1983, Yim and Tam 1999). For example, PNUE differed among mangrove species and decreased with increased nutrient availability and salinity (Martin et al. Similar and even higher values were found for A. marina and R. stylosa in Western Australia (Alongi et al. 2006), in addition to directly affecting nutrient availability (see above). In addition to altering the availability of nutrients in soils, the anoxic conditions in mangrove soils can have adverse effects on growth as they facilitate the microbial conversion of sulphate, which is abundant in seawater, to sulphides, which are toxic to plants (Nickerson and Thibodeau 1985). However, recent evidence suggests that nitrification can occur in anaerobic environments, including mangroves (Krishnan et al. 1988), but in those areas, low NRE was usually accompanied by high P RE (Feller et al. Mangroves grown in pots appear to readily use nitrate over ammonium and showed a major reduction in plant N uptake when a nitrification inhibitor (N-Serve) was added to the soil (Boto et al. 2005) is amongst the highest recorded for trees, reflecting a high level of adaptation to growth under nutrient-limited conditions (reviewed in Feller et al. Microbial soil respiration rates are also strongly temperature dependent, doubling every 10 Â°C (Kirschbaum 1995, Lovelock 2008); thus, soil nutrient availability for tree growth could be strongly temperature dependent, as bacteria and trees compete for the limited nutrient supply. However, in a field experiment in a mangrove forest, nitrate did not seem to be taken up by the trees (Whigham et al. 2008), resulting in non-linear relationships between soil conditions and root/shoot ratios. Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of, Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation, Nitrification and denitrification as sources of sediment nitrous oxide production: a microsensor approach, Critical analysis of root:shoot ratios in terrestrial biomes, Responses of coastal wetlands to rising sea level, The habitat function of mangroves for terrestrial and marine fauna: a review. 2000, Kothamasi et al. Trees adapted to drier, less salty soil can be found farther from the shoreline. 1997 and references therein). affect survival of the crabs. 2007b, Naidoo 2009). 2003). For example, in an A. marina stand in Kenya, the resorption from senescent tissue was more than two-thirds of the N and P requirements of that stand (Ochieng and Erftemeijer 2002). The bark is waxy to stop the water from getting into the bark. 1962, Snedaker 1995 and references therein). This makes the contribution of epibiotic fauna to the nutrient pool available for tree growth highly variable between sites and seasons, but evidence suggests that animalâplant interactions can significantly enhance nutrient supply for plant growth and should be included in the analysis of mangrove forest nutrient fluxes. Variation in leaf N:P, particularly where N:P is >32 (which is a global average for mangroves; Lovelock et al. 1982). 1992), outcompetes the trees for nitrate and, consequently, nitrate does not play a major role in N nutrition of mangrove trees in the field despite a possible preference for nitrate in pot experiments. 2005), for R. mangle in Belize (Feller et al. 2003a) and for Kandelia candel in China (Wang et al. In high-salinity environments, K is also vitally important for osmotic regulation (Downton 1982) and helps form the electrical potential required to facilitate water uptake against the strong external salt (mostly Na) gradient. 2003b), indicating the complexity of internal nutrient conservation and the interacting effects of growth rates (and the demand for nutrients) and their supply. Other fauna, such as gastropods and worms, promote nutrient recycling by consuming plant litter and microorganisms from the sediment (Kristensen et al. Acetylene reduction was shown to occur under a nitrogen atmosphere in slurries of anaerobic saltmarsh sediment. 2009). Mangroves range in size from small bushes to the 60-meter giants found in Ecuador. In other areas, such as Nigerian mangrove forests, percent cover was not strongly correlated with K availability in the soil (Ukpong 2000), but rather with other macronutrients and micronutrients such as P, calcium (Ca) and magnesium (Mg). Most mangrove trees are evergreen with sclerophyllous leaves and high root/shoot biomass ratios (Komiyama et al. These high N and P resorption values indicate that internal cycling of N and P can supply a significant fraction of the required nutrients for plant growth in mangroves. The goals of our project were to evaluate the prevalence of MPs on different environmental matrices of a mangrove ecosystem and to determine the potential ingestion of MPs by aquatic organisms. 2003). I. Many of the fish caught commercially in tropical regions reproduce and spend time in the mangroves as juveniles or adults. If you want to plant red mangrove in an indoor marine aquarium, then provide the propagules with bright light from daylight-spectrum bulbs. In particular the biotic features whereby the autotrophic feeders are the producers and beginning of the food chain as they are the food source for the primary consumers which are heterotrophic and are consequently unable to produce food themselves. 1998). At some sites, crabs can consume more than a quarter of the leaf litter fall, producing faecal material that has higher nutritional content and significantly lower tannin concentrations than the leaves themselves, promoting recycling of the detrital matter (Robertson 1986). The availability of K in mangrove soils is variable, and there is some evidence for K limitation in some mangroves (Ukpong 1997). PNUE measured for mangroves (e.g., Alongi et al. The stability of urea levels over the last three decades suggests that the upgrade of wastewater treatment technologies was probably balanced by the concomitant increase of the anthropogenic pressure in the area (477,000 to 1,300,000 inhabitant equivalent). Without getting way too complicated really quickly, letâs look at how roots work for a second. Mangroves inhabit environments that have a wide range of nutrient availability, even over small spatial scales (e.g., high compared with low intertidal zone). These processes, together with a potential competition between phytoplankton and bacteria for the utilization of this nitrogen form, suggest that the biogeochemical role of urea should be better investigated in mid-latitude coastal zones subjected to highly variable ambient conditions and to overloads of this compound. Mangrove Ecosystem The new images obtained were analysed. Mangroves: 11 facts you need to know These unique trees lead tough lives â but weâre all the better for it. 1997 and references therein). Thus, convergence in some strategies for nutrient conservation among species might also be expected. Crab-processed organic matter In June 2001 NIWA set up the first field site in Waikopua Creek (Whitford, Auckland) where the substrate is fine sand/mud. 1999) and on decomposition processes (Bosire et al. Forests fringing the ocean were N limited while those internal to the islands and permanently flooded were P limited. 