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Above- to Belowground Vegetation Biomass Ratio in Temperate North-East Atlantic Saltmarshes Increases Strongly with Soil Nitrogen Gradient

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Abstract

Saltmarshes provide a broad range of ecosystem services, but have been degraded globally and are further threatened by sea-level rise. Changes in biomass partitioning between above- and belowground components of plant community biomass as a consequence of nutrient enrichment can impact those services profoundly. However, the evidence for such impacts is largely confined to North America, leaving a gap in global understanding of coastal ecosystem resilience. Using field surveys across 15 saltmarshes along the south and east coasts of Ireland, we tested whether aboveground (AG) and belowground (BG) plant biomass allocation across all plant assemblages combined and within individual plant assemblages is related to soil nutrients. AG biomass and AG/BG biomass ratio were positively related, and BG biomass was negatively related to NO−x, both across all assemblages combined and within individual assemblages. AG biomass and AG/BG ratio were also positively related to NH4+ within individual assemblages, but not across all of them combined. The relationships between biomass and labile P were weaker, and their direction varied across the whole P gradient and among individual assemblages. These findings demonstrate broad, community-wide links between biomass allocation and soil nutrients in saltmarshes. The up to 6.6-fold increase in AG/BG biomass ratio along the N gradient, coupled with differential responses among functionally contrasting plants, could have significant implications for multiple saltmarsh functions such as energy fixation for consumers, wave attenuation, sediment binding and carbon storage. Improved understanding of the underlying causalities would help promoting saltmarsh resilience.

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References

  • Aziz SA, Nedwell DB. 1986a. The nitrogen cycle of an East Coast, U.K., saltmarsh: I. Nitrogen assimilation during primary production; detrital mineralization. Estuarine, Coastal and Shelf Science 22:559–75.

    CAS  Google Scholar 

  • Aziz SA, Nedwell DB. 1986b. The nitrogen cycle of an East Coast, U.K. saltmarsh: II. Nitrogen fixation, nitrification, denitrification, tidal exchange. Estuarine, Coastal and Shelf Science 22:689–704.

    Google Scholar 

  • Adam P. 2002. Saltmarshes in a time of change. Environmental Conservation 29:39–61.

    Google Scholar 

  • Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81:169–93.

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48.

    Google Scholar 

  • Bertness MD, Crain C, Holdredge C, Sala N. 2008. Eutrophication and consumer control of New England salt marsh primary productivity. Conservation Biology 22:131–9.

    PubMed  Google Scholar 

  • Boudsocq S, Niboyet A, Lata JC, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S. 2012. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? The American Naturalist 180:60–9.

    CAS  PubMed  Google Scholar 

  • Bradley PM, Morris JT. 1990. Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71:282–7.

    CAS  Google Scholar 

  • Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC. 2003. Global carbon sequestration in tidal, saline wetland soils. Global Biogeochemical Cycles . https://doi.org/10.1029/2002GB001917.

    Article  Google Scholar 

  • Curtis TGF, Sheehy-Skeffington MJ. 1998. The salt marshes of Ireland: an inventory and account of their geographical variation. Biology and Environment: Proceedings of the Royal Irish Academy 98B:87–104.

    Google Scholar 

  • Davidson KE, Fowler MS, Skov MW, Doerr SH, Beaumont N, Griffin JN. 2017. Livestock grazing alters multiple ecosystem properties and services in salt marshes: a meta-analysis. Journal of Applied Ecology 54:1395–405.

    CAS  Google Scholar 

  • Davy AJ, Brown MJH, Mossman HL, Grant A. 2011. Colonization of a newly developing salt marsh: disentangling independent effects of elevation and redox potential on halophytes. Journal of Ecology 99:1350–7.

    CAS  Google Scholar 

  • de Groot R, Brander L, van der Ploeg S, Costanza R, Bernard F, Braat L, Christie M, Crossman N, Ghermandi A, Hein L, Hussain S, Kumar P, McVittie A, Portela R, Rodriguez LC, ten Brink P, van Beukering P. 2012. Global estimates of the value of ecosystems and their services in monetary units. Ecosystem Services 1:50–61.

    Google Scholar 

  • Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–92.

