, Volume 723, Issue 1, pp 41–52 | Cite as

Local, among-site, and regional diversity patterns of benthic macroinvertebrates in high altitude waterbodies: do ponds differ from lakes?

  • Ladislav Hamerlík
  • Marek Svitok
  • Milan Novikmec
  • Miroslav Očadlík
  • Peter Bitušík


In this study we aimed at comparing invertebrate diversity of high altitude lakes and ponds along hierarchical spatial scales. We compared local, among-site, and regional diversity of benthic macroinvertebrates in 25 ponds and 34 lakes in the Tatra Mountains, central Europe. The ponds showed significantly lower local diversity, higher among-site diversity and similar regional diversity than the lakes. The species–area relationships (SAR), habitat heterogeneity, and environmental harshness are assumed as drivers for the local diversity patterns. An ecological threshold separating pond and lake systems emerged at an area of 2 ha, where the SAR pattern changed significantly. Differences in species turnover between these systems were likely driven by greater environmental variability and isolation of the ponds. High altitude ponds neither significantly support greater regional diversity nor higher number of unique taxa than lakes. The higher among-site diversity of ponds relative to lakes highlights the relevance of ponds for regional diversity in mountain areas.


Zoobenthos Small waterbodies Alpha diversity Beta diversity Gamma diversity Tatra Mountains 



We thank our colleagues and students participating in field sampling and laboratory processing. This work was supported by the Slovak Research and Development Agency under the contract No. APVV-0059-11. This study was also partially funded by the Slovak Scientific Grant Agency (VEGA, projects No. 1/0180/12 and 2/0081/13). We acknowledge the language correction and helpful notes by Heather Mariash. Last, we are grateful to Prof. Beat Oertli and to two anonymous reviewers whose comments to the previous versions of the manuscript considerably improved the paper.

Supplementary material

10750_2013_1621_MOESM1_ESM.pdf (186 kb)
Supplementary material (PDF 186 kb)


