Skip to main content

Advertisement

Log in

Geographic Linkages of Root Traits to Salt Marsh Productivity

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Root traits are fundamental characteristics of belowground ecosystems that regulate plant growth and drive ecosystem functioning. Nevertheless, the way root traits respond to environmental factors and consequently influence productivity remains unexplored on large geographic scales. We examined the root traits of exotic Spartina alterniflora and native Phragmites australis across China’s coastal salt marshes. Using structural equation models (SEMs), we quantified the direct and indirect effects of mean annual temperature, soil nutrients (e.g., soil dissolved inorganic nitrogen and phosphorus), and root traits on aboveground net primary productivity. Our results showed that root traits of S. alterniflora were more sensitive to changing soil nutrient availability than those of P. australis. The SEMs indicated that soil nutrient availability increased S. alterniflora productivity by increasing root nitrogen concentration and root length density. In P. australis, temperature could increase productivity by both increasing root length density and soil nutrient-mediated root nitrogen concentration. The studied root architectural trait (root length density) and nutrient trait (root nitrogen concentration) were effective in predicting productivity, whereas none of the root morphological traits (i.e., specific root length, root tissue density, and root diameter) significantly affected productivity. We provide the first empirical evidence that root trait-based responses modulate the effects of climate and soil nutrients on geographic variation in vegetation productivity, but these effects are species specific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • Abalos D, van Groenigen JW, De Deyn GB. 2018. What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands? Global Change Biology 24:e248–58.

    Article  PubMed  Google Scholar 

  • Agapit C, Gigon A, Puga-Freitas R, Zeller B, Blouin M. 2017. Plant-earthworm interactions: influence of age and proportion of casts in the soil on plant growth, morphology and nitrogen uptake. Plant and Soil 424:49–61.

    Article  CAS  Google Scholar 

  • Alber M, O’Connell JL. 2019. Elevation drives gradients in surface soil temperature within salt marshes. Geophysical Research Letters 46:5313–22.

    Article  Google Scholar 

  • Bardgett RD, Mommer L, De Vries FT. 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology and Evolution 29:692–9.

    Article  PubMed  Google Scholar 

  • Bassirirad H. 2000. Kinetics of nutrient uptake by roots: responses to global change. New Phytologist 147:155–69.

    Article  CAS  Google Scholar 

  • Bergmann J, Weigelt A, van der Plas F, Laughlin DC, Kuyper TW, Guerrero-Ramirez N, Valverde-Barrantes OJ, Bruelheide H, Freschet GT, Iversen CM, Kattge J, McCormack ML, Meier IC, Rillig MC, Roumet C, Semchenko M, Sweeney CJ, van Ruijven J, York LM, Mommer L. 2020. The fungal collaboration gradient dominates the root economics space in plants. Science Advances 6:eaba3756.

    Article  CAS  PubMed  PubMed Central  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.

    Article  PubMed  Google Scholar 

  • Berzaghi F, Wright IJ, Kramer K, Oddou-Muratorio S, Bohn FJ, Reyer CPO, Sabate S, Sanders TGM, Hartig F. 2020. Towards a new generation of trait-flexible vegetation models. Trends in Ecology and Evolution 35:191–205.

    Article  PubMed  Google Scholar 

  • Carboni M, Calderon-Sanou I, Pollock L, Violle C, Thuiller W. 2018. Functional traits modulate the response of alien plants along abiotic and biotic gradients. Global Ecology and Biogeography 27:1173–85.

    Article  Google Scholar 

  • Carey JC, Kroeger KD, Zafari B, Tang J. 2018. Passive experimental warming decouples air and sediment temperatures in a salt marsh. Limnology and Oceanography: Methods 16:640–8.

    Google Scholar 

  • Chen H, Zou J, Cui J, Nie M, Fang C. 2018. Wetland drying increases the temperature sensitivity of soil respiration. Soil Biology and Biochemistry 120:24–7.

    Article  CAS  Google Scholar 

  • Cheng J, Chu P, Chen D, Bai Y, Niu S. 2016. Functional correlations between specific leaf area and specific root length along a regional environmental gradient in Inner Mongolia grasslands. Functional Ecology 30:985–97.

