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Variable effects of nutrient enrichment on soil respiration in mangrove forests

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Abstract

Background and Aims

Mangrove forests are globally important sites of carbon burial that are increasingly exposed to nutrient pollution. Here we assessed the response of soil respiration, an important component of forest carbon budgets, to nutrient enrichment over a wide range of mangrove forests.

Methods

We assessed the response of soil respiration to nutrient enrichment using fertilization experiments within 22 mangrove forests over ten sites. We used boosted regression tree (BRT) models to determine the importance of environmental and plant factors for soil respiration and its responsiveness to fertilizer treatments.

Results

Leaf area index explained the largest proportion of variation in soil respiration rates (LAI, 45.9 %) followed by those of site, which had a relative influence of 39.9 % in the BRT model. Nutrient enrichment enhanced soil respiration only in nine out of 22 forests. Soil respiration in scrub forests showed a positive response to nutrient addition more frequently than taller fringing forests. The response of soil respiration to nutrient enrichment varied with changes in specific leaf area (SLA) and stem extension, with relative influences of 14.4 %, 13.6 % in the BRT model respectively.

Conclusions

Soil respiration in mangroves varied with LAI, but other site specific factors also influenced soil respiration and its response to nutrient enrichment. Strong enhancements in aboveground growth but moderate increases in soil respiration with nutrient enrichment indicated that nutrient enrichment of mangrove forests has likely increased net ecosystem production.

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References

  • Adame MF, Wright SF, Grinham A, Lobb K, Reymond CE, Lovelock CE (2012) Terrestrial-marine connectivity: Patterns of terrestrial soil carbon deposition in coastal sediments determined by analysis of glomalin-related soil protein. Limnol Oceanogr 57:1492–1502

    Article  CAS  Google Scholar 

  • Agren GI, Bosatta E, Magill AH (2001) Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94–98

    Article  Google Scholar 

  • Alongi DM (1988) Bacterial productivity and microbial biomass in tropical mangrove sediments. Microb Ecol 15:59–79

    Article  CAS  PubMed  Google Scholar 

  • Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349

    Article  Google Scholar 

  • Alongi DM (2008) Mangrove forests: Resilience, protection from tsunamis, and responses to global climate change. Estuar Coast Shelf Sci 76:1–13

    Article  Google Scholar 

  • Alongi DM (2009) The energetics of mangrove ecosystems. Springer, Dortrecht

    Google Scholar 

  • Alongi DM, Clough BF, Dixon P, Terendi F (2003) Nutrient partitioning and storage in arid-zone forests of the mangrove Rhizophora stylosa and Avicennia marina. Trees Struct Funct 17:51–60

    Article  CAS  Google Scholar 

  • Alongi DM, de Carvalho NA, Amaral AL, da Costa A, Trott L, Tirendi F (2012) Uncoupled surface and below-ground soil respiration in mangroves: Implications for estimates of dissolved inorganic carbon export. Biogeochemistry 109:151–162

    Article  CAS  Google Scholar 

  • Ball MC (1988) Salinity tolerance in mangroves Aegiceras corniculatum and Avicennia marina. I. Water use in relation to growth, carbon partitioning, and salt balance. Aust J Plant Physiol 15:447–464

    Article  Google Scholar 

  • Ball MC, Pidsley SM (1995) Growth responses to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata, in northern Australia. Funct Ecol 9:77–85

    Article  Google Scholar 

  • Bouillon S, Borges AV, Castaneda-Moya E, Diele K, Dittmar T (2008) Mangrove production and carbon sinks: a revision of global budget estimates. Glob Biogeochem Cycl 22: doi:10.1029/2007GB003052

  • Breithaupt JL, Smoak JM, Smith III TJ, Sanders CJ, Hoare A (2012) Organic carbon burial rates in mangrove sediments: Strengthening the global budget, Glob Biogeochem Cycl 501: doi 10.1029/2012GB004375

  • Brouwer R (1962) Distribution of dry matter in the plant. Nether J Agric Sci: 399–408

  • Butnor JR, Johnse KH, Oren R, Katul GG (2003) Reduction of forest floor respiration by fertilization on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands. Glob Change Biol 6:849–861

    Article  Google Scholar 

  • Burchett MD, Field CD, Pulkownik A (1984) Salinity, growth and root respiration in the grey mangrove, Avicennia marina. Physiol Planta 60:113–118

    Article  Google Scholar 

  • Cannell MGR, Dewar RC (1994) Carbon allocation in trees - a review of concepts for modeling. Advan Ecol Res 25:59–104

