Skip to main content

Advertisement

Log in

Morphological plasticity in mangrove trees: salinity-related changes in the allometry of Avicennia germinans

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key Message

Morphological plasticity helps plants to cope to environmental conditions. Allometric responses of the mangrove Avicennia germinans to increasing salinity are easily detectable when focusing on the top height trees.

Abstract

Several studies show that mangrove trees possess high species- and site-related trait allometry, suggesting large morphological plasticity that might be related to environmental conditions, but the causes of such variation are not clearly understood and systematic quantification is still missing. Both aspects are essential for a mechanistic understanding of the development and functioning of forests. We analyzed the role of salinity in the allometric relations of the mangrove Avicennia germinans, using: (1) the top height trees (trees with the largest diameters at breast height, which reflect forest properties at the maximum use of resources); (2) the slenderness coefficient (which indicates competition and environmental conditions); and (3) the crown to DBH ratio. These standard tools for forest scientists dealing with terrestrial forests are suitable to analyze the plastic responses of mangroves to salinity. First, the top height trees help to recognize structural forest properties that are not detectable when studying the whole stand. Second, we found that at salinities above 55 ‰, trees are less slender and develop wider crowns in relation to DBH than when growing at lower salinities. Our results suggest a significant change in allometric traits in relation to salinity, and reflect the plastic responses of tree traits in response to environmental variation. Understanding the plastic responses of plants to their environment can help to better model, predict, and manage forests in changing environments.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abetz P (1988) Untersuchungen zum Wachstum von Buchen auf der Schwäbischen Alb. Allg Forst-u J-Ztg 159:215–223

    Google Scholar 

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

    Article  Google Scholar 

  • Ball MC (2002) Interactive effects of salinity and irradiance on growth: implications for mangrove forest structure along salinity gradients. Trees Struct Funct 16:126–139

    Article  Google Scholar 

  • Ball MC, Farquhar GD (1984) Photosynthetic and stomatal responses of the grey mangrove, Avicennia marina, to transient salinity conditions. Plant Physiol 74:7–11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Boizard SD, Mitchell SJ (2011) Resistance of red mangrove (Rhizophora mangle L.) seedlings to deflection and extraction. Trees 25:371–381

    Article  Google Scholar 

  • Burchett MD, Field CD, Pulkownik A (1984) Salinity, growth and root respiration in the grey mangrove, Avicennia marina. Physiol Plant 60:113–118

    Article  Google Scholar 

  • Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128

    Article  Google Scholar 

  • Cardona-Olarte P, Twilley RR, Krauss KW, Rivera-Monroy VH (2006) Responses of neotropical mangrove seedlings grown in monoculture and mixed culture under treatments of hydroperiod and salinity. Hydrobiologia 569:325–341

    Article  Google Scholar 

  • Castañeda-Moya E, Twilley RR, Rivera-Monroy VH et al (2011) Patterns of root dynamics in mangrove forests along environmental gradients in the Florida Coastal Everglades USA. Ecosystems 14:1178–1195

    Article  Google Scholar 

  • Chapin FS (1991) Effects of multiple environmental stresses on nutrient availability and use. In: Mooney H, Winner WE, Pell E (eds) Response plants to multiple stresses. Academic press, San Diego, pp 67–88

  • Chapin FS, Bloom A, Field C, Waring R (1987) Plant responses to multiple environmental factors. Bioscience 37(49):57

    Google Scholar 

  • Chave J, Andalo C, Brown S et al (2005) Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145:87–99

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Twilley RR (1998) A gap dynamic model of mangrove forest development along gradients of soil salinity and nutrient resources. J Ecol 86:37–51

    Article  Google Scholar 

  • Cheng H, Liu Y, Tam NFY et al (2010) The role of radial oxygen loss and rot anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut 158:1189–1196

