Skip to main content

Advertisement

SpringerLink
Log in

The effect of heterogeneous soil bulk density on root growth of field-grown mangrove species

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Mangroves harbour large organic carbon (C) reservoirs in their soils that are important in the global C cycle. The below-ground biomass of mangrove trees is a major contributor to these organic C stocks. Root system development tends to be highly plastic in response to environmental conditions such as soil bulk density (BD). Hence, this study aimed to assess the role of soil BD on mangrove root growth.

Methods

Root in-growth bags filled with root-free soil ranging in BD from 0.2 to 1.2 g cm−3 were buried in the soil of three mangrove species.

Results

Root image analysis indicated that BD had a significant positive effect on root length and root biomass suggesting trees increase biomass allocation to roots and enhance root elongation, possibly to increase the acquisition of water and nutrients in dense soils. However, the responses to variation in BD were species-specific which was attributed to differences in species growth rates and the background soil conditions.

Conclusion

Soil BD affects mangrove root growth with dense patches likely to have increased root growth and organic C sequestration potential compared to less dense soil patches.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adame FM, Cherian S, Reef R, Stewart-Koster B (2017) Mangrove root biomass and the uncertainty of belowground carbon estimations. For Ecol Manag 403:52–60

    Article  Google Scholar 

  • Alameda D, Villar R (2009) Moderate soil compaction: implications on growth and architecture in seedlings of 17 woody plant species. Soil Tillage Res 103:325–331

    Article  Google Scholar 

  • Alameda D, Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environ Exp Bot 79:49–57

    Article  Google Scholar 

  • Albright LJ (1976) In situ degradation of mangrove tissues (note). N Z J Mar Freshw Res 10:385–389

    Article  Google Scholar 

  • Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219

    Article  Google Scholar 

  • Amato M, Ritchie JT (2002) Spatial distribution and water uptake of maize (Zea mays L.) as affected by soil structure. Crop Sci 42:773–780

    Article  Google Scholar 

  • Are D, Kemp GP, Dalla Giustina F, Day JW, Scarton F (2002) A portable, electrically-driven Dutch cone penetrometer for geotechnical measurements in soft estuarine sediments. J Coast Res 18:372–378

    Google Scholar 

  • Atwell BJ (1993) Response of roots to mechanical impedance. Environ Exp Bot 33:27–40

    Article  Google Scholar 

  • Atwood TB, Connolly RM, Almahasheer H, Carnell PE, Duarte CD, Ewers Lewis CJ, Irigoien X, Kelleway JJ, Lavery PS, Macreadie PI, Serrano O, Sanders CJ, Santos I, Steven ADL, Lovelock CE (2017) Global patterns in mangrove soil carbon stocks and losses. Nat Clim Chang 7:523–529

    Article  CAS  Google Scholar 

  • Ball MC (1988) Ecophysiology of mangroves. Trees 2:129–142

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. https://doi.org/10.18637/jss.v067.i01

  • Bauma TJ, Nielsen KL, Koutstaal B (2000) Sample preparation and scanning protocol for computerised analysis of root length and diameter. Plant Soil 218:185–196

    Article  Google Scholar 

  • Bécel C, Vercambre G, Pagès L (2012) Soil penetration resistance, a suitable soil property to account for variations in root elongation and branching. Plant Soil 353:169–180

    Article  Google Scholar 

  • Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68

    Article  CAS  Google Scholar 

  • Bingham IJ, Bengough AG (2003) Morphological plasticity of wheat and barley roots in response to spatial variation in soil strength. Plant Soil 250:273–282

    Article  CAS  Google Scholar 

  • Bingham IJ, Bengough AG, Rees RM (2010) Soil compaction–N interactions in barley: Root growth and tissue composition. Soil Tillage Res 106:241–246

    Article  Google Scholar 

  • Bouillon S, Connolly RM, Lee SY (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. J Sea Res 59:44–58

