Journal of Paleolimnology

, Volume 60, Issue 2, pp 299–309 | Cite as

Paleolimnological records reveal biotic homogenization driven by eutrophication in tropical reservoirs

  • Simone Wengrat
  • Andre A. Padial
  • Erik Jeppesen
  • Thomas A. Davidson
  • Luciane Fontana
  • Sandra Costa-Böddeker
  • Denise C. Bicudo
Original paper


Biodiversity changes in response to eutrophication, climate variability and species invasions. These pressures have been shown to reduce community heterogeneity at various scales; however, how productivity drives homogenization patterns in a community of primary producers, such as diatoms, has not been studied. Using a dataset with good temporal resolution, obtained from cores collected from seven tropical reservoirs, we evaluated patterns of spatial and temporal homogenization, i.e. the trends in temporal α-diversity and spatial β-diversity (change in community composition), of diatom assemblages over the past 60–100 years. The paleolimnological records allowed us to study biodiversity trends since the initial community (reservoir construction) in those systems with low anthropogenic impact and also those undergoing eutrophication. No clear trend of spatial β-diversity change over time was found when all reservoirs were analyzed together. However, when only eutrophic reservoirs were considered, a marked decrease in the spatial β-diversity occurred, suggesting that eutrophication leads to homogenization of the diatom assemblage. These findings were reinforced by the lack of change in β-diversity when the age of the reservoirs was standardized, indicating that the reservoirs’ ontogeny did not influence the spatial β-diversity trend and β-diversity did not increase even in the reservoirs with low anthropogenic impact. In addition, the results showed a decrease of α-diversity over time for almost all the eutrophic reservoirs, as well as a decrease in the total species pool for the reservoirs, although periphytic diatoms may be favored by the appearance and sometimes mass development of floating macrophytes in warm, shallow eutrophic reservoirs. This study supports the role of eutrophication as one of the main drivers of diatom assemblage homogenization in tropical reservoirs, with a significant loss of species over time.


α-diversity β-diversity Biotic homogenization Diatoms Initial communities 



We gratefully acknowledge Janet Reid for improvement of the English language and Anne Mette Poulsen for valuable editorial comments. This study was carried out within the framework of the AcquaSed project, supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, No. 2009/53898–9) and was undertaken as part of S.W. Ph.D. thesis (FAPESP, No. 2012/25366-5 and CNPq No. 140550/2012-7) at the Institute of Botany (São Paulo, Brazil). L.F. and S.C.B. also thank FAPESP (08/57139-2 and 04/08675). D.C.B thanks CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, No. 310404/2016-9). A.A. Padial also acknowledges CNPq for continuous research grants. E.J. was supported by the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No. 603378 (

Supplementary material

10933_2017_9997_MOESM1_ESM.docx (334 kb)
Supplementary material 1 (DOCX 334 kb)


