Abstract
Aims
Natural sedimentation rates may not affect mangrove trees adversely, but large and sometimes episodic delivery of sediment may result in decreased growth, dieback or mortality. In this study, we aim to assess the effects of different levels of partial sediment burial on mangrove tree structure and function.
Methods
Trees of Avicennia marina, Ceriops tagal and Rhizophora mucronata were experimentally buried with terrestrial sediment to simulate different sedimentation levels (15, 30 and 45 cm). After 14 months, branch hydraulic conductivity, xylem structure and stomatal properties were assessed.
Results
Sedimentation resulted in general increase in hydraulic conductivity following intermediate levels of burial. The process is also associated with varied anatomical modification in vessel grouping, vessel lumen size and potential conductive area in the three investigated mangrove tree species. Additionally, stomatal adjustment was observed in C. tagal with up to 37% reduction of total stomata area in leaves of buried trees.
Conclusions
Although sedimentation may stimulate modification in vessel and stomatal properties of buried mangrove trees after a relatively short period of exposure, these traits may not necessarily be important in ensuring hydraulic conductivity which either increases or remains the same as in control following burial.
Similar content being viewed by others
References
Alongi DM (2009) The energetics of mangrove forests. Springer Science + Business Media B.V, Townsville
Alongi DM, Pfitzner J, Trott LA, Tirendi F, Dixon P, Klumpp DW (2005) Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang estuary, China. Estuar Coast Shelf Sci 63:605–618
Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiol Plant 139:280–288
Ball MC (1988) Salinity tolerance in the 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
Ball MC, Canny MJ, Huang CX, Egerton JJG, Wolfe J (2006) Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis. Plant Cell and Environment 29:729–745
Bamroongrugsa N, Yuanlaie P (1995) Mangrove afforestation on newly formed mudflats of Patani Bay, Southern Thailand. In: Khemnark C (ed) Ecology and management of mangrove restoration and regeneration in East and South East Asia. Proceedings of the ECOTONE IV, 18-22 January 1995, Bangkok, pp 230-238
Brokaw N, Thompson J (2000) The H for DBH. For Ecol Manag 129(1–3):89–91
Caldeira K (2012) The great climate experiment. Sci Am 307(3):78–83
Carlquist S (1984) Vessel grouping in dicotyledon wood: significance and relationship to imperforate tracheary elements. Aliso 10:505–525
Carlquist S (2001) Comparative wood anatomy: systematic, ecological, and evolutionary aspects of dicotyledon wood, 2nd edn. Springer Verlag, Berlin
Carlquist S (2009) Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications. Bot J Linn Soc 161:26–65
Choat B, Cobb AR, Jansen S (2007) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function xylem. New Phytol 177:608–625
Choat B, Medek DE, Stuart SA, Pasquet-Kok J, Egerton JJG, Salari H, Sack L, Ball MC (2011) Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytol 191:996–1005
Coder KD (2000) Soil compaction and trees: causes symptoms and effects. University of Georgia Warnell School of Forest Resources Extension Publication FOR00-3
Cruiziat P, Cochard H, Améglio T (2002) Hydraulic architecture of trees: main concepts and results. Ann For Sci 59:723–752
Curtis PS, Ackerly DD (2008) Introduction to a virtual special issue on plant ecological strategy axes in leaf and wood traits. New Phytol 179:905–907
Dahdouh-Guebas F, De Bondt R, Abeysinghe PD, Kairo JG, Cannicci S, Triest L, Koedam N (2004) Comparative study of the disjunct zonation pattern of the grey mangrove Avicennia marina (Forsk.) Vierh. In Gazi Bay (Kenya). Bull Mar Sci 74:237–252
De Deurwaerder H, Okello JA, Schmitz N, Koedam N, Steppe K (2016) How are anatomical and hydraulic features of mangroves Avicennia marina and Rhizophora mucronata influenced by siltation. Trees. doi:10.1007/s00468-016-1357-x
de Silva NDG, Cholewa E, Ryser P (2012) Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.) J Exp Bot 63:5957–5966
Gärtner H, Lucchinetti S, Schweingruber FH (2014) New perspectives for wood anatomical analysis in dendrosciences: the GSL1-microtome. Dendrochronologia 32:47–51
Gitz DC, Baker JT (2009) Methods for creating stomatal impressions directly onto archivable slides. Agron J 101:232–236
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao K-F, Cochard H, Delzon S, Domec JC, Fan Z-X, Field TS, Jacobsen AL, Johnson, D.M., Lens, F., Maherali, H., Martínez-Vilalta J, Mayr S, McCulloh KA, Mencuccini M, Mitchell PJ, Morris H, Nardini A, Pittermann J, Plavcová L, Schreiber SG, Sperry JS, Wright IJ, Zanne AE (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209, 123–136.
