Microbial Ecology

, Volume 68, Issue 1, pp 47–59 | Cite as

Diversity of Benthic Biofilms Along a Land Use Gradient in Tropical Headwater Streams, Puerto Rico

  • Sofía Burgos-Caraballo
  • Sharon A. Cantrell
  • Alonso Ramírez
Microbiology of Aquatic Systems

Abstract

The properties of freshwater ecosystems can be altered, directly or indirectly, by different land uses (e.g., urbanization and agriculture). Streams heavily influenced by high nutrient concentrations associated with agriculture or urbanization may present conditions that can be intolerable for many aquatic species such as macroinvertebrates and fishes. However, information with respect to how benthic microbial communities may respond to changes in stream ecosystem properties in relation to agricultural or urban land uses is limited, in particular for tropical ecosystems. In this study, diversity of benthic biofilms was evaluated in 16 streams along a gradient of land use at the Turabo watershed in Puerto Rico using terminal restriction fragment length polymorphism. Diversity indices and community structure descriptors (species richness, Shannon diversity, dominance and evenness) were calculated for both bacteria and eukaryotes for each stream. Diversity of both groups, bacteria and eukaryotes, did not show a consistent pattern with land use, since it could be high or low at streams dominated by different land uses. This suggests that diversity of biofilms may be more related to site-specific conditions rather than watershed scale factors. To assess this contention, the relationship between biofilm diversity and reach-scale parameters (i.e., nutrient concentrations, canopy cover, conductivity, and dissolved oxygen) was determined using the Akaike Information Criterion (AICc) for small sample size. Results indicated that nitrate was the variable that best explained variations in biofilm diversity. Since nitrate concentrations tend to increase with urban land use, our results suggest that urbanization may indeed increase microbial diversity indirectly by increasing nutrients in stream water.