    CAS  PubMed  Google Scholar 

  • Emery NC, Ewanchuk PJ, Bertness MD. 2001. Competition and salt-marsh plant zonation: stress tolerators may be dominant competitors. Ecology 82:2471–85.

    Google Scholar 

  • Falkengren-Grerup U. 1995. Interspecies differences in the preference of ammonium and nitrate in vascular plants. Oecologia 102:305–11.

    PubMed  Google Scholar 

  • Fanning A, Craig M, Webster P, Bradley C, Tierney D, Wilkes R, Mannix A, Treacy P, Kelly F, Geoghegan R, Kent T, Mageean M. 2017. Water quality in Ireland 2010–2015. Wexford: Environmental Protection Agency.

    Google Scholar 

  • Fox J, Weisberg S. 2011. An R companion to applied regression. Thousand Oaks: Sage Publishing.

    Google Scholar 

  • Gedan KB, Silliman BR, Bertness MD. 2009. Centuries of human-driven change in salt marsh ecosystems. Annual Review of Marine Science 1:117–41.

    PubMed  Google Scholar 

  • Gedan KB, Kirwan ML, Wolanski E, Barbier EB, Silliman BR. 2011. The present and future role of coastal wetland vegetation in protecting shorelines: answering recent challenges to the paradigm. Climatic Change 106:7–29.

    Google Scholar 

  • Graham SA, Mendelssohn IA. 2016. Contrasting effects of nutrient enrichment on below-ground biomass in coastal wetlands. Journal of Ecology 104:249–60.

    CAS  Google Scholar 

  • Hassler M. 2018. World plants: synonymic checklists of the vascular plants of the world (version Dec 2017). In: Roskov Y, Abucay L, Orrell T, Nicolson D, Bailly N, Kirk PM, Bourgoin T, DeWalt RE, Decock W, De Wever A, van Nieukerken E, Zarucchi J, Penev L, Eds. Species 2000 & ITIS catalogue of life, 28th March 2018. Leiden: Species 2000: Naturalis.

    Google Scholar 

  • Hautier Y, Niklaus PA, Hector A. 2009. Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–8.

    CAS  PubMed  Google Scholar 

  • Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hillebrand H, Lind EM, MacDougall AS, Stevens CJ, Bakker JD, Buckley YM, Chu C, Collins SL, Daleo P, Damschen EI, Davies KF, Fay PA, Firn J, Gruner DS, Jin VL, Klein JA, Knops JMH, La Pierre KJ, Li W, McCulley RL, Melbourne BA, Moore JL, O’Halloran LR, Prober SM, Risch AC, Sankaran M, Schuetz M, Hector A. 2014. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508:521.

    CAS  PubMed  Google Scholar 

  • Hector A, Bagchi R. 2007. Biodiversity and ecosystem multifunctionality. Nature 448:188.

    CAS  PubMed  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11:610–17.

    CAS  PubMed  Google Scholar 

  • Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S. 2013. Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proceedings of the National Academy of Sciences 110:11911–16.

    CAS  Google Scholar 

  • Jefferies RL, Perkins N. 1977. Effects on vegetation of additions of inorganic nutrients to salt-marsh soils at Stiffkey, Norfolk. Journal of Ecology 65:867–82.

    CAS  Google Scholar 

  • Johnson DS, Warren RS, Deegan LA, Mozdzer TJ. 2016. Saltmarsh plant responses to eutrophication. Ecological Applications 26:2649–61.

    Google Scholar 

  • Kell DB. 2012. Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367:1589–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiehl K, Esselink P, Bakker PJ. 1997. Nutrient limitation and plant species composition in temperate salt marshes. Oecologia 111:325–30.

    CAS  PubMed  Google Scholar 

  • Kirwan ML, Megonigal JP. 2013. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53.

    CAS  PubMed  Google Scholar 

  • Lamers LPM, Govers LL, Janssen ICJM, Geurts JJM, Van der Welle MEW, Van Katwijk MM, Van der Heide T, Roelofs JGM, Smolders AJP. 2013. Sulfide as a soil phytotoxin-a review. Frontiers in Plant Science 4:268.

    PubMed  PubMed Central  Google Scholar 

  • Lawrence PJ. 2018. How to create a saltmarsh: understanding the roles of topography, redox and nutrient dynamics. Doctoral thesis (PhD), Manchester Metropolitan University. https://e-space.mmu.ac.uk/id/eprint/620851. Accessed 19 June 2019.