1994, Ochieng and Erftemeijer 2002). This initial retention of production in the forest refines earlier 2003). Pneumatophore - Cross-section 1977). (2006) observed AM associations in the low-salinity soils (<11 PSU) of the Ganges River estuary in India and that all of the 31 mangrove species in that study were receptive to mycorrhizal colonization. 1986, Alongi et al. It is clear that further investigation into the colonization and abundance of AM fungi in mangrove roots and soils is needed. They have long roots to get at the nutrients below and around the mangrove. The delivery of nutrients in sediments and water during tidal inundation and sporadically in floodwaters associated with cyclones and hurricanes provides significant sources of nutrients for mangroves (Lugo and Snedaker 1974, Davis et al. Within a given mangrove forest, different species occupy distinct niches. crabs may in turn be influenced by the associated mangrove species, mainly 2009b), indicating that nutrient limitation is determined by multiple factors, including sediment and nutrient fluxes, tidal range and substrate type. 1999, 2007, Lovelock et al. Additionally, variation in soil anoxia (flooding) and salinity may also affect the nutrient demand imposed by tree growth and, thus, the extent to which growth is nutrient limited (Krauss et al. 1983) and in the saltmarsh halophyte Aster tripolium (Carvalho et al. A mangrove is a shrub or small tree that grows in coastal saline or brackish water.The term is also used for tropical coastal vegetation consisting of such species. Mangroves store gases directly inside the roots, using them even when the roots are submerged during high tide. Temperature. Our preliminary results provide evidence to better characterize the complex mixtures of MPs within the estuarine environment and the likely interactions of MPs with the estuarine aquatic species. After separation of the red, green and blue bands, an unsupervised classification was achieved, then various masks each corresponding to a given range of depths were built and applied to the initial image. These are all likely to have a significant impact on mangrove physiology and ecosystem function and impact nutrient availability and cycling. The evergreen habit implies a smaller nutrient investment in new leaves and lower nutrient loss rates due to the long lifespan of the tissue (Aerts 1995). It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. The high concentration of sulphate in seawater makes sulphide toxicity more probable in mangrove forests compared with terrestrial ecosystems (Raven and Scrimgeour 1997). Great care was taken in the selection of training sites to gather the pixels characterized by a high spectral similarity which corresponded to precise themes. Black mangrove roots create oxidized rhizospheres substantially larger than those described for other plant species. Many mangrove soils have extremely low nutrient availability (e.g., Lovelock et al. The high RE found in Kenya is consistent with other studies that indicate that RE in mangroves is high compared with other angiosperms (Feller et al. Growth and reproduction of the In Belize, both N and P limitation were observed, depending on location within the forest (Feller et al. 2003a). Aluminium can be relatively abundant in mangrove soils (Naidoo and Raiman 1982) and the acidic conditions of mangrove soils may result in aluminium being mobilized to toxic levels. 2001) where the total N and P content of the soils was likely to have been very low due to strong weathering of the old highly leached soils of the tropics (Romine and Metzger 1939). Fibers and filaments were more abundant in the water column. Topographic factors such as elevation determine the frequency and duration of tidal inundation, which subsequently affects the salinity, oxidation state and nutrient availability of the soil, resulting in complex patterns of nutrient demand and supply that contribute to the variable structure of mangrove forests. Under anoxic conditions, sulphate-reducing bacteria reduce Fe to forms that are unfavourable for P binding (Holmer et al. The effects of phosphorus in reducing the detrimental effects of soil acidity on plant growth, History and biogeography of the mangrove ecosystem, based on a critical reassessment of the paleontological record, Carbon, nitrogen contents and stable carbon isotope abundance in mangrove leaves from an east African coastal lagoon (Kenya), The influence of anoxia on plants of saline habitats with special reference to the sulphur cycle, Global patterns of plant leaf N and P in relation to temperature and latitude, Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems, Leaf-burying crabs: Their influence on energy flow and export from mixed mangrove forests (, The epiphyte community of mangrove roots in a tropical estuary: distribution and biomass, Phosphorus fixation by horizons of variuos soil types in relation to dilute acid, extractable iron, and aluminium, Mangrove ecology, silviculture and conservation, Above- and below-ground biomasses of two species of mangrove on the Hawkesbury River estuary, New South Wales. Both nitrogen-use efficiency and nutrient resorption efficiencies in mangroves are amongst the highest recorded for angiosperms. Nutrient recycling processes in trees include resorption of nutrients prior to leaf fall (Chapin 1980), a process where nutrients resorbed from senescent leaves are directly available for continued plant growth (Hortensteiner and Feller 2002). Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings: response to light and nutrient availability, Growth and physiological responses of neotropical mangrove seedlings to root zone hypoxia. Maximum resorption efficiencies appear to be rather uniform amongst different co-occurring mangrove species; a comparison between eight mangrove species in Gazi Bay, Kenya revealed similar RE values of around 65% (Rao et al. Sengupta and Chaudhuri (2002) and Kothamasi et al. The ratio N:P in plant tissue has also been used to infer N or P limitations to growth (GÃ¼sewell 2004). Mangroves can be either open, having regular tidal or riverine exchange, or with more restricted exchange, e.g., high intertidal and microtidal settings. How do mangroves deal with nutrients? In the southern USA, mangroves have been experimentally shown to be both N limited (Feller et al. Mangrove photosynthesis is usually limited by high midday leaf temperatures (Cheeseman 1994); thus, increases in temperature with declines in humidity and rainfall could reduce productivity in some mangrove forests by accentuating midday depressions in photosynthesis. The common issues and problems that need to be tackled urgently for ensuring an effective management setup of the MPAs of the country are discussed. 