Rhizophora mangle and Laguncularia racemosa cooccur along many intertidal floodplains in the Neotropics. Their patterns of dominance shift along various gradients, coincident with salinity, soil fertility, and tidal flooding. We used leaf gas exchange metrics to investigate the strategies of these two species in mixed culture to simulate competition under different salinity concentrations and hydroperiods. Semidiurnal tidal and permanent flooding hydroperiods at two constant salinity regimes (10？g？L？1 and 40？g？L？1) were simulated over 10 months. Assimilation ( ), stomatal conductance ( ), intercellular CO2 concentration ( ), instantaneous photosynthetic water use efficiency (PWUE), and photosynthetic nitrogen use efficiency (PNUE) were determined at the leaf level for both species over two time periods. Rhizophora mangle had significantly higher PWUE than did L. racemosa seedlings at low salinities; however, L. racemosa had higher PNUE and and, accordingly, had greater intercellular CO2 (calculated) during measurements. Both species