    Article  CAS  Google Scholar 

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

  • Bushamuka VN, Zobel RW (1998) Differential genotypic and root type penetration of compacted soil layers. Crop Sci 38:776–781

    Article  Google Scholar 

  • Calvo-Polanco M, Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, Martínez Andújar C, Albacete A, Ruiz-Lozano JM (2016) Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ Exp Bot 131:47–57

    Article  CAS  Google Scholar 

  • Cambi M, Certini G, Neri F, Marchi E (2015) The impact of heavy traffic on forest soils: a review. For Ecol Manag 338:124–138

    Article  Google Scholar 

  • Castañeda-Moya E, Twilley RR, Rivera-Monroy V, Marx BD, Coronado-Molina C, Ewe SML (2011) Patterns of root dynamics in mangrove forests along environmental gradients in the Florida Coastal Everglades, USA. Ecosystems 14:1178–1195

    Article  Google Scholar 

  • Chen R, Twilley RR (1999) A simulation model of organic matter and nutrient accumulation in mangrove wetland soils. Biogeochemistry 44:93–118

    Google Scholar 

  • Cubera E, Moreno G, Solla A (2009) Quercus ilex root growth in response to heterogeneous conditions of soil bulk density and soil NH4-N content. Soil Tillage Res 103:16–22

    Article  Google Scholar 

  • Day SD, Bassuk NL (1994) A review of the effects of soil compaction and amelioration techniques on landscape trees. J Arboric 20:9–17

    Google Scholar 

  • Day SD, Seiler JR, Persaud N (2000) A comparison of root growth dynamics of silver maple and flowering dogwood in compacted soil at differing soil water contents. Tree Physiol 20:257–263

    Article  Google Scholar 

  • De Baets S, Poesen J, Gyssels G, Knapen A (2006) Effects of grass roots on the erodibility of topsoil during concentrated flow. Geomorphology 76:54–67

    Article  Google Scholar 

  • De Kroon H, Visser EJW, Huber H, Mommer L, Hutchings MJ (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ 32:704–712

    Article  Google Scholar 

  • Donato DC, Kauffman JB, Murdiuarso 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 

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

    Article  Google Scholar 

  • Federer CA, Turcotte DE, Smith CT (1993) The organic fraction–bulk density relationship and the expression of nutrient content in forest soils. Can J For Res 23:1026–1032

    Article  CAS  Google Scholar 

  • Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224

    Article  CAS  Google Scholar 

  • Froehlich HA, Miles DWR, Robbins RW (1986) Growth of young Pinus ponderosa and Pinus contorta on compacted soil in central Washington. Forest Ecology Management 15:285–294

    Article  Google Scholar 

  • Fujimoto K, Imaya A, Tabuchi R, Kuramoto S, Utsugi H, Murofushi T (1999) Belowground carbon storage of Micronesian mangrove forests. Ecol Res 14:409–413

    Article  Google Scholar 

  • Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2011) Status and distribution of mangrove forests of the world using earth observation satellite data. Glob Ecol Biogeogr 20:154–159

    Article  Google Scholar 

  • Gill AM, Tomlinson PB (1977) Studies of the growth of Red Mangrove (Rhizophora mangle L.) 4. The adult root system. Biotropica 9:145–155

    Article  Google Scholar 

  • Gleason SM, Ewel KC (2002) Organic matter dynamics on the forest floor of a Micronesian mangrove forest: an investigation of species composition shifts. Biotropica 43:190–198

    Article  Google Scholar 

  • Godefroid S, Koedam N (2004) Interspecific variation in soil compaction sensitivity among forest floor species. Biol Conserv 119:207–217

    Article  Google Scholar 

  • Greacen EL, Sands R (1980) Compaction of forest soils: a review. Aust J Soil Res 18:163–189

    Article  Google Scholar 

  • Hayes MA, Jesse A, Hawke B, Baldock J, Tabet B, Lockington D, Lovelock CE (2017) Dynamics of sediment carbon stocks across intertidal wetland habitats of Moreton Bay, Australia. Glob Chang Biol 23:1–13