1995), e.g., as a consequence of sea level rise and with low humidity and high salinity (Ball and Munns 1992, Ball et al. Mangrove forests or mangals are a type of intertidal wetland ecosystems. through the provision of food. Root/shoot ratios in many trees are sensitive to soil moisture, usually decreasing with increased waterlogging (Kozlowski 1984), but this is not necessarily the case for all mangrove species (Ye et al. In some cases, RE of an initially non-limiting nutrient has been shown to increase as a result of the alleviation of a limiting nutrient (e.g., N enrichment in N-limited trees results in higher RE of P; Feller et al. Elevated CO2 conditions (twice ambient) enhance stem elongation, leaf production, photosynthesis rates and root production in R.mangle (Farnsworth et al. The roots and branches of mangroves provide an ideal site for animals to feed, mate, and give birth. 1995). 2007) and eutrophication of mangrove soils can cause an increase in the rate of release of N2O to the atmosphere. Although increases in atmospheric CO2 result in elevated growth rates, these are smaller than the reductions in growth rates observed when mangroves are increasingly inundated (Farnsworth et al. Additionally, nutrient availability has repeatedly been found to be an important factor limiting productivity in mangroves (e.g., Onuf et al. 2010). Although, India has a very long coastline and varied coastal habitats, contribution of the MPAs is only 4.0 % to the total area of the Protected Areas (PAs) and 1.3 % of the continental shelf area of the country. Interspecific differences in nutrient-use efficiency have been observed between mangrove species (Lovelock and Feller 2003) and are also modified by plant interactions with environmental variables (Martin et al. Is sclerophylly of Mediterranean evergreens an adaptation to drought? Part of her research includes carefully dosing individual mangrove trees with small amounts of nitrogen and phosphorus to understand how excess nutrients, which are a major global threat to mangroves and other coastal ecosystems âlike those from industrial, residential, and agricultural sourcesâaffect mangrove ecosystems. Photosynthesis and respiration are both highly sensitive to temperature. They form unique intertidalforests at the edge of land and sea, see Fig. Bacteria solubilize phosphate in areas where the soil is oxygenated (e.g., near the mangrove roots) and may, therefore, serve an important role in P uptake by the plant. consumption by crabs of mangrove propagules also affects mangrove community Too much-Death to part or all of plant, seedlings and flowers affected. Increasing the efficiency of metabolic processes is also an effective nutrient conservation strategy (Chapin 1980). Mangroves have an average leaf life span of 16 months (1.33 years), although this can vary between species and over latitude (Saenger 2002, SuÃ¡rez and Medina 2005). Similar results were found for the effects of shrimp pond effluent on a mangrove estuary (Trott and Alongi 2000). 2007a). Studies in the Indo-Pacific and the African continent have also shown variation in whether N or P limits growth, although in these mostly mesotidal settings, N is the nutrient most frequently observed to limit growth (Lovelock et al. 2004). 2008). 1977, Boto and Wellington 1983, Feller 1995, Koch 1997, Feller et al. The semi-terrestrial and air-breathing habit of 1987). Root biomass in mangroves can be high, partially because of the contribution of aboveground roots, which have both supportive functions and roles for aerating roots in anoxic soils and also due to high belowground root biomass (Golley et al. The final map consisted of 31 themes. These initial results demonstrate the presence of MPs in estuarine environments and the possibility that MPs may have a detrimental impact in aquatic species. Bioturbation by the crabs also results in changes in Spore germination and hyphal growth of a vesicularâarbuscular mycorrhizal fungus, Effect of irrigation, water salinity and rootstock on the vertical distribution of vesicularâarbuscular mycorrhiza in citrus roots, Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (, Nutrient conservation strategies of a mangrove species, Nitrogen and phosphorus dynamics and nutrient resorption of, A nutritional interpetation of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves, Soil respiration in tropical and subtropical mangrove forests, Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest, The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama, Variation in mangrove forest structure and sediment characteristics in Bocas del Toro, Panama, Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients, Mangrove growth in New Zealand estuaries: the role of nutrient enrichment at sites with contrasting rates of sedimentation, Nutrient enrichment increases mortality of mangroves, Convergence in hydraulic architecture, water relations and primary productivity amongst habitats and across seasons in Sydney, A mangrove stand under sewage pollution stress: Red Sea, Nitrogen fertilization enhances water-use efficiency in a saline environment, Molecular mechanisms of potassium and sodium uptake in plants. Those that can handle tidal soakings grow in the open sea, in sheltered bays, and on fringe islands. 2006). The redox state of the soil surrounding the mangrove roots is important for determining the nutrients available for plant uptake (FigureÂ 1). 2008). 2001) where the total N and P content of the soils was likely to have been very low due to strong weathering of the old highly leached soils of the tropics (Romine and Metzger 1939). 2007a), indicates that P may limit growth in many mangrove habitats (e.g., Malaysia, Kenya, China, Puerto Rico, Venezuela, Victoria, Australia, Florida and Honduras; reviewed in Lovelock et al. High rates of ammonification (Alongi et al. 1977, Boto and Wellington 1984, Feller et al. Mangroves have evolved in the oligotrophic tidal environment of the tropics (Plaziat et al. In other parts of the world, people have utilized mangrove trees as a renewable resource. Digitized aerial photographs meet these requirements by providing higher-resolution images than orbital remote sensing devices. 2002) and N fixation also contribute to the production of ammonium. Sclerophylly is also linked to low water availability and, in mangroves, to high-salinity habitats (e.g., Naidoo 1987), as sclerophyllous leaves can lose a great deal of their water content before wilting and can exhibit extremely low leaf water potentials (Salleo et al. 1998). 2007b). Furthermore, ammonium adsorption to mangrove soil particles is lower than in terrestrial environments due to the high concentration of cations from the seawater that compete for binding sites, making the ammonium available for plant uptake (Holmboe and Kristensen 2002). Such processes include biotic and abiotic stressors such as herbivory (Feller and Chamberlain 2007) and destructive weather (wind, hail, etc.). sustainable use. 2001). Nutrient resorption from senescing leaves of perennials: are there general patterns? 