    Article  Google Scholar 

  • Clark MD, Gilmour JT. 1983. The effect of temperature on decomposition at optimum and saturated soil water contents. Soil Science Society of America Journal 47:927–9.

    Article  CAS  Google Scholar 

  • Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA. 2013. Root traits contributing to plant productivity under drought. Frontiers in Plant Science 4:442.

    Article  PubMed  PubMed Central  Google Scholar 

  • Crosby SC, Angermeyer A, Adler JM, Bertness MD, Deegan LA, Sibinga N, Leslie HM. 2016. Spartina alterniflora biomass allocation and temperature: implications for salt marsh persistence with sea-level rise. Estuaries and Coasts 40:213–23.

    Article  CAS  Google Scholar 

  • Darby FA, Turner RE. 2008. Effects of eutrophication on salt marsh root and rhizome biomass accumulation. Marine Ecology Progress Series 363:63–70.

    Article  Google Scholar 

  • Davidson AM, Jennions M, Nicotra AB. 2011. Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecology Letters 14:419–31.

    Article  PubMed  Google Scholar 

  • De Deyn GB, Cornelissen JH, Bardgett RD. 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters 11:516–31.

    Article  PubMed  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.

    Article  CAS  PubMed  Google Scholar 

  • Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL. 2000. Building roots in a changing environment: implications for root longevity. New Phytologist 147:33–42.

    Article  CAS  Google Scholar 

  • Erktan A, McCormack ML, Roumet C. 2018. Frontiers in root ecology: recent advances and future challenges. Plant and Soil 424:1–9.

    Article  CAS  Google Scholar 

  • Finegan B, Peña-Claros M, de Oliveira A, Ascarrunz N, Bret-Harte MS, Carreño-Rocabado G, Casanoves F, Díaz S, Eguiguren Velepucha P, Fernandez F, Licona JC, Lorenzo L, Salgado Negret B, Vaz M, Poorter L, Canham C. 2015. Does functional trait diversity predict above-ground biomass and productivity of tropical forests? Testing three alternative hypotheses. Journal of Ecology 103:191–201.

    Article  Google Scholar 

  • Fransen B, de Kroon H, Berendse F. 1998. Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115:351–8.

    Article  PubMed  Google Scholar 

  • Freschet GT, Roumet C, Treseder K. 2017. Sampling roots to capture plant and soil functions. Functional Ecology 31:1506–18.

    Article  Google Scholar 

  • Gedan KB, Bertness MD. 2010. How will warming affect the salt marsh foundation species Spartina patens and its ecological role? Oecologia 164:479–87.

    Article  PubMed  Google Scholar 

  • Ghimire B, Riley WJ, Koven CD, Mu M, Randerson JT. 2016. Representing leaf and root physiological traits in CLM improves global carbon and nitrogen cycling predictions. Journal of Advances in Modeling Earth Systems 8:598–613.

    Article  Google Scholar 

  • Giurgevich J, Dunn E. 1979. Seasonal patterns of CO2 and water vapor exchange of the tall and short height forms of Spartina alterniflora Loisel in a Georgia salt marsh. Oecologia 43:139–56.

    Article  CAS  PubMed  Google Scholar 

  • Giurgevich JR, Dunn EL. 1981. A comparative analysis of the CO2 and water vapor responses of two Spartina species from Georgia coastal marshes. Estuarine, Coastal and Shelf Science 12:561–8.

    Article  Google Scholar 

  • Gustafsson C, Norkko A. 2018. Quantifying the importance of functional traits for primary production in aquatic plant communities. Journal of Ecology 107:154–66.

    Article  Google Scholar 

  • He N, Liu C, Tian M, Li M, Yang H, Yu G, Guo D, Smith MD, Yu Q, Hou J. 2017. Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions. Functional Ecology 32:10–19.

    Article  Google Scholar 

  • Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162:9–24.

