Abstract
Mangrove forests are characterized by distinctive tree-height gradientsthat reflect complex spatial, within-stand differences in environmentalfactors,including nutrient dynamics, salinity, and tidal inundation, across narrowgradients. To determine patterns of nutrient limitation and the effects ofnutrient availability on plant growth and within-stand nutrient dynamics, weused a factorial experiment with three nutrient treatment levels (control, N,P)and three zones along a tree-height gradient (fringe, transition, dwarf) onoffshore islands in Belize. Transects were laid out perpendicular to theshoreline across a mangrove forest from a fringe stand along the seaward edge,through a stand of intermediate height, into a dwarf stand in the interior ofthe island. At three sites, three trees were fertilized per zone for 2yr. Although there was spatial variability in response, growth byR. mangle was generally nitrogen (N) -limited in thefringe zone;phosphorus (P) -limited in the dwarf zone; and, N- and/or P-limited in thetransition zone. Phosphorus-resorption efficiency decreased in all three zones,and N-resorption efficiency increased in the dwarf zone in response to Penrichment. The addition of N had no effect on either P or N resorptionefficiencies. Belowground decomposition was increased by P enrichment in allzones, whereas N enrichment had no effect. This study demonstrated thatessential nutrients are not uniformly distributed within mangrove ecosystems;that soil fertility can switch from conditions of N to P limitation acrossnarrow ecotonal gradients; and, that not all ecological processes respondsimilarly to, or are limited by, the same nutrient.
Similar content being viewed by others
References
Aber J.D. and Melillo J.M. 1982. Nitrogen immobilization in decaying hardwood leaf litter as a function of initial nitrogen and lignin content. Can. J. Bot. 60: 2263–2269.
Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: Are there general patterns? J. Ecol. 84: 597–608.
Aerts R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79: 439–449.
Aerts R. and De Caluwe H. 1989. Aboveground productivity and nutrient turnover of Molinia caerulea along an experimental gradient of nutrient availability. Oikos 54: 320–324.
Aerts R., Verhoeven J.T.A. and Whigham D.F. 1999. Plant-mediated controls in nutrient cycling in temperate fens and bogs. Ecology 80: 2170–2181.
Armstrong W., Justin S.H.F.W., Beckett P.M. and Lythe S. 1991. Root adaptation to soil waterlogging. Aquat. Bot. 39: 57–73.
Baddeley J.A., Woodin S.J. and Alexander I.J. 1994. Effects of increased nitrogen and phosphorus availability on the photosynthesis and nutrient relations of three arctic dwarf schrubs from Svalbard. Funct. Ecol. 8: 676–685.
Bennett L.T., Weston C.J., Judd T.S., Attiwill P.M. and Whiteman P.H. 1996. The effects of fertilizers on early growth and foliar nutrient concentrations of three plantation eucalypts on high quality sites in Gippsland, southeastern Australia. For. Ecol. Manag. 89: 213–226.
Berendse 1994. Litter decomposability–a neglected component of plant fitness. Journal of Ecology 82: 187–190.
Boerner R.E.J. 1984. Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to site fertility. J. Appl. Ecol. 21: 1029–1040.
Boto K.G. and Wellington J.T. 1983. Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Mar. Ecol. Prog. Ser. 11: 63–69.
Boto K.G. and Wellington J.T. 1984. Soil characteristics and nutrient status in a northern Australian mangrove forest. Estuaries 71: 61–69.
Bowman W.D. 1994. Accumulation and use of nitrogen and phosphorus following fertilization in two alpine tundra communities. Oikos: 262–270.
Bradley P.M. and Morris J.T. 1990. Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71: 282–287.
Bradley P.M. and Morris J.T. 1991. The influence of salinity on the kinetics of NH4 + uptake in Spartina alterniflora. Oecologia 85: 375–380.
Bradley P.M. and Morris J.T. 1992. Effect of salinity on the critical nitrogen concentration of Spartina alterniflora Loisel. Aquat. Bot. 43: 149–161.
Broome S.W., Woodhouse W.W. Jr and Seneca E.D. 1975. The relationship of mineral nutrients to growth of Spartina alterniflora in North Carolina. II. The effects of N, P, and Fe fertilizers. Soil Sci. Soc. Am. Proc. 39: 301–307.
