Abstract
Microbial processes are key elements in determining the productivity of mangroves, and reductions in these processes reflect the loss of microbial biodiversity and function due to fabricated disturbances. Because nitrogen is a major limiting nutrient for the productivity of these ecosystems, the goal of this study was to determine profiles of inorganic nitrogen combined with several environmental parameters, all in relation to the degree of long-term hydraulic impairment of a tropical, monospecific black mangrove (Avicennia germinans) forest that showed degradation ranging from total loss of mangrove cover to no disturbance. N2-fixation, oxygen levels, and nitrite contents decreased significantly with the severity of the disturbance, and almost null levels were reached in the completely degraded zone, whereas salinity achieved very high values. Concomitantly, total N, ammonium, and P contents and ammonia volatilization increased significantly. Pore-water temperature and pH increased moderately. Other soil physical properties (sand, silt, clay, organic matter, and total C), which varied among the sampling sites, were not correlated with the level of disturbance. Principal component analyses, including environmental and biological parameters, suggested that the most significant finding was the considerable loss of N2-fixation with increasing impairment, which was concomitant with significant increases in volatilization of ammonia and salinity. The results show that microbial N-cycling processes are highly sensitive to salinity and to man-made disturbances that modify the water level and flow.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray J, Sala E (2008) Mangroves in the Gulf of California increase fishery yields. Proc Natl Acad Sci USA 105:10456–10459
Alongi DM (1996) The dynamics of benthic nutrient pools and fluxes in tropical mangrove forests. J Mar Res 54:123–148
Andreote FD, Dias ACF, Taketani RG, Tsai SM, Azevedo JL, Melo I S (2009) The diversity of ammonium-oxidizing archaea and anammox bacteria in Brazilian mangrove sediments. In: 11th Symposium on Aquatic Microbial Ecology, Piran, Slovenia, 30 August to 4 September 2009 (abstract)
Bashan Y, Puente ME, Myrold DD, Toledo GG (1998) In vitro transfer of fixed nitrogen from diazotrophic filamentous cyanobacteria to black mangrove seedlings. FEMS Microbiol Ecol 26:165–170
Beutel MC (2006) Inhibition of ammonia release from anoxic profundal sediments in lakes using hypolimnetic oxygenation. Ecol Eng 28:271–279
Blasco F, Aizpuru M, Gers C (2001) Depletion of the mangroves of continental Asia. Wetlands Ecol Manage 9:245–256
Bosire JO, Dahdough-Guebas F, Walton M, Crona B, Lewis RR, Field C, Kairo JG, Koedam N (2008) Functionality of restored mangroves: a review. Aquat Bot 89:251–259
Boto KG (1982) Nutrient and organic fluxes in mangroves. In: Clough BF (ed) Mangrove ecosystems in Australia: structure, function and management. Australian Institute of Marine Science in Association with Australian National University Press, pp 239–246
Brokaw N, Thompson J (2000) The H for DBH. For Ecol Manage 129:89–91
Buring AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96
Cintron G, Novelli YS (1984) Methods for studying mangrove structure. In: Snedaker SC, Snedaker JG (eds) Mangrove ecosystem: research methods. UNESCO, Paris, pp 91–113
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth, p 91
Dicker HJ, Smith DW (1981) Effects of salinity on acetylene reduction (nitrogen fixation) and respiration in a marine Azotobacter. Appl Environ Microbiol 42:740–744
Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373
Folk RL (1966) A review of grain-size parameters. Sedimentology 6:73–93
Holguin G, Gonzalez-Zamorano P, de-Bashan LE, Mendoza R, Amador E, Bashan Y (2006) Mangrove health in an arid environment encroached by urban development: a case study. Sci Total Environ 363:260–274
Holguin G, Guzman MA, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees, isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol Ecol 101:207–216
Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fert Soils 33:265–278
Howarth RW, Marino R (1988) Nitrogen fixation in freshwater, estuarine and marine ecosystems. 2. Biogeochemical controls. Limnol Oceanogr 33:688–701
Hutchinson GL, Livingston GP (1993) Use of chamber systems to measure trace gas fluxes. In: Harper LA, Mosier AR, Duxbury JM, Rolston DE (eds) Agricultural ecosystem effects on trace gases and global change. ASA Spec. Pbl. No. 55. ASA, CSSA and SSSA, Madison, pp 63–78
Kaly UL, Eugelink G, Robertson AI (1997) Soil conditions in damaged North Queensland mangroves. Estuaries Coast 20:291–300
