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How are anatomical and hydraulic features of the mangroves Avicennia marina and Rhizophora mucronata influenced by siltation?

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This article provides significant data in the debate on whether siltation might have a negative impact on the hydraulic functioning of two widespread mangrove tree species Avicennia marina and Rhizophora mucronata.

Abstract

Elevated sediment addition, or siltation, within mangrove ecosystems is considered as being negative for trees and saplings, resulting in stress and higher mortality rates. However, little is known about how siltation influences the hydraulic functioning of mangrove trees. Comparing two mangrove tree species (Avicennia marina Vierh. Forsk. and Rhizophora mucronata Lam.) from low and high-siltation plots led to the detection of anatomical and morphological differences and tendencies. Adaptations to high siltation were found to be either mutual among both species, e.g., significant smaller single leaf area (p A.marina  = 0.058, F1.38 = 3.8; p R.mucronata  = 0.005, F1.38 = 8.7; n = 20 × 20) and a tendency towards smaller stomatal areas (p A.marina  = 0.131, F1.8 = 2.8; p R.mucronata  = 0.185, F1.8 = 2.1, n = 5 × 60), or species-specific trends for A. marina, such as higher phloem band/growth layer ratios (p = 0.101, F1.8 = 3.4, n = 5 × 3) and stomatal density (p = 0.052, F1.8 = 5.2, n = 5 × 4). All adaptations seemingly contributed to a comparable hydraulic conductivity independent of the degree of siltation. These findings indicate that silted trees level off fluctuations in their hydraulic performance as a survival mechanism to cope with this less favourable environment. Most of the trees’ structural adaptations to cope with siltation are similar to known drought stress-imposed adaptations.

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References

  • Abuodha PAW, Kairo JG (2001) Human-induced stresses on mangrove swamps along the Kenyan coast. Hydrobiologia 458:255–265. doi:10.1023/a:1013130916811

    Article  Google Scholar 

  • Alongi DM (2008) Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuar Coast Shelf Sci 76:1–13. doi:10.1016/j.ecss.2007.08.024

    Article  Google Scholar 

  • Angeles G, Lopez-Portillo J, Ortega-Escalona F (2002) Functional anatomy of the secondary xylem of roots of the mangrove Laguncularia racemosa (L.) Gaertn. (Combretaceae). Trees Struct Funct 16:338–345. doi:10.1007/s00468-002-0171-9

    Article  Google Scholar 

  • Anyia AO, Herzog H (2004) Water-use efficiency, leaf area and leaf gas exchange of cowpeas under mid-season drought. Eur J Agron 20:327–339. doi:10.1016/s1161-0301(03)00038-8

    Article  Google Scholar 

  • APHA (1998) Standard method for the examination of water and waste-water. 20th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Baas P, Werker E, Fahn A (1983) Some ecological trends in vessel characters. Iawa Bull 4:141–159

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brakel W (1982) Tidal patterns on the East African coast and their implications for the littoral biota. In: Proceedings of the symposium on the coastal and marine environment of the Red Sea, Gulf of Aden and tropical Western Indian Ocean, pp 403–418

  • Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiol 95:628–635. doi:10.1104/pp.95.2.628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Burghardt M, Burghardt A, Gall J, Rosenberger C, Riederer M (2008) Ecophysiological adaptations of water relations of Teucrium chamaedrys L. to the hot and dry climate of xeric limestone sites in Franconia (Southern Germany). Flora 203:3–13. doi:10.1016/j.flora.2007.11.003

    Article  Google Scholar 

  • Carr DJ (2000) On the supposed changes in stomatal frequency and size with height of leaf insertion. Ann Bot 86:911–912. doi:10.1006/anbo.2000.1258

    Article  Google Scholar 

  • Castañeda-Moya E, Twilley RR, Rivera-Monroy VH, Zhang K, Davis SE III, Ross M (2010) Sediment and nutrient deposition associated with Hurricane Wilma in mangroves of the Florida Coastal Everglades. Estuar Coasts 33:45–58