    Article  Google Scholar 

  • Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Non-point pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568

    Article  Google Scholar 

  • Castaneda-Moya E, Twilley RR, Rivera-Monroy VH (2011) Patterns of root dynamics in mangrove forests along environmental gradients in the Florida Coastal Everglades, USA. Ecosystems 14:1178–1195

    Article  CAS  Google Scholar 

  • Chapin FS (2003) Effects of plant traits on ecosystem and regional processes, a conceptual framework for predicting the consequences of global change. Ann Bot 91:455–463

    Article  PubMed  Google Scholar 

  • Cheeseman JC, Lovelock CE (2004) Photosynthetic characteristics of dwarf and fringe Rhizophora mangle in a Belizean mangrove. Plant Cell Environ 27:768–780

    Article  Google Scholar 

  • Clough BF (1998) Mangrove forest productivity and biomass accumulation in Hinchinbrook Channel, Australia. Mangr Salt Marsh 2:191–198

    Article  Google Scholar 

  • Clough BF (1994) Growth and salt balance of the mangroves Avicennia marina (Forsk.) Vierh. and Rhizophora stylosa Griff. in relation to salinity. Austr J Plant Physiol 11:419–430

    Article  Google Scholar 

  • Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005) Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86:12–19

    Article  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • Diaz S, Lavorel S, de Bello F, Quetier F, Grigulus K, Robson TM (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci U S A 104:20684–20689

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M (2011) Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–297

    Article  CAS  Google Scholar 

  • Duarte CM, Middelburg J, Caraco N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8

    Article  CAS  Google Scholar 

  • Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7:27–47

    Article  Google Scholar 

  • Elith J, Leathwick JR, Hastie T (2008) Boosted regression trees - a new technique for modelling ecological data. J Anim Ecol 77:802–813

    Article  CAS  PubMed  Google Scholar 

  • Ellis J, Nicholls P, Craggs R, Hofstra D, Hewitt J (2004) Effects of terrigenous sedimentation on mangrove physiology and associated macrobenthic communities. Mar Ecol Progr Ser 270:71–82

    Article  Google Scholar 

  • Fang H, Cheng S, Yu G, Zheng J, Zhang P, Xu M, Li Y, Yang X (2012) Responses of CO2 efflux from an alpine meadow soil on the Qinghai Tibetan plateau to multi-form and low-level N addition. Plant Soil 351:177–190

    Article  CAS  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • Feller IC, Whigham DF, McKee KL, O’Neill JP (2002) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175

    Article  Google Scholar 

  • Feller IC, Lovelock CE, McKee KL (2007) Nutrient addition differentially affects ecological processes of Avicennia germinans in nitrogen vs. phosphorus limited mangrove ecosystems. Ecosystems 10:347–359

    Article  CAS  Google Scholar 

  • Feller IC, Whigham DF, McKee KL, Lovelock CE (2003) Nitrogen limitation of growth and nutrient dynamics in a mangrove forest, Indian River Lagoon, Florida. Oecologia 134:405–414

    PubMed  Google Scholar 

  • Fisk MC, Fahey TJ (2001) Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53:201–223

    Article  CAS  Google Scholar 

  • Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS (2004) Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–550

    Article  PubMed  Google Scholar 

  • Grace J, Rayment M (2000) Respiration in the balance. Nature 404:819–820

    Article  CAS  PubMed  Google Scholar 

  • Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshwater Biol 48:123–134

    Article  Google Scholar 

  • Hastie TJ, Tibshirani RJ, Friedman JH (2001) The elements of statistical learning: Data mining, inference, and prediction. Springer series in statistics, New York

    Book  Google Scholar 

  • Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci 16:614–623

    Article  CAS  PubMed  Google Scholar 

  • Janssens IA, Dieleman W, Luyssaert S, Subke J-A, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322

    Article  CAS  Google Scholar 

  • Klumpp KJA, Soussana JF (2009) Using functional traits to predict grassland ecosystem change, a mathematical test of the response-and-effect trait approach. Glob Change Biol 15:2921–2934

    Article  Google Scholar 

  • Krauss KW, McKee KL, Lovelock CE, Cahoon DR, Saintilan N, Reef R, Chen L (2013) How mangrove forests adjust to rising sea level. Tansley Review. New Phytol

  • Kristensen E, Bouillon S, Dittmar T, Marchand C (2008a) Organic carbon dynamics in mangrove ecosystems: A review. Aquat Bot 89:201–219