Bryant J.P., Chapin F.S. III and Klein D.R. 1983. Carbon/nutrient balance of boreal plants in relation to herbivory. Oikos 40: 357–386.
Cavalieri A.J. and Huang A.H.C. 1981. Accumulation of proline and glycinebetaine in Spartina alterni-flora Loisel. in response to NaCl and nitrogen in the marsh. Oecologia (Berlin) 49: 224–228.
Chabot B.F. and Hicks D.J. 1982. The ecology of leaf life spans. Annu. Rev. Ecol. Syst. 13: 229–260.
Chapin F.S. III and Kedrowski R.A. 1983. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64: 376–391.
Chapin F.S. III and Moilanen L. 1991. Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72: 709–715.
Chapin F.S. III and Shaver G.R. 1989. Differences in growth and nutrient use among arctic plant growth forms. Funct. Ecol. 3: 73–80.
Chapin F.S. III and Van Cleve K. 1989. Approaches to studying nutrient uptake, use and loss in plants. In: Pearcy R.W., Ehleringer J.R., Mooney H.A. and Rundel P.W. (eds), Plant Physiological Ecology. Field Methods and Instrumentation. Chapman and Hall, New York, pp. 185–207.
Cheeseman J.M. 1988. Mechanisms of salinity tolerance in plants. Plant Physiol. 87: 547–550.
Cintrón G., Lugo A.E. and Martinez R. 1985. Structural and functional properties of mangrove forests. In: D'Arcy W.G. and Correa M.D. (eds), The Botany and Natural History of Panama: La Botanica e Historia Natural de Panama. Monographs in Systematic Botany 10. Missouri Botanical Garden, St. Louis, MO, pp. 53–66.
Clough B.F., Andrews T.J. and Cowan I.R. 1982. Physiological processes in mangroves. In: Clough B.F. (ed.), Mangrove Ecosystems in Australia: Structure, Function and Management. Australian Institute of Marine Science in association with Australian National University Press, Canberra, Australia, pp. 193–210.
Cordell S., Goldstein G., Meinzer F.C. and Vitousek P.M. 2001. Regulation of leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees at two extremes of a long chronosequence in Hawaii. Oecologia 127: 198–207.
Correia P.J. and Martins-Loucao M.A. 1997. Leaf nutrient variation in mature carob (Ceratonia siliqua) trees in response to irrigation and fertilization. Tree Physiol. 17: 813–819.
Cromack K. Jr and Monk C.D. 1975. Litter production, decomposition, and nutrient cycling in a mixed hardwood watershed and a white pine watershed. In: Howell F.G., Gentry J.B. and Smith M.H. (eds), Mineral Cycling in Southeastern Ecosystems. US Energy Research and Development Division, pp. 609–624.
Day F.P. Jr 1982. Litter decomposition rates in the seasonally flooded Great Dismal Swamp. Ecology 63: 670–678.
Del Arco J.M., Escudero A. and Garrido M.V. 1991. Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology 72: 701–708.
DeLucia E.H. and Schlesinger W.H. 1995. Photosynthetic rates and nutrient-use efficiency among evergreen and deciduous shrubs in Okefenokee Swamp. Internatl. J. Plant. Sci. 156: 19–28.
Dierberg F.E., Straub P.A. and Hendry C.D. 1986. Leaf-to-twig transfer conserves nitrogen and phosphorus in nutrient poor and enriched cypress swamps. For. Sci. 32: 900–913.
Eckstein R.L. and Karlsson P.S. 1999. Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol. 143: 177–189.
EPA, Environmental Monitoring and Support Laboratory, Office of Research and Development 1983. Methods for chemical analysis of water and wastes.
Escudero A., del Arco J.M., Sanz I.C. and Ayala J. 1992. Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different wood species. Oecologia 90: 80–87.
Fell J.W. and Master I.M. 1984. Litter decomposition and nutrient enrichment. In: Moss S.T. (ed.), The Biology of Marine Fungi. Cambridge University Press, Cambridge, USA, pp. 239–251.
Feller I.C. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove. Georgetown University.
Feller I.C. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol. Monogr. 65: 477–505.
Feller I.C. 1996. Effects of nutrient enrichment on leaf anatomy of dwarf Rhizophora mangle L. (red mangrove). Biotropica 28: 13–22.
