Biological Invasions

, Volume 14, Issue 7, pp 1353–1363 | Cite as

Lower biodiversity of native fish but only marginally altered plankton biomass in tropical lakes hosting introduced piscivorous Cichla cf. ocellaris

  • Rosemberg F. Menezes
  • José Luiz Attayde
  • Gissell Lacerot
  • Sarian Kosten
  • Leonardo Coimbra e Souza
  • Luciana S. Costa
  • Egbert H. Van Nes
  • Erik Jeppesen
Original Paper


We compared the species richness and abundance of fish, zooplankton and phytoplankton in nine mesotrophic coastal shallow lakes (Northeastern Brazil) with and without the exotic predator cichlid tucunaré or ‘peacock bass’ (Cichla cf. ocellaris). We hypothesized that the introduction of tucunaré would lead to decreased abundance and species diversity of native fish assemblages and cause indirect effects on the abundance and species diversity of the existing communities of zooplankton and phytoplankton and on water transparency. Our hypotheses were only partly confirmed. Although fish richness and diversity were, in fact, drastically lower in the lakes hosting tucunaré, no significant differences were traced in total fish catch per unit of effort, zooplankton and phytoplankton biomass, plankton diversity or the zooplankton:phytoplankton biomass (TZOO:TPHYTO) ratio. However, zooplankton biomass and TZOO:TPHYTO tended to be higher and the phytoplankton biomass lower in lakes with tucunaré. Our analyses therefore suggest that the introduction of tucunaré had marked effect on the fish community structure and diversity in these shallow lakes, but only modest cascading effects on zooplankton and phytoplankton.


Biological invasion Cichla Piscivorous fish Primary production Shallow tropical lakes Trophic cascade 



We thank Michele Rodrigues and Zeca Rodrigues for their hospitality during the field campaign, Andy Lotter, Fabrício Camacho, Elinez Rocha, Nils Okun, Jandeson Brasil, Wanessa Sousa and Vanessa Mosca for field assistance, and Anne Mette Poulsen and Kirsten van der Meer for reviewing the English grammar of the article. We also acknowledge the two anonymous reviewers for providing valuable comments and suggestions to improve our manuscript. Funding was given by NWO/WOTRO, The National Geographic Society, The Schure-Beijerinck-Popping fund, Kosten Watersport bv., Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Banco de Seguros del Estado through the SALGA project, the EU REFRESH and EU WISER projects, CLEAR (a Villum Kann Rasmussen Centre of Excellence project), the Danish Research Council for Nature and Universe (272-08-0406) and CRES.