Hacke UG (2014) Variable plant hydraulic conductance. Tree Physiol 34:105–108
Hao GY, Jones TJ, Luton C, Zhang YJ, Manzane E, Scholz FG, Bucci SJ, Cao KF, Goldstein G (2009) Hydraulic redistribution in dwarf Rhizophora mangle trees driven by interstitial soil water salinity gradients: impacts on hydraulic architecture and gas exchange. Tree Physiol 29:697–705
Herrera A (2013) Responses to flooding of plant water relations and leaf gas exchange in tropical tolerant trees of a black-water wetland. Front Plant Sci 4:106
Hutchings P, Saenger P (1987) Ecology of mangroves. Queensland University Press, Brisbane
Jain SM, Minocha SC (2000) Molecular biology of woody plants, volume 1. Springer Science+Business Media, Dordrecht, p 485
Johnstone R, Preston M (1993) Nutrient analysiss in tropical waters: Practical guidance and safety notes for the performance of dissolved micronutrient analysis in sea water with particular reference to tropical waters. IOC-UNESCO, 25pp
Jones HG, Sutherland RA (1991) Stomatal control of xylem embolism. Plant Cell Environ 14:607–612
Kimeli AK (2013) Sedimentation in response to sea level rise in mangroves of Mwache Creek, Mombasa-Kenya: a field and modeling study. Vrije Universiteit Brussels
Ladjal M, Huc R, Ducrey M (2005) Drought effects on hydraulic conductivity and xylem vulnerability to embolism in diverse species and provenances of Mediterranean cedars. Tree Physiol 25:1109–1117
Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Plant development: signals from mature to new leaves. Nature 411:154–154
Laur J, Hacke UG (2014) The role of water channel proteins in facilitating recovery of leaf hydraulic conductance from water stress in Populus trichocarpa. PLoS One 9:e111751
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus acer. New Phytol 190:709–723
Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S (2013) Embolism resistance as a key mechanism to understand adaptive plant strategies. Curr Opin Plant Biol 16:287–292
Lewis AM (1992) Measuring the hydraulic diameter of a pore or conduit. Am J Bot 79(10):1158–1161
Loepfe L, Martίnez-Vilalta J, Piñol J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol 247:788–803
Lopez-Portillo J, Ewers FW, Angeles G (2005) Sap salinity effects on xylem conductivity in two mangrove species. Plant Cell Environ 28:1285–1292
Lovelock CE, Feller IC, McKee KL, Engelbrecht BMJ, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panamá. Funct Ecol 18:25–33
Lovelock CE, Ball MC, Feller IC, Engelbrecht BMJ, Ewe ML (2006) Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorous availability. Pysiologia Plantarum 127:457–464
Lovelock CE, Sorrell BK, Hancock N, Hua Q, Swales A (2010) Mangrove forest and soil development on a rapidly accreting shore in New Zealand. Ecosystems 13:437–451
Martίnez-Vilalta J, Mencuccini M, Alvarez X, Camacho J, Loepfe L, Pinol J (2012) Spatial distribution and packing of xylem conduits. Am J Bot 99:1–8
Matthijs S, Tack J, van Speybroeck D, Koedam N (1999) Mangrove species zonation and soil redox state, sulphide concentration and salinity in Gazi Bay (Kenya), a preliminary study. Mangrove Salt Marshes 3:243–249
McDowell N, Pockman WT, Allen C, Breshears DD, Cobb N, Kolb T, Sperry JS, West A, Williams D, Yepez E (2008) Mechanisms of plant survival and plant mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739
McDowell N, Fisher RA, Xu CG, Domec JC, Holtta T, Mackay DS, Sperry JS, Boutz A, Dickman L, Gehres N (2013) Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytol 200:304–321
Meinzer FC, Grantz DA (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant Cell Environ 13:383–388
Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930
Neukermans G, Dahdouh-Guebas F, Kairo JG, Koedam N (2008) Mangrove species and stand mapping in Gazi bay (Kenya) using quickbird satellite imagery. J Spat Sci 53:75–86
Okello JA, Robert EMR, Beeckman H, Kairo JG, Dahdouh-Guebas F, Koedam N (2014) Effects of experimental sedimentation on the phenological dynamics and leaf traits of replanted mangroves at Gazi bay. Ecol Evol 4:3187–3200
Parsons TR (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press. Pons Point, N.S.W. Australia
Pergamon Press, (1984) Publication from Pergamon. Vacuum 34 (5):607
PUMPSEA (2005) Part I; determination of sediment characteristics (density, water content and organic content). In: experimental protocol for PUMPSEA work package 1- SDU. Institute of Biology, University of Southern Denmark