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Wang Y-S, Ye Z-H et al (2012) Influence of N deficiency and salinity on metal (Pb, Zn and Cu) accumulation and tolerance by Rhizophora stylosa in relation to root anatomy and permeability. Environ Pollut 164:110–117

    Article  PubMed  CAS  Google Scholar 

  • Cintrón G, Lugo AE, Pool DJ, Morris G (1978) Mangroves of arid environments in Puerto Rico and adjacent islands. Biotropica 10:110–121

    Article  Google Scholar 

  • Clough BF, Scott K (1989) Allometric relationships for estimating above-ground biomass in six mangrove species. For Ecol Manag 27:117–127

    Article  Google Scholar 

  • Clough BF, Sim RG (1989) Changes in gas exchange characteristics and water use efficiency of mangroves in response to salinity and vapour pressure deficit. Oecologia 79:38–44

  • Comley BWT, McGuinness KA (2005) Above- and below-ground biomass and allometry of four common northern Australian mangroves. Aust J Bot 53:431–436

    Article  Google Scholar 

  • Crawley M (2012) The R book. Wiley, West Sussex

    Book  Google Scholar 

  • Curtis R, Marshall DD (2000) Why quadratic mean diameter ? West J Appl For 15:137–139

    Google Scholar 

  • Dahdouh-Guebas F, De Bondt R, Abeysinghe PD et al (2004) Comparative study of the disjunct zonation pattern of the gray mangrove Avicennia marina (Forsk.) Vierh. in Gazi Bay (Kenya). Bull Mar Sci 74:237–252

    Google Scholar 

  • Enquist BJ, Brown JH, West GB (1998) Allometric scaling of plant energetics and population density. Nature 395:163–165

    Article  CAS  Google Scholar 

  • Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168(169):205–214

    Article  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • Feller IC, Lovelock CE, Piou C (2009) Growth and nutrient conservation in Rhizophora mangle in response to fertilization along latitudinal and tidal gradients. Smithson Contrib to Mar Sci 38:345–359

    Google Scholar 

  • Feller IC, Lovelock CE, Berger U et al (2010) Biocomplexity in mangrove ecosystems. Ann Rev Mar Sci 2:395–417

    Article  PubMed  CAS  Google Scholar 

  • Fromard F, Puig H, Mougin E et al (1998) Structure above-ground biomass and dynamics of mangrove ecosystems: new data from French Guiana. Oecologia 115:39–53

    Article  Google Scholar 

  • Gersani M, Brown JS, O’Brien EE et al (2001) Tragedy of the commons as a result of root competition. J Ecol 89:660–669

    Article  Google Scholar 

  • Gould SJ (1966) Allometry in size in ontogeny and phylogeny. Biol Rev 41:587–640

    Article  PubMed  CAS  Google Scholar 

  • He B, Lai T, Fan H et al (2007) Comparison of flooding-tolerance in four mangrove species in a diurnal tidal zone in the Beibu Gulf. Estuar Coast Shelf Sci 74:254–262

    Article  Google Scholar 

  • Hemery GE, Savill PS, Pryor SN (2005) Applications of the crown diameter–stem diameter relationship for different species of broadleaved trees. For Ecol Manag 215:285–294

    Article  Google Scholar 

  • Hernández-Trejo H, Priego-Santander, López-Portillo JA, Isunza-Vera E (2006) Los paisajes físico-geográficos de los manglares de la laguna de la Mancha, Veracruz México. Interciencia 31:211–219

    Google Scholar 

  • Hussain SA, Badola R (2008) Valuing mangrove ecosystem services: linking nutrient retention function of mangrove forests to enhanced agroecosystem production. Wetl Ecol Manag 16:441–450

    Article  CAS  Google Scholar 

  • Janzen DH (1985) Mangroves: where’s the understory? J Trop Ecol 1:89–92

    Article  Google Scholar 

  • Kairo JG, Bosire J, Langat J et al (2009) Allometry and biomass distribution in replanted mangrove plantations at Gazi Bay Kenya. Aquat Conserv Mar Freshw Ecosyst 19:S63–S69