  1. Agostinho AA, Julio HF Jr (1996) Ameaça ecológica: peixes de outras águas. Ciência Hoje 21(124):36–44Google Scholar
  2. Agostinho AA, Gomes LC, Latini JD (2004) Fisheries management in Brazilian reservoirs: lessons from/for South America. Interciencia 29(6):334–338Google Scholar
  3. Appelberg M (2000) Swedish standard methods for sampling freshwater fish with multi-mesh gillnets. Fiskeriverket, GöteborgGoogle Scholar
  4. Bertolo A, Carignan R, Magnan P, Pinel-Alloul B, Planas D, Garcia E (2005) Decoupling of pelagic and littoral food webs in oligotrophic Canadian Shield lakes. Oikos 111:534–546CrossRefGoogle Scholar
  5. Borer ET, Seabloom EW, Shurin JB, Anderson KE, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2005) What determines the strength of a trophic cascade? Ecology 86(2):528–537CrossRefGoogle Scholar
  6. Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzing A, Hillbricht-Ilkowska A, Kurasawa H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Nor J Zool 24:419–456Google Scholar
  7. Carpenter SR, Kitchell JF (1993) The trophic cascade in lakes. Cambridge University Press, Great BritainCrossRefGoogle Scholar
  8. Carpenter SR, Christensen DL, Cole JJ, Cottingham KL, He X, Hodgson JR, Kitchell JF, Knight SE, Pace ML, Post DM, Schindler DE, Voichick N (1995) Biological control of eutrophication in lakes. Environ Sci Technol 29:784–785CrossRefGoogle Scholar
  9. Carpenter SR, Cole JJ, Hodgson JR, Kitchell JF, Pace ML, Bade D, Cottingham KL, Essington TE, Houser JN, Schindler DE (2001) Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecol Monogr 71(2):163–186CrossRefGoogle Scholar
  10. Clavero M, García-Berthou E (2005) Invasive species are leading cause of animal extinctions. Trends Ecol Evol 20(3):110PubMedCrossRefGoogle Scholar
  11. Culver DA, Boucherle MM, Bean DJ, Fletcher JW (1985) Biomass of freshwater crustacean zooplankton from length-weight regressions. Can J Fish Aquat Sci 42:1380–1390CrossRefGoogle Scholar
  12. Cunha EMS, Silveira IM, Nogueira AMB, Vilaça JG (1990) Análise ambiental do setor costeiro Maxaranguape—Touros/RN. In: Anais do Congresso Brasileiro de Geologia, 36, Natal, vol 2, pp 770–783Google Scholar
  13. Danger M, Lacroix G, Kâ S, Ndour EH, Corbin D, Lazzaro X (2009) Food-web structure and functioning of temperate and tropical lakes: a stoichiometric viewpoint. Ann Limnol Int J Limnol 45:11–21CrossRefGoogle Scholar
  14. Dumont HJ, Van de Velde I, Dumont S (1975) The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19:75–97CrossRefGoogle Scholar
  15. Eby LA, Roach WJ, Crowder LB, Stanford JA (2006) Effects of stocking-up freshwater food webs. Trends Ecol Evol 21:576–584PubMedCrossRefGoogle Scholar
  16. Fager EW (1972) Diversity: a sampling study. Am Nat 106:293–310CrossRefGoogle Scholar
  17. Fernando CH (1991) Impacts of fish introductions in tropical Asia and América. Can J Fish Aquat Sci 48(Suppl. 1):24–32CrossRefGoogle Scholar
  18. Fisher GW, Grant WE (1994) Use of a native predator to control overcrowding in warm-water polyculture ponds: simulation of a tucunare (Cichla monoculus)-tilapia (Oreochromis niloticus) system. Ecol Model 72:205–227CrossRefGoogle Scholar
  19. Gelós M, Teixeira-de Mello F, Goyenola G, Iglesias C, Fosalba C, García-Rodríguez JP, Pacheco S, García S, Meerhoff M (2010) Seasonal and diel changes in fish activity and potential cascading effects in subtropical shallow lakes with different water transparency. Hydrobiologia 646(1):173–185CrossRefGoogle Scholar
  20. Godinho AL, Fonseca MT, Araújo LM (1994) The ecology of predator fish introductions: the case of Rio Doce valley lakes. In: Pinto-Coelho RM, Giani A, von Sperling E (eds) Ecology and human impact on lakes and reservoirs in Minas Gerais with special reference to future development and management strategies. Belo Horizonte, SEGRAC, pp 77–83Google Scholar
  21. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  22. Güntzel AM, Matsumura-Tundisi T, Rocha O (2003) Life cycle of Macrothrix flabelligera Smirnov, 1992 (Cladocera, Macrothricidae), recently reported from the Neotropical region. Hydrobiologia 490:87–92CrossRefGoogle Scholar
  23. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19(9):470–474PubMedCrossRefGoogle Scholar
  24. Hansson LA, Annadotter H, Bergman E, Stellan FH, Jeppesen E, Kairesalo T, Luokkanen E, Nilsson PA, Søndergaard M, Strand J (1998) Biomanipulation as an application food-chain theory: constraints, synthesis, and recommendations for temperate lakes. Ecosystems 1(6):558–574CrossRefGoogle Scholar