    Article  Google Scholar 

  • Huang J, Xu X, Wang M, Nie M, Qiu S, Wang Q, Quan Z, Xiao M, Li B. 2016. Responses of soil nitrogen fixation to Spartina alterniflora invasion and nitrogen addition in a Chinese salt marsh. Scientific reports 6:20384.

    Article  CAS  PubMed  PubMed Central  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, USA 110:11911–16.

    Article  CAS  Google Scholar 

  • Jackson ML. 1958. Soil chemical analysis. Englewood Cliffs: Prentice Hall.

    Google Scholar 

  • Kapulnik Y, Okon Y, Henis Y. 1987. Yield response of spring wheat cultivars (Triticum aestivum and T. turgidum) to inoculation with Azospirillum brasilense under field conditions. Biology and Fertility of Soils 4:27–35.

    Google Scholar 

  • Kirwan ML, Guntenspergen GR, Morris JT. 2009. Latitudinal trends in Spartina alterniflora productivity and the response of coastal marshes to global change. Global Change Biology 15:1982–9.

    Article  Google Scholar 

  • Kong D, Wang J, Wu H, Valverde-Barrantes OJ, Wang R, Zeng H, Kardol P, Zhang H, Feng Y. 2019. Nonlinearity of root trait relationships and the root economics spectrum. Nature Communications 10:2203.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC, Mommer L. 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology 104:1299–310.

    Article  Google Scholar 

  • Kramer-Walter KR, Laughlin DC. 2017. Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant and Soil 416:539–50.

    Article  CAS  Google Scholar 

  • Laliberte E. 2017. Below-ground frontiers in trait-based plant ecology. New Phytologist 213:1597–603.

    Article  PubMed  Google Scholar 

  • Lefcheck JS, Freckleton R. 2016. piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution 7:573–9.

    Article  Google Scholar 

  • Liu C, Xiang W, Lei P, Deng X, Tian D, Fang X, Peng C. 2013. Standing fine root mass and production in four Chinese subtropical forests along a succession and species diversity gradient. Plant and Soil 376:445–59.

    Article  CAS  Google Scholar 

  • Liu W, Chen X, Strong DR, Pennings SC, Kirwan ML, Chen X, Zhang Y. 2020. Climate and geographic adaptation drive latitudinal clines in biomass of a widespread saltmarsh plant in its native and introduced ranges. Limnology and Oceanography 65:1399–409.

    Article  Google Scholar 

  • Lohbeck M, Poorter L, Martínez-Ramos M, Bongers F. 2015. Biomass is the main driver of changes in ecosystem process rates during tropical forest succession. Ecology 96:1242–52.

    Article  PubMed  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M. 2015. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytologist 207:505–18.

    Article  PubMed  Google Scholar 

  • Mendelssohn IA, Morris JT. 2000. Eco-physiological controls on the productivity of Spartina alterniflora Loisel. In: Kreeger DA, Weinstein MP, Eds. Concepts and controversies in tidal marsh ecology. Dordrecht: Springer. p 59–80.

    Google Scholar 

  • Moore GE, Burdick DM, Peter CR, Keirstead DR. 2012. Belowground biomass of Phragmites australis in coastal marshes. Northeastern Naturalist 19:611–26.

    Article  Google Scholar 

  • Morris JT, Bowden WB. 1986. A mechanistic, numerical model of sedimentation, mineralization, and decomposition for marsh sediments. Soil Science Society of America Journal 50:96–105.

    Article  CAS  Google Scholar 

  • Morris JT, Dacey JWH. 1984. Effects of O2 on ammonium uptake and root respiration by Spartina alterniflora. American Journal of Botany 71:979–85.

    Article  CAS  Google Scholar 

  • Myers-Smith IH, Hik DS. 2013. Shrub canopies influence soil temperatures but not nutrient dynamics: an experimental test of tundra snow-shrub interactions. Ecology and Evolution 3:3683–700.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nie M, Lu M, Bell J, Raut S, Pendall E. 2013. Altered root traits due to elevated CO2: a meta-analysis. Global Ecology and Biogeography 22:1095–105.

    Article  Google Scholar 

  • Niu S, Classen AT, Luo Y. 2018. Functional traits along a transect. Functional Ecology 32:4–9.