Feller I.C. and Mathis W.N. 1997. Primary herbivory by wood-boring insects along an architectural gradient of Rhizophora mangle L. Biotropica 29: 440–451.
Feller I.C., Whigham D.F., O'Neill J.P. and McKee K.M. 1999. Effects of nutrient enrichment on within-stand nutrient cycling in mangrove ecosystems in Belize. Ecology 80: 2193–2205.
Flanagan P.W. and Van Cleve K. 1983. Nutrient cycling in relation to decomposition and organic-matter quality in taiga ecosystems. Can. J. For. Res. 13: 795–817.
Gallagher J.L. 1975. Effect of an ammonium nitrate pulse on the growth and elemental composition of natural stands of Spartina alterniflora and Juncus roemerianus. Am. J. Bot. 62: 644–648.
Gallardo A. and Merino J. 1993. Leaf decomposition in two Mediterranean ecosystems of southwest Spain: influence of substrate quality. Ecology 74: 152–161.
Golley G., Odum H.T. and Wilson R.F. 1962. The structure and metabolism of a Puerto Rican red mangrove forest in May. Ecology 43: 9–19.
Hawkins B.J., Henry G. and Kiiskila S.B.R. 1998. Biomass and nutrient allocation in Douglas fir and amabilis fir seedlings: influence of growth rate and nutrition. Tree Physiol. 18: 803–810.
Heald E.J. 1971. The production of organic detritus in a south Florida estuary. Sea Grant Tech. Bull. No. 6. U. of Miami Sea Grant Program, Miami, Florida, USA.
Howes B.L., Dacey J.W.H. and Goehringer D.D. 1986. Factors controlling the growth form of Spartina alterniflora: feedbacks between above-ground production, sediment oxidation, nitrogen, and salinity. J. Ecol. 74: 881–898.
Ingestad T. 1979. Nitrogen stress in birch seedlings. II. N, K, P, Ca, and Mg nutrition. Physiol. Plan 45: 149–157.
Jiménez J. and Sauter K. 1991. Structure and dynamics of mangrove forests along a flooding gradient. Estuaries 14: 49–56.
Kennish M.J. 1992. Ecology of estuaries: anthropogenic effects. CRC Press, Boca Raton.
Killingbeck K.T. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77: 1716–1727.
Killingbeck K.T. and Costigan S.A. 1988. Element resorption in a guild of understory shrub species: niche differentiation and resorption thresholds. Oikos 53: 366–374.
King G.M., Klug M.J., Wiegert R.G. and Chalmers A.G. 1982. Relation of soil water movement and sulfide concentration to Spartina alterniflora production in a Georgia salt marsh. Science 218: 61–63.
Koch M.S. and Mendelssohn I.A. 1989. Sulfide as a soil phytotoxin: differential responses in two marsh species. J. Ecol. 77: 565–578.
Koch M.S., Mendelssohn I.A. and McKee K.L. 1990. Mechanism for hydrogen sulfide-induced growth limitation in wetland macrophytes. Limnol. Oceanogr. 35: 399–408.
Koltes K., Tschirky J. and Feller I.C. 1998. Carrie Bow Cay, Belize. In: Kjerfve B. (ed.), CARICOMP–Caribbean Coral Reef, Seagrass and Mangrove Sites. Coastal Region and Small Island Papers 3. UNESCO, Paris, pp. 79–94.
Kost J.A. and Boerner R.E.J. 1985. Foliar nutrient dynamics and nutrient use efficiency in Cornus florida. Oecologia (Berlin) 66: 602–606.
Lajtha K. 1988. The use of ion-exchange resin bags for measuring nutrient availability in an arid ecosystem. Plant Soil 105: 105–111.
Lajtha K. and Klein M. 1988. The effect of varying nitrogen and phosphorus availability on nutrient use by Larrea tridentata, a desert evergreen shrub. Oecologia (Berlin) 75: 348–353.
Linthurst R.A. 1979. The effect of aeration on the growth of Spartina alterniflora Loisel. Am. J. Bot. 66: 685–691.
Lin G.H. and Sternberg L.da S.L. 1992. Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.). Aust. J. Plant Physiol. 19: 509–517.
