Hydrobiologia

, Volume 632, Issue 1, pp 347–353 | Cite as

Bottom-up regulation of bacterial growth in tropical phytotelm bromeliads

  • Camilla S. Haubrich
  • Aliny P. F. Pires
  • Francisco A. Esteves
  • Vinicius F. Farjalla
Short research note

Abstract

Evaluating the factors that regulate bacterial growth in natural ecosystems is a major goal of modern microbial ecology. Phytotelm bromeliads have been used as model ecosystems in aquatic ecology as they provide many independent replicates in a small area and often encompass a wide range of limnological conditions. However, as far as we know, there has been no attempt to evaluate the main regulatory factors of bacterial growth in these aquatic ecosystems. Here, we used field surveys to evaluate the main bottom-up factors that regulate bacterial growth in the accumulated water of tank bromeliads. Bacterial production, water temperature, water color, chlorophyll-a, and nutrient concentrations were determined for 147 different tank bromeliads in two different samplings. Bromeliad position and the season of sampling were also noted. Bacterial production was explained by ion ammonium concentration and water temperature, but the total variance explained was low (r 2 = 0.104). Sampling period and bromeliad position were included in additional models that gave empirical support for predicting bacterial production. Bromeliad water tanks are extremely variable aquatic ecosystems in space (among bromeliads) and time (environmental conditions can change within hours), and it is well known that bacterial production responds rapidly to environmental change. Therefore, we concluded that several factors could independently regulate bacterial growth in phytotelm bromeliads depending on the characteristics of each bromeliad, such as location, amount of detritus, and ambient nutrient concentrations. A clear bottom-up limitation pattern of bacterial production in tropical phytotelm bromeliads was not found.

Keywords

Bacterial production Bottom-up regulation Bromeliads Phytotelmata Model ecosystems 

Notes

Acknowledgments

C.S.H. and A.P.F.P. are, respectively, grateful to PIBIC-UFRJ and FAPERJ Institution for undergraduate scholarships. D.S. Srivastava kindly reviewed early draft versions of the manuscript and offered helpful suggestions for its improvement. Petroleo Brasileiro SA (PETROBRAS) supported this research.

References

  1. Azam, F. & F. Malfatti, 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology 5: 782–791.PubMedCrossRefGoogle Scholar
  2. Benzing, D. H., K. Henderson, B. Kessel & J. Sulak, 1976. The absorptive capacities of bromeliad trichomes. American Journal of Botany 63: 1009–1014.CrossRefGoogle Scholar
  3. Berg, A., B. Orthen, E. A. Mattos, H. M. Duarte & U. Lüttge, 2004. Expression of crassulacean acid metabolism in Clusia hilariana Schelechtendal in different stages of development in the field. Trees 18: 553–558.CrossRefGoogle Scholar
  4. Carlson, R. E., 1977. A trophic state index for lakes. Limnology and Oceanography 22: 361–369.Google Scholar
  5. Carpenter, S. R., 1996. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77: 677–680.CrossRefGoogle Scholar
  6. Cascante-Marin, A., J. H. D. Wolf, J. G. B. Oostermeijer, J. C. M. den Nijs, O. Sanahuja & A. Duran-Apuy, 2006. Epiphytic bromeliad communities in secondary and mature forest in a tropical premontane area. Basic and Applied Ecology 7: 520–532.CrossRefGoogle Scholar
  7. Church, M. J., D. A. Hutchins & H. W. Ducklow, 2000. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Applied and Environmental Microbiology 66: 455–466.PubMedCrossRefGoogle Scholar
  8. Downing, J. A., Y. T. Prairie, J. J. Cole, C. M. Duarte, L. J. Tranvik, R. G. Striegl, W. H. McDowell, P. Kortelainen, N. F. Caraco, J. M. Melack & J. J. Middelburg, 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnology and Oceanography 51: 2388–2397.Google Scholar
  9. Drenner, R. W. & A. Mazumder, 1999. Microcosm experiments have limited relevance for community and ecosystem ecology: comment. Ecology 80: 1081–1085.Google Scholar
  10. Farjalla, V. F., F. A. Esteves, R. L. Bozelli & F. Roland, 2002. Nutrient limitation of bacterial production in clear water Amazonian ecosystems. Hydrobiologia 489: 197–205.CrossRefGoogle Scholar
  11. Farjalla, V. F., T. Laque, A. L. Suhett, A. M. Amado & F. A. Esteves, 2005. Diel variation of bacterial abundance and productivity in tropical costal lagoons: the importance of bottom-up factors in a short-time scale. Acta Limnologica Brasiliensia 17: 373–383.Google Scholar
  12. Farjalla, V. F., D. A. Azevedo, F. A. Esteves, R. L. Bozelli, F. Roland & A. Enrich-Prast, 2006. Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microbial Ecology 52: 334–344.PubMedCrossRefGoogle Scholar
  13. Foissner, W., M. Strüder-Kypke, G. W. M. van der Staay, S.-Y. Moon-van der Staay & J. H. P. Hackstein, 2003. Endemic ciliates from tank bromeliads: a combined morphological, molecular, and ecological study. European Journal of Protistology 39: 365–372.CrossRefGoogle Scholar
  14. Golterman, H. L., R. S. Clymo & M. A. M. Ohnstad, 1978. Methods for Physical and Chemical Analysis of Fresh Waters. Blackwell, Oxford: 214.Google Scholar
  15. Granéli, W., S. Bertilsson & A. Philibert, 2004. Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquatic Science 66: 430–439.CrossRefGoogle Scholar
  16. Guimarães-Souza, B. A., G. B. Mendes, L. Bento, H. Marotta, A. L. Santoro, F. A. Esteves, L. Pinho, V. F. Farjalla & A. Enrich-Prast, 2006. Limnological parameters in the water accumulated in tropical bromeliads. Acta Limnologica Brasiliensia 18: 47–53.Google Scholar
  17. Hall, E. K. & J. B. Cotner, 2007. Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities. Aquatic Microbial Ecology 49: 35–45.CrossRefGoogle Scholar
  18. Hu, C. M., F. E. Muller-Karger & R. G. Zepp, 2002. Absorbance, absorption coefficient, and apparent quantum yield: a comment on common ambiguity in the use of these optical concepts. Limnology and Oceanography 47: 1261–1267.Google Scholar
  19. Inselsbacher, E., C. A. Cambui, A. Richter, C. F. Stange, H. Mercier & W. Wanek, 2007. Microbial activities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea. New Phytologist 175: 311–320.PubMedCrossRefGoogle Scholar
  20. Jansson, M., A.-K. Bergström, D. Lymer, T. Vrede & J. Karlsson, 2006. Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microbial Ecology 52: 358–364.PubMedCrossRefGoogle Scholar
  21. Kitching, R. L., 2000. Food Webs and Container Habitats: The Natural History and Ecology of Phytotelmata. Cambridge University Press, Cambridge.Google Scholar
  22. Koroleff, F., 1978. Determination of ammonia. In Grasshoff, K., M. Ehrhardt & K. Remling (eds.), Methods of Seawater Analysis. Verlag Chemie, Republic of Germany: 151–157.Google Scholar
  23. Kritzberg, E. S., J. J. Cole, M. L. Pace & W. Graneli, 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquatic Microbial Ecology 38: 103–111.CrossRefGoogle Scholar
  24. Lennon, J. T. & L. E. Pfaff, 2005. Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquatic Microbial Ecology 39: 107–119.CrossRefGoogle Scholar
  25. Ngai, J. T. & D. S. Srivastava, 2006. Predators accelerate nutrient cycling in a bromeliad ecosystem. Science 314: 963.PubMedCrossRefGoogle Scholar
  26. Pace, M. L. & J. J. Cole, 1996. Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnology and Oceanography 41: 1448–1460.CrossRefGoogle Scholar
  27. Pomeroy, L. R. & W. J. Wiebe, 2001. Temperature and substrate as interactive limiting factors for marine heterotrophic bacteria. Aquatic Microbial Ecology 23: 187–204.CrossRefGoogle Scholar
  28. Rangel, T. F. L. V. B., J. A. F. Diniz-Filho & L. M. Bini, 2006. Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecology and Biogeography 15: 321–327.CrossRefGoogle Scholar
  29. Rejas, D., K. Muylaert & L. De Meester, 2005. Nutrient limitation of bacteria and sources of nutrients supporting nutrient-limited bacterial growth in an Amazonian floodplain lake. Aquatic Microbial Ecology 39: 57–67.CrossRefGoogle Scholar
  30. Richards, S. A., 2005. Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86: 2805–2814.CrossRefGoogle Scholar
  31. Rocha-Pessoa, T. C., A. F. Nunes-Freitas, L. Cogliatti-Carvalho & C. F. D. Rocha, 2008. Species composition of Bromeliaceae and their distribution at the Massambaba Restinga in Arraial do Cabo, Rio de Janeiro, Brazil. Brazilian Journal of Biology 68: 251–257.CrossRefGoogle Scholar
  32. Salas, R. J. & P. Martino, 1991. A simplified phosphorus trophic state model for warm-water tropical lakes. Water Research 25: 341–350.CrossRefGoogle Scholar
  33. Smith, D. C. & F. Azam, 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Marine Microbial Food Webs 6: 107–774.Google Scholar
  34. Smith, E. M. & Y. T. Prairie, 2004. Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnology and Oceanography 49: 137–147.Google Scholar
  35. Srivastava, D. S., J. Kolasa, J. Bengtsson, A. Gonzalez, S. P. Lawler, T. E. Miller, P. Munguia, T. Romanuk, D. C. Schneider & M. K. Trzcinski, 2004. Are natural microcosms useful model systems for ecology? Trends in Ecology and Evolution 19: 379–384.PubMedCrossRefGoogle Scholar
  36. Wambeke, F., S. Bonnet, T. Moutin, P. Raimbault, G. Alarcon & C. Guieu, 2008. Factors limiting heterotrophic bacterial production in the southern Pacific Ocean. Biogeosciences 5: 833–845.CrossRefGoogle Scholar
  37. Wetzel, R. G. & G. E. Likens, 1991. Limnological Analyses. Springer, New York.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Camilla S. Haubrich
    • 1
    • 2
  • Aliny P. F. Pires
    • 1
    • 2
  • Francisco A. Esteves
    • 1
    • 3
  • Vinicius F. Farjalla
    • 1
    • 3
  1. 1.Lab. Limnologia, Dept. Ecologia, Inst. de BiologiaCCS-UFRJRio de JaneiroBrazil
  2. 2.Programa de Pós-Graduação em EcologiaUFRJ (PPGE-UFRJ)Rio de JaneiroBrazil
  3. 3.Núcleo em Ecologia e Desenvolvimento Sustentável de Macaé (NUPEM/UFRJ), Agência Correio Macaé, Centro, MacaéRio de JaneiroBrazil

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