Robert EMR, Koedam N, Beeckman H, Schmitz N (2009a) A safe hydraulic architecture as wood anatomical explanation for the difference in distribution of the mangroves Avicennia and Rhizophora. Funct Ecol 23:649–657
Robert EMR, Schmitz N, Kirauni HA, Beeckman H, Koedam N (2009b) Salinity fluctuations in mangrove forest of Gazi bay, Kenya: lessons for future research. Nature and Faune 24:89–95
Robert EMR, Schmitz N, Okello JA, Boeren I, Beeckman H, Koedam N (2010) Mangrove growth rings: fact or fiction? Trees-Struct Funct 25:49–58
Rowland L, da Costa ACL, Galbraith DR, Oliveira RS, Binks OJ, Oliveira AAR, Pullen AM, Doughty CE, Metcalfe DB, Vasconcelos SS, Ferreira LV, Malhi Y, Grace J, Mencuccini M, Meir P (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature. doi:10.1038/nature15539
Schmitz N, Verheyden A, Beeckman H, Kairo JG, Koedam N (2006) Influence of a salinity gradient on the vessel characters of the mangrove species Rhizophora mucronata. Ann Bot 98:1321–1330
Schmitz N, Jansen S, Verheyden A, Kairo JG, Beeckman H, Koedam N (2007) Comparative anatomy of intervessel pits in two mangrove species growing along a natural salinity gradient in Gazi Bay, Kenya. Ann Bot 100:271–281
Schmitz N, Koch G, Schmitt U, Koedam N, Beeckman H (2008) Intervessel pit structure and histochemistry of two mangrove species as revealed by cellular UV micro-spectrophotometry and electron microscopy: intraspecific variation and functional significance. Microsc Microanal 14:387–397
Scholander PF, Bradstreet ED, Hammel HT, Hemmingsen EA (1966) Sap concentrations in halophytes and some other plants. Plant Physiol 41:529–532
Scholz A, Rabaey D, Stein A, Cochard H, Smets E, Jansen S (2013) The evolution and function of vessel and pit characters with respect to cavitation resistance across 10 Prunus species. Tree Physiol 33(7):684–694
Sojka RE (1992) Stomatal closure in oxygen-stressed plants. Soil Sci 154:269–280
Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell Environ 21:347–359
Stuart S (2003) What sets the latitudinal limit of the mangrove habitat? In: Department of Biology Harvard University. Massachusetts, Cambridge, p 45
Swift CC, Jacobs SM, Esler KJ (2008) Drought induced xylem embolism in four riparian trees from the western Cape Province: insights and implications for planning and evaluation of restoration. S Afr J Bot 74:508–516
Thrush SF, Hewitt J, Cummings VJ, Ellis J, Hatton JC, Lohrer A, Norkko A (2004) Muddy waters: elevating sediment input to coastal and estuarine habitats. Front Ecol Environ 2:299–306
Tomlinson PB (1994) The botany of mangroves. Cambridge University Press, Cambridge, p 433
Twilley RR, Snedaker SC, Yáñez-Arancibia A, Medina E (1996) Biodiversity and ecosystem processes in tropical estuaries: perspectives of mangrove ecosystems. In: Mooney HA, Cushman JH, Medina E, Sala OE, Schulze ED (eds) Functional roles of biodiversity: a global perspective. Wiley-Blackwell, NewYork, pp 327–370
Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Answers from model. Plant Physiol 88:574–580
Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Funct Ecol 6:469–475
Yeung EC (1998) A beginner's guide to the study of plant structure. In: Karcher SJ (ed) tested studies for laboratory teaching, volume 19. Proceedings of the 19th workshop/conference of Association for Biology Laboratory Education (ABLE), pp 365
Zotz G, Tyree MT, Patiño S (1997) Hydraulic architecture and water relations of a flood-tolerant tropical tree, Annona glabra. Tree Physiol 17:359–365
Acknowledgements
The authors acknowledge financial support by the Flemish Interuniversity Council-University Development Cooperation (VLIR-UOS, Flanders, Belgium) and the “Fonds Alice en David Van Buuren” (Brussels, Belgium). E.M.R.R. and N.S. were supported by the Research Foundation - Flanders (FWO, Flanders, Belgium). P.C. was supported by The C.T. de Wit Graduate School for Production Ecology and Resource Conservation. This work has been carried out under the framework of the VLIR-UOS International Course Programme (ICP) PhD and is also linked to activities conducted within the project ‘CREC’ (EU IRSES #247514).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Susan Schwinning.
Electronic supplementary material
ESM 1
(DOCX 41 kb)
Rights and permissions
About this article
Cite this article
Okello, J.A., Schmitz, N., Beeckman, H. et al. Hydraulic conductivity and xylem structure of partially buried mangrove tree species. Plant Soil 417, 141–154 (2017). https://doi.org/10.1007/s11104-017-3247-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3247-4