Lodhiyal L.S. and Lodhiyal N. 1997. Nutrient cycling and nutrient use efficiency in short rotation, high density central Himalayan Tarai poplar plantations. Ann. Bot. London 79: 517–527.
Loveless A.R. 1961. A nutritional interpretation of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves. Ann. Bot. n.s. 25: 168–183.
Lugo A.E. 1990. Fringe wetlands. In: Lugo A.E., Brinson M. and Brown S. (eds), Forested Wetlands: Ecosystems of the World 15. Elsevier, Amsterdam, pp. 143–169.
Lugo A.E. 1997. Old-growth mangrove forests in the United States. Conserv. Biol. 11: 11–20.
Lugo A.E., Brinson M.M. and Brown S. 1990. Synthesis and search for paradigms in wetland ecology. In: Lugo A.E., Brinson M.M. and Brown S. (eds), Forested Wetlands: Ecosystems of the World 15. Elsevier, Amsterdam, pp. 447–460.
Lugo A.E. and Snedaker S.C. 1974. The ecology of mangroves. Annu. Rev. Ecol. Syst. 5: 39–64.
Macintyre I.G., Littler M.M. and Littler D.S. 1995. Holocene history of Tobacco Range, Belize, Central America. Atoll Res. Bull. No. 43, 18 pp.
MacNae W. 1968. A general account of the fauna and flora of mangrove swamps and forests in the Indo-West-Pacific Region. Adv. Mar. Bio. 6: 73–270.
Malik V. and Timmer V.R. 1998. Biomass partitioning and nitrogen retranslocation in black spruce seedlings on competitive mixed wood sites: a bioassay study. Can. J. For. Res. 28: 206–215.
Maltby E. 1988. Use of cotton strip assay in wetland and upland environments–an international perspective. In: Harrison A.F. (ed.), Cotton Strip Assay: An Index of Decomposition in Soils. Institute of Terrestrial Ecosystems, UK, pp. 140–154.
McKee K.L. 1993. Soil physicochemical patterns and mangrove species distribution: reciprocal effects. J. Ecol. 81: 477–487.
McKee K.L. 1995. Seedling recruitment patterns in a Belizean mangrove forest: effects of establishment ability and physico-chemical factors. Oecologia 101: 448–460.
McKee K.L. 1996. Growth and physiological responses of neotropical mangrove seedlings to root zone hypoxia. Tree Physiol. 16: 883–889.
McKee K.L. and Mendelssohn I.A. 1989. Response of a freshwater marsh plant community to increased salinity and water level. Aquat. Bot. 34: 301–316.
McKee K.L., Mendelssohn I.A. and Hester M.W. 1988. Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans. Am. J. Bot. 5: 1352–1359.
Melillo J.M., Aber J.D. and Muratore J.F. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63: 621–626.
Mendelssohn I.A. 1979a. Nitrogen metabolism in the height forms of Spartina alterniflora in North Carolina. Ecology 60: 574–584.
Mendelssohn I.A. 1979b. The influence of nitrogen level, form, and application method on the growth response of Spartina alterniflora in North Carolina. Estuaries 2: 106–112.
Mendelssohn I.A., McKee K.L. and Patrick W.H. Jr 1981. Oxygen deficiency in Spartina alterniflora roots: metabolic adaptation to anoxia. Science 214: 439–441.
Mendelssohn I.A. and McKee K.L. 1983. Root metabolic response of Spartina alterniflora to hypoxia. In: Crawford R.M.M. (ed.), Plant Life in Aquatic and Amphibious Habitats. Brit. Ecol. Soc. Special Publication No. 5., pp. 239–253.
Mendelssohn I.A. and McKee K.L. 1988. Spartina alternifiora die-back in Louisiana: Time-course investigation of soil waterlogging effects. J. Ecol. 76: 509–521.
Middleton B.A. and McKee K.L. 2001. Degradation of mangrove tissues and implications for peat formation in Belizean island forests. J Ecol. 89: 818–828.
Millard P. 1993. A review of internal cycling of nitrogen within trees in relation to soil fertility. In: Fragoso M.A.C. and Van Beusichem M.L. (eds), Optimization of Plant Nutrition. Kluwer Academic Publishers, The Netherlands, pp. 623–628.
