Abstract
Mangroves store large amounts of organic carbon (C) in their soils and are important in the global C cycle. These C stocks have been attributed to the below-ground productivity of mangroves, yet there is limited knowledge about the environmental factors that influence mangrove root growth. Thus, this study aimed to assess the role of variation in soil bulk density (BD) on the early development of mangroves. Seedlings of four mangrove species were grown in a pot-experiment in soils with a BD ranging from 0.2 to 1.2 g cm−3. Nine functional above- and below-ground plant traits were measured. Above- and below-ground traits of mangrove seedlings were influenced by variation in soil BD, but the effect was species specific. The reaction norms for most plant traits of Bruguiera gymnorrhiza and Rhizophora stylosa suggested a growth optimum at a specific soil BD (0.6 and 0.4 g cm−3, respectively), whilst the reaction norm of Avicennia marina was highly variable among traits, and Ceriops australis showed a very limited response. Moreover, A. marina was the most plastic species above-ground, while R. stylosa was the most plastic species below-ground. Ceriops australis was the least plastic species. Hence, soil BD is an environmental factor that influences mangrove root traits and seedling establishment, and may therefore affect mangrove species distributions and ecosystem C stocks.
Similar content being viewed by others
References
Adame, F.M., S. Cherian, R. Reef, and B. Stewart-Koster. 2017. Mangrove root biomass and the uncertainty of belowground carbon estimations. Forest Ecology and Management 403: 52–60.
Alameda, D., and R. Villar. 2009. Moderate soil compaction: Implications on growth and architecture in seedlings of 17 woody plant species. Soil and Tillage Research 103: 325–331.
Alameda, D., and R. Villar. 2012. Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environmental and Experimental Botany 79: 49–57.
Alongi, D.M. 2014. Carbon cycling and storage in mangrove forests. Annual Review of Marine Science 6: 195–219.
Alongi, D.M., F. Tirendi, and B.F. Clough. 2000. Below-ground decomposition of organic matter in forests of the mangroves Rhizophora stylosa and Avicennia marina along the arid coast of Western Australia. Aquatic Botany 68: 97–122.
Atwood, T.B., R.M. Connolly, H. Almahasheer, P.E. Carnell, C.D. Duarte, C.J. Ewers Lewis, X. Irigoien, J.J. Kelleway, P.S. Lavery, P.I. Macreadie, O. Serrano, C.J. Sanders, I. Santos, A.D.L. Steven, and C.E. Lovelock. 2017. Global patterns in mangrove soil carbon stocks and losses. Nature Climate Change 7: 523–529.
Ball, M.C. 1988. Ecophysiology of mangroves. Trees 2: 129–142.
Ball, M.C. 1998. Mangrove species richness in relation to salinity and waterlogging: a case study along the Adelaide River Floodplain, Northern Australia. Global Ecology and Biogeography Letters7: 73–82.
Begg, J.E., and N.C. Turner. 1970. Water potential gradients in field tobacco. Plant Physiology 46: 343–346.
Bell, D.L., and S.E. Sultan. 1999. Dynamic phenotypic plasticity for root growth in Polygonum: a comparative study. American Journal of Botany 86 (6): 807–819.
Bengough, A.G., B.M. McKenzie, P.D. Hallett, and T.A. Valentine. 2011. Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. Journal of Experimental Botany 62: 59–68.
Bingham, I.J., A.G. Bengough, and R.M. Rees. 2010. Soil compaction–N interactions in barley: Root growth and tissue composition. Soil & Tillage Research 106: 241–246.
Cambi, M., G. Certini, F. Neri, and E. Marchi. 2015. The impact of heavy traffic on forest soils: A review. Forest Ecology and Management 338: 124–138.
Coleman, J.S., K.D.M. McConnaughay, and D.D. Ackerly. 1994. Interpreting phenotypic variation in plants. Tree 9: 187–191.
Day, S.D., and N.L. Bassuk. 1994. A review of the effects of soil compaction and amelioration techniques on landscape trees. Journal of Arboriculture 20: 9–17.
Donato, D.C., J.B. Kauffman, D. Murdiuarso, S. Kurnianto, M. Stidham, and M. Kanninen. 2011. Mangroves among the most carbon-rich forests in the tropics. Nature Geoscience 4: 293–297.
Duarte, C.M., J.J. Middelburg, and N. Caraco. 2005. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2: 1–8.
Duke, N.C., M.C. Ball, and J.C. Ellison. 1998. Factors influencing biodiversity and distributional gradients in mangroves. Global Ecology and Biogeography Letters 7: 27–47.
Federer, C.A., D.E. Turcotte, and C.T. Smith (1993). The organic fraction–bulk density relationship and the expression of nutrient content in forest soils. Canadian Journal of Forest Research 23: 1026–1032.
Froehlich, H.A., D.W.R. Miles, and R.W. Robbins. 1986. Growth of young Pinus ponderosa and Pinus contorta on compacted soil in central Washington. Forest Ecology Management 15: 285–294.