References

  1. 1.
    Allan D (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Evol Syst 35:257–284CrossRefGoogle Scholar
  2. 2.
    Allison S, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 105(Supplement 1):11512–11519PubMedCentralCrossRefPubMedGoogle Scholar
  3. 3.
    Battin TJ, Kaplan LA, Newbold JD, Cheng X, Hansen C (2003) Effects of current velocity on the nascent architecture of stream microbial biofilms. Appl Environ Microbiol 69(9):5443–5452PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Blackwood CB, Hudleston D, Zak DR, Buyer J (2007) Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl Environ Microbiol 73(16):5276–5283PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Boëchat IG, Krüger A, Giani A, Figueredo CC, Gücker B (2011) Agricultural land-use affects the nutritional quality of stream microbial communities. FEMS Microbiol Ecol 77(3):568–576CrossRefPubMedGoogle Scholar
  6. 6.
    Burgos-Caraballo S (2013) Function and diversity of benthic biofilm communities in tropical stream ecosystems: the relevance of land use and reach factors. Dissertation, University of Puerto Rico, Rio Piedras (Puerto Rico). ProQuest Dissertations and Theses, 110. Retrieved from http://search.proquest.com/docview/1286729784?accountid=44825. (1286729784)
  7. 7.
    Camargo JA, Alonso A, Salamanca A (2005) Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere 58(9):1255–1267Google Scholar
  8. 8.
    Carrino-Kyker SR, Swanson AK, Burke DJ (2011) Changes in eukaryotic microbial communities of vernal pools along an urban–rural land use gradient. Aquat Microb Ecol 62(1):13–24CrossRefGoogle Scholar
  9. 9.
    De Jesus-Crespo R, Ramirez A (2011) Effects of urbanization on stream physicochemistry and macroinvertebrate assemblages in a tropical urban watershed in Puerto Rico. J N Am Benthol Soc 30(3):739–750CrossRefGoogle Scholar
  10. 10.
    Dopheide A, Lear G, Stott R, Lewis G (2009) Relative diversity and community structure of ciliates in stream biofilms according to molecular and microscopy methods. Appl Environ Microbiol 75(16):5261–5272PubMedCentralCrossRefPubMedGoogle Scholar
  11. 12.
    Falkowski R (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  12. 13.
    Fierer N, Morse JL, Berthrong ST, Bernhardt BS, Jackson RB (2007) Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecology 88(9):2162–2173CrossRefPubMedGoogle Scholar
  13. 15.
    Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe GC et al (2005) Global consequences of land use. Science 309(5743):570–574CrossRefPubMedGoogle Scholar
  14. 16.
    Fujioka RS, Shizumura LK (1985) Clostridium perfringens, a reliable indicator of stream water quality. J Water Pollut Control Fed 57(10):986–992Google Scholar
  15. 17.
    Grant A, Ogilvie LA (2003) Terminal restriction fragment length polymorphism data analysis. Appl Environ Microbiol 69(10):6342–6343PubMedCentralCrossRefPubMedGoogle Scholar
  16. 18.
    Helmer EH, Ramos O, Del M López T, Quiñones M, Díaz W (2002) Mapping the forest type and land cover of Puerto Rico, a component of the Caribbean biodiversity hotspot. Caribb J Sci 38(3–4):165–183Google Scholar
  17. 19.
    Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge D, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75(1):3–35CrossRefGoogle Scholar
  18. 20.
    Humber JF, Dorigo U, Cecchi P, Le Berre B, Debrosas D, Bouvy M (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11(9):2339–2350CrossRefGoogle Scholar
  19. 21.
    Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19(2):101–108CrossRefPubMedGoogle Scholar
  20. 22.
    Kobayashi Y, Kim C, Yoshimizu C, Kohzu A, Tayasu I, Nagata T (2009) Longitudinal changes in bacterial community composition in river epilithic biofilms: influence of nutrients and organic matter. Aquat Microb Ecol 54(2):135–152CrossRefGoogle Scholar
  21. 23.
    Lear G, Boothroyd IKG, Turner SJ, Roberts K, Lewis SGD (2009) A comparison of bacteria and benthic invertebrates as indicators of ecological health in streams. Freshw Biol 54(7):1532–1543CrossRefGoogle Scholar
  22. 24.
    Lefrançois E, Coat S, Lepoint G, Vachiéry N, Gros O, Monti D (2011) Epilithic biofilm as a key factor for small-scale river fisheries on Caribbean islands. Fish Manag Ecol 18(3):211–220CrossRefGoogle Scholar
  23. 25.
    Legendre P, Legendre L (1998) Numerical ecology. 2nd English edn. Elsevier Science BV, Amsterdam, p XVGoogle Scholar
  24. 26.
    Lenat DR, Crawford JK (1994) Effects of land use on water quality and aquatic biota of three North Carolina piedmont streams. Hydrobiology 294(3):185–199CrossRefGoogle Scholar