    Article  Google Scholar 

  • Ketterings QM, Coe R, van Noordwijk M et al (2001) Reducing uncertainty in the use of allometric biomass equations for predicting above-ground tree biomass in mixed secondary forests. For Ecol Manag 146:199–209

    Article  Google Scholar 

  • Komiyama A, Poungparn S, Kato S (2005) Common allometric equations for estimating the tree weight of mangroves. J Trop Ecol 21:471–477

    Article  Google Scholar 

  • Komiyama A, Ong JE, Poungparn S (2008) Allometry, biomass, and productivity of mangrove forests: a review. Aquat Bot 89:128–137

    Article  Google Scholar 

  • Kramer H (1975) Herhöhung der Produktionssichereit zur Forderung einer nachaltigen Fichtenwirtschaft. Forstarchiv 46:9–13

    Google Scholar 

  • Krishnamorthy P, Ranathunge K, Franke R et al (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230:119–134

    Article  Google Scholar 

  • Lara-Domínguez AL, Day JW, Yáñez-Arancibia A, Sáinz-Hernandez E (2006) A dynamic characterization of water flux through a tropical ephemeral inlet, La Mancha lagoon, Gulf of Mexico. In: Singh VP, Xu YJ (eds) Coastal hydrology and processes. Water Resources Publications LLC, Colorado, pp 413–422

    Google Scholar 

  • Lin Y, Berger U, Grimm V, Ji Q (2012) Differences between symmetric and asymmetric facilitation matter: exploring the interplay between modes of positive and negative plant interactions. J Ecol. doi:10.1111/j.1365-2745.2012.02019.x

    Google Scholar 

  • López-Portillo JA, Ezcurra E (1989) Response of three mangroves to salinity in two geoforms. Funct Ecol 3:355–361

    Article  Google Scholar 

  • López-Portillo JA, Ewers FW, Angeles G (2005) Sap salinity effects on xylem conductivity in two mangrove species. Plant Cell Environ 28:1285–1292

    Article  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

    PubMed  Google Scholar 

  • Lovelock CE, Feller IC, McKee KL, Thompson R (2005) Variation in mangrove forest structure and sediment characteristics in Bocas del Toro, Panama. Caribb J Sci 41:456–464

    Google Scholar 

  • Méndez-Alonzo R, Hernández-Trejo H, López-Portillo JA (2012) Salinity constrains size inequality and allometry in two contrasting mangrove habitats in the Gulf of Mexico. J Trop Ecol 28:171–179. doi:10.1017/S0266467412000016

    Article  Google Scholar 

  • Menezes M, Berger U, Worbes M (2003) Annual growth rings and long-term growth patterns of mangrove trees from the Bragança peninsula, North Brazil. Wetl Ecol Manag 11:233–242

    Article  Google Scholar 

  • Michailoff I (1943) Zahlenmäßiges verfahren für die Ausführung der bestandeshöhenkurven. Forstw Cbl u Thar Jahrb 6:273–279

    Google Scholar 

  • Minden V, Kleyer M (2011) Testing the effect-response framework: key response and effect traits determining above-ground biomass of salt marshes. J Veg Sci 22:387–401

    Article  Google Scholar 

  • Moretzsohn F, Sánchez-Chávez JA, Tunnell JW (2013) GulfBase: resource database for Gulf of Mexico research. http://www.gulfbase.org. Accessed 15 Mar 2013

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Naidoo G (1985) Effects of waterlogging and salinity on plant-water relations and on the accumulation of solutes in three mangrove species. Aquat Bot 22:133–143

    Article  Google Scholar 

  • Naidoo G (1987) Effects of salinity and nitrogen on growth and water relations in the mangrove Avicennia marina (Forsk) Vierh. New Phytol 107:317–325

    Article  Google Scholar 

  • Naidoo G, Willert DJ (1995) Diurnal gas exchange characteristics and water use efficiency of three salt-secreting mangroves at low and high salinities. Hydrobiologia 295:13–22