    Article  CAS  Google Scholar 

  • Kristensen E, Flindt MR, Borges AV, Bouillon S (2008b) Emission of CO2 and CH4 to the atmosphere by sediments and open waters in two Tanzanian mangrove forests. Mar Ecol Prog Ser 370:53–67

    Article  CAS  Google Scholar 

  • Kristensen E, Mangion P, Tang M, Flindt MR, Holmer M, Ulomi S (2011) Microbial carbon oxidation rates and pathways in sediments of two Tanzanian mangrove forests. Biogeochemistry 103:143–158

    Article  CAS  Google Scholar 

  • Keuskamp JA, Schmitt H, Laanbroek HJ, Verhoeven JT, Hefting MM (2013) Nutrient amendment does not increase mineralisation of sequestered carbon during incubation of a nitrogen limited mangrove soil. Soil Biol Biochem 57:822–829

    Article  CAS  Google Scholar 

  • Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Change Biol 13:2089–2109

    Article  Google Scholar 

  • Lopez-Hoffman L, Anten NPR, Martınez-Ramos M, Ackerly D (2007) Salinity and light interactively affect neotropical mangrove seedlings at the leaf and whole plant levels. Oecologia 150:545–556

    Article  PubMed  Google Scholar 

  • Lovelock CE (2008) Soil respiration and belowground carbon allocation in mangrove forests. Ecosystems 11:342–354

    Article  CAS  Google Scholar 

  • Lovelock CE, Ball MC, Martin KC, Feller IC (2009) Nutrient enrichment increases mortality of mangroves. PloS ONE 4(5):e5600. doi:10.1371/journal.pone.0005600

    Article  PubMed Central  PubMed  Google Scholar 

  • Lovelock CE, Feller IC, Adame MF, Reef R, Penrose HM, Wei L, Ball MC (2011) Intense storms and the delivery of materials that relieve nutrient limitations in mangroves of an arid zone estuary. Funct Plant Biol 38:514–522

    Article  CAS  Google Scholar 

  • Lovelock CE, Feller IC, Ball MC, Ellis J, Sorrell B (2007a) Testing the growth rate vs. Geochemical hypothesis for latitudinal variation in plant nutrients. Ecol Lett 10:1154–1163

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Feller IC, Ball MC, Engelbrecht BMJ, Ewe ML (2006a) Differences in plant function in phosphorus-and nitrogen-limited mangrove ecosystems. New Phytol 172:514–522

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Feller IC, Ellis J, Schwarz AM, Hancock N, Nichols P, Sorrell B (2007b) Mangrove growth in New Zealand estuaries: The role of nutrient enrichment at sites with contrasting rates of sedimentation. Oecologia 153:633–641

    Article  PubMed  Google Scholar 

  • Lovelock CE, Feller IC, McKee KL, Engelbrecht BM, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Funct Ecol 18:25–33

    Article  Google Scholar 

  • Lovelock CE, Ruess RW, Feller IC (2006b) Fine root respiration in the mangrove Rhizophora mangle over variation in forest stature and nutrient availability. Tree Physiol 26:1601–1606

    Article  CAS  PubMed  Google Scholar 

  • Mack MC, Schuur EA, Bret-Harte MS, Shaver GR, Chapin FS (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443

    Article  CAS  PubMed  Google Scholar 

  • Magnani M, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentin R, Grace J (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:849–851

    Article  CAS  Google Scholar 

  • Maher DT, Santos IR, Golsby-Smith L, Gleeson J, Eyre BD (2013) Groundwater-derived dissolved inorganic and organic carbon exports from a mangrove tidal creek: The missing mangrove carbon sink? Limnol Oceanogr 58:475–488

    CAS  Google Scholar 

  • Mcleod E, Chmura GL, Bouillon S, Salm R, Bjork M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman B (2011) A blueprint for blue carbon, towards an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560

    Article  Google Scholar 

  • McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants, ontogeny or optimality? a test along three resource gradients. Ecology 80:2581–2593

    Article  Google Scholar 

  • McKee KL (1995) Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings: Response to light and nutrient availability. Am J Bot 82:299–307

    Article  Google Scholar 

  • McKee KL, Cahoon DR, Feller IC (2007) Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation. Glob Ecol Biogeogr 16:545–556

    Article  Google Scholar 

  • McKee KL, Feller IC, Popp M, Wanek W (2002) Mangrove isotopic fractionation (δ15N and δ13C) across a nitrogen versus phosphorus limitation gradient. Ecology 83:1065–1075

    Google Scholar 

  • McKee KL, Mendelssohn IA, Hester MW (1988) Reexamination of pore water sulphide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans. Am J Bot 75:1352–1359