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–9.

    CAS  PubMed  Google Scholar 

  • Maynard DG, Kalra YP, Crumbaugh JA. 2008. Nitrate and exchangeable ammonium nitrogen. In: Carter MR, Gregorich EG, Eds. Canadian society for soil science: soil sampling and methods of analysis. Boca Raton: CRC Press. p 71–80.

    Google Scholar 

  • McCorry M, Ryle T. 2009. Saltmarsh monitoring project 2007–2008. Dublin: National Parks and Wildlife Service.

    Google Scholar 

  • McGlathery KJ. 2008. Chapter 23—seagrass habitats. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ, Eds. Nitrogen in the marine environment. 2nd edn. San Diego: Academic Press. p 1037–71.

    Google Scholar 

  • Mcleod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman BR. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Frontiers in Ecology and the Environment 9:552–60.

    Google Scholar 

  • Mudd SM, D’Alpaos A, Morris JT. 2010. How does vegetation affect sedimentation on tidal marshes? Investigating particle capture and hydrodynamic controls on biologically mediated sedimentation. Journal of Geophysical Research: Earth Surface . https://doi.org/10.1029/2009JF001566.

    Article  Google Scholar 

  • Penk MR, Wilkes R, Perrin PM, Waldren S. 2019. Nutrients in saltmarsh soils are weakly related to those in adjacent coastal waters. Estuaries and Coasts 42:675–87.

    CAS  Google Scholar 

  • Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA. 2013. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications 4:2934.

    PubMed  Google Scholar 

  • Perrin PM. 2016. Irish Vegetation Classification: technical progress report no. 2. Waterford: National Biodiversity Data Centre.

    Google Scholar 

  • Perrin PM. 2017. Irish Vegetation Classification ERICA: engine for relevés to Irish communities assignment v2.1. Waterford: National Biodiversity Data Centre.

    Google Scholar 

  • Prager CM, Naeem S, Boelman NT, Eitel JUH, Greaves HE, Heskel MA, Magney TS, Menge DNL, Vierling LA, Griffin KL. 2017. A gradient of nutrient enrichment reveals nonlinear impacts of fertilization on Arctic plant diversity and ecosystem function. Ecology and Evolution 7:2449–60.

    PubMed  PubMed Central  Google Scholar 

  • R Core Team. 2018. R: a Language and environment for statistical computing, version 3.5.1. Vienna: R Foundation for Statistical Computing. http://www.R-project.org. Accessed 1 Aug 2018.

  • Rozema J, Leendertse P, Bakker J, Wijnen H. 2000. Nitrogen and vegetation dynamics in European salt marshes. In: Weinstein MP, Kreeger DA, Eds. Concepts and controversies in tidal marsh ecology. Dordrecht: Springer. p 469–91.

    Google Scholar 

  • Schoenau JJ, O’Halloran IP. 2008. Sodium bicarbonate-extractable phosphorus. In: Carter MR, Gregorich EG, Eds. Canadian society for soil science: soil sampling and methods of analysis. Boca Raton: CRC Press. p 89–94.

    Google Scholar 

  • Schrama M, Jouta J, Berg MP, Olff H. 2013. Food web assembly at the landscape scale: using stable isotopes to reveal changes in trophic structure during succession. Ecosystems 16:627–38.

    Google Scholar 

  • Schubauer JP, Hopkinson CS. 1984. Above- and belowground emergent macrophyte production and turnover in a coastal marsh ecosystem, Georgia. Limnology and Oceanography 29:1052–65.

    Google Scholar 

  • Schutten J, Dainty J, Davy AJ. 2005. Root anchorage and its significance for submerged plants in shallow lakes. Journal of Ecology 93:556–71.

    Google Scholar 

  • Silliman BR, Zieman JC. 2001. Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–45.

    Google Scholar 

  • Smith KK, Good RE, Good NF. 1979. Production dynamics for above and belowground components of a New Jersey Spartina alterniflora tidal marsh. Estuarine and Coastal Marine Science 9:189–201.

    CAS  Google Scholar 

  • Smith TJ, Odum WE. 1981. The effects of grazing by snow geese on coastal salt marshes. Ecology 62:98–106.