  1. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of β diversity. Ecol Lett 9:683–693CrossRefGoogle Scholar
  2. Apha (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, WashingtonGoogle Scholar
  3. Battarbee RW, Jones V, Flower RJ, Cameron N, Bennion H, Carvalho L, Juggins S (2001) Diatoms. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments terrestrial, algal, and siliceous indicators, vol 3. Kluwer Academic Publishers, London, pp 155–203CrossRefGoogle Scholar
  4. Bennion H, Simpson GL, Goldsmith BJ (2015) Assessing degradation and recovery pathways in lakes impacted by eutrophication using the sediment record. Front Ecol Evol 3:1–20CrossRefGoogle Scholar
  5. Bicudo DC, Fonseca BM, Bini LM, Crossetti LO, Bicudo CEM, Araújo-Jesus T (2007) Undesirable side-effects of water hyacinth control in a shallow tropical reservoir. Freshw Biol 52:1120–1133CrossRefGoogle Scholar
  6. Bicudo DC, Tremarin PI, Almeida PD, Zorzal-Almeida S, Wengrat S, Faustino SB, Costa LF, Bartozek ECR, Rocha ACR, Bicudo CEM, Morales EA (2016) Ecology and distribution of Aulacoseira species (Bacillariophyta) from tropical reservoirs in Brazil. Diatom Res 36:199–215CrossRefGoogle Scholar
  7. Birks HJB, Felde VA, Seddon AWR (2016) Biodiversity trends within the Holocene. The Holocene 26:994–1001CrossRefGoogle Scholar
  8. Branco SM (1966) Estudos das condições sanitárias da Represa Billings. Arquivos da Faculdade de Higiene e Saúde Pública da Universidade de São Paulo 20:57–86CrossRefGoogle Scholar
  9. Capobianco JPR, Whately M (2002) Billings 2000, Ameaças e Perspectivas para o maior Reservatório de Água da Região Metropolitana de São Paulo. Instituto Socioambiental, São PauloGoogle Scholar
  10. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Zarwani A, Mace GM, Tilman D, Wardle DA, Kinzing AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivasta DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67CrossRefGoogle Scholar
  11. CETESB (2010) Relatório de qualidade das águas superficiais do Estado de São Paulo: 2009. Companhia de Tecnologia de Saneamento Ambiental (CETESB), São PauloGoogle Scholar
  12. Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci USA 104:17430–17434CrossRefGoogle Scholar
  13. Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391CrossRefGoogle Scholar
  14. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos T Roy Soc B 366:2351–2363CrossRefGoogle Scholar
  15. Chase JM, Knight TM (2013) Scale-dependent effect sizes of ecological drivers on biodiversity: why standardized sampling is not enough. Ecol Lett 16:17–26CrossRefGoogle Scholar
  16. Costa-Böddeker S, Bennion H, Jesus TA, Albuquerque ALS, Figueira RCL, Bicudo DC (2012) Paleolimnologically inferred eutrophication of a shallow, tropical, urban reservoir in southeast Brazil. J Paleolimnol 48:751–766CrossRefGoogle Scholar
  17. Cunha DGF, Calijuri MC (2011) Limiting factors for phytoplankton growth in subtropical reservoirs: the effect of light and nutrient availability in different longitudinal compartments. Lake Reserv Manage 27:162–172CrossRefGoogle Scholar
  18. Cunha DGF, Calijuri MC, Lamparelli MC (2013) A trophic state index for tropical/subtropical reservoirs (TSItsr). Ecol Eng 60:126–134CrossRefGoogle Scholar
  19. Davidson TA, Reid MA, Sayer CD, Chilcott S (2013) Palaeolimnological records of shallow lake biodiversity change: exploring the merits of single versus multi-proxy approaches. J Paleolimnol 49:431–446CrossRefGoogle Scholar
  20. Devictor V, Julliard R, Clavel J, Jiguet F, Lee A, Couvet D (2008) Functional biotic homogenization of bird communities in disturbed landscapes. Global Ecol Biogeogr 17:252–261CrossRefGoogle Scholar
