, Volume 777, Issue 1, pp 183–196 | Cite as

Variation of benthic algal assemblages among habitats in subalpine Karstic Lakes and implications for bioassessment

  • Yangdong PanEmail author
  • Lizhu Wang
  • Yong Cao
  • Wanting Pang
  • Quanxi Wang
  • Zhongfu Zhu
  • Xiaoping Zhang
  • Guiping Deng
Primary Research Paper


Detecting early warning signs of ecosystem degradation in nature reserves requires ultrasensitive biological indicators. We assessed the potential of using multihabitat assessment of benthic algae (growing on submerged vegetation, rocks, and dead trees) to detect early warning signs of nutrient enrichment in nine karstic lakes in Jiuzhaigou Nature Reserve, a World Natural Heritage site in China. Nonmetric multidimensional scaling analysis showed that variability in benthic diatom assemblages among the major habitats within lakes were generally higher than among lakes. Permutational multivariate analysis of variance indicated that epiphytic diatom assemblages dominated by Achnanthidium minutissimum (Kützing) Czarnecki differed significantly from both epilithic and epidendric assemblages. Epilithon and epidendron, both dominated by Delicata delicatula (Kützing) Krammer and Denticula tenuis Kützing, were not significantly different within lakes. Mean Bray–Curtis dissimilarity index values among the three assemblages in each lake were negatively correlated with the tourism-stress index but the correlation was not statistically significant. Increasing homogeneity in benthic diatom assemblages among habitats within a lake may be due to cumulative nutrient enrichment associated with tourism development. Links among tourisms, nutrient enrichment, and dissimilarity in benthic algae among habitats should be viewed with caution until the cause–effect relationships can be confirmed by in situ manipulative experiments.


Jiuzhaigou Nature Reserve Epiphyton Epilithon Epidendron Permutational multivariate analysis of variance (PERMANOVA) Nonmetric multidimensional scaling (NMDS) 



This study was funded by a grant from the International Science & Technology Cooperation Program of China (2013DFR90670) and the Jiuzhaigou Bureau of Administration. The authors are grateful for all the logistic supports provided by the Jiuzhaigou Bureau of Administration, Dr. Beixin Wang’s research group in Nanjing Agricultural University, and Dr. Quanxi Wang’s research group in Shanghai Normal University. We would like to thank Patrick Edwards, Nadia Gillett, Mathew Dorfman, anonymous reviewers, and the associate editor for their thoughtful comments and suggestions.