    Google Scholar 

  • Smith VH, Schindler DW. 2009. Eutrophication science: where do we go from here? Trends in Ecology & Evolution 24:201–7.

    Google Scholar 

  • Svensson CJ, Hyndes GA, Lavery PS. 2007. Food web analysis in two permanently open temperate estuaries: consequences of saltmarsh loss? Marine Environmental Research 64:286–304.

    CAS  PubMed  Google Scholar 

  • Theodose TA, Roths JB. 1999. Variation in nutrient availability and plant species diversity across forb and graminoid zones of a Northern New England high salt marsh. Plant Ecology 143:219–28.

    Google Scholar 

  • Torio DD, Chmura GL. 2013. Assessing coastal squeeze of tidal wetlands. Journal of Coastal Research 29:1049–61.

    Google Scholar 

  • Turner RE, Howes BL, Teal JM, Milan CS, Swenson EM, Goehringer-Toner DD. 2009. Salt marshes and eutrophication: an unsustainable outcome. Limnology and Oceanography 54:1634–42.

    CAS  Google Scholar 

  • Valiela I, Kinney E, Culberston J, Peacock E, Smith S. 2009. Global losses of mangroves and salt marshes. In: Duarte CM, Ed. Global loss of coastal habitats: rates, causes and consequences. Madrid: Fundación BBVA. p 107–38.

    Google Scholar 

  • Valiela I, Teal JM. 1979. The nitrogen budget of a salt marsh ecosystem. Nature 280:652–6.

    CAS  Google Scholar 

  • Valiela I, Teal JM, Persson NY. 1976. Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnology and Oceanography 21:245–52.

    Google Scholar 

  • Van Wijnen HJ, Bakker JP. 1999. Nitrogen and phosphorus limitation in a coastal barrier salt marsh: the implications for vegetation succession. Journal of Ecology 87:265–72.

    Google Scholar 

  • Walker NA, Henry HAL, Wilson DJ, Jefferies RL. 2003. The dynamics of nitrogen movement in an Arctic salt marsh in response to goose herbivory: a parameterized model with alternate stable states. Journal of Ecology 91:637–50.

    Google Scholar 

  • Weis JS, Segarra KEA, Bernal P. 2016. Chapter 49: salt marshes. In: Inis L, Simcock A, Eds. The first global integrated marine assessment: world ocean assessment I. Cambridge: Cambridge University Press/United Nations.

    Google Scholar 

  • Wood S. 2017. Generalized additive models: an introduction with R. Boca Raton: Chapman and Hall/CRC.

    Google Scholar 

  • Wong JXW, Van Colen C, Airoldi L. 2015. Nutrient levels modify saltmarsh responses to increased inundation in different soil types. Marine Environmental Research 104:37–46.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Robert Wilkes (Environmental Protection Agency) for retrieving tidal height data. Yana Bersunukayeva and Alanna Kirwan helped in the laboratory. Fionnuala O’Neill and Emmi Virkki assisted with fieldwork. We thank David Samuel Johnson and an anonymous reviewer whose comments helped improving the manuscript.

Funding

This study was funded by the Environmental Protection Agency, Ireland (EPA) as part of the SAMFHIRES Project (Saltmarsh Function and Human Impacts in Relation to Ecological Status; 2015-W-MS-19).

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  1. Department of Botany and Centre for the Environment, Trinity College Dublin, The University of Dublin, Dublin 2, Ireland

    Marcin R. Penk & Stephen Waldren

  2. Botanical, Environmental and Conservation Consultants, 43 Herbert Lane, Dublin 2, Ireland

    Philip M. Perrin

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  1. Marcin R. Penk
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Correspondence to Marcin R. Penk.

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MP, PP and SW conceived the ideas, MP and PP collected data, MP analysed data and lead writing, and all authors contributed substantially to the manuscript.

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Penk, M.R., Perrin, P.M. & Waldren, S. Above- to Belowground Vegetation Biomass Ratio in Temperate North-East Atlantic Saltmarshes Increases Strongly with Soil Nitrogen Gradient. Ecosystems 23, 648–661 (2020). https://doi.org/10.1007/s10021-019-00428-z

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