Millard P. and Proe M.F. 1991. Leaf demography and the seasonal internal cycling of nitrogen in sycamore (Acer pseudoplatanus L.) seedlings in relation to nitrogen supply. New Phytol. 117: 587–596.
Miller H.G., Cooper J.M. and Miller J.D. 1976. Effect of nitrogen supply on nutrients in litter fall and crown leaching in a stand of Corsican pine. J. Appl. Ecol. 13: 238–248.
Minoletti M.L. and Boerner R.E.J. 1994. Drought and site fertility effects on foliar nitrogen and phosphorus dynamics and nutrient resorption by the forest understory shrub Viburnum acerifolium L. Am. Mid. Nat. 131: 109–119.
Moore P.A. and Reddy K.R. 1994. Role of Eh and pH on phosphorus geochemistry in sediments of Lake Okeechobee, FL. J. Environ. Qual. 23: 955–964.
Morris J.T. 1984. Effect of oxygen and salinity on ammonium uptake by Spartina alterniflora Loisel. and Spartina patens (Aiton) Muhl. J. Exper. Mar. Bio. Ecol. 78: 87–98.
Morris J.T. 1988. Pathways and controls of the carbon cycle in salt marshes. In: Hook D.D. (ed.), The Ecology and Management of Wetlands, Vol 1: Ecology of Wetlands. Croom Helm, London, pp. 497–510.
Naidoo G., McKee K.L. and Mendelssohn I.A. 1992. Anatomical and metabolic responses to waterlogging and salinity in Spartina alterniflora and S. patens (Poaceae). Am. J. Bot. 79: 765–770.
Nye P.H. and Tinker P.B. 1977. Solute movement in the soil-root system. Blackwell, Oxford.
Odum W.E. and Heald E.J. 1975. The detritus-based food web of an estuarine mangrove community. In: Cronin L.E. (ed.), Estuarine Research. Academic Press Inc., New York, NY, USA, pp. 265–286.
Olson J.S. 1963. Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44: 322–331.
Onuf C.P., Teal J.M. and Valiela I. 1977. Interactions of nutrients, plant growth and herbivory in a mangrove ecosystem. Ecology 58: 514–526.
Ostman N.L. and Weaver G.T. 1982. Autumnal nutrient transfers by retranslocation, leaching & litter fall in a chestnut oak forest in southern Illinois. Can. J. For. Res. 12: 40–51.
Pastor J., Aber J.D., McClaugherty C.A. and Melillo J.M. 1984. Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65: 256–268.
Patrick W.H. Jr and DeLaune R.D. 1976. Nitrogen and phosphorus utilization by Spartina alterniflora in a salt marsh in Barataria Bay, Louisiana. Estuarine Coastal Mar. Sci. 4: 59–64.
Pool D.J., Snedaker S.C. and Lugo A.E. 1977. Structure of mangrove forests in Florida, Puerto Rico, Mexico, and Costa Rica. Biotropica 9: 195–212.
Popp M., Polania J. and Weiper M. 1988. Physiological adaptations to different salinity levels in mangroves. In: Lieth H. and Al Masoom A. (eds), Towards the Rational Use of High Salinity Tolerant Plants. Kluwer Academic Publishers, The Netherlands, pp. 217–224.
Pugnaire F.I. and Chapin F.C. III 1993. Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74: 124–129.
Reddy K.R. 1983. Soluble phosphorus release from organic soils. Agri. Ecosyst. Environ. 9: 373–382.
Richardson C.J., Ferrell G.M. and Vaithiyanathan P. 1999. Effects of N and P additions on stand structure, nutrient resorption efficiency and secondary compounds of sawgrass (Cladium mamaicense Crantz) in the subtropical everglades. Ecology 80: 2182–2192.
Robertson A.I. 1988. Decomposition of mangrove litter in tropical Australia. J. Exp. Mar. Biol. Ecol. 116: 235–247.
Robertson A.I., Alongi D.M. and Boto K.G. 1992. Food chains and carbon fluxes. In: Robertson A.I. and Alongi D.M. (eds), Tropical Mangrove Ecosystems. American Geophysical Union, Washington, DC, USA, pp. 293–326.
Robinson D. 1996. Resource capture by localized root proliferation: why do plants bother? Ann. Bot. 77: 179–185.
Rützler K. and Feller C. 1988. Mangrove swamp communities. Oceanus 30: 16–24.