  1. Anderson, M. J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245–253.PubMedCrossRefGoogle Scholar
  2. Anderson, M. J., K. E. Ellingsen & B. H. McArdle, 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9: 683–693.PubMedCrossRefGoogle Scholar
  3. Anderson, M. J., T. O. Crist, J. M. Chase, M. Vellend, B. D. Inouye, A. L. Freestone, N. J. Sanders, H. V. Cornell, L. S. Comita, K. F. Davies, S. P. Harrison, N. J. B. Kraft, J. C. Stegen & N. G. Swenson, 2011. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecology Letters 14: 19–28.PubMedCrossRefGoogle Scholar
  4. AQEM Consortium, 2002. Manual for the Application of the AQEM System. A comprehensive method to assess European streams using benthic macroinvertebrates, developed for the purpose of the Water Framework Directive, Version 1.0, February 2002.Google Scholar
  5. Biggs, J., P. Williams, M. Whitfield, P. Nicolet & A. Weatherby, 2005. 15 years of pond assessment in Britain: results and lessons learned from the work of Pond Conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 693–714.CrossRefGoogle Scholar
  6. Bitušík, P., J. Kopáček, E. Stuchlík & F. Šporka (eds), 2006a. Limnology of Lakes in the Tatra Mountains, Vol. 61(Supplement 18). Biologia, Bratislava: 222 pp.Google Scholar
  7. Bitušík, P., M. Svitok, P. Kološta & M. Hubková, 2006b. Classification of the Tatra Mountain Lakes (Slovakia) Using Chironomids (Diptera, Chironomidae), Vol. 61(Supplement 18). Biologia, Bratislava: 191–201.Google Scholar
  8. Canty, A. & B. Ripley, 2011. boot: Bootstrap R (S-Plus) functions. R package version 1.3-2.Google Scholar
  9. Catalan, J., C. J. Curtis & M. Kernan, 2009a. Remote European mountain lake ecosystems: regionalisation and ecological status. Freshwater Biology 54: 2419–2432.CrossRefGoogle Scholar
  10. Catalan, J., M. G. Barbieri, F. Bartumeus, P. Bitušík, I. Botev, A. Brancelj, D. Cogălniceanu, M. Manca, A. Marchetto, N. Ognjanova-Rumenova, S. Pla, M. Rieradevall, S. Sorvari, E. Štefková, E. Stuchlík & M. Ventura, 2009b. Ecological thresholds in European alpine lakes. Freshwater Biology 54: 2494–2517.CrossRefGoogle Scholar
  11. Céréghino, R., J. Biggs, B. Oertli & S. Declerck, 2008. The ecology of European ponds: defining the characteristics of a neglected freshwater habitat. Hydrobiologia 597: 1–6.CrossRefGoogle Scholar
  12. Chao, A., 1987. Estimating the population size for capture–recapture data with unequal catchability. Biometrics 43: 783–791.PubMedCrossRefGoogle Scholar
  13. Chao, A. & T.-J. Shen, 2010. Program SPADE (Species Prediction and Diversity Estimation). Program and user’s guide available at
  14. Chao, A. & T. J. Shen, 2012. User’s Guide for Program SPADE (Species Prediction And Diversity Estimation). National Tsing Hua University, Taiwan.Google Scholar
  15. Chomitz, K. & F. Šamaj, 1974. Zrážkové pomery. In Konček, M. (ed.), Klíma Tatier. Veda, Bratislava: 443–536.Google Scholar
  16. Čiamporová-Zaťovičová, Z. & F. Čiampor Jr, 2011. Aquatic beetles of the alpine lakes: diversity, ecology and small-scale population genetics. Knowledge and Management of Aquatic Ecosystems 402: 10.Google Scholar
  17. Colwell, R. K., 2009. EstimateS: statistical estimation of species richness and shared species from samples, Version 8.2. User guide and application published at
  18. Colwell, R. K. & J. A. Coddington, 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 345: 101–118.PubMedCrossRefGoogle Scholar
  19. Colwell, R. K., C. X. Mao & J. Chang, 2004. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717–2727.CrossRefGoogle Scholar
  20. Colwell, R. K., A. Chao, N. J. Gotelli, S. Y. Lin, Ch. X. Mao, R. L. Chazdon & J. T. Longino, 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5: 3–21.CrossRefGoogle Scholar
  21. Cribari-Neto, F., 2004. Asymptotic inference under heteroskedasticity of unknown form. Computational Statistics & Data Analysis 45: 215–233.CrossRefGoogle Scholar
  22. Davies, R. B., 1987. Hypothesis testing when a nuisance parameter is present only under the alternative. Biometrika 74: 33–43.Google Scholar
  23. Davies, R. B., J. Biggs, P. J. Williams, J. T. Lee & S. Thompson, 2008a. A comparison of the catchment sizes of rivers, streams, ponds, ditches and lakes: implications for protecting aquatic biodiversity in an agricultural landscape. Hydrobiologia 597: 7–17.CrossRefGoogle Scholar
  24. Davies, R. B., J. Biggs, P. Williams, M. Whitfield, P. Nicolet, D. Sear, S. Bray & S. Maund, 2008b. Comparative biodiversity of aquatic habitats in the European agricultural landscape. Agriculture, Ecosystems and Environment 125: 1–8.CrossRefGoogle Scholar
  25. Drakare, S., J. J. Lennon & H. Hillebrand, 2006. The imprint of the geographical, evolutionary and ecological context on species–area relationships. Ecology Letters 9: 215–227.PubMedCrossRefGoogle Scholar