    Article  CAS  Google Scholar 

  • National Oceanic and Atmospheric Administration (NOAA) (2013) Historical hurricane tracks. http://maps.csc.noaa.gov/hurricanes. Accessed 5 Aug 2013

  • Navratil S, Brace LG, Sauder EA, Lux S (1994) Silvicultural and harvesting options to favor immature white spruce and aspen regeneration in boreal mixedwoods. Aspen Bibliogr. Paper 2077

  • Odum WC, McIvor CC, Smith TJ (1982) The ecology of the mangroves of south Florida: a community profile. p 144

  • Orzel S (2007) A comparative analysis of slenderness of the main tree species of the Niepolomice forest. Electron J polish Agric Univ 10:#13

  • Peters R, Vovides AG, Luna S, Grüters U, Berger U (2014) Changes in allometric relations of mangrove trees due to resource availability: a new mechanistic modeling approach. Ecol Model 283:53–61

    Article  Google Scholar 

  • Pezeshki SR, DeLaune RD, Meeder JF (1997) Carbon assimilation and biomass partitioning in Avicennia germinans and Rhizophora mangle seedlings in response to soil redox conditions. Environ Exp Bot 37:161–171

    Article  CAS  Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607

    Article  CAS  Google Scholar 

  • Poorter L, Bongers F, Sterck FJ, Woll H (2005) Beyond the regeneration phase: differentiation of height-light trajectories among tropical tree species. J Ecol 93:256–267

    Article  Google Scholar 

  • Popescu SC, Wynne RH, Nelson RF (2003) Measuring individual tree crown diameter with lidar and assessing its influence on estimating forest volume and biomass. Can J Remote Sens 29:564–577

    Article  Google Scholar 

  • Pretzsch H (2009) Forest dynamics growth and yield. Springer, Berlin

    Google Scholar 

  • Proisy C, Couteron P, Fromard F (2007) Predicting and mapping mangrove biomass from canopy grain analysis using Fourier-based textural ordination of IKONOS images. Remote Sens Environ 109:379–392

    Article  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for statistical computing

  • Rivera-Monroy VH, Twilley RR, Bone D et al (2004) A Conceptual framework to develop long-term ecological research and management objectives in the Wider Caribbean Region. Bioscience 54:843–856

    Article  Google Scholar 

  • Ross MS, Ruiz PL, Telesnicki GJ, Meeder JF (2001) Estimating above-ground biomass and production in mangrove communities of Biscayne National Park Florida (USA). Wetl Ecol Manag 9:27–37

    Article  Google Scholar 

  • Shannon MC, Grieve CM, Francois LE (1994) Whole plant response to salinity. In: Wilkinson RE (ed) Plant-environment interactions. Dekker, New York, pp 199–244

    Google Scholar 

  • Sherman RE, Fahey TJ, Martinez P (2003) Spatial patterns of biomass and aboveground net primary productivity in a mangrove ecosystem in the Dominican Republic. Ecosystems 6:384–398

    Article  Google Scholar 

  • Shimano K (1997) Analysis of the relationship between DBH and crown projection area using a new model. J For Res 2:237–242

    Article  Google Scholar 

  • Smith TJ, Whelan KRT (2006) Development of allometric relations for three mangrove species in South Florida for use in the Greater Everglades Ecosystem restoration. Wetl Ecol Manag 14:409–419

    Article  Google Scholar 

  • Soares MLG, Schaeffer-Novelli Y (2005) Above-ground biomass of mangrove species I. Analysis of models. Estuar Coast Shelf Sci 65:1–18

    Article  Google Scholar 

  • Sobrado MA (2006) Differential leaf gas exchange responses to salinity and drought in the mangrove tree Avicennia germinans (Avicenniaceae). Rev Biol Trop 54:371–375