    Article  Google Scholar 

  • Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411

    Article  CAS  Google Scholar 

  • Hutchings P, Saenger P (1987) Ecology of Mangroves. Australia, University of Queensland Press, St. Lucia

    Google Scholar 

  • Huxham M, Langat J, Tamooh F, Kennedy H, Mencuccini M, Skov MW, Kairo J (2010) Decomposition of mangrove roots: effects of location, nutrients, species identity and mix in a Kenyan forest. Estuar Coast Shelf Sci 88:135–142

    Article  Google Scholar 

  • Inoue T, Nohara S, Takagi H, Anzai Y (2011) Contrast of nitrogen contents around roots of mangrove plants. Plant Soil 339:471–483

    Article  CAS  Google Scholar 

  • Koller M (2016) Robustlmm: an r package for robust estimation of linear mixed-effects models. J Stat Softw 75:1–24

    Article  Google Scholar 

  • Konôpka B, Pagès L, Doussan C (2009) Soil compaction modifies morphological characteristics of seminal maize roots. Plant Soil Environ 55:1–10

    Article  Google Scholar 

  • Kozlowski TT (1999) Soil compaction and growth of woody plants. Scand J For Res 14:596–619

    Article  Google Scholar 

  • Kristensen E (2007) Carbon balance in mangrove sediments: the driving processes and their controls. Greenhouse gas and carbon balances in mangrove coastal ecosystems, In: Tateda Y et al. (ed) Gendai Tosho, Kanagawa, pp 61–78

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw. https://doi.org/10.18637/jss.v082.i13

  • Lovelock CE, Adame MF, Bennion V, Hayes M, Reef R, Santini N, Cahoon DR (2015) Sea level and turbidity controls on mangrove soil surface elevation change. Estuar Coast Shelf Sci 153:1–9

    Article  Google Scholar 

  • Lovelock CE, Ball MC, Feller IC, Engelbrecht BMJ, Ewe ML (2006) Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorus availability. Physiol Plant 127:457–464

    Article  CAS  Google Scholar 

  • Lovelock CE, Bennion V, Grinham A, Cahoon DR (2011) The role of surface and subsurface processes in keeping pace with sea level rise in intertidal wetlands of Moreton Bay, Queensland, Australia. Ecosystems 14:745–757

    Article  CAS  Google Scholar 

  • Lovelock CE, Feller IC (2003) Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest. Oecologia 134:455–462

    Article  Google Scholar 

  • Ludovici KH (2008) Compacting coastal plain soils changes midrotation loblolly pine allometry by reducing root biomass. Can J For Res 38:2169–2176

    Article  CAS  Google Scholar 

  • Materechera SA, Dexter AR, Alston AM (1991) Penetration of very strong soils by seedling roots of different plant species. Plant Soil 135:31–41

    Article  Google Scholar 

  • McKee KL (1996) Growth and physiological responses of neotropical mangrove seedlings to root zone hypoxia. Tree Physiol 16:883–889

    Article  Google Scholar 

  • McKee KL (2001) Root proliferation in decaying roots and old root channels: a nutrient conservation mechanism in oligotrophic mangrove forests? J Ecol 89:876–887

    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 

  • 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 

  • Middleton BA, McKee KL (2001) Degradation of mangrove tissues and implications for peat formation in Belizean island forests. J Ecol 89:818–828

    Article  Google Scholar 

  • Misra RK, Gibbons AK (1996) Growth and morphology of eucalypt seedling roots in relation to soil strength arising from compaction. Plant Soil 182:1–11

    Article  CAS  Google Scholar 

  • Montagu KD, Conroy JP, Francis GS (1998) Root and shoot response of fieldgrown lettuce and broccoli to a compact subsoil. Aust J Agric Res 49:89–97

    Article  Google Scholar 

  • Montagu KD, Conroy JP, Atwell BJ (2001) The position of localized soil compaction determines root and subsequent shoot growth responses. J Exp Bot 364:2127–2133