  21. Donohue I, Jackson AL, Pusch MT, Irvine K (2009) Nutrient enrichment homogenizes lake benthic assemblages at local and regional scales. Ecology 90:3470–3477CrossRefGoogle Scholar
  22. Dornelas M, Gotelli NJ, McGill B, Shimadzu H, Moyes F, Sievers C, Magurran AE (2014) Assemblage time series reveal biodiversity change but not systematic loss. Science 344:296–299CrossRefGoogle Scholar
  23. Essl F, Dullinger S, Rabitsch W, Hulme PE, Pysek P, Wilson JRU, Richardson DM (2015) Delayed biodiversity change: no time to waste. Trends Ecol Evol on 7:375–378CrossRefGoogle Scholar
  24. Fontana L, Albuquerque ALS, Brenner M, Bonotto DM, Sabaris TPP, Pires MAF, Cotrim MEB, Bicudo DC (2014) The eutrophication history of a tropical water supply reservoir in Brazil. J Paleolimnol 51:29–43CrossRefGoogle Scholar
  25. Forzza RC, Baumgratz JFA, Bicudo CEM, Canhos DAL, Carvalho JAA, Coelho MAN, Costa AF, Costa DP, Hopkins MG, Leitman PM, Lohmann LG, Lughadha EN, Maia LC, Martinelli G, Menezes M, Morim MP, Peixoto AL, Pirani JR, Prado J, Queiroz LP, Souza S, Souza VC, Stehmann JR, Sylvestre LS, Walter BMT, Zanni DC (2012) New Brazilian floristic list highlights conservation challenges. Bioscience 62:39–45CrossRefGoogle Scholar
  26. Froyd CA, Willis KJ (2008) Emerging issues in biodiversity & conservation management: the need for a palaeoecological perspective. Quaternary Sci Rev 27:1723–1732CrossRefGoogle Scholar
  27. Gillson L, Marchant R (2014) From myopia to clarity: sharpening the focus of ecosystem management through the lens of palaeoecology. Trends Ecol Evol 29:317–325CrossRefGoogle Scholar
  28. Gong C, Chen J, Yu S (2013) Biotic homogenization and differentiation of the flora in artificial and near-natural habitats across urban green spaces. Landsc Urban Plan 120:158–169CrossRefGoogle Scholar
  29. Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338CrossRefGoogle Scholar
  30. Gregory-Eaves I, Beisner BE (2011) Palaeolimnological insights for biodiversity science: an emerging field. Freshw Biol 56:2653–2661CrossRefGoogle Scholar
  31. Houk V (2003) Atlas of freshwater centric diatoms with a brief key and descriptions part I. Melosiraceae, Orthoseiraceae, Paraliaceae and Aulacoseiraceae. Czech Phycology Supplement, Olomouc, Czech Republic, p 114Google Scholar
  32. Jeppesen E, Sondergaard M, Jensen JP, Havens KE, Anneville O, Carvalho L, Coveney MF, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Köhler J, Lammens EHHR, Lauridsen TL, Manca M, Miracle MM, Moss B, Nõges P, Persson G, Phillips G, Portielje R, Romo S, Schelske CL, Straile D, Tatrai I, Willén E, Winder M (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771CrossRefGoogle Scholar
  33. Keith SA, Newton AC, Morecroft MD, Bealey CE, Bullock JM (2009) Taxonomic homogenization of woodland plant communities over 70 years. P Roy Soc B-Biol Sci 276:3539–3544CrossRefGoogle Scholar
  34. Kraft NJB, Adler PB, Godoy O, James E, Fuller S, Levine JM (2014) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599CrossRefGoogle Scholar
  35. Langenheder S, Berga M, Örjan Ö, Székely AJ (2012) Temporal variation of β-diversity and assembly mechanisms in a bacterial metacommunity. ISME J 6:1107–1114CrossRefGoogle Scholar
  36. Lougheed VL, McIntosh MD, Parker CA, Stevenson R (2008) Wetland degradation leads to homogenization of the biota at local and landscape scales. Freshw Biol 53:2402–2413CrossRefGoogle Scholar
  37. McGill BJ, Dornelas M, Gotelli NJ, Magurran AE (2015) Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol Evol 30:104–113CrossRefGoogle Scholar
  38. Menezes RF, Borchsenius F, Svenning JC, Davidson TA, Sondergaard M, Lauridsen TL, Landkildehus F, Jeppesen E (2015) Homogenization of fish assemblages in different lake depth strata at local and regional scales. Freshw Biol 60:745–757CrossRefGoogle Scholar
