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      Soil organic carbon stocks in estuarine and marine mangrove ecosystems are driven by nutrient colimitation of P and N

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          Abstract

          Mangroves play an important role in carbon sequestration, but soil organic carbon ( SOC) stocks differ between marine and estuarine mangroves, suggesting differing processes and drivers of SOC accumulation. Here, we compared undegraded and degraded marine and estuarine mangroves in a regional approach across the Indonesian archipelago for their SOC stocks and evaluated possible drivers imposed by nutrient limitations along the land‐to‐sea gradients. SOC stocks in natural marine mangroves (271–572 Mg ha −1 m −1) were much higher than under estuarine mangroves (100–315 Mg ha −1 m −1) with a further decrease caused by degradation to 80–132 Mg ha −1 m −1. Soils differed in C/N ratio (marine: 29–64; estuarine: 9–28), δ 15N (marine: −0.6 to 0.7‰; estuarine: 2.5 to 7.2‰), and plant‐available P (marine: 2.3–6.3 mg kg −1; estuarine: 0.16–1.8 mg kg −1). We found N and P supply of sea‐oriented mangroves primarily met by dominating symbiotic N 2 fixation from air and P import from sea, while mangroves on the landward gradient increasingly covered their demand in N and P from allochthonous sources and SOM recycling. Pioneer plants favored by degradation further increased nutrient recycling from soil resulting in smaller SOC stocks in the topsoil. These processes explained the differences in SOC stocks along the land‐to‐sea gradient in each mangrove type as well as the SOC stock differences observed between estuarine and marine mangrove ecosystems. This first large‐scale evaluation of drivers of SOC stocks under mangroves thus suggests a continuum in mangrove functioning across scales and ecotypes and additionally provides viable proxies for carbon stock estimations in PES or REDD schemes.

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          Most cited references5

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          Nitrogen metabolism and remobilization during senescence.

          Senescence is a highly organized and well-regulated process. As much as 75% of total cellular nitrogen may be located in mesophyll chloroplasts of C(3)-plants. Proteolysis of chloroplast proteins begins in an early phase of senescence and the liberated amino acids can be exported to growing parts of the plant (e.g. maturing fruits). Rubisco and other stromal enzymes can be degraded in isolated chloroplasts, implying the involvement of plastidial peptide hydrolases. Whether or not ATP is required and if stromal proteins are modified (e.g. by reactive oxygen species) prior to their degradation are questions still under debate. Several proteins, in particular cysteine proteases, have been demonstrated to be specifically expressed during senescence. Their contribution to the general degradation of chloroplast proteins is unclear. The accumulation in intact cells of peptide fragments and inhibitor studies suggest that multiple degradation pathways may exist for stromal proteins and that vacuolar endopeptidases might also be involved under certain conditions. The breakdown of chlorophyll-binding proteins associated with the thylakoid membrane is less well investigated. The degradation of these proteins requires the simultaneous catabolism of chlorophylls. The breakdown of chlorophylls has been elucidated during the last decade. Interestingly, nitrogen present in chlorophyll is not exported from senescencing leaves, but remains within the cells in the form of linear tetrapyrrolic catabolites that accumulate in the vacuole. The degradation pathways for chlorophylls and chloroplast proteins are partially interconnected.
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            Nutrition of mangroves.

            Mangrove forests dominate the world's tropical and subtropical coastlines. Similar to other plant communities, nutrient availability is one of the major factors influencing mangrove forest structure and productivity. Many mangrove soils have extremely low nutrient availability, although nutrient availability can vary greatly among and within mangrove forests. 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. Both nitrogen-use efficiency and nutrient resorption efficiencies in mangroves are amongst the highest recorded for angiosperms. A complex range of interacting abiotic and biotic factors controls the availability of nutrients to mangrove trees, and mangroves are characteristically plastic in their ability to opportunistically utilize nutrients when these become available. Nitrogen and phosphorus have been implicated as the nutrients most likely to limit growth in mangroves. Ammonium is the primary form of nitrogen in mangrove soils, in part as a result of anoxic soil conditions, and tree growth is supported mainly by ammonium uptake. Nutrient enrichment is a major threat to marine ecosystems. 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.
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              Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients.

              Two hypotheses have been proposed to explain increases in plant nitrogen (N) and phosphorus (P) concentrations with latitude: (i) geochemical limitation to P availability in the tropics and (ii) temperature driven variation in growth rate, where greater growth rates (requiring greater nutrient levels) are needed to complete growth and reproduction within shorter growing seasons in temperate than tropical climates. These two hypotheses were assessed in one forest type, intertidal mangroves, using fertilized plots at sites between latitudes 36 masculine S and 27 masculine N. The N and P concentrations in mangrove leaf tissue increased with latitude, but there were no trends in N : P ratios. Growth rates of trees, adjusted for average minimum temperature showed a significant increase with latitude supporting the Growth Rate Hypothesis. However, support for the Geochemical Hypothesis was also strong; both photosynthetic P use efficiency and nutrient resorption efficiency decreased with increasing latitude, indicating that P was less limiting to metabolism at the higher latitudes. Our study supports the hypothesis that historically low P availability in the tropics has been an important selective pressure shaping the evolution of plant traits.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                26 June 2016
                July 2016
                : 6
                : 14 ( doiID: 10.1002/ece3.2016.6.issue-14 )
                : 5043-5056
                Affiliations
                [ 1 ] Institute of Soil ScienceLeibniz Universität Hannover Herrenhäuser Str. 2 D‐30419 HannoverGermany
                [ 2 ] Department of Soil Science and Land ResourcesBogor Agricultural University Kampus IPB Dramaga Bogor 16680Indonesia
                [ 3 ] Soil Science and Soil ProtectionMartin Luther Universität Halle Wittenberg Von‐Seckendorff‐Platz 3 D‐06120 Halle (Saale)Germany
                Author notes
                [*] [* ] Correspondence

                Jens Boy, Institute for Soil Science, Leibniz University Hannover, Herrenhäuser Str. 2, D‐30419 Hannover, Germany.

                Tel: +49 511 7623561;

                Fax: +49 511 7625559;

                E‐mail: Boy@ 123456ifbk.uni-hannover.de

                Author information
                http://orcid.org/0000-0002-2751-957X
                Article
                ECE32258
                10.1002/ece3.2258
                4979726
                27547332
                84605206-0c33-4333-a517-39c38117fa3e
                © 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 March 2016
                : 23 May 2016
                : 25 May 2016
                Page count
                Pages: 14
                Funding
                Funded by: Federal Ministry of Education and Research (BMBF)
                Award ID: 03F0644
                Funded by: German Indonesian joint research project SPICE III
                Award ID: 030F0644C
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32258
                July 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:10.08.2016

                Evolutionary Biology
                ecosystem functioning,global change,indonesia,marine and estuarine mangroves,nitrogen,phosphorus,soil organic carbon,stable isotopes

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