    Article  Google Scholar 

  • Choat B et al (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. doi:10.1111/j.1469-8137.2011.03772.x

    Article  CAS  PubMed  Google Scholar 

  • Ellison JC (1998) Impacts of sediment burial on mangroves. Mar Pollut Bull 37:420–426

    Article  CAS  Google Scholar 

  • Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347. doi:10.1073/pnas.0904209106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franks PJ, Farquhar GD (2001) The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol 125:935–942. doi:10.1104/pp.125.2.935

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant Cell Environ 32:1737–1748. doi:10.1111/j.1365-3040.2009.002031.x

    Article  PubMed  Google Scholar 

  • Furukawa K, Wolanski E, Mueller H (1997) Currents and sediment transport in mangrove forests. Estuar Coast Shelf Sci 44:301–310. doi:10.1006/ecss.1996.0120

    Article  CAS  Google Scholar 

  • Gartner H, Nievergelt D (2010) The core-microtome: a new tool for surface preparation on cores and time series analysis of varying cell parameters. Dendrochronologia 28:85–92. doi:10.1016/j.dendro.2009.09.002

    Article  Google Scholar 

  • Gordon DM (1987) Disturbance to mangroves in tropical-arid Western Australia: hypersalinity and restricted tidal exchange as factors leading to mortality/David M. Gordon. Technical series (Western Australia. Environmental Protection Authority); no. 12. Environmental Protection Authority, Perth. Accessed from http://nla.gov.au/nla.cat-vn1827098

  • Gu MM, Rom CR, Robbins JA, Oosterhuis DM (2007) Effect of water deficit on gas exchange, osmotic solutes, leaf abscission, and growth of four birch genotypes (Betula L.) under a controlled environment. HortScience 42:1383–1391

    Google Scholar 

  • Hameed M, Ashraf M (2008) Physiological and biochemical adaptations of Cynodon dactylon (L.) Pers. from the Salt Range (Pakistan) to salinity stress. Flora 203:683–694. doi:10.1016/j.flora.2007.11.005

    Article  Google Scholar 

  • Hao GY et al (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. doi:10.1093/treephys/tpp005

    Article  PubMed  Google Scholar 

  • Heckenberger U, Roggatz U, Schurr U (1998) Effect of drought stress on the cytological status in Ricinus communis. J Exp Bot 49:181–189. doi:10.1093/jexbot/49.319.181

    Article  CAS  Google Scholar 

  • Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. In: Southward AJ, Tyler PA, Young CM, Fuiman LA (eds) Advances in marine biology, vol 40. Advances in marine biology. pp 81–251. doi:10.1016/s0065-2881(01)40003-4

  • Krauss KW, Lovelock CE, McKee KL, Lopez-Hoffman L, Ewe SML, Sousa WP (2008) Environmental drivers in mangrove establishment and early development: a review. Aquat Bot 89:105–127. doi:10.1016/j.aquabot.2007.12.014

    Article  Google Scholar 

  • Lieth H, Berlekamp J, Fuest S, Riediger S (1999) Climate diagrams of the world. CD-series: climate and biosphere. Blackhuys Publishers, Leiden

    Google Scholar 

  • López-Portillo J, Ewers FW, Angeles G (2005) Sap salinity effects on xylem conductivity in two mangrove species. Plant, Cell Environ 28:1285–1292. doi:10.1111/j.1365-3040.2005.01366.x

    Article  Google Scholar 

  • Lovelock CE, Ball MC, Choat B, Engelbrecht BMJ, Holbrook NM, Feller IC (2006) Linking physiological processes with mangrove forest structure: phosphorus deficiency limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf Rhizophora mangle. Plant, Cell Environ 29:793–802. doi:10.1111/j.1365-3040.2005.01446.x

    Article  CAS  Google Scholar 

  • Lugo AE, Cintron G (1975) The mangrove forests of Puerto Rico and their management. In: Proceedings of the international symposium on biology and management of mangroves, Gainesville, University of Florida

  • Mauseth JD, Plemons Rodriguez BJ (1997) Presence of paratracheal water storage tissue does not alter vessel characters in cactus wood. Am J Bot 84:815–822. doi:10.2307/2445817