  1. Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.Google Scholar
  2. Anderson, M. J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245–253.CrossRefPubMedGoogle Scholar
  3. Burkholder, J. M., 1996. Interactions of benthic algae with their substrata. In Stevenson, R. J., M. L. Boxwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego: 253–298.CrossRefGoogle Scholar
  4. Burkholder, J. M., R. G. Wetzel & K. L. Klomparens, 1990. Direct comparison of phosphate uptake by adnate and loosely attached microalgae within an intact biofilm matrix. Applied and Environmental Microbiology 56: 2882–2890.PubMedPubMedCentralGoogle Scholar
  5. Camacho, A., W. A. Wurtsbaugh, M. R. Miracle, X. Armengol & E. Vicente, 2003. Nitrogen limitation of phytoplankton in a Spanish karst lake with a deep chlorophyll maximum: a nutrient enrichment bioassay approach. Journal of Plankton Research 25: 397–404.CrossRefGoogle Scholar
  6. Cao, Y., B. Wang, J. Zhang, L. Wang, Y. Pan, Q. Wang & G. Deng, 2016. Spatial variation of lake macroinvertebrate assemblages and relationship with natural environment and tourism stress in Jiuzhaigou Natural Reserve, China. Ecological Indicators 62: 182–190.CrossRefGoogle Scholar
  7. Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.CrossRefGoogle Scholar
  8. Dufrêne, M. & P. Legendre, 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.Google Scholar
  9. Eminson, D. & B. Moss, 1980. The composition and ecology of periphyton communities in freshwaters: 1 the influence of host type and external environment on community composition. British Phycological Journal 15: 429–446.CrossRefGoogle Scholar
  10. Florsheim, J. L., S. L. Ustin, Y. Tang, B. Di, C. Huang, X. Qiao & Y. Cai, 2013. Basin-scale and travertine dam-scale controls on fluvial travertine, Jiuzhaigou, southwestern China. Geomorphology 180: 267–280.CrossRefGoogle Scholar
  11. Gaulke, L. S., X. Weiyang, A. Scanlon, A. Henck & T. Hinckley, 2010. Evaluation criteria for implementation of a sustainable sanitation and wastewater treatment system at Jiuzhaigou National Park, Sichuan Province, China. Environmental Management 45: 93–104.CrossRefPubMedGoogle Scholar
  12. Gu, Y., J. Du, Y. Tang, X. Qiao, C. Bossard & G. Deng, 2013. Challenges for sustainable tourism at the Jiuzhaigou World Natural Heritage site in western China. Natural Resources Forum 37: 103–112.CrossRefGoogle Scholar
  13. Ibelings, B. W., R. Portielje, E. H. Lammens, R. Noordhuis, M. S. van den Berg, W. Joosse & M. L. Meijer, 2007. Resilience of alternative stable states during the recovery of shallow lakes from eutrophication: Lake Veluwe as a case study. Ecosystems 10: 4–16.CrossRefGoogle Scholar
  14. Kralj, K., A. Plenković-Moraj, M. Gligora, B. Primc-Habdija & L. Šipoš, 2006. Structure of periphytic community on artificial substrata: influence of depth, slide orientation and colonization time in karstic Lake Visovačko, Croatia. Hydrobiologia 560: 249–258.CrossRefGoogle Scholar
  15. Krammer, K., 2003. Cymbopleura, Delicata, Navicymbula, Gomphocymbellopsis, Afrocymbella. In Lange-Bertalot, H. (ed.), Diatoms of Europe, Diatoms of the European Inland Waters and Comparable Habitats, Vol. 4. A.R.G. Gantner Verlag K.G., Rugell: 1–529.Google Scholar
  16. Krammer, K. & H. Lange-Bertalot, 1986. Bacillariophyceae, teil 1. Naviculaceae. Spektrum AkademischerVerlag, Heidelberg.Google Scholar
  17. Krammer, K. & H. Lange-Bertalot, 1988. Bacillariophyceae, teil 2. SpektrumAkademischerVerlag, Heidelberg, Germany, Epithemiaceae, Bacillariophyceae, Surirellaceae.Google Scholar
  18. Krammer, K. & H. Lange-Bertalot, 1991a. Bacillariophyceae, teil 3. Centrales, Fragilariaceae, Eunotiaceae, Achnanthaceae. SpektrumAkademischerVerlag, Heidelberg.Google Scholar
  19. Krammer, K. & H. Lange-Bertalot, 1991b. Bacillariophyceae, teil 4. Achnanthaceae, kritische erganzungenzuNavicula (lineolate) und Gomphonema. SpektrumAkademischerVerlag, Heidelberg.Google Scholar
  20. Kufel, L. & I. Kufel, 2002. Chara beds acting as nutrient sinks in shallow lakes – a review. Aquatic Botany 72: 249–260.CrossRefGoogle Scholar
  21. Levene, H., 1960. Robust tests for equality of variances. In Olkin, I., S. G. Ghurye, W. Hoeffding, W. G. Madow & H. B. Mann (eds), Contributions to Probability and Statistics. Stanford University Press, Stanford: 278–292.Google Scholar
  22. Lowe, R. L. & Y. Pan, 1996. Benthic algal communities as biological monitors. In Stevenson, R. J., M. L. Boxwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego: 705–739.CrossRefGoogle Scholar