  25. Heck KL, VanBelle G Jr, Simberloff DS (1975) Explicit calculation of the rarefaction diversity measurements and the determination of sufficient sample size. Ecology 56:1459–1461CrossRefGoogle Scholar
  26. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54(2):427–432CrossRefGoogle Scholar
  27. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  28. Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586CrossRefGoogle Scholar
  29. James FC, Rathbun S (1981) Rarefaction, relative abundance, and diversity of avian communities. Auk 98:785–800Google Scholar
  30. Jeppesen E, Søndergaard M, Kanstrup E, Petersen B, Henriksen RB, Hammershøj M, Mortensen E, Jensen JP, Have A (1994) Does the impact of nutrients on the biological structure and function of brackish and freshwater lakes differ? Hydrobiologia 275(276):15–30CrossRefGoogle Scholar
  31. Jeppesen E, Jensen JP, Jensen C, Faafeng B, Brettum P, Hessen D, Søndergaard M, Lauridsen T, Christoffersen K (2003) The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: study of 466 lakes from the temperate zone to the arctic. Ecosystems 6:313–325CrossRefGoogle Scholar
  32. Jeppesen E, Meerhoff M, Jacobsen BA, Hansen RS, Søndergaard M, Jensen JP, Lauridsen TL, Mazzeo N, Branco CWC (2007) Restoration of shallow lakes by nutrient control and biomanipulation—the successful strategy varies with lake size and climate. Hydrobiologia 581:269–285CrossRefGoogle Scholar
  33. Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SAJ, De Meester L, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM, Mazzeo N, Iglesias C, Reizenstein M, Malmquist HJ, Liu ZW, Balayla D, Lazzaro X (2010) Impacts of climate warming on lake fish community structure and dynamics, and potential ecosystem effects. Hydrobiologia 646:73–90CrossRefGoogle Scholar
  34. Kosten S, Lacerot G, Jeppesen E, da Motta Marques D, van Nes EH, Mazzeo N, Scheffer M (2009) Effects of submerged vegetation on water clarity across climates. Ecosystems 12:1117–1129CrossRefGoogle Scholar
  35. Latini AO, Petrere M Jr (2004) Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fish Manag Ecol 11:71–79CrossRefGoogle Scholar
  36. Lazzaro X (1997) Do the trophic cascade hypothesis and classical biomanipulation approaches apply to tropical lakes and reservoirs? 26th Congress of the international-association-of-theoretical-and-applied-limnology. In: International association of theoretical and applied limnology—proceedings, vol 26, Part 2, pp 719–730Google Scholar
  37. Lund JWG, Kipling C, Lecren ED (1958) The inverted microscope method of estimating algae number and the statistical basis of estimating by counting. Hydrobiologia 11:143–170CrossRefGoogle Scholar
  38. MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of chance in degraded ecosystems? Ecology 86(1):42–55CrossRefGoogle Scholar
  39. Mack RN, Simberloff D, Londsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  40. Margalef R (1983) Limnologia. Ômega, BarcelonaGoogle Scholar
  41. McCauley E (1984) The estimation of the abundance and biomass of zooplankton in samples. In: Downing JA, Riegler FH (eds) A manual on methods for the assesment of secondary productivity in fresh waters. Blackwell, Oxford, pp 228–265Google Scholar
  42. Meiners SJ, Cadenasso ML (2005) The relationship between community diversity and exotic plants: cause or consequence of invasion?. Birkhauser Verlag Ag, BaselGoogle Scholar
  43. Molina WF, Gurgel HCB, Vieira LJS, Canan B (1996) Ação de um predador exógeno sobre um ecossistema aquático equilibrado, I Extinções locais e medidas de conservação genética. UNIMAR 18(2):335–345Google Scholar
  44. NNI (1986) Water—Photometric determination of the content of dissolved orthophosphate and the total content of phosphorous compounds by continuous flow analysis. In: Nederlands Normalisatie-instituut, Normcommissie 390 147 “Waterkwaliteit”, p 8Google Scholar
  45. NNI (1990) Water—Photometric determination of the content of ammonium nitrogen and the sum of the contents of ammoniacal and organically bound nitrogen according to Kjeldahl by continuous flow analysis. Pages 8 in. Nederlands Normalisatie-instituut, Normcommissie 390 147 “Waterkwaliteit”Google Scholar
  46. Nusch E (1980) Comparison of different methods for chlorophyll and phaeopigments determination. Arch Hydrobiol Beih Ergeb Limnol 14:14–36Google Scholar