    Article  CAS  PubMed  Google Scholar 

  • Mauseth JD, Stevenson JF (2004) Theoretical considerations of vessel diameter and conductive safety in populations of vessels. Int J Plant Sci 165:359–368. doi:10.1086/382808

    Article  Google Scholar 

  • McClenahan K, Macinnis-Ng C, Eamus D (2004) Hydraulic architecture and water relations of several species at diverse sites around Sydney. Aust J Bot 52:509–518. doi:10.1071/bt03123

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mohamed MOS, Neukermans G, Kairo JG, Dahdouh-Guebas F, Koedam N (2009) Mangrove forests in a peri-urban setting: the case of Mombasa (Kenya). Wetlands Ecol Manage 17:243–255. doi:10.1007/s11273-008-9104-8

    Article  Google Scholar 

  • Naz N, Hameed M, Ashraf M, Al-Qurainy F, Arshad M (2010) Relationships between gas-exchange characteristics and stomatal structural modifications in some desert grasses under high salinity. Photosynthetica 48:446–456. doi:10.1007/s11099-010-0059-7

    Article  Google Scholar 

  • 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, Kenya. doi:10.1002/ece3.1154

    Google Scholar 

  • Ounis A, Cerovic Z, Briantais J, Moya I (2005) Rasband WS, Image J. US National Institutes of Health, Bethesda

  • Parson TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Quarrie SA, Jones HG (1977) Effects of abscisic-acid and water stress on development and morphology of wheat. J Exp Bot 28:192. doi:10.1093/jxb/28.1.192

    Article  CAS  Google Scholar 

  • Quisthoudt K, Adams J, Rajkaran A, Dahdouh-Guebas F, Koedam N, Randin CF (2013) Disentangling the effects of global climate and regional land-use change on the current and future distribution of mangroves in South Africa. Biodivers Conserv 22:1369–1390. doi:10.1007/s10531-013-0478-4

    Article  Google Scholar 

  • Robert EMR, Koedam N, Beeckman H, Schmitz N (2009) A safe hydraulic architecture as wood anatomical explanation for the difference in distribution of the mangroves Avicennia and Rhizophora. Funct Ecol 23:649–657. doi:10.1111/j.1365-2435.2009.01551.x

    Article  Google Scholar 

  • Robert EMR et al (2011) Successive cambia: a developmental oddity or an adaptive structure? PLoS ONE. doi:10.1371/journal.pone.0016558

    Google Scholar 

  • Salleo S, Lo Gullo MA, Trifilo P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell Environ 27:1065–1076. doi:10.1111/j.1365-3040.2004.01211.x

    Article  Google Scholar 

  • Salleo S, Trifilo P, Lo Gullo MA (2006) Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel). Funct Plant Biol 33:1063–1074. doi:10.1071/fp06149

    Article  Google Scholar 

  • 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. doi:10.1093/aob/mcl224

    Article  PubMed Central  PubMed  Google Scholar 

  • 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. doi:10.1093/aob/mcm103

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmitz N, Robert EMR, Verheyden A, Kairo JG, Beeckman H, Koedam N (2008) A patchy growth via successive and simultaneous cambia: key to success of the most widespread mangrove species Avicennia marina? Ann Bot 101:49–58. doi:10.1093/aob/mcm280

    Article  PubMed Central  PubMed  Google Scholar 

  • Scholander PF, Hemmingsen EA, Hammel HT, Bradstreet EDP (1964) Hydrostatic pressure and osmotic potential in leaves of mangroves and some other plants. Proc Natl Acad Sci USA 52:119. doi:10.1073/pnas.52.1.119

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schurr U, Heckenberger U, Herdel K, Walter A, Feil R (2000) Leaf development in Ricinus communis during drought stress: dynamics of growth processes, of cellular structure and of sink-source transition. J Exp Bot 51:1515–1529. doi:10.1093/jexbot/51.350.1515

    Article  CAS  PubMed  Google Scholar 

  • Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell Environ 11:35–40. doi:10.1111/j.1365-3040.1988.tb01774.x