    Article  Google Scholar 

  • Morrisey DA, Swales A, Dittmann S, Morrison MA, Lovelock CE, Beard CM (2010) The ecology and management of temperate mangroves. Oceanogr Mar Biol Ann Rev 48:43–160

    Google Scholar 

  • Nui S, Wu M, Han Y, Xia J, Zhang Z, Yang J, Wan S (2009) Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Glob Change Biol 16:144–155

    Google Scholar 

  • Poungparna S, Komiyama A, Tanaka A, Sangtiean T, Maknuala C, Kato S, Tanapermpoola P, Patanaponpaiboon P (2009) Carbon dioxide emission through soil respiration in a secondary mangrove forest of eastern Thailand. J Trop Ecol 25:393–400

    Article  Google Scholar 

  • Raich JW (1998) Aboveground productivity and soil respiration in three Hawaiian rain forests. For Ecol Manag 107:309–318

    Article  Google Scholar 

  • Raich JW, Nadelhoffer KJ (1989) Belowground carbon allocation in forest ecosystems. Glob Trend Ecol 70:1346–1354

    Google Scholar 

  • Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99

    Article  CAS  Google Scholar 

  • Raich JW, Tufekcioglu A (2000) Vegetation and soil respiration: Correlations and controls. Biogeochemistry 48:71–90

    Article  CAS  Google Scholar 

  • Ridgeway G (2006) Generalized boosted regression models. Documentation on the R package “gbm”, version 1.5-7. http://www.i-pensieri.com/gregr/gbm.shtml.

  • Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854

    Article  CAS  Google Scholar 

  • Robertson AI, Alongi DM, Boto KG (1992) Food chains and carbon fluxes. In: Roberston AI, Alongi DM (eds) Tropical mangrove ecosystems. Coastal and Estuarine Studies 41. American Geophysical Union, Washington, pp 293–326

    Chapter  Google Scholar 

  • Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornsson B, Allen MF, Maurer G (2003) Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecol Monogr 74:643–662

    Article  Google Scholar 

  • Rustad LE, Thomas G, Huntington M, Boone RD (2000) Controls on soil respiration, implications for climate change. Biogeochemistry 48:1–6

    Article  Google Scholar 

  • Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20

    Article  CAS  Google Scholar 

  • Schwarz AM (2004) Contribution of photosynthetic gains during tidal emersion to production of Zostera capricorni in a North Island, New Zealand estuary. New Zeal J Mar Freshwater Res 38:809–818

    Article  Google Scholar 

  • Tang J, Baldocchi DD, Xu L (2005) Tree photosynthesis modulates soil respiration on a diurnal time scale. Glob Change Biol 11:1298–1304

    Article  Google Scholar 

  • Valiela I, Cole ML (2002) Comparative evidence that salt marshes and mangroves may protect seagrass meadows from land-derived nitrogen loads. Ecosystems 5:92–102

    Article  Google Scholar 

  • Walsh DA, Thane Papke R, Doolittle WF (2005) Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 7:1655–1666

    Article  CAS  PubMed  Google Scholar 

  • Witherington JM, Reich PB, Oleksyn J, Eissenstat DM (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–397

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M (2001) Strategy-shifts in leaf physiology, structure and nutrient content between species of high and low rainfall, and high and low nutrient habitats. Funct Ecol 15:423–434

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

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Acknowledgement

This study was supported by the National Science Foundation under Grant DEB 99-81309, a WISC award from the American Association for the Advancement, the New Zealand Foundation for Research, Science and Technology (C01X0024, C01X0215, and C01X0307), the Smithsonian’s Marine Science Network, the Smithsonian Marine Station at Fort Pierce, the Caribbean Coral Reef Ecosystems Program and Australian Research Council awards LP0561498 and DP0774491. I thank Marilyn Ball and the staff of Carrie Bow Cay Research Station and Pelican Beach Resort, Belize. Thanks are also extended to the many people who helped in the field, including Fernanda Adame, Dianne Allen, Don Cahoon, Anne Chamberlain, Beth Clegg, Bettina Engelbrecht, Sharon Ewe, Ray Feller, Jane Halliday, Nicole Hancock, Helen Penrose, Brian Sorrell, Ann Maree Schwarz, and Rachel Tenni.

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Correspondence to Catherine E. Lovelock.

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Lovelock, C.E., Feller, I.C., Reef, R. et al. Variable effects of nutrient enrichment on soil respiration in mangrove forests. Plant Soil 379, 135–148 (2014). https://doi.org/10.1007/s11104-014-2036-6

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