  39. Metzeltin D, Lange-Bertalot H (1998) Tropische Diatomeen in Südamerika I. 700 überwiegend wenig bekannte oder neue Taxa repräsentativ als Elemente der neotropischen Flora. In: Lange-Bertalot H (ed) Iconographia Diatomologica: annotated Diatom Monographs, vol 5. Koeltz Scientific Books, Koenigstein, pp 1–695Google Scholar
  40. Moro RS, Fürtenberg CB (1997) Catálogo dos principais parâmetros ecológicos de diatomáceas não marinhas. Ed. UEPG, Ponta Grossa. p 282Google Scholar
  41. Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2015) vegan: Community Ecology Package. R package version 2.2-1.
  42. Olden JD, Poff NL (2004) Ecological processes driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867–1875CrossRefGoogle Scholar
  43. Olden JD, Rooney TP (2006) On defining and quantifying biotic homogenization. Global Ecol Biogeogr 15:113–120CrossRefGoogle Scholar
  44. Pappas JL, Stoermer EF (1996) Quantitative method for determining a representative algal count. J Phycol 32:693–696CrossRefGoogle Scholar
  45. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  46. Rahel FJ (2010) Homogenization, differentiation, and the widespread alteration of fish faunas. Am Fish S S 73:311–326Google Scholar
  47. Round FE, Crawford RM, Mann DG (1990) The Dia-toms. Biology & morphology of the genera. Cambridge University Press, Cambridge, p 747Google Scholar
  48. Salgado J, Sayer CD, Brooks SJ, Davidson TA, Okamura B (2017) Eutrophication erodes inter-basin variation in macrophytes and co-occurring invertebrates in a shallow lake: combining ecology and palaeoecology. J Paleolimnol. doi: 10.1007/s10933-017-9950-6 Google Scholar
  49. Sartory DP, Grobbelaar JE (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–187CrossRefGoogle Scholar
  50. Sayer CD, Roberts N, Sadler J, David C, Wade PM (1999) Biodiversity changes in a shallow lake ecosystem: a multi-proxy palaeolimnological analysis. J Biogeog 26:97–114CrossRefGoogle Scholar
  51. Siqueira T, Lacerda CGT, Saito VS (2015) How does landscape modification induce biological homogenization in tropical stream metacommunities? Biotropica 47:509–516CrossRefGoogle Scholar
  52. Smol JP (1981) Problems associated with the use of “species diversity” in paleolimnological studies. Quat Res 15:209–212CrossRefGoogle Scholar
  53. Smol JP, Wolfe AP, Birks HJB, Douglas MSV, Jones VJ, Korhola A, Pienitz R, Rühland K, Sorvari S, Antoniades D, Brooks SJ, Fallu M-A, Hughes M, Keatley BE, Laing TE, Michelutti N, Nazarova L, Nyman M, Paterson AM, Perren B, Quinlan R, Rautio M, Saulnier-Talbot E, Silitonen S, Solovieva N, Weckström J (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Natl Acad Sci USA 102:4397–4402CrossRefGoogle Scholar
  54. Soininen J (2007) Environmental and spatial control of freshwater diatoms—a review. Diatom Res 22:473–490CrossRefGoogle Scholar
  55. Spaulding SA, Lubinski DJ, Potapova M (2010) Diatoms of the United States. Accessed on 18 Jan 2016
  56. StatSoft, Inc. (2005) STATISTICA (data analysis software system), version 7.1.
  57. Straskraba M, Tundisi JG (1999) Reservoir ecosystem functioning: theory and application. In: Tundisi JG, Straskraba M (eds) Theoretical reservoir ecology and its applications. International Institute of Ecology, Brazilian Academy of Sciences and Backhuys Publishers, Rio de Janeiro, pp 565–597Google Scholar
  58. Strayer D, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29:344–358CrossRefGoogle Scholar