1988). A recent study on mangrove nitrogen isotope composition in Belize suggested that amino acid uptake was unlikely given the isotopic signature of the soil, roots and leaves (Fogel et al. 2008). In a Belizean mangrove where P was a limiting factor for growth, the addition of K did not result in greater growth rates even when P limitation was lifted (Feller 1995), but K-use efficiency increased with growth rates, indicating that, when N or P limitation is relieved, K limitation to growth may develop. Pneumatophores allow mangroves to absorb gases directly from the atmosphere, and other nutrients such as iron, from the poor soil. Mangroves are also capable of absorbing pollutants such as heavy metals and other toxic substances as well as nutrients and suspended matter. structure by diminishing the relative abundance of species whose propagules We also expect that mangroves will have evolved traits for the acquisition and conservation of nutrients in low-fertility environments (see âMangrove nutrient conservation strategiesâ, below). 1999, Morris et al. However, evidence is mounting that eutrophication can also have negative consequences for mangrove growth. 2001, Oxmann et al. 2009), but there does appear to be a threshold of 20 PSU to AM fungi salinity tolerance, above which it is unable to colonize soils (Johnson-Green et al. The emerging explanation is that high productivity of mangroves is achieved where nutrients limit growth through efficient nutrient cycling and nutrient conservation strategies. Amino acid availability in mangrove soils can be high (Stanley et al. Clean water. Sclerophylly has also been linked to leaf longevity and evergreen traits and to ecosystem nutrient retention through slowed decomposition (Schlesinger and Hasey 1981) and through reductions in herbivory by primary consumers (Coley 1983). 1991). 1987). Thus, the redox state of the soil can be highly heterogeneous, facilitating a plethora of biogeochemical processes, which influence nutrient availability. 1986, Alongi 1994, Kristensen et al. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. 2002), thereby reducing the efficiency of K+ uptake from the soil. Birds nesting in mangroves can contribute a significant source of nutrients for mangrove growth (Onuf et al. Nitrogen fixing bacteria from warty lenticellate bark of a mangrove tree, Vegetation and its relation to soil nutrient and salinity in the Calabar mangrove swamp, Nigeria, Ecological classification of Nigerian mangroves using soil nutrient gradient analysis, Quantification of toxic and inhibitory impact of copper and zinc on mixed cultures of sulfate-reducing bacteria, Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon, Regional and global concerns over wetlands and water quality, Litterfall, nutrient cycling, and nutrient limitation in tropical forests, Seasonal changes in element contents in mangrove element retranslocation during leaf senescene, Effect of wastewater discharge on nutrient contamination of mangrove soils and plants, Production of mangrove litter in a macrotidal embayment, Darwin Harbour, N.T., Australia, Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats, Responses to nitrogen, phosphorus, potassium and sodium chloride by three mangrove species in pot culture, Growth and physiological responses of two mangrove species (, Effects of wastewater-borne heavy metals on mangrove plants and soil microbial activities, Â© The Author 2010. All three mangrove species flower in the spring and early summer. This work was supported by awards DP0774491 and DP0986170 from the Australian Research Council and by a UQ Early Career Researcher award to R.R. invertebrates, or be re-exported as micro-particulates. Oxford University Press is a department of the University of Oxford. These results might imply that the microbial community in the mangroves, with its high rates of denitrification (Alongi et al. Furthermore, due to the saline conditions, Na+ cations can interfere with K+ uptake (MÃ¤ser et al. The picture emerging is that climate change will influence mangroves ecosystems in the form of a suite of many interacting factors, the result of which will probably be specific to the conditions at each site. The interest in mangroves as treatment systems for sewage and aquaculture effluent has increased greatly over the past few years. High plasticity confers the capacity to withstand low-nutrient conditions while still permitting the ability to exploit high levels of nutrients when they are available (e.g., Fromard et al. MPs pellets and granules were mostly found in the intertidal and subtidal sediments. These are cable roots which have grown-above the surface and then back down into the mud again, looking like small knees buried in mud. mangroves may not propagate on the tree and true propagules are not formed. Although mangrove ecosystems are rich in carbon, they are in a paradox often nutrient poor. surface topography, particle size distribution and degree of aeration and, 2008). N was found to limit growth of A. marina in South Africa (Naidoo 2009) and New Zealand (Lovelock et al. The role of Mycorrhizal infection in heavy metal resistance, Spatial and temporal dynamics of mycorrhizas in, The influence of surface and shallow subsurface soil processes on wetland elevation: a synthesis, Effects of salinity and flooding on the infectivity of salt marsh arbuscular mycorrhizal fungi in, Depressions of photosynthesis in mangrove canopies, Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, Net primary production in tropical forests: an evaluation and synthesis of existing field data, Our evolving conceptual model of the coastal eutrophication problem, Herbivory and defensive characteristics of tree species in a lowland tropical forest, Nitrate depuration of secondary sewage effluents in mangrove sediments, Atmospheric nitrous oxide fluxes from mangrove sediments, Biological nitrogen fixation in two tropical forests: ecosystem-level patterns and effects of nitrogen fertilization, Temporally dependent C, N, and P dynamics associated with the decay of, An assessment of metal contamination in mangrove sediments and leaves from Punta Mala Bay, Pacific Panama, Growth and osmotic relations of the mangrove, The fate of marine autotrophic production, Alteration of the chemical composition of mangrove (, Facultative mutualism between red mangroves and root-fouling sponges in Belizean mangal, Stoichiometry and the new biology: the future is now, Arbuscular mycorrhizal fungi in alleviation of salt stress: a review, Status and trends in mangrove area extent worldwide, Forest Resources Assessment Working Paper, Ecophysiological responses of mangrove seedlings to two facets of climate change, Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (, Herbivore responses to nutrient enrichment and landscape heterogeneity in a mangrove ecosystem, Effects of nutrient enrichment on within-stand cycling in a mangrove forest, Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest, Nitrogen limitation of growth and nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida, Nutrient addition differentially affects ecological processes of, The uptake of amino acids by microbes and trees in three cold-temperate forests, Unusually negative nitrogen isotopic compositions (Î´15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem, Half a century of dynamic coastal change affecting mangrove shorelines of French Guiana. » Mangrove peat absorbs water during heavy rains and storm surge, reducing A large accumulation of urea can occur during summer periods characterized by stable weather conditions and weak circulation, whereas a biologically mediated degradation to ammonium is observed in autumn in concomitance to a strong shift of the marine ecosystem toward heterotrophic conditions. 