    Article  Google Scholar 

  • Stuart SA, Choat B, Martin KC, Holbrook NM, Ball MC (2007) The role of freezing in setting the latitudinal limits of mangrove forests. New Phytol 173:576–583. doi:10.1111/j.1469-8137.2006.01938.x

    Article  CAS  PubMed  Google Scholar 

  • Terrados J et al (1997) The effect of increased sediment Accretion on the survival and growth of Rhizophora apiculata seedlings. Estuar Coast Shelf Sci 45:697–701. doi:10.1006/ecss.1997.0262

    Article  Google Scholar 

  • Thomas L (1997) Retrospective power analysis. Conserv Biol 11:276–280

    Article  Google Scholar 

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

    Google Scholar 

  • Vaiphasa C, De Boer WF, Panitchart S, Vaiphasa T, Bamrongrugsa N, Santitamnont P (2007) Impact of solid shrimp pond waste materials on mangrove growth and mortality: a case study from Pak Phanang, Thailand. Hydrobiologia 591:47–57. doi:10.1007/s10750-007-0783-6

    Article  Google Scholar 

  • van Mensvoort T (1998) Mangrove research discussion list. Communication

  • Villar-Salvador P, Castro-Diez P, Perez-Rontome C, Montserrat-Martí G (1997) Stem xylem features in three Quercus (Fagaceae) species along a climatic gradient in NE Spain. Trees Struct Funct 12:90–96. doi:10.1007/pl00009701

    Google Scholar 

  • Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM (2000) Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant, Cell Environ 23:407–414. doi:10.1046/j.1365-3040.2000.00554.x

    Article  Google Scholar 

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Acknowledgments

The authors are very grateful for the attribution of George Onduso and Eric Okuku, without whom the measurement campaign never would have succeeded. For all the help during the measurement campaign and laboratory work, we would like to thank Samuel Njoroge, Naftali Mukua, Oduor Nancy Awuor, Jan Van Den Bulcke and Piet Dekeyser. Soil analysis was performed by Sturcky Okumu and Oliver Ochola. For statistical support, the authors are grateful towards Rosanna Overholser (FIRE—Fostering Innovative Research based on Evidence—statistical consulting). We also want to thank Veerle De Schepper and Elisabeth M.R. Robert for commenting the M.Sc. text. For logistic support we like to thank Jared Bosire (Kenya Marine and Fisheries Research Institute, KMFRI), Hans Beeckman (Laboratory of Wood Biology and Xylarium, Royal Museum for Central Africa) and Joris Van Acker (Laboratory of Wood Technology—Woodlab, UGent). Additionally, the authors gratefully thank the 3 anonymous reviewers for their constructive comments.

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    Authors and Affiliations

    1. Laboratory of Plant Ecology, Faculty of Bioscience Engineering, Ghent University (UGent), Coupure links 653, 9000, Ghent, Belgium

      Hannes De Deurwaerder & K. Steppe

    2. Kenya Marine and Fisheries Research Institute (KMFRI), Headquarter and Mombasa Station, P.O. Box 81651 080100, Mombasa, Kenya

      J. A. Okello

    3. Laboratory of Plant Biology and Nature Management (APNA), Vrije Universiteit Brussel (VUB), Pleinlaan 2, 1050, Brussels, Belgium

      J. A. Okello, N. Koedam & N. Schmitz

    4. Universität für Bodenkultur Wien (BOKU), Gregor-Mendel-Straße 33, 1180, Vienna, Austria

      N. Schmitz

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    1. Hannes De Deurwaerder
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    Correspondence to Hannes De Deurwaerder.

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    Communicated by R. Reef.

    N. Schmitz and K. Steppe contributed equally to this work.

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    De Deurwaerder, H., Okello, J.A., Koedam, N. et al. How are anatomical and hydraulic features of the mangroves Avicennia marina and Rhizophora mucronata influenced by siltation?. Trees 30, 35–45 (2016). https://doi.org/10.1007/s00468-016-1357-x

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