  26. Dumnicka, E. & J. Galas, 2012. Temporal changes in oligochaete fauna of three alpine ponds in the Tatra Mountains (Poland). Boreal Environment Research 17: 252–262.Google Scholar
  27. Efron, B., 1987. Better bootstrap confidence interval. Journal of the American Statistical Association 82: 171–200.CrossRefGoogle Scholar
  28. Frost, S., A. Huni & W. E. Kershaw, 1971. Evaluation of a kicking technique for sampling stream bottom fauna. Canadian Journal of Zoology 49: 167–173.CrossRefGoogle Scholar
  29. Füreder, L., R. Ettinger, A. Boggero, B. Thaler & H. Thies, 2006. Macroinvertebrate diversity in Alpine lakes: effect of altitude and catchment properties. In Lami, I. & A. Boggero (eds), Ecology of High Altitude Aquatic Systems in the Alps. Hydrobiologia 562: 123–144.Google Scholar
  30. Gee, J. H. R., B. D. Smith, K. M. Lee & S. Wynne-Griffiths, 1997. The ecological basis of freshwater pond management for biodiversity. Aquatic Conservation: Marine and Freshwater Ecosystems 7: 91–104.CrossRefGoogle Scholar
  31. Gorek, A. & Š. Kahan, 1973. Prehľad geologického vývoja a stavby Vysokých Tatier. Zborník TANAP 15: 5–88.Google Scholar
  32. Gotelli, N. J. & R. K. Colwell, 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379–391.CrossRefGoogle Scholar
  33. Gregor, V. & J. Pacl, 2005. Hydrológia tatranských jazier. Acta Hydrologica Slovaca 6: 161–187.Google Scholar
  34. Hamerlík, L. & K. P. Brodersen, 2010. Non-biting midges (Diptera: Chironomidae) from fountains of two European cities: micro-scale island biogeography. Aquatic Insects 32: 67–79.CrossRefGoogle Scholar
  35. Hinden, H., B. Oertli, N. Menetrey, L. Sage & J.-B. Lachavanne, 2005. Alpine pond biodiversity: what are the related environmental variables? Aquatic Conservation: Marine and Freshwater Ecosystems 15: 613–624.CrossRefGoogle Scholar
  36. Jeffries, M. J., 2005. Small ponds and big landscapes: the challenge of invertebrate spatial and temporal dynamics for European pond conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 541–548.CrossRefGoogle Scholar
  37. Kiflawi, M., A. Eitam & L. Blaustein, 2003. The relative impact of local and regional processes on macro-invertebrate species richness in temporary pools. Journal of Animal Ecology 72: 447–452.CrossRefGoogle Scholar
  38. Koleff, P., K. J. Gaston & J. J. Lennon, 2003. Measuring beta diversity for presence–absence data. Journal of Animal Ecology 72: 367–382.CrossRefGoogle Scholar
  39. Konček, M. & M. Orlicz, 1974. Teplotné pomery. In Konček, M. (ed.), Klíma Tatier. Veda, Bratislava: 89–179.Google Scholar
  40. Kopáček, J., E. Stuchlík, J. Veselý, J. Schaumburg, I. C. Anderson, J. Fott, J. Hejzlar & J. Vrba, 2002. Hysteresis in reversal of Central European mountain lakes from atmospheric acidification. Water, Air and Soil Pollution: Focus 2: 91–114.CrossRefGoogle Scholar
  41. Kopáček, J., D. Hardekopf, V. Majer, P. Pšenáková, E. Stuchlík & J. Veselý, 2004. Response of alpine lakes and soils to changes in acid deposition: the MAGIC model applied to the Tatra Mountain region, Slovakia–Poland. Journal of Limnology 63: 143–156.Google Scholar
  42. Kopáček, J., E. Stuchlík & D. Hardekopf, 2006. Chemical Composition of the Tatra Mountain Lakes: Recovery from Acidification, Vol. 61(Supplement 18). Biologia, Bratislava: 21–33.Google Scholar
  43. Kownacki, A., E. Dunmicka, J. Kwandrans, J. Galas & M. Ollik, 2006. Benthic communities in relation to environmental factors in small high mountain ponds threatened by air pollutants. Boreal Environment Research 1: 481–492.Google Scholar
  44. Kruskal, J. B., 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1–27.CrossRefGoogle Scholar
  45. Lencioni, V., 2004. Survival strategies of freshwater insects in cold environments. Journal of Limnology 63(Supplement 1): 45–55.Google Scholar
  46. Longino, J. T., J. Coddington & R. K. Colwell, 2002. The ant fauna of a tropical rain forest: estimating species three different ways. Ecology 83: 689–702.CrossRefGoogle Scholar
  47. MacArthur, R. & E. O. Wilson, 1967. The Theory of Island Biogeography. Princeton University Press, Princeton.Google Scholar
  48. Manly, B. F. J., 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall, London.Google Scholar
  49. Martínez-Sanz, C., C. S. S. Cenzano, M. Fernández-Aláez & F. García-Criado, 2012a. Relative contribution of small mountain ponds to regional richness of littoral macroinvertebrates and the implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 22: 155–164.CrossRefGoogle Scholar
  50. Martínez-Sanz, C., C. Fernandez-Aláez & F. Garcia-Criado, 2012b. Richness of littoral macroinvertebrate communities in mountain ponds from NW Spain: what factors does it depend on? Journal of Limnology 71: 154–163.CrossRefGoogle Scholar