2003, Krauss et al. 2009). 1983), although it is possible that the thin oxygenated layer surrounding the roots can provide enough oxygen for their survival (Brown and Bledsoe 1996). N2O is a highly potent greenhouse gas produced as an intermediate product of both nitrification and denitrification by microbial organisms. However, this process also releases H+ protons, which results in acidification of the soil. 2002). Although experimental additions of P have yielded increases in growth in mangroves, it has long been recognized that it is possible that some of the beneficial effect of applied phosphate in acid soils is due to fixation of aluminium and not just due to phosphate uptake by the plant (Pierre and Stuart 1933). On the other hand, sulphate-reducing bacteria also play a pivotal role in increasing P availability in the soil (Sherman et al. Harvested for durable, water-resistant wood, mangroves have been used in building houses, boats, pilings, and furniture. Mangroves support rich biodiversity and high levels of productivity, supplying seafood at capacities large enough to feed millions of people. organic enrichment, but development of the landward mangroves will strongly 2003). Heavy metal concentrations in some mangrove soils are high (Ong Che 1999, Defew et al. 1995) and increased herbivory rates of some bark-mining moths (Feller and Chamberlain 2007). Mangroves are utilized in many parts of the world as a renewable resource. How mangroves can sustain high levels of productivity in spite of nutrient limitation is the focus of many studies on mangrove nutrition. Mangrove forests also contain several salt-tolerant plant species which are not classed as mangroves. There are a total of 31 Marine Protected Areas (MPAs) in India, primarily in marine environment, which cover a total area of 6271.2 km 2 with an average size of 202.1 km 2. Mangroves have evolved in the oligotrophic tidal environment of the tropics (Plaziat et al. Aerial photographs were first subjected to true-colour digitization. Radial oxygen loss from the roots creates an aerobic zone in the area immediately adjacent to the roots, which may vary in extent among mangrove tree species due to differences in the rate of oxygen loss from the roots to the rhizosphere among species (McKee 1996, Pi et al. Remote sensing techniques adapted to high resolution mapping of tropical coastal marine ecosystems (... Anthropogenic loads and biogeochemical role of urea in the Gulf of Trieste, Occurrence of Microplastics in the Mangrove Ecosystem of the Gulf of Guayaquil, Ecuador. By transplanting epibiotic invertebrate fauna onto roots of the mangrove R. mangle, Ellison et al. 1992). Thus, the use of ammonium may in part be responsible for the low respiration rates observed in mangrove roots (McKee 1996, Lovelock et al. 2007, Lovelock et al. Nitrogen and phosphorus showed marked decreases (ca. We thank Prof. Marilyn Ball. Mangroves often go unappreciated by the casual observer. This can be achieved, for example, if the higher photosynthesis rates observed under increased CO2 conditions result in increased carbon allocation to roots, increasing the soil root volume and thus soil elevation (Langley et al. 2007a). Changed water flows into mangroves due to urban development and drainage can cause declines in mangrove crab populations. The presence of phosphate can precipitate aluminium, thus suppressing aluminium uptake (Hesse 1963). 2009), often resulting in almost complete resorption of limiting nutrients. This is vital for seagrass, marine life and yes, humans. For example, in a fertilization experiment of A.germinans vs. L.racemosa, the increase in photosynthetic performance in N-fertilized A. germinans was much greater than that of N-fertilized L. racemosa (Lovelock and Feller 2003). 2008). As summarized above, nutrient additions can stimulate mangrove growth. When plants evolved to live on land, they needed a way to get to water to continue absorbing nutrients. Frequently too dense to get into, we only see these areas from a distance or the edge. Phosphate (P) in mangrove soils can be immobile and unavailable for plant use (FigureÂ 1), thus organisms that solubilize P can have important implications for plant growth, especially in nutrient-limited environments. Isotopic analysis of the N in sponges and along the mangrove root indicated that the sponges provided a source of inorganic N for the tree. (discarded of when the levels are too high) - Mangroves can restrict the opening of their stomata. Comparación morfo-fisiológica del desarrollo de los propágulos de manglar de franja y chaparro de Rhizophora mangle L. de Celestún, Yucatán. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns, What have we learned from 15 years of free-air CO, Spatial and temporal variation of nitrous oxide and methane flux between subtropical mangrove sediments and the atmosphere, Bacterial productivity and microbial biomass in tropical mangrove sediments, The role of bacteria in nutrient recycling in tropical mangrove and other coastal benthic ecosystems, Experimental evidence that dissolved iron supply limits early growth of estuarine mangroves, Below-ground nitrogen cycling in relation to net canopy production in mangrove forests of southern Thailand, Nutrient partitioning and storage in arid-zone forests of the mangroves, Nutrient-use efficiency in arid-zone forests of the mangroves, Regeneration in fringe mangrove forests damaged by Hurricane Andrew, Plant responses to salinity under elevated atmospheric concentrations of CO. Salinity-induced potassium deficiency causes loss of functional photosystem II in leaves of the grey mangrove, Root respiration associated with ammonium and nitrate absorption and assimilation by barley, Litter degradation and C:N dynamics in reforested mangrove plantations, The relationship between nitrogen fixation and tidal exports of nitrogen in a tropical mangrove system, Phosphorus and nitrogen nutritional status of a Northern Australian mangrove forest, Soil characteristics and nutrient status in a Northern Australian mangrove forest, Role of nitrate in nitrogen nutrition of the mangrove, The biology of Mycorrhiza in the Ericaceae. Eutrophication is one of the major changes coastal ecosystems are facing worldwide (Cloern 2001, Verhoeven et al. The lowest levels of NRE were recorded for A. germinans at Twin Cays (<5%; Feller et al. Furthermore, the large root biomass in mangroves may overcome the relative immobility of ammonium in the soil by covering large soil volumes. 