    Article  Google Scholar 

  • Mósena M, Dillenburg LR (2004) Early growth of Brazilian Pine (Araucaria angustifolia [Bertol.] Kuntze) in response to soil compaction and drought. Plant Soil 258:293–306

    Article  Google Scholar 

  • Omi SK (1985) Soil compaction: effects on seedling growth. In: Research paper M-125, USDA Forestry Service, GTR Res. Colorado State University, Ft. Collins

    Google Scholar 

  • Ouyang X, Lee SY, Connolly RM (2017) Structural equation modelling reveals factors regulating surface sediment organic carbon content and CO2 efflux in a subtropical mangrove. Sci Total Environ 578:513–522

    Article  CAS  Google Scholar 

  • Pfeifer J, Faget M, Walter A, Blossfeld S, Fiorani F, Schurr U, Nagel KA (2014) Spring barley shows dynamic compensatory root and shoot growth responses when exposed to localised soil compaction and fertilisation. Funct Plant Biol 41:581–597

    Article  CAS  Google Scholar 

  • Pi N, Tam NFY, Wu Y, Wong MH (2009) Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot 90:222–230

    Article  Google Scholar 

  • Place G, Bowman D, Burton M, Rufty T (2008) Root penetration through a high bulk density soil layer: differential response of a crop and weed species. Plant Soil 307:179–190

    Article  CAS  Google Scholar 

  • Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670

    Article  Google Scholar 

  • Rayment GE, Higginson FR (1992) Australian Laboratory Handbook of Soil and Water Chemical Methods. Australia, Inkata Press, Melbourne

    Google Scholar 

  • Reef R, Ball MC, Feller IC, Lovelock CE (2010a) Relationships among RNA:DNA ratio, growth and elemental stoichiometry in mangrove trees. Funct Ecol 24:1064–1072

    Article  Google Scholar 

  • Reef R, Feller IC, Lovelock CE (2010b) Nutrition of mangroves. Tree Physiol 30:1148–1160

    Article  CAS  Google Scholar 

  • Reef R, Winter K, Morales J, Adame MF, Reef DL, Lovelock CE (2015) The effect of atmospheric carbon dioxide concentrations on the performance of the mangrove Avicennia germinans over a range of salinities. Physiol Plant 154:358–368

    Article  CAS  Google Scholar 

  • Saintilan N, Rogers K, Mazunder D, Woodroffe D (2013) Allochthonous and autochthonous contributions to carbon accumulation and carbon storage in southeastern Australian coastal wetlands. Estuar Coast Shelf Sci 128:84–92

    Article  CAS  Google Scholar 

  • Siegel-Issem CM, Burger JA, Powers RF, Ponder F, Patterson SC (2005) Seedling root growth as a function of soil density and water content. Soil Sci Soc Am J 69:215–226

    Article  CAS  Google Scholar 

  • Smith KD, May PB, Moore GM (2001) The influence of compaction and soil strength on the establishment of four Australian landscape trees. J Arboric 27:1–7

    Google Scholar 

  • Smoak JM, Breithaupt JL, Smith TJ III, Sanders CJ (2013) Sediment accretion and organic carbon burial relative to sea-level rise and storm events in two mangrove forests in Everglades National Park. Catena 104:58–66

    Article  CAS  Google Scholar 

  • Steen E, Håkansson I (1987) Use of in-growth soil cores in mesh bags for studies of relations between soil compaction and root growth. Soil Tillage Res 10:363–371

    Article  Google Scholar 

  • Stockmann U, Adams MA, Crawford JW, Field DJ, Henakaarchchi N, Jenkins M, Minasny B, McBratney AB, de Remy de Courcelles V, Singh K, Wheeler I, Abbott L, Angers DA, Baldock J, Bird M, Brookes PC, Chenu C, Jastrow JD, Lal R, Lehmann J, O’Donnell AG, Parton WJ, Whitehead D, Zimmermann M (2013) The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agric Ecosyst Environ 164:80–99