  25. 27.
    Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63(11):4516–4522PubMedCentralPubMedGoogle Scholar
  26. 29.
    Lock MA (1993) Attached microbial communities in rivers. In: Ford TE (ed) Aquatic microbiology: an ecological approach. Blackwell Scientific Publication, Oxford, pp 113–138Google Scholar
  27. 30.
    Lyautey E, Teissier S, Charcosset JY, Rols JL, Garabetian F (2003) Bacterial diversity of epilithic biofilm assemblages of an anthropised river section, assessed by DGGE analysis of a 16S rDNA fragment. Aquat Microb Ecol 33(3):217–224CrossRefGoogle Scholar
  28. 31.
    Magurran AE (2004) Measuring biological diversity. Blackwell Science, OxfordGoogle Scholar
  29. 32.
    McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software, OregonGoogle Scholar
  30. 33.
    Mills MM, Moore CM, Langlois R, Milne A, Achterberg E, Nachtigall K, Lochte K, Geider RJ, La Roche J (2008) Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol Oceanogr 53(2):824–834CrossRefGoogle Scholar
  31. 34.
    Morgan RP, Cushman SF (2005) Urbanization effects on stream fish assemblages in Maryland, USA. J N Am Benthol Soc 24(3):643–655CrossRefGoogle Scholar
  32. 35.
    Mueller-Spitz SR, Stewart LB, Val-Kulmp J, McLellan SL (2010) Freshwater suspended sediments and sewage are reservoirs for enterotoxin-positive Clostridium perfringens. Appl Environ Microbiol 76(16):5556–5562PubMedCentralCrossRefPubMedGoogle Scholar
  33. 36.
    Osborn AM, Moore ERB, Timmis KN (2000) An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2(1):39–50CrossRefPubMedGoogle Scholar
  34. 37.
    Paul BJ, Duthie HC, Taylor WD (1991) Nutrient cycling by biofilms in running waters of differing phosphorus status. J N Am Benthol Soc 10(1):31–41CrossRefGoogle Scholar
  35. 38.
    Paul M, Meyer JL (2001) Streams in the urban landscape. Annu Rev Ecol Syst 32:333–365CrossRefGoogle Scholar
  36. 39.
    Perryman SE, Rees GN, Walsh CJ (2008) Analysis of denitrifying communities in streams from an urban and non-urban catchment. Aquat Ecol 42(1):95–101CrossRefGoogle Scholar
  37. 40.
    Puckett LJ (1994) Nonpoint and point sources of nitrogen in major watersheds of the United States. US Geological Survey. Water resources investigation Report 94–4001Google Scholar
  38. 41.
    Ramirez A, De Jesus-Crespo R, Martino-Cardona DM, Martinez-Rivera N, Burgos-Caraballo S (2009) Urban streams in Puerto Rico: what can we learn from the tropics? J N Am Benthol Soc 28(4):1070–1079CrossRefGoogle Scholar
  39. 42.
    Rees GN, Baldwin DS, Watson GO, Perryman S, Nielsen D (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie Van Leeuwenhoek 86(4):339–347CrossRefPubMedGoogle Scholar
  40. 44.
    Rubin MA, Leff LG (2007) Nutrients and other abiotic factors affecting bacterial communities in an Ohio River (USA). Microb Ecol 54(2):374–383CrossRefPubMedGoogle Scholar
  41. 45.
    Shyu C, Soule T, Bent SJ, Foster JA, Forney LJ (2007) MiCA: a web-based tool for the analysis of microbial communities based on terminal-restriction fragment length polymorphisms of 16S and 18S rRNA genes. J Microb Ecol 53(4):562–570CrossRefGoogle Scholar
  42. 46.
    Szabo KE, Makk J, Kiss TK, Eiler A, Acs E, Toth B, Kiss AK, Bertilsson S (2008) Sequential colonization by river peryphyton analysed by microscopy and molecular fingerprinting. Freshw Biol 53(7):1359–1371CrossRefGoogle Scholar
  43. 47.
    Veve T, Taggart B (1996) Atlas of ground-water resources in Puerto Rico and the US Virgin Islands. U. S. Geological Survey, San JuanGoogle Scholar
  44. 48.
    Walsh CJ, Roy AH, Feminella JW, Cottingham PD, Groffman PM, Morgan RP II (2005) The urban stream syndrome: current knowledge and the search for a cure. J N Am Benthol Soc 24(3):706–723CrossRefGoogle Scholar
  45. 49.
    Wang SY, Sudduth EB, Wallenstein MD, Wright JP, Bernhardt ES (2011) Watershed urbanization alters the composition and function of stream bacterial communities. PLoS ONE 6(8):e22972PubMedCentralCrossRefPubMedGoogle Scholar
  46. 50.
    Washington VJ, Lear L, Neale MW, Lewis GD (2013) Environmental effects on biofilm bacterial communities: a comparison of natural and anthropogenic factors in New Zealand streams. Freshw Biol 58(11):2277–2286Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Sofía Burgos-Caraballo
    • 1
  • Sharon A. Cantrell
    • 2
  • Alonso Ramírez
    • 3
  1. 1.Department of BiologyUniversity of Puerto RicoSan JuanUSA
  2. 2.Department of BiologyUniversidad del TuraboGuraboUSA
  3. 3.Department of Environmental SciencesUniversity of Puerto RicoSan JuanUSA

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