1991) and the occurrence and abundance of mangrove roots. Root proliferation in decaying roots and old root channels: a nutrient conservation mechanism in oligotrophic mangrove forests? Mangroves which are cultivated in aquariums normally do not need any fertilizers if the aquarium is in a proper balance of nutrients. The leaf life spans of mangroves are typical for broadleaved tropical and subtropical evergreens (Reich et al. In a study on mangrove soils in the Dominican Republic, nitrate concentrations in the soil were found to be negligible, with the vast majority of inorganic N being in the form of ammonium (Sherman et al. 2008). Mangroves have high nutrient use efficiencies by conserving nutrients through translocating nutrients from leaves prior to loss (Reef et al., 2010). Trophic levels in the mangrove ecosystem: In the mangrove ecosystem the abiotic and biotic features rely on one another to survive. Mangroves which do not grow in aquariums should be grown in the effective and sustainable long-term fertilizer Mangrove Mud Basic or even better in Mangrove Mud Special . are preferred foods. Mangrove crabs mulch the mangrove leaves, adding nutrients to the mud for other bottom feeders. 2001). Nutrient availability is another factor that plays a role determining the allocation to root biomass. Mangroves are highly productive, fixing and storing significant amounts of carbon (Duarte and Cebrian 1996). 2008) as do insects, such as termites, that feed on dead wood or decaying organic matter (Nagelkerken et al. High rates of denitrification deplete the nitrate and nitrite pools and produce ammonia, making ammonium the most common form of nitrogen (N) observed in mangrove soils (e.g., Twilley et al. Propagules fall from late summer through early autumn. Conversely, in anoxic environments where sulphate reduction occurs, the solubility and toxicity of low levels of zinc, cadmium and other chalcophilic heavy metals can be reduced by metal sulphide formation (Klerks and Bartholomew 1991). thus, the concentration of phytotoxins in the substratum. However, above certain thresholds, these heavy metals become toxic to the sulphate-reducing bacteria due to their ability to compete with essential cations for cellular activity, denaturize proteins and deactivate enzymes (Utgikar et al. Mangroves take up nitrogen and phosphorus to build roots, stems and leaves. Mangroves protect both the saltwater and the freshwater ecosystems they straddle. However, the overall high root biomass in mangroves, especially the abundance of fine roots (Komiyama et al. After ground identification, these training sites enabled a supervized classification to be established, then a confusion matrix was built. In many marine ecosystems, N was considered the primary nutrient that limits growth, although more recent analysis found that N and P limit growth in approximately equal proportions (Elser and Hamilton 2007). 2001). Macrofaunal assemblages are emerging as important biotic factors for nutrient cycling in mangroves. A symbiotic relationship exists between many animals and the mangrove; for example, crabs feeds on the mangrove leaves, as well as other nutrients and then recycle minerals into the mangrove forest. Root/shoot ratios have been observed that are sometimes an order of magnitude higher than those for tropical terrestrial forests and similar or higher than those found in desert plants (Mokany et al. 2001). Mangroves are tropical trees that thrive in conditions most timber could never tolerate â salty, coastal waters, and the interminable ebb and flow of the tide. Fisheries and other sectors, economies, and communities around the world will only be sustained through the restoration and protection of mangrove â¦ 1997). 2001). 1994). 2006). Although mangroves have been proposed to protect the marine environment from land-derived nutrient pollution, nutrient enrichment can have negative consequences for mangrove forests and their capacity for retention of nutrients may be limited. Thus, we expect and find both N and P limitation in mangroves. 1992). Mangrove trees are highly productive and this is due in part to the evolution of many adaptations for nutrient conservation (FigureÂ 2). In more tropical latitudes, P was found to limit growth in high intertidal scrub forests (Boto and Wellington 1983, Lovelock et al. Mangroves are a significant source of nitrous oxide (N2O; Allen et al. Nutrients produced by primary producers are passed on to the community and eventually to the detrital pool via the breakdown of leaf litter and timber. Forests internal to the island in Puerto Rico were also found to be P limited (Medina et al. 2003a). Soil physicochemical patterns and mangrove species distributionâreciprocal effects? However, mangroves also appear to be highly plastic in their responses to changes in nutrient availability, achieving high growth rates when nutrient limitations are relieved that are accompanied by associated reductions in nutrient-use efficiency and other nutrient conservation mechanisms. Eutrophication results in higher activities of marine wood-borers (Kohlmeyer et al. Effects of salinity and nitrogen on growth and water relations in the mangrove, Factors contributing to dwarfing in the mangrove, Differential effects of nitrogen and phosphorus enrichment on growth of dwarf, Some physical and chemical properties of mangrove soils at Sipingo and Mgeni, Natal, Inorganic nitrogen metabolism in a eutrophicated tropical mangrove estuary, Heterotrophic nitrogen fixation in an intertidal saltmarsh sediment, Dynamic nature of the turnover of organic carbon, nitrogen and sulphur in the sediments of a Jamaican mangrove forest, Association between pore water sulphide concentrations and the distribution of mangroves, Phenology, litterfall and nutrient resorption in, Concentration of 7 heavy metals in sediments and mangrove root samples from Mai Po Hong Kong, Interactions of nutrients, plant growth and herbivory in a mangrove ecosystem, Mangrove reforestation in Vietnam: the effect of sediment physicochemical properties on nutrient cycling, Transformation and availability to rice of nitrogen and phosphorus in waterlogged soils, Plants can use protein as a nitrogen source without assistance from other organisms, Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species, Soluble aluminum studies: IV. MPs ingestion in aquatic organisms was determined by the presence of different types of MPs in the gastrointestinal tract of different aquatic species. 1987) but amino acid uptake by mangrove trees has not been investigated directly. 1999, 2003b, 2007, Lovelock et al. Mangroves are a good source of wood and timber, nipa The role of mangroves in nutrient cycling and productivity of adjacent seagrass communities Chawka Bay, Zanzibar Mangroves therefore serve as natural wastewater filters, preventing many land-based and nearshore pollutants from reaching deeper waters (UNEP, 2006). Nutrient-conserving processes in mangroves are well developed and include evergreeness, resorption of nutrients prior to leaf fall, the immobilization of nutrients in leaf litter during decomposition, high root/shoot ratios and the repeated use of old root channels. Watering the seedlings isn't necessary when they are planted in a coastal or marine environment. Is sclerophylly of Mediterranean evergreens an adaptation to drought? 