  51. Muggeo, V. M. R., 2003. Estimating regression models with unknown break-points. Statistics in Medicine 22: 3055–3071.PubMedCrossRefGoogle Scholar
  52. Muggeo, V. M. R., 2008. segmented: an R package to fit regression models with broken-line relationships. R News 8: 20–25.Google Scholar
  53. Nemčok, J., V. Bezák, M. Janák, Š. Kahan, W. Ryja, M. Kohút, I. Lehotský, J. Wieczorek, J. Zelman, J. Mello, R. Halouzka, W. Raczkowski & P. Reichwalder, 1993. Vysvetlivky ku geologickej mape Tatier. Geologický ústav Dionýza Štúra, Bratislava.Google Scholar
  54. Nicolet, P., J. Biggs, G. Fox, M. J. Hodson, C. Reynolds, M. Whitfield & P. Williams, 2004. The wetland plant and macroinvertebrate assemblages of temporary ponds in England and Wales. Biological Conservation 120: 261–278.CrossRefGoogle Scholar
  55. Novikmec, M., M. Svitok, D. Kočický, F. Šporka & P. Bitušík, 2013. Surface water temperature and ice cover of Tatra Mountain lakes depend on altitude, topographic shading and bathymetry. Arctic, Antarctic, and Alpine Research 45. doi:  10.1657/1938-4246-45.1.
  56. Oertli, B., D. M. Joye, E. Castella, R. Juge, D. Cambin & J.-B. Lachavanne, 2002. Does size matter? The relationship between pond area and biodiversity. Biological Conservation 104: 59–70.CrossRefGoogle Scholar
  57. Oertli, B., N. Indermuehle, S. Angelibert, H. Hinden & A. Stoll, 2008. Macroinvertebrate assemblages in 25 high alpine ponds of the Swiss National Park (Cirque of Macun) and relation to environmental variables. Hydrobiologia 597: 29–41.CrossRefGoogle Scholar
  58. 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, 2011. vegan: Community ecology package. R package version 2.0-0.Google Scholar
  59. R Development Core Team, 2011. R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  60. Richardson, D. M. & R. J. Whittaker, 2010. Conservation biogeography – foundations, concepts and challenges. Diversity and Distributions 16: 313–320.CrossRefGoogle Scholar
  61. Rossi, J.-P., 2011. rich: species richness estimation and comparison. R package version 0.1.Google Scholar
  62. Scheffer, M., G. J. van Geest, K. Zimmer, E. Jeppesen, M. Søndergaard, M. G. Butler, M. A. Hanson, S. Declerck & L. De Meester, 2006. Small habitat size and isolation can promote species richness: second-order effects on biodiversity in shallow lakes and ponds. Oikos 112: 227–231.CrossRefGoogle Scholar
  63. Simpson, G. L., 2011. permute: functions for generating restricted permutations of data. R package version 0.6-2.Google Scholar
  64. Smol, J. P., 1988. Paleoclimate proxy data from freshwater Arctic diatoms. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 23: 837–844.Google Scholar
  65. Søndergaard, M., E. Jeppesen & J. P. Jensen, 2005. Pond or lake: does it make any difference? Archiv für Hydrobiologie 162: 143–165.CrossRefGoogle Scholar
  66. Suurkuukka, H., K. K. Meissner & T. Muotka, 2012. Species turnover in lake littorals: spatial and temporal variation of benthic macroinvertebrate diversity and community composition. Diversity and Distributions 18: 931–941.CrossRefGoogle Scholar
  67. Svitok, M., R. Hrivnák, H. Oťaheľová, D. Dúbravková, P. Paľove-Balang & V. Slobodník, 2011. The importance of local and regional factors on the vegetation of created wetlands in central Europe. Wetlands 31: 663–674.CrossRefGoogle Scholar
  68. Triantis, K. A. & S. Sfenthourakis, 2005. Island biogeography is not a single-variable discipline: the small island effect debate. Diversity and Distributions 18: 92–96.CrossRefGoogle Scholar
  69. Tuomisto, H., 2010. A diversity of beta diversities: straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33: 2–22.CrossRefGoogle Scholar
  70. Whittaker, R. H., 1960. Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 30: 279–338.CrossRefGoogle Scholar
  71. Williams, C. B., 1964. Patterns in the Balance of Nature. Academic Press, London.Google Scholar
  72. Williams, P., M. Whitfield, J. Biggs, S. Bray, G. Fox, P. Nicolet & D. Sear, 2003. Comparative biodiversity of rivers, streams, ditches and ponds in an agricultural landscape in Southern England. Biological Conservation 115: 329–341.CrossRefGoogle Scholar
  73. Zeileis, A., 2004. Econometric computing with HC and HAC covariance matrix estimators. Journal of Statistical Software 11: 1–17.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Ladislav Hamerlík
    • 1
  • Marek Svitok
    • 2
  • Milan Novikmec
    • 2
  • Miroslav Očadlík
    • 2
  • Peter Bitušík
    • 1
  1. 1.Faculty of ScienceMatthias Belius UniversityBanská BystricaSlovakia
  2. 2.Department of Biology and General EcologyTechnical University in ZvolenZvolenSlovakia

Personalised recommendations