Rützler K. and Feller C. 1996. Caribbean mangrove swamps. Sci. Am. 274: 94–99.
Rützler K. and Feller C. 1999. Mangrove swamp communities: an approach in Belize. In: Yáñez-Arancibia A. and Lara-Domínguez A.L. (eds), Mangrove Ecosystems in Tropical America. Instituto de Ecología, A.C. Xalapa, México.
Saur E., Nambiar E.K.S. and Fife D.N. 2000. Foliar nutrient retranslocation in Eucalyptus globulus. Tree Physiol. 20: 1105–1112.
Schlesinger W.H., DeLucia E.H. and Billings W.D. 1989. Nutrient-use efficiency of woody plants on contrasting soils in the western Great Basin, Nevada. Ecology 70: 105–113.
Shaver G.R. and Melillo J.M. 1984. Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65: 1491–1510.
Small E. 1972. Water relations of plants in raised sphagnum peat bogs. Ecology 53: 726–728.
Son Y., Lee I.K. and Ryu S.R. 2000. Nitrogen and phosphorus dynamics in foliage and twig of pitch pine and Japanese larch plantations in relation to fertilization. J. Plant Nutri. 23: 697–710.
Sorrell B.K. 1994. Airspace structure and mathematical modelling of oxygen diffusion, aeration and anoxia in Eleocharis sphacelata R. Br. roots. Aust. J. Mar. Freshwater Res. 45: 1529–1541.
Staaf H. 1982. Plant nutrient changes in beech leaves during senescence as influenced by site characteristics. Acta Oecol., Oecologica Plant 3: 161–170.
Stachurski A. and Zimka J.R. 1975. Methods of studying forest ecosystems: leaf area, leaf production and withdrawal of nutrients from leaves of trees. Ekol. Pol. 23: 637–648.
Sullivan M.J. and Daiber F.C. 1974. Response in production of cordgrass, Spartina alterniflora, to inorganic nitrogen and phosphorus fertilizer. Chesapeake Sci. 15: 121–123.
Taylor B.R., Parkinson D. and Parsons W.F.J. 1989. Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70: 97–104.
Tilton D.L. 1977. Seasonal growth and foliar nutrients of Larix laricina in three wetland ecosystems. Can. J. Bot. 55: 1291–1298.
Turner J. 1977. Effect of nitrogen availability on nitrogen cycling in a Douglas-fir stand. For. Sci. 623: 307–316.
Twilley R.R. 1988. Coupling of mangroves to the productivity of estuarine and coastal waters. In: Jansson B.O. (ed.), Coastal-Offshore Ecosystem Interactions. Springer-Verlag, Germany, pp. 155–180.
Ulanowicz R.E. and Baird D. 1999. Nutrient controls on ecosystem dynamics: the Chesapeake mesohaline community. J. Mar. Sys. 19: 159–172.
Valiela I. and Teal J.M. 1974. Nutrient limitation in salt marsh vegetation. In: Reimold R.J. and Queen W.H. (eds), Ecology of Halophytes. Academic Press, New York, NY, USA, pp. 547–563.
Valiela I. and Teal J.M. 1979. The nitrogen budget of a salt marsh ecosystem. Nature 280: 652–656.
Van den Driessche R. 1974. Prediction of mineral nutrient status of trees by foliar analysis. Bot. Rev. 40: 347–394.
Vitousek P.M. 1984. Litterfall, nutrient cycling, and nutrient limitations in tropical forests. Ecology 65: 285–298.
Vitousek P.M. 1998. Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1: 401–407.
Wilkinson L. 1996. Systat©, Inc., Evanston, IL, USA.
Woodroffe C.D. 1995. Mangrove vegetation of Tobacco Range and nearby mangrove ranges, central Belize barrier reef. Atoll Res. Bull. No. 427, 35 pp.
Wright R.M., Urish D.W. and Runge I. 1991. The hydrology of a Caribbean mangrove island. In: Proc. of the Coastlines of the Caribbean Coastal Zone 1991 Conference., pp. 170–184.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Feller, I.C., McKee, K.L., Whigham, D.F. et al. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62, 145–175 (2003). https://doi.org/10.1023/A:1021166010892
Issue Date:
DOI: https://doi.org/10.1023/A:1021166010892