Fujimoto, K., A. Imaya, R. Tabuchi, S. Kuramoto, H. Utsugi, and T. Murofushi. 1999. Belowground carbon storage of Micronesian mangrove forests. Ecological Research 14: 409–413.
Genthner, F.J., M.A. Lewis, J.A. Nestlerode, C.M. Elonen, C.A. Chancy, A. Teague, M.C. Harwell, M.F. Moffett, and B.H. Hill. 2013. Relationships among habitat quality and measured condition variables in Gulf of Mexico mangroves. Wetlands Ecology and Management 21: 173–191.
Gill, A.M., and P.B. Tomlinson. 1977. Studies of the growth of Red Mangrove (Rhizophora mangle L.) 4. The adult root system. Biotropica 9: 145–155.
Giri, C., E. Ochieng, L.L. Tieszen, Z. Zhu, A. Singh, T. Loveland, J. Masek, and N. Duke. 2011. Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography 20: 154–159.
Godefroid, S., and N. Koedam. 2004. Interspecific variation in soil compaction sensitivity among forest floor species. Biological Conservation 119: 207–217.
Greacen, E.L., and R. Sands. 1980. Compaction of forest soils. A review. Australian Journal of Soil Research 18: 163–189.
Hayes, M.A., A. Jesse, B. Tabet, R. Reef, J.A. Keuskamp, and C.E. Lovelock. 2017. The contrasting effects of nutrient enrichment on growth, biomass allocation and decomposition of plant tissue in coastal wetlands. Plant and Soil 416: 193–204.
He, B., T. Lai, H. Fan, W. Wang, and H. Zheng. 2007. Comparison of flooding-tolerance in four mangrove species in a diurnal tidal zone in the Beibu Gulf. Estuarine, Coastal and Shelf Science 74: 254–262.
Hodge, A. 2006. Plastic plants and patchy soils. Journal of Experimental Botany 57: 401411.
Hummel, I., D. Vile, C. Violle, J. Devaux, B. Ricci, A. Blanchard, É. Garnier, and C. Roumet (2007). Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species. New Phytologist 173: 313–321.
Huxham, M., J. Langat, F. Tamooh, H. Kennedy, M. Mencuccini, M.W. Skov, and J. Kairo. 2010. Decomposition of mangrove roots: effects of location, nutrients, species identity and mix in a Kenyan forest. Estuarine. Coastal and Shelf Science 88: 135–142.
Jordan, D., F. Ponder Jr., and V.C. Hubbard. 2003. Effects of soil compaction, forest leaf litter and nitrogen fertilizer on two oak species and microbial activity. Applied Soil Ecology 23: 33–41.
Kaly, U.L., G. Eugelink, and A.I. Robertson. 1997. Soil conditions in damaged North Queensland mangroves. Estuaries 20: 291–300.
Keller, T., and I. Håkansson. 2010. Estimation of reference bulk density from soil particle size distribution and soil organic matter content. Geoderma 154: 398–406.
Klepper, B. 1968. Diurnal pattern of water potential in woody plants. Plant Physiology 43 (12): 1931–1934.
Kloke, J.D., and J.W. McKean. 2012. Rfit: rank-based estimation for linear models. The R Journal 4: 57–65.
Komiyama, A., J.E. Ong, and S. Poungparn. 2008. Allometry, biomass, and productivity of mangrove forests: A review. Aquatic Botany 89: 128–137.
Krauss, K.W., T.W. Doyle, R.R. Twilley, V.H. Rivera-Monroy, and J.K. Sullivan. 2006. Evaluating the relative contributions of hydroperiod and soil fertility on growth of south Florida mangroves. Hydrobiologia 569: 311–324.
Lawton, J.R., A. Todd, and D.K. Naidoo. 1981. Preliminary investigations into the structure of the roots of the mangroves Avicennia marina and Bruguiera gymnorrhiza in relation to ion uptake. New Phytologist 88: 713–722.
Leopold, A., C. Marchand, J. Deborde, C. Chaduteau, and M. Allenbach. 2013. Influence of mangrove zonation on CO2 fluxes at the sediment–air interface (New Caledonia). Geoderma 202: 62–70.
López-Hoffman, L., N.P.R. Anten, M. Martinez-Ramos, and D.D. Ackerly. 2007. Salinity and light interactively affect neotropical mangrove seedlings at the leaf and whole plant levels. Oecologia 150: 545–556.
Lovelock, C.E., and I.C. Feller. 2003. Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest. Oecologia 134 (4): 455–462.
Lovelock, C.E., M.C. Ball, I.C. Feller, B.M.J. Engelbrecht, and M.L. Ewe. 2006. Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorus availability. Physiologia Plantarum 127: 457–464.
Lovelock, C.E., I.C. Feller, M.C. Ball, J. Ellis, and B. Sorrell. 2007. Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients. Ecology Letters 10: 1154–1163.
Masle, J., and J. Passioura. 1987. The effect of soil strength on the growth of young wheat plants. Australian Journal of Plant Physiology 14: 643–656.