    Article  CAS  Google Scholar 

  • Stokes A, Atger C, Bengough AG, Fourcaud T, Sidle RC (2009) Desirable plant root traits for protecting natural and engineered slopes against landslides. Plant Soil 324:1–30

    Article  CAS  Google Scholar 

  • Tamooh F, Huxham M, Karachi M, Mencuccini M, Kairo JG, Kirui B (2008) Below-ground root yield and distribution in natural and replanted mangrove forests at Gazi bay, Kenya. For Ecol Manag 256:1290–1297

    Article  Google Scholar 

  • Tardieu F (1994) Growth and functioning of roots and root systems subjected to soil compaction towards a system with multiple signalling? Soil Tillage Res 30:217–243

    Article  Google Scholar 

  • Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, Cambridge

    Google Scholar 

  • Tracy SR, Black CR, Roberts JA, Dodd IC, Mooney SJ (2015) Using X-ray computed tomography to explore the role of abscisic acid in moderating the impact of soil compaction on root system architecture. Environ Exp Bot 110:11–18

    Article  CAS  Google Scholar 

  • van Genuchten M T, Leij F J, Yates SR (1991) The RETC code for quantifying the hydraulic functions of unsaturated soils. US EPA, Ada, OK. 90

  • Viscarra Rossel RA, Webster R, Bui EN, Baldock JA (2014) Baseline map of organic carbon in Australian soil to support national carbon accounting and monitoring under climate change. Glob Chang Biol 20:2953–2970

    Article  Google Scholar 

  • Vogt KA, Vogt DJ, Bloomfield J (1998) Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level. Plant Soil 200:71–89

    Article  CAS  Google Scholar 

  • Warnaars BC, Eavis BW (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 Soil 36:623–634

    Article  Google Scholar 

  • Wehr JB, So HB, Menzies NW, Fulton I (2015) Hydraulic properties of layered soils influence survival of Rhodes grass (Chloris gayana Kunth.) during water stress. Plant Soil 270:287–297

    Article  Google Scholar 

  • Whelan KRT, Smith TJ III, Anderson GH, Ouellette ML (2009) Hurricane Wilma's impact on overall sediment elevation and zones within the sediment profile in a mangrove forest. Wetlands 29:16–23

    Article  Google Scholar 

  • Xiong Y, Liu X, Guan W, Liao B, Chen Y, Li M, Zhong C (2016) Fine root functional group based estimates of fine root production and turnover rate in natural mangrove forests. Plant Soil. https://doi.org/10.1007/s11104-016-3082-z

    Article  Google Scholar 

  • Ye Y, Baipeng P, Guangcheng C, Yan C (2011) Processes of organic carbon in mangrove ecosystems. Acta Ecol Sin 31:169–173

    Article  Google Scholar 

  • Zisa R P, Halverson H G, Stout B B (1980) Establishment and early growth of conifers on compact soils in urban areas. Research paper NE-451, USDA forest service, Northeastern forest experiment station, Broomall, Pa

Download references

Acknowledgements

We would like to thank V. Bennion, E. Hopkins Snavely and Dr. S. Razniewski for their help during fieldwork. Further, we would like to thank Dr. B. Wehr for guidance on the use of the pressure plate apparatus.

Author information

Authors and Affiliations

  1. School of Biological Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia

    Anne Ola & Catherine E. Lovelock

  2. School of Agriculture and Food Science, The University of Queensland, Brisbane, QLD, 4072, Australia

    Susanne Schmidt

Authors
  1. Anne Ola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susanne Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine E. Lovelock
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne Ola.

Additional information

Responsible Editor: W Richard Whalley

Electronic supplementary material

ESM 1

(DOCX 81 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ola, A., Schmidt, S. & Lovelock, C.E. The effect of heterogeneous soil bulk density on root growth of field-grown mangrove species. Plant Soil 432, 91–105 (2018). https://doi.org/10.1007/s11104-018-3784-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3784-5

Keywords

Search

Navigation