  23. Moeller, R. E., J. M. Burkholder & R. G. Wetzel, 1988. Significance of sedimentary phosphorus to a rooted submersed macrophyte (Najasflexilis (Willd.) Rostk. and Schmidt) and its algal epiphytes. Aquatic Botany 32: 261–281.CrossRefGoogle Scholar
  24. Nugent, P. W., J. A. Shaw & M. Vollmer, 2015. Colors of thermal pools at Yellowstone National Park. Applied Optics 54: 128–139.CrossRefGoogle Scholar
  25. Oksanen, J. F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B., O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, & H. Wagner. 2013. vegan: Community Ecology Package. R package version 2.0-10.
  26. Otsuki, A. & R. G. Wetzel, 1972. Coprecipitation of phosphate with carbonates in a marl lake. Limnology and Oceanography 17: 763–767.CrossRefGoogle Scholar
  27. Pentecost, A., 2005. Travertine. Springer Science & Business Media, Berlin.Google Scholar
  28. Pringle, C. M., 1990. Nutrient spatial heterogeneity: effects on community structure, physiognomy, and diversity of stream algae. Ecology 71: 905–920.CrossRefGoogle Scholar
  29. R Development Core Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0,
  30. Scheffer, M. & S. R. Carpenter, 2003. Catastrophic regime shifts in ecosystems: linking theory to observation. Trends in Ecology & Evolution 18: 648–656.CrossRefGoogle Scholar
  31. Scheffer, M., S. Carpenter, J. A. Foley, C. Folke & B. Walker, 2001. Catastrophic shifts in ecosystems. Nature 413: 591–596.CrossRefPubMedGoogle Scholar
  32. Schwartz, M. W., C. R. Dolanc, H. Gao, S. Y. Strauss, A. C. Schwartz, J. N. Williams & Y. Tang, 2013. Forest structure, stand composition, and climate-growth response in montane forests of Jiuzhaigou National Nature Reserve, China. PloS One 8: e71559.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Stevenson, R. J., Y. Pan & H. Van Dam, 2010. Assessing environmental conditions in rivers and streams with diatoms. The diatoms: applications for the environmental and earth sciences, 2nd ed. Cambridge University Press, Cambridge: 57–85.CrossRefGoogle Scholar
  34. UNESCO 2013. Operational Guidelines for the Implementation of the World Heritage Convention. UNESCO World Heritage Centre 7, place de Fontenoy 75352 Paris 07 SP France.Google Scholar
  35. Van Dam, H., A. Mertens & J. Sinkeldam, 1994. A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Netherland Journal of Aquatic Ecology 28: 117–133.CrossRefGoogle Scholar
  36. Veillon, R. 2014. The state of conservation of world heritage properties: a statistical analysis (1979–2013). UNESCO World Heritage Centre 7, place de Fontenoy 75352 Paris 07 SP France.Google Scholar
  37. Wang, Y. K., R. J. Stevenson & L. Metzmeier, 2005. Development and evaluation of a diatom-based Index of Biotic Integrity for the Interior Plateau Ecoregion, USA. Journal of the North American Benthological Society 24: 990–1008.CrossRefGoogle Scholar
  38. Wang, J., W. Bao, B. He & Y. Liu, 2006. Effect of tourism on nitrogen and phosphorus loss in surface runoff in Jiuzhaigou world nature heritage reserve. Ecology and Environment 15: 284–288. (in Chinese with English abstract).Google Scholar
  39. Yu, L. X. & G. N. Sun, 2006. Empirical study on economic transformation induced by tourism development in Jiuzhaigou. Market Modernization 1: 280–282. (in Chinese).Google Scholar
  40. Zhang, J., H. Wang, Z. Liu, D. An & W. Dreybrodt, 2012. Spatial-temporal variations of travertine deposition rates and their controlling factors in Huanglong Ravine, China – A world’s heritage site. Applied Geochemistry 27: 211–222.CrossRefGoogle Scholar
  41. Zhou, X., X. Gao, X. Yang & Y. Li, 2009. Autumn diatom variation in lakes along altitude gradient in the Jiuzhaigou National Park, Sichuan, China. Journal of Applied Environmental Biology 15: 161–168. (in Chinese with English abstract).Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Yangdong Pan
    • 1
    Email author
  • Lizhu Wang
    • 2
  • Yong Cao
    • 3
  • Wanting Pang
    • 4
  • Quanxi Wang
    • 4
  • Zhongfu Zhu
    • 5
  • Xiaoping Zhang
    • 5
  • Guiping Deng
    • 5
    • 6
  1. 1.Department of Environmental Science and ManagementPortland State UniversityPortlandUSA
  2. 2.International Joint CommissionGreat Lakes Regional OfficeWindsorCanada
  3. 3.University of Illinois at Urbana-ChampaignChampaignUSA
  4. 4.College of Life and Environmental ScienceShanghai Normal UniversityShanghaiChina
  5. 5.Jiuzhaigou Nature Reserve Administrative BureauSichuanChina
  6. 6.School of Natural Resource & EnvironmentUniversity of MichiganAnn ArborUSA

Personalised recommendations