2005), but nutrient availability varies greatly between mangroves and also within a mangrove stand (Feller et al. Australia). All rights reserved. estimates of tidal export from the mangroves. North and South America, Africa and Middle-East, Asia and Oceania (incl. 2007a). The capacity to sustain low growth rates and consequently reduced nutrient requirements over periods of time are an adaptation to low-nutrient environments (Chapin 1980). Mean estimates of net primary productivity (NPP) for mangrove range from 2 to 50 Mg C haâ1 yearâ1 (Alongi 2009), rivalling some of the most productive old-growth tropical forests (Clark et al. 2003). 2005), and this can result in reduced leaf numbers and stem diameter (Yim and Tam 1999). The N2O produced in mangrove soils is rapidly released to the atmosphere because pneumatophores facilitate the transport of N2O from the soil to the atmosphere (Krithika et al. An early theoretical analysis suggests that P limitation should be expected in areas with low exchange rates with the oceans and N limitation in more âopenâ systems (Smith 1984). A case study based on remote sensing data analyses and field surveys, The structure and metabolism of a Puerto Rican red mangrove forest in May, N:P ratios in terrestrial plants: variation and functional significance, Evolved strategies in nitrogen acquisition by plants, Phosphorus relationships in a mangrove-swamp mud with particular reference to aluminium toxicity, The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview, Ammonium adsorption in sediments of a tropical mangrove forest (Thailand) and a temperate Wadden Sea area (Denmark), Biogeochemical cycling of sulfur and iron in sediments of a South-East Asian mangrove, Phuket Island, Thailand, Nitrogen metabolism and remobilization during senescence, Soil salinity and arbuscular mycorrhizal colonization of, The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage, Cadium accumulation and detoxification in a Cd-resistant population of the oligochaete, Decomposition of mangrove wood by marine fungi and teredinids in Belize, Top/root biomass ratio of a secondary mangrove (, Allometry, biomass and productivity of mangrove forests: a review, Arbuscular mycorrhizae and phosphate solubilising bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India, Effects of season, rainfall, and hydrogeomorphic setting on mangrove tree growth in Micronesia, Environmental drivers in mangrove establishment and early development: a review, Organic carbon and iron modulate nitrification rates in mangrove swamps of Goa, south west coast of India, Bacterial contribution to mitigation of iron and manganese in mangrove sediments, Benthic metabolism and sulfate reduction in a southeast Asian mangrove swamp, Transformation and transport of inorganic nitrogen in sediments of a southeast Asian mangrove forest, Organic carbon dynamics in mangrove ecosystems: a review, Fluxes of methane and nitrous oxide from an Indian mangrove, Conifer root discrimination against soil nitrate and the ecology of forest succession, Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats, Ecological role of grapsid crabs in mangrove ecosystems: a review, A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. ecosystems. 1994, Baldwin et al. The effect of soil salinity on AM fungi has been under much debate (Evelin et al. The microbial communities in the soil are also capable of depurating large amounts of wastewater inorganic N (Corredor and Morell 1994). 2004). surges, currents, waves and tides. 1998). Photosynthetic nitrogen-use efficiency (PNUE) is an index of resource-use efficiency and can be estimated as the ratio of photosynthetic capacity to leaf N content. 2007), A. marina trees in New Zealand (as low as 20%; Lovelock et al. Water Use in Relation to Growth, Carbon Partitioning, and Salt Balance, Bacterial productivity and microbial biomass In tropical mangrove sediments, The uptake of amino acids by microbes and trees in three cold-temperate forests, Plant Responses to Salinity Under Elevated Atmospheric Concentrations of CO 2, Convergence in hydraulic architecture, water relations and primary productivity amongst habitats and across seasons in Sydney, Above- and below-ground biomasses of two species of mangrove on the Hawkesbury River Estuary, New South Wales. Search for other works by this author on: Smithsonian Environmental Research Center. 2008) in conjunction with mangrove litter fall and the low rates of decomposition imposed by anoxic soils results in mangrove ecosystems being rich in organic matter (Nedwell et al. Based on the few studies that have addressed the effects of aluminium on mangrove growth, it has been concluded that mangroves are relatively tolerant to aluminium, having a large storage capacity in the canopy (Rout et al. FAST FACTS . Such a flexible strategy permits rapid colonization of newly available marine sediments but can also accommodate persistence under unfavourable conditions in environments where replacement by competing plant communities (succession) is prevented by tidal inundation. 2003b, Lovelock et al. Often this is accomplished by the action of grazing herbivores which accelerates the transfer of energy to detrital feeders. The sequence of reductive processes in flooded soils, as a function of the decrease in soil redox potential (Eh) (data from Patrick and Mahapatra 1968) and its control over the nutrients available for plant growth. However, the mangroves represent an extremely important part of the equation of life in all of the world's tropical ocean ecosystems. Benthic microbial mats are found in many intertidal mangrove habitats and can also contribute significantly to the N cycle of the mangrove particularly when the mat is dominated by N-fixing cyanobacteria (Lee and Joye 2006). Despite low rates of decomposition in anoxic soils, decomposition of mangrove vegetative material is also a major source of nutrients in the mangrove ecosystem, as well as for adjacent coastal ecosystems via tidal flushing (Lee 1995). However, convergent evolution has led to similar adaptations among mangrove species in traits such as water relations (Ball 1988a, Macinnis-Ng et al. Most mangrove species that have been studied have been found to be highly sensitive to variation in nutrient availability both in the laboratory (e.g., Boto et al. 2009a). Nutrients and carbon from mangrove forests provide essential support to other near shore marine ecosystems such as coral reefs and seagrass areas, and enrich coastal food webs and fishery production. Mangroves are the only trees that are capable of thriving in salt water. The poor nitrate assimilation potential in mangroves, demonstrated by low activity levels of nitrate reductase under field conditions (Smirnoff et al. Climate change can affect both plant and soil biochemical processes by means of increased CO2 levels, elevated temperatures, rising sea levels and higher storm frequency. N2O production