Materechera, S.A., A.R. Dexter, and A.M. Alston. 1991. Penetration of very strong soils by seedling roots of different plant species. Plant and Soil 135: 31–41.
McKee, K.L. 1993. Soil physicochemical patterns and mangrove species distribution -- reciprocal effects? Journal of Ecology 81: 477–487.
McKee, K.L. 1996. Growth and physiological responses of neotropical mangrove seedlings to root zone hypoxia. Tree Physiology 16 (11_12): 883–889.
McKee, K.L., and P.L. Faulkner. 2000. Restoration of biogeochemical function in mangrove forests. Restoration Ecology 8: 247–259.
McKee, K.L., D.R. Cahoon, and I.C. Feller. 2007. Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation. Global Ecology and Biogeography 16: 545–556.
Mcleod, E., G.L. Chmura, S. Bouillon, R. Salm, M. Bjork, C.M. Duarte, C.E. Lovelock, W.H. Schlesinger, and B. Silliman. 2011. A blueprint for blue carbon: towards an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Frontiers in Ecology and the Environment 9: 552–560.
Middleton, B.A., and K.L. McKee. 2001. Degradation of mangrove tissues and implications for peat formation in Belizean island forests. Journal of Ecology 89: 818–828.
Morris, J.T., D.C. Barber, J.C. Callaway, R. Chambers, S.C. Hagen, C.S. Hopkinson, B.J. Johnson, P. Megonigal, S.C. Neubauer, T. Troxler, and C. Wigand. 2016. Contributions of organic and inorganic matter to sediment volume and accretion in tidal wetlands at steady state. Earth's Future 4: 110–121.
Naidoo, G. 1985. Effects of waterlogging and salinity on plant-water relations and on the accumulation of solutes in three mangrove species. Aquatic Botany 22: 133–143.
Ola, A., I.C. Dodd, and J.N. Quinton. 2015. Can we manipulate root system architecture to control soil erosion? Soil 1: 603–612.
Ola, A., S. Schmidt, and C.E. Lovelock. 2018. The effect of soil bulk density on root growth of field-grown mangrove species. Plant and Soil 432: 91–105.
Omi, S.K. 1985. Soil compaction: effects on seedling growth. In Research paper M-125, USDA Forestry Service, GTR Res. Ft. Collins: Colorado State University.
Pfeiffer, J., M. Faget, A. Walter, S. Blossfeld, F. Fiorani, U. Schurr, and K.A. Nagel. 2014. Spring barley shows dynamic compensatory root and shoot growth responses when exposed to localised soil compaction and fertilisation. Functional Plant Biology 41: 581–597.
Pi, N., N.F.Y. Tam, Y. Wu, and M.H. Wong. 2009. Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquatic Botany 90: 222–230.
Poungparn, S., T. Charoenphonphakdi, T. Sangtiean, and P. Patanaponpaiboon. 2015. Fine root production in three zones of secondary mangrove forest in eastern Thailand. Trees 30: 467–474.
Reef, R., K. Winter, J. Morales, M.F. Adame, D.L. Reef, and C.E. Lovelock. 2015. The effect of atmospheric carbon dioxide concentrations on the performance of the mangrove Avicennia germinans over a range of salinities. Physiologia Plantarum 154 (3): 358–368.
Robertson, A.I., and D.M. Alongi. 2016. Massive turnover rates of fine root detrital carbon in tropical Australian mangroves. Oecologia 180: 841–851.
Suárez, N., M.A. Sobrado, and E. Medina. 1998. Salinity effects on the leaf water relations components and ion accumulation patterns in Avicennia geminans (L.) L. seedlings. Oecologia 114: 299–304.
Valladares, F., S.J. Wright, E. Lasso, K. Kitajima, and R.W. Pearcy. 2000. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81: 1925–1936.
Valladares, F., D. Sanchez-Gomez, and M.A. Zavala. 2006. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology 94: 1103–1116.
Valladares, F., E. Gianoli, and J.M. Gómez. 2007. Ecological limits to plant phenotypic plasticity. New Phytologist 176: 749–763.
Warnaars, B.C., and B.W. Eavis (1972). Soil physical conditions affecting seedling root growth, II. Mechanical impedance, aeration and moisture availability, as influenced by grain-size distribution and moisture content in silica sands. Plant and Soil 36:623–634.
Whalley, W.R., E. Dumitru, and A.R. Dexter. 1995. Biological effects of soil compaction. Soil and Tillage Research 35: 53–68.
Acknowledgements
Thanks to Amy Watson and Vicki Bennion for watering the experimental plants.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by John C. Callaway
Electronic supplementary material
ESM 1
(DOCX 16 kb)
Rights and permissions
About this article
Cite this article
Ola, A., Staples, T.L., Robinson, N. et al. Plasticity in the Above- and Below-Ground Development of Mangrove Seedlings in Response to Variation in Soil Bulk Density. Estuaries and Coasts 43, 111–119 (2020). https://doi.org/10.1007/s12237-019-00660-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-019-00660-9