Kristensen E, Andersen FO, Kofoed LH (1988) Preliminary assessment of benthic community metabolism in a south-east Asian mangrove swamp. Mar Ecol Prog Ser 48:137–145
Lee RY, Joye SB (2006) Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats. Mar Ecol Prog Ser 307:127–141
Lee SY (1995) Mangrove outwelling: a review. Hydrobiologia 295:203–212
Lee SY, Dunn RJK, Young RA, Connolly RM, Dale PER, Dehayr R, Lemckert CJ, McKinnon S, Powell B, Teasdale PR, Welsh DT (2006) Impact of urbanization on coastal wetland structure and function. Austral Ecol 31:149–163
McKee KL, Mendelssohn IA, Hester MW (1988) Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans. Am J Bot 75:1352–1359
Meyer RL, Risgaard-Petersen N, Allen DE (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71:6142–6149
Pessarakli M, Zhou M (1990) Effect of salt stress on nitrogen fixation by different cultivars of green beans. J Plant Nutr 13:611–629
Polman JK, Larkin JM (1988) Properties of in vivo nitrogenase activity in Beggiatoa alba. Arch Microbiol 150:126–130
Primavera JH (1998) Mangroves are nurseries: shrimp populations in mangrove and non-mangrove habitats. Estuar Coast Shelf Sci 46:457–464
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org
Ravikumar S, Kathiresan K, Ignatiammal STM, Selvam MB, Shanthy S (2004) Nitrogen-fixing azotobacters from mangrove habitat and their utility as marine biofertilizers. J Exp Mar Biol Ecol 312:5–17
Sengupta A, Chaudhuri S (1991) Ecology of heterotrophic dinitrogen fixation in the rhizosphere of mangrove plant community at the Ganges River estuary in India. Oecologia 87:560–564
Sjöling S, Mohammed SM, Lyimo TJ, Kyaruzi JJ (2005) Benthic bacterial diversity and nutrient processes in mangroves: impact of deforestation. Estuar Coast Shelf Sci 63:397–406
Strömberg H, Patterson C, Johnstone R (1998) Spatial variations in benthic macrofauna and nutrient dynamics in a mangrove forest subject to intense deforestation: Zanzibar, Tanzania. Ambio 27:734–739
Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801
Spalding M, Kainuma M, Collins L (2010) World atlas of mangroves. Earthscan, London, p 319
Strangmann A, Bashan Y, Giani L (2008) Methane in pristine and impaired mangrove soils and its possible effect on establishment of mangrove seedlings. Biol Fert Soils 44:511–519
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bulletin 167 (2nd edn). Fisheries Research Board of Canada, pp 310
Toledo G, Bashan Y, Soeldner A (1995a) In vitro colonization and increase in nitrogen fixation of seedling roots of black mangrove inoculated by a filamentous cyanobacteria. Can J Microbiol 41:1012–1020
Toledo G, Bashan Y, Soeldner A (1995b) Cyanobacteria and black mangroves in Northwestern Mexico: colonization, and diurnal and seasonal nitrogen fixation on aerial roots. Can J Microbiol 41:999–1011
Twilley RR, Rivera-Monroy VH (2009) Ecogeomorphic models of nutrient biogeochemistry for mangrove wetlands. In: Perillo GME, Wolanski E, Chaoon RD, Brinson MM (eds) Coastal wetlands: an integrated ecosystem approach. Elsevier, Amsterdam, pp 641–683
Vovides AG, Bashan Y, López-Portillo J, Guevara R (2011) Nitrogen fixation in preserved, reforested, naturally regenerated and impaired mangroves as an indicator of functional restoration in mangroves in an arid region of Mexico. Restor Ecol. 19:236–244
Woitchik AF, Ohowa B, Kazungu JM, Rao RG, Goeyens L, Dehairs F (1997) Nitrogen enrichment during decomposition of mangrove leaf litter in an east African coastal lagoon (Kenya): relative importance of biological nitrogen fixation. Biogeochemistry 39:15–35
Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Acknowledgments
We thank Victor Vásquez (INECOL) for technical support in the field and for performing the laboratory analyses and Manuel Trasviña and Rene Rebollar (CIBNOR) for performing the soil analyses and gas chromatography. Ira Fogel provided editorial assistance. This study was mainly supported by INECOL (20011/10016) and CONABIO (HH025) to J.L.P and by The Bashan Foundation, USA. This study is in partial fulfillment of the doctorate degree of A.G.V. at the Posgrado de Ecología y Manejo de Recursos (INECOL) with the support of a CONACYT grant and a small grant from the Bashan Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
This study is dedicated to the memory of the Mexican mangrove researcher Dr. Gina Holguin (1957–2007) of CIBNOR, Mexico.
Rights and permissions
About this article
Cite this article
Vovides, A.G., López-Portillo, J. & Bashan, Y. N2-fixation along a gradient of long-term disturbance in tropical mangroves bordering the gulf of Mexico. Biol Fertil Soils 47, 567–576 (2011). https://doi.org/10.1007/s00374-011-0562-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-011-0562-4