    Article  Google Scholar 

  • Olsen SR, Sommers LE. 1982. Phosphorus. In: Page AL, Miller RH, Keeney DR, Eds. Methods of soil analysis, Part 2, Chemical and microbial properties. Madison: Agronomy Society of American. p 403–30.

    Google Scholar 

  • Ostonen I, Helmisaari H-S, Borken W, Tedersoo L, Kukumägi M, Bahram M, Lindroos A-J, Nöjd P, Uri V, Merilä P, Asi E, Lõhmus K. 2011. Fine root foraging strategies in Norway spruce forests across a European climate gradient. Global Change Biology 17:3620–32.

    Article  Google Scholar 

  • Piccolo MC, Perillo GME, Daborn GR. 1993. Soil temperature variations on a tidal flat in Minas Basin, Bay of Fundy, Canada. Estuarine, Coastal and Shelf Science 36:345–57.

    Article  Google Scholar 

  • Qiu S, Xu X, Liu S, Liu W, Liu J, Nie M, Shi F, Zhang Y, Weiner J, Li B. 2018. Latitudinal pattern of flowering synchrony in an invasive wind-pollinated plant. Proceedings of the Royal Society B: Biological Sciences 285:20181072.

    Article  PubMed  PubMed Central  Google Scholar 

  • Quemada M, Cabrera ML. 1997. Temperature and moisture effects on C and N mineralization from surface applied clover residue. Plant and Soil 189:127–37.

    Article  CAS  Google Scholar 

  • Reich PB. 2014. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102:275–301.

    Article  Google Scholar 

  • Reichstein M, Bahn M, Mahecha MD, Kattge J, Baldocchi DD. 2014. Linking plant and ecosystem functional biogeography. Proceedings of the National Academy of Sciences, USA 111:13697–702.

    Article  CAS  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M. 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9:981–93.

    Article  PubMed  Google Scholar 

  • Scheiter S, Langan L, Higgins SI. 2013. Next-generation dynamic global vegetation models: learning from community ecology. New Phytologist 198:957–69.

    Article  PubMed  Google Scholar 

  • Seybold CA, Mersie W, Huang JY, McNamee C. 2002. Soil redox, pH, temperature, and water-table patterns of a freshwater tidal wetland. Wetlands 22:149–58.

    Article  Google Scholar 

  • Shipley B, De Bello F, Cornelissen JH, Laliberte E, Laughlin DC, Reich PB. 2016. Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180:923–31.

    Article  PubMed  Google Scholar 

  • Šímová I, Sandel B, Enquist BJ, Michaletz ST, Kattge J, Violle C, McGill BJ, Blonder B, Engemann K, Peet RK, Wiser SK, Morueta-Holme N, Boyle B, Kraft NJB, Svenning J-C. 2019. The relationship of woody plant size and leaf nutrient content to large-scale productivity for forests across the Americas. Journal of Ecology 107:2278–90.

    Article  CAS  Google Scholar 

  • Smith VH. 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research 10:126–39.

    Article  CAS  PubMed  Google Scholar 

  • Suding KN, Lavorel S, Chapin FS, Cornelissen JHC, DÍAz S, Garnier E, Goldberg D, Hooper DU, Jackson ST, Navas ML. 2008. Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Global Change Biology 14:1125–40.

    Article  Google Scholar 

  • Tang Z, Xu W, Zhou G, Bai Y, Li J, Tang X, Chen D, Liu Q, Ma W, Xiong G, He H, He N, Guo Y, Guo Q, Zhu J, Han W, Hu H, Fang J, Xie Z. 2018. Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems. Proceedings of the National Academy of Sciences, USA 115:4033–8.

    Article  Google Scholar 

  • Valverde-Barrantes OJ, Blackwood CB, Austin A. 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum: commentary on Kramer-Walter et al. (2016). Journal of Ecology 104:1311–13.

    Article  Google Scholar 

  • Violle C, Reich PB, Pacala SW, Enquist BJ, Kattge J. 2014. The emergence and promise of functional biogeography. Proceedings of the National Academy of Sciences, USA 111:13690–6.