increases exponentially with external input of inorganic N to the soil (Corredor et al. How do plants get nutrients from the soil into their roots? The grey mangrove ( Avicennia marina ) grows a series of snorkels or pencil roots which poke out of the mud to get oxygen, while the orange mangrove ( Bruguiera gymnorrhiza ) has developed knee roots. Added to anthropogenic eutrophication, increased nutrient delivery to the mangroves could result from coastal erosion following sea level rise or due to changing rainfall patterns. Limitations to growth imposed by iron are also likely (Alongi 2010), but have yet to be assessed in the field. The high biomass and productivity of mangrove forests and their extensive root systems make them potential candidates for uptake of discharged nutrients and heavy metals. This paper reports on the method applied to map coral reefs, mangroves and seagrass beds in the Bay of Robert in Martinique Island (French West Indies) by digitizing true-colour aerial photographs. (1996) demonstrate that root-fouling sponges growing on the roots of the mangrove can significantly increase root elongation rates. However, for mangrove trees, resorption of nutrients has been mostly observed to become less efficient when nutrients become more available in the soil (Feller et al. Sclerophylly is a trait related to low soil nutrient availability, especially low P (Loveless 1961, Wright et al. 8%). RE can vary greatly between species but, on average, plants resorb â¼50% of the nutrients (N and P) from their senescent tissue (Aerts and Chapin 2000). Soil bacteria have been shown to significantly respond to nitrate additions (Whigham et al. Also, another 100 PAs (10 in main Indian coast and 90island PAs in Andaman & Nicobar) have terrestrial or fresh water ecosystems which constitute boundaries with seawater or partly contain marine environment, but they are not listed as MPAs as per the criteria. A general pattern in mangrove forests is that taller, more robust trees tend to grow along the edges of channels, while farther back from the channel the trees are much smaller. The possible absence of AM fungi from many mangrove ecosystems is countered by the occurrence of phosphate-solubilizing bacteria in association with mangrove roots (Vazquez et al. 2006). The concentration of particles suspended in water column ranged from 0.09 to 0.15 g/l in the mangrove-lined bank. While nutrient availability strongly influences short-term root accumulation, the long-term effects of nutrient enrichment on mangrove peat are unclear and can be negative (McKee et al. Live and decaying mangrove leaves and roots provide nutrients that nourish plankton, algae, fish and shellfish. forest. 1992, Kristensen et al. The vast majority of the nutrient pool of mangrove forests is stored in the soil and not in the trees (Alongi et al. In some neotropical mangrove forests, K concentrations in green leaves were weakly but positively correlated with growth rates (Feller et al. Nitrogen and phosphorus have been implicated as the nutrients most likely to limit growth in mangroves. 2005). Similar to other plant communities, nutrient availability is one of the major factors influencing mangrove forest structure and productivity. The mangroves' complex root systems filter nitrates and phosphates that rivers and streams carry to the sea. Low oxygen levels in the soil due to flooding can have an opposite effect to salinity, reducing root extension rates and even cause root tip dieback in some species (McKee 1996). This figure appears in color in the online version of Tree Physiology. 2003b). MANGROVES: - Grey mangroves have leaves with glands that excrete salt - Some species such as the Grey Mangrove can also tolerate the storage of large amounts of salt in their leaves. Vierh, Unusually negative nitrogen isotopic compositions (δ15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem, REEXAMINATION OF PORE WATER SULFIDE CONCENTRATIONS AND REDOX POTENTIALS NEAR THE AERIAL ROOTS OF RHIZOPHORA MANGLE AND AVICENNIA GERMINANS, INTERSPECIFIC VARIATION IN GROWTH, BIOMASS PARTITIONING, AND DEFENSIVE CHARACTERISTICS OF NEOTROPICAL MANGROVE SEEDLINGS: RESPONSE TO LIGHT AND NUTRIENT AVAILABILITY, DIFFERENTIAL OXIDATION OF MANGROVE SUBSTRATE BY AVICENNIA GERMINANS AND RHIZOPHORA MANGLE, CRITICAL POTASSIUM CONCENTRATIONS FOR GROWTH AND THE DISTRIBUTION AND FUNCTIONS OF POTASSIUM IN PLANT-CELLS, Transformation and Availability to Rice of Nitrogen and Phosphorus in Waterlogged Soils, Tasks for vegetation science. Presence of red mangrove appears to have no effect on the oxidation state of surrounding anaerobic soils.-from Authors. 2010). Accordingly, we expect many mangrove environments to be nutrient limited and that, in general, tropical soils will be less fertile, particularly in P, which in contrast to N cannot be replaced through biological fixation (Vitousek 1984, Reich and Oleksyn 2004, Lovelock et al. It is likely that the discrepancy between pot and field studies is due to competition for available nitrate. Trees that occur in habitats where the soil is ammonium rich generally exhibit a preference for ammonium uptake and do not appear to suffer from ammonium toxicity, which can have a significant metabolic cost in ammonium-sensitive plants (Kronzucker et al. 2003). In Bocas del Toro, Panama, growth of trees was found to be both N and P limited (Lovelock et al. These dwarf (or scrub) trees can experience periods of rapid growth when nutrient limitation is lifted (e.g., Feller et al. Many mangrove soils have extremely low nutrient availability, although nutrient availability can vary greatly among and within mangrove forests. These tiny plastic fragments called microplastics (MPs) that measure less than 5mm. This was also suggested in a pot study where interacting effects between N, P and K availability and mangrove seedling growth were detected (Yates et al. Nitrogen resorption efficiency (NRE) in the Kenyan mangroves was as high as 69% for Avicennia marina (Rao et al. could also form the basis of a coprophagous food chain involving small While very common and important in terrestrial ecosystems, AM fungi have been found only in low-salinity mangrove soils (Sengupta and Chaudhuri 2002). 2007). 2009). 1. Nutrient enrichment is a major threat to marine ecosystems. mangrove leaves, are recycled within the For example, increased soil salinity leads to reduced colonization by AM fungi in citrus (Levy et al. 2005, Feller et al. 1984), suggests that the mangroves are well suited for utilizing ammonium as their primary N source. Massive loss of aboveground biomass and its effect on sediment organic carbon concentration: Less mangrove, more carbon? A mangrove lives in a very inhospitable environment for a plant. K+ deficiencies in mangroves as in other plants have been shown to result in loss of chlorophyll and photosynthetic function (Ball et al. In an analysis of 60 published nutrient-enrichment experiments, only 32% of the cases exhibited reduced nutrient RE as a result of nutrient enrichment (Aerts 1996).
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