  59. Tucci A, Deberdt GLB, Deberdt AJ (2004) Análise da comunidade de fitoplâncton do reservatório de Salto Grande (Americana, SP): uma revisão dos estudos desenvolvidos em um sistema eutrófico. In: ELG Espíndola, Leita MA, Dornfeld (eds) Reservatório de Salto Grande (Americana): caracterização, impactos e propostas de manejo. RiMa Editora, São Carlos, pp 107–153Google Scholar
  60. Tundisi JG, Abe DS, Matsumura-Tundisi T, Tundisi JE, Vannucci D (2006) Reservatórios da região metropolitana de São Paulo: consequências e impactos da eutrofização e perspectivas para o gerenciamento e recuperação. In: Tundisi JG, Matsumura-Tundisi T, Sidagis-Galli (eds) Eutrofização na América do Sul: causas, conseqüências e tecnologias de gerenciamento e controle. Instituto Internacional de Ecologia, São Carlos, pp 161–182Google Scholar
  61. Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup HH, Cristoffersen K, Lodge DM (2003) From Greenland to Green Lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1418CrossRefGoogle Scholar
  62. Vanormelingen P, Verleyen E, Vyverman W (2008) The diversity and distribution of diatoms: from cosmopolitanism to narrow endemism. Biodivers Conserv 17:393–405CrossRefGoogle Scholar
  63. Velghe K, Vermaire JC, Gregory-Eaves I (2012) Declines in littoral species richness across both spatial and temporal nutrient gradients: a palaeolimnological study of two taxonomic groups. Freshw Biol 57:2378–2389CrossRefGoogle Scholar
  64. Vilar AG, van Dam H, van Loon EE, Vonk JA, van Der Geest H, Admiraal W (2014) Eutrophication decreases distance decay of similarity in diatom communities. Freshw Biol 59:1522–1531CrossRefGoogle Scholar
  65. Villéger S, Blanchet S, Beauchard O, Oberdorff T, Brosse S (2011) Homogenization patterns of the world’s freshwater fish faunas. Proc Natl Acad Sci USA 108:18003–18008CrossRefGoogle Scholar
  66. Vyverman W, Verleyen E, Sabbe K, Vanhoutte K, Sterken M, Hodgson DA, Mann DG, Juggins S, Van de Vijver B, Jones V, Flower R, Roberts D, Chepurnov VA, Kilroy C, Vanormelingen P, Wever AD (2007) Historical processes constrain patterns in global diatom diversity. Ecology 88:1924–1931CrossRefGoogle Scholar
  67. Wengrat S, Bicudo DC (2011) Spatial evaluation of water quality in an urban reservoir (billings complex, southeastern Brazil). Acta Limnol Bras 23:200–216CrossRefGoogle Scholar
  68. Willis KJ, Birks HJB (2006) What is natural? The need for a long-term perspective in biodiversity conservation. Science 314:1261–1265CrossRefGoogle Scholar
  69. Willis KJ, Bailey RM, Bhagwat SA, Birks HJB (2010) Biodiversity baselines, thresholds, and resilience: testing predictions and assumptions using palaeoecological data. Trends Ecol Evol 25:583–591CrossRefGoogle Scholar
  70. Wojciechowski J, Heino J, Bini LM, Padial AA (2017) Temporal variation in phytoplankton beta diversity patterns and metacommunity structures across subtropical reservoirs. Freshw Biol 62:751–766CrossRefGoogle Scholar
  71. Zorzal-Almeida S, Bini LM, Bicudo DC (2017) Beta diversity of diatoms is driven by environmental heterogeneity, spatial extent and productivity. Hydrobiologia 800:7–16CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Departamento de EcologiaInstituto de BotânicaSão PauloBrazil
  2. 2.Laboratório de Análise e Síntese em Biodiversidade, Departamento de Botânica, Programa de Pós-graduação em Ecologia e ConservaçãoUniversidade Federal do ParanáCuritibaBrazil
  3. 3.Department of BioscienceAarhus UniversitySilkeborgDenmark
  4. 4.Arctic Research Centre (ARC)Aarhus UniversityAarhusDenmark
  5. 5.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  6. 6.Departamento de GeoquímicaUniversidade Federal FluminenseNiteróiBrazil
  7. 7.Institute of Geosystems and BioindicationTechnische Universität BraunschweigBraunschweigGermany

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