    Article  CAS  Google Scholar 

  • Wang R, Wang Q, Liu C, Kou L, Zhao N, Xu Z, Zhang S, Yu G, He N. 2018a. Changes in trait and phylogenetic diversity of leaves and absorptive roots from tropical to boreal forests. Plant and Soil 432:389–401.

    Article  CAS  Google Scholar 

  • Wang R, Wang Q, Zhao N, Xu Z, Zhu X, Jiao C, Yu G, He N, Niu S. 2018b. Different phylogenetic and environmental controls of first-order root morphological and nutrient traits: evidence of multidimensional root traits. Functional Ecology 32:29–39.

    Article  Google Scholar 

  • Wang R, Yu G, He N, Wang Q, Zhao N, Xu Z, Ge J. 2015. Latitudinal variation of leaf stomatal traits from species to community level in forests: linkage with ecosystem productivity. Scientific Reports 5:14454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weatherburn MW. 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39:971–4.

    Article  CAS  Google Scholar 

  • Weemstra M, Mommer L, Visser EJ, van Ruijven J, Kuyper TW, Mohren GM, Sterck FJ. 2016. Towards a multidimensional root trait framework: a tree root review. New Phytologist 211:1159–69.

    Article  CAS  PubMed  Google Scholar 

  • Wieder WR, Cleveland CC, Smith WK, Todd-Brown K. 2015. Future productivity and carbon storage limited by terrestrial nutrient availability. Nature Geoscience 8:441.

    Article  CAS  Google Scholar 

  • Więski K, Pennings SC. 2013. Climate drivers of Spartina alterniflora saltmarsh production in Georgia, USA. Ecosystems 17:473–84.

    Article  CAS  Google Scholar 

  • Xu X, Liu H, Liu Y, Zhou C, Pan L, Fang C, Nie M, Li B. 2020. Human eutrophication drives biogeographic salt marsh productivity patterns in China. Ecological Applications 30:e02045.

    Article  PubMed  Google Scholar 

  • Zadworny M, McCormack ML, Mucha J, Reich PB, Oleksyn J. 2016a. Scots pine fine roots adjust along a 2000-km latitudinal climatic gradient. New Phytologist 212:389–99.

    Article  PubMed  Google Scholar 

  • Zadworny M, McCormack ML, Zytkowiak R, Karolewski P, Mucha J, Oleksyn J. 2016b. Patterns of structural and defense investments in fine roots of Scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe. Global Change Biology 23:1218–31.

    Article  PubMed  Google Scholar 

  • Zhang Y, Pennings SC, Li B, Wu J. 2019. Biotic homogenization of wetland nematode communities by exotic Spartina alterniflora in China. Ecology 100:e02596.

    PubMed  Google Scholar 

  • Zhao H, Yang W, Xia L, Qiao Y, Xiao Y, Cheng X, An S. 2015. Nitrogen-enriched eutrophication promotes the invasion of Spartina alterniflora in coastal China. CLEAN - Soil, Air, Water 43:244–50.

    Article  CAS  Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. New York: Springer Science and Business Media.

    Book  Google Scholar 

Download references

Acknowledgements

We thank Yuanzhan Liu, Bingkui Huang, Junyu Zou, Lianghao Pan, Songshuo Li, and Yan Zhang for help in the field sampling and laboratory measurements. We also thank Dana M Blumenthal for his insightful comments.

Funding

This work was funded by the National Key Research and Development Program of China (2018YFC1406402), the National Natural Science Foundation of China (91951112, 41630528, and 31670491), and the Institute of Eco-Chongming (ECNU-IEC-202001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ming Nie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Author Contributions

HL, XX, and MN conceived the study; HL and XX performed the research with assistance from CZ and JZ; HL analyzed the data with advice from XX; and HL wrote the paper with important input from all other authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 495 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Xu, X., Zhou, C. et al. Geographic Linkages of Root Traits to Salt Marsh Productivity. Ecosystems 24, 726–737 (2021). https://doi.org/10.1007/s10021-020-00546-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-020-00546-z

Keywords

Navigation