology & Environment, Vol. 21. Kluwer Academic Publishers, New York: 65–96.Google Scholar
  68. Vanderpoorten, A., G. Thiebaut, M. Tremolieres & S. Muller, 2000. A model for assessing water chemistry by using aquatic bryophyte assemblages in North-eastern France. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 27: 807–810.Google Scholar
  69. Veech, J. A. & T. O. Crist, 2006. PARTITION: software for hierarchical additive partitioning of species diversity.
  70. Veech, J. A., K. S. Summerville, T. O. Crist & J. C. Gering, 2002. The additive partitioning of species diversity: recent revival of an old idea. Oikos 99: 3–9.CrossRefGoogle Scholar
  71. Vieira, C., L. Luís, A. Séneca, M. Sim-Sim & C. Sérgio, 2004. New National and Regional Bryophyte records: Radula holtii Spruce. Journal of Bryology 26: 307.Google Scholar
  72. Vieira, C., A. Séneca & C. Sérgio, 2005. Threatened bryophytes occurence in Portuguese stream habitat. Boletín de la Sociedad Española de Bríologia 26–27: 103–118.Google Scholar
  73. Vieira, C., C. Sérgio & A. Séneca, 2007. Some remarkable bryophytes from the aquatic habitats of the northwest of Portugal. Cryptogamie, Bryologie 28: 1–8.Google Scholar
  74. Vieira, C., A. Séneca, M. T. Ferreira & C. Sérgio, 2011. The use of bryophytes for fluvial assessment of mountain streams. In Boon, P. & P. Raven (eds), River Conservation and Management. Wiley, New York: 134–158.Google Scholar
  75. Vieira, C., A. Séneca & C. Sérgio, 2012a. Floristic and ecological survey of bryophytes from Portuguese watercourses. Cryptogamie, Bryologie 33: 113–134.CrossRefGoogle Scholar
  76. Vieira, C., A. Séneca, C. Sérgio & M. T. Ferreira, 2012b. Bryophyte taxonomic and functional groups as indicators of fine scale ecological gradients in mountain streams. Ecological Indicators 18: 98–107.CrossRefGoogle Scholar
  77. Vitt, D. H. & J. M. Glime, 1984. The structural adaptations of aquatic Musci. Lindbergia 10: 95–110.Google Scholar
  78. Whitton, B. A., 2003. Use of plants for monitoring heavy metals in freshwaters. In Ambasht, R. S. & N. K. Ambasht (eds), Modern trends in applied aquatic ecology. Kluwer Academic, New York: 43–63.CrossRefGoogle Scholar
  79. Zechmeister, H. G. & L. Mucina, 1994. Vegetation of European springs: high rank syntaxa of the Montio-Cardaminetea. Journal of Vegetation Science 5: 385–402.CrossRefGoogle Scholar
  80. Zechmeister, H. G., K. Grodzinska & S. Szarek-Lukazewska, 2003. Bioindicators in use: Bryophytes. In B. A. Markert, A. M. Breure & H. G. Zechmeister (eds), Bioindicators and Biomonitors: Principles, Concepts and Applications. Elsevier, Amsterdam: 329–375.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Cristiana Vieira
    • 1
    Email author
  • Francisca C. Aguiar
    • 2
  • Maria Teresa Ferreira
    • 2
  1. 1.Research Center In Biodiversity and Genetic Resources - CIBIO (Research Network In Biodiversity and Evolutionary Biology - InBIO)PortoPortugal
  2. 2.Center of Forestry Research, Institute of AgronomyUniversity of LisbonLisbonPortugal

Personalised recommendations