  47. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17-4.
  48. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14(12):483–488PubMedCrossRefGoogle Scholar
  49. Paiva MP (1974) Crescimento, alimentação e reprodução de traíra, Hoplias malabaricus (Bloch), no nordeste brasileiro. Imprensa Universitária da UFC, FortalezaGoogle Scholar
  50. Pauli HR (1989) A new method to estimate individual dry weight of rotifers. Hydrobiologia 186(187):355–361CrossRefGoogle Scholar
  51. Pelicice FM, Agostinho AA (2009) Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biol Invasion 11:1789–1801CrossRefGoogle Scholar
  52. Persson L (1999) Abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85(3):385–397CrossRefGoogle Scholar
  53. Pinto-Coelho RM, Bezerra-Neto JF, Miranda F, Mota TG, Resck R, Santos AM, Maia-Barbosa PM, Mello NAST, Marques MM, Barbosa FAR (2008) The inverted trophic cascade in tropical plankton communities: Impacts of exotic fish in the Middle Rio Doce lake district, Minas Gerais, Brazil. Braz J Biol 68(4, Suppl):1025–1037PubMedCrossRefGoogle Scholar
  54. Rahel FJ (2002) Homogenization of freshwater faunas. Ann Rev Ecol Syst 33:291–315CrossRefGoogle Scholar
  55. Ruttner-Kolisko A (1977) Suggestions for biomass calculation of plankton rotifers. Arch Hydrobiol Beih Ergeb Limnol 8:71–76Google Scholar
  56. Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243–282CrossRefGoogle Scholar
  57. Schindler DE, Scheuerell M (2002) Habit coupling in lake ecosystems. Oikos 98:117–189CrossRefGoogle Scholar
  58. Shannon C, Weaver W (1949) The mathematical theory of communication. University Illinois Press, UrbanaGoogle Scholar
  59. Simberloff D (1972) Properties of the rarefaction diversity measurement. Am Nat 106:414–418CrossRefGoogle Scholar
  60. Simberloff D (2003) Confronting introduced species: a form of xenophobia? Biol Invasion 5(3):179–192CrossRefGoogle Scholar
  61. Simon KS, Townsend CR (2003) Impacts of freshwater invaders at different levels of ecological organization, with emphasis on salmonids and ecosystem consequences. Freshw Biol 48:982–994CrossRefGoogle Scholar
  62. Simpson EH (1949) Measurement of diversity. Nature 163:688CrossRefGoogle Scholar
  63. Søndergaard M, Liboriussen L, Pedersen AR, Jeppesen E (2008) Lake restoration by fish removal: long-term effects in 36 Danish lakes. Ecosystems 11:1291–1305CrossRefGoogle Scholar
  64. Tessier AJ, Woodruff P (2002) Cryptic trophic cascade along a gradient of lake. Ecology 83(5):1263–1270CrossRefGoogle Scholar
  65. Uhelinger V (1964) Étude statisque des méthodes de dénobrement planctonique. Arch Sci 17:121–123Google Scholar
  66. Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitt Int Ver Theo Angew Limnol 9:1–38Google Scholar
  67. Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the lake back together: reintegrating benthic pathways into lake food web models. Bioscience 52:44–55CrossRefGoogle Scholar
  68. Zaret TM, Paine RT (1973) Species introduction in a tropical lake. Science 182:449–455PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Rosemberg F. Menezes
    • 1
    • 2
    • 3
  • José Luiz Attayde
    • 1
  • Gissell Lacerot
    • 4
  • Sarian Kosten
    • 5
    • 10
  • Leonardo Coimbra e Souza
    • 6
  • Luciana S. Costa
    • 7
  • Egbert H. Van Nes
    • 5
  • Erik Jeppesen
    • 2
    • 8
    • 9
  1. 1.Centro de Biociências, Departamento de Botânica, Ecologia e ZoologiaUniversidade Federal do Rio Grande do NorteNatalBrazil
  2. 2.Department of BioscienceAarhus UniversitySilkeborgDenmark
  3. 3.Department of BioscienceAarhus UniversityAarhusDenmark
  4. 4.Grupo Interdisciplinario en Ecología Acuática de Ambientes Marinos y Continentales, Centro Universitario Regional EsteUniversidad de la RepúblicaRochaUruguay
  5. 5.Department of Aquatic Ecology and Water Quality ManagementWageningen UniversityWageningenThe Netherlands
  6. 6.Núcleo de Estudos Limnológicos—NEL, Departamento de Zoologia, Instituto de Biologia (IB)Universidade Federal do Estado do Rio de Janeiro—UNIRIORio de JaneiroBrazil
  7. 7.Departamento de Botânica, Museu NacionalUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  8. 8.Greenland Climate Research Centre, Greenland Institute of Natural ResourcesNuukGreenland
  9. 9.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  10. 10.Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB)Berlin, NeuglobsowGermany

Personalised recommendations