    Article  PubMed  CAS  Google Scholar 

  • Sobrado MA, Ball MC (1999) Light use in relation to carbon gain in the mangrove Avicennia marina under hypersaline conditions. Aust J Plant Physiol 26:245–251

    Article  CAS  Google Scholar 

  • Thom BG (1967) Mangrove ecology and deltaic geomorphology: Tabasco Mexico. J Ecol 55:301–343

    Article  Google Scholar 

  • Thomas SC (1996) Asymptotic height as a predictor of growth and allometric characteristics in Malaysian rain forest trees. Am J Bot 83:556–566

    Article  Google Scholar 

  • Tomlinson PB (1987) Architecture of tropical plants. Annu Rev Ecol Syst 18:1–21

    Article  Google Scholar 

  • Tuffers A, Naidoo G, Willert DJ (2001) Low salinities adversely affect photosynthetic performance of the mangrove Avicennia marina. Wetl Ecol Manag 9:225–232

    Article  CAS  Google Scholar 

  • Vieilledent G, Vaudry R, Andriamanohisoa SFD et al (2012) A universal approach to estimate biomass and carbon stock in tropical forests using generic allometric models. Ecol Appl 22:572–583

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Titus SJ, LeMay VM (1998) Relationships between tree slenderness coefficients and tree or stand characteristics for major species in boreal mixedwood forests. Can J For Res 28:1171–1183

    Article  Google Scholar 

  • Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215

    Article  Google Scholar 

  • Weiner J, Thomas SC (1992) Competition and allometry in three species of annual plants. Ecology 73:648–656

    Article  Google Scholar 

  • West PW (2009) Tree and Forest Measurement, 2d edn. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Yañez-Espinosa L, Flores J (2011) A review of sea-level rise effect on mangrove forest species: anatomical and morphological modifications. In: Casalegno S (ed) Global warming impacts: case study on the economy, human health and on urban and natural environments, pp 253–276. ISBN: 978-953-307-785-7

  • Zeide B (1987) Analysis of the 3/2 power law of self-thinning. For Sci 33:517–537

    Google Scholar 

Download references

Author contribution statement

Alejandra G. Vovides: Wrote the paper and was responsible for database management. Contributed in choosing and executing statistical analyses. Juliane Vogt and Uwe Grueters: Field sampling strategies, discussions on manuscript editing, manuscript revisions and contribution in choosing statistical methods. Uta Berger and Jorge López-Portillo: Contributed to designing project, advised on lines of research, data analyses, and manuscript revision. Funding of the study through the CREC project. Armin Kollert: Collected part of the data during the development of his master’s thesis. The data analysis concerning Michailoff (1943) and Thomas (1996) was the main contribution of this co-author to this manuscript. Ronny Peters: Comments and suggestions on trends and ideas concerning data analyses. Ana Laura Lara-Domínguez: Contributed with new salinity data from 2013, suggestions on data analyses and contributed with comments on morphological plasticity.

Acknowledgments

We are grateful to Victor Vasquez from the Institute of Ecology in México (INECOL, A.C.) for his field assistance and tireless devotion to mangrove ecology research and to Andreas Tharang for his valuable methodological expertise on data analysis. This study is a result of the close collaboration between the INECOL and the Technische Universität Dresden through their joint project “Coastal Research Network on Environmental Changes” (CREC), funded by the European Commission to support international cooperation through its 7th Framework Programme. The CREC project is classified as a Marie Curie Action (FP7-PEOPLE-2009-IRSES). The project was also partially supported by the German Research Foundation (DFG, Project Number BE-1960/7-1).

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alejandra G. Vovides.

Additional information

Communicated by C. Lovelock.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vovides, A.G., Vogt, J., Kollert, A. et al. Morphological plasticity in mangrove trees: salinity-related changes in the allometry of Avicennia germinans . Trees 28, 1413–1425 (2014). https://doi.org/10.1007/s00468-014-1044-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1044-8

Keywords

Navigation