Skip to main content
Log in

Bottom-up regulation of bacterial growth in tropical phytotelm bromeliads

  • Short research note
  • Published:
Hydrobiologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • Azam, F. & F. Malfatti, 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology 5: 782–791.

    Article  PubMed  CAS  Google Scholar 

  • Benzing, D. H., K. Henderson, B. Kessel & J. Sulak, 1976. The absorptive capacities of bromeliad trichomes. American Journal of Botany 63: 1009–1014.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Carlson, R. E., 1977. A trophic state index for lakes. Limnology and Oceanography 22: 361–369.

    CAS  Google Scholar 

  • Carpenter, S. R., 1996. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77: 677–680.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Drenner, R. W. & A. Mazumder, 1999. Microcosm experiments have limited relevance for community and ecosystem ecology: comment. Ecology 80: 1081–1085.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Granéli, W., S. Bertilsson & A. Philibert, 2004. Phosphorus limitation of bacterial growth in high Arctic lakes and ponds. Aquatic Science 66: 430–439.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kitching, R. L., 2000. Food Webs and Container Habitats: The Natural History and Ecology of Phytotelmata. Cambridge University Press, Cambridge.

    Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Lennon, J. T. & L. E. Pfaff, 2005. Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquatic Microbial Ecology 39: 107–119.

    Article  Google Scholar 

  • Ngai, J. T. & D. S. Srivastava, 2006. Predators accelerate nutrient cycling in a bromeliad ecosystem. Science 314: 963.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pomeroy, L. R. & W. J. Wiebe, 2001. Temperature and substrate as interactive limiting factors for marine heterotrophic bacteria. Aquatic Microbial Ecology 23: 187–204.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Richards, S. A., 2005. Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86: 2805–2814.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Salas, R. J. & P. Martino, 1991. A simplified phosphorus trophic state model for warm-water tropical lakes. Water Research 25: 341–350.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wetzel, R. G. & G. E. Likens, 1991. Limnological Analyses. Springer, New York.

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vinicius F. Farjalla.

Additional information

Handling editor: Luigi Naselli-Flores

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haubrich, C.S., Pires, A.P.F., Esteves, F.A. et al. Bottom-up regulation of bacterial growth in tropical phytotelm bromeliads. Hydrobiologia 632, 347–353 (2009). https://doi.org/10.1007/s10750-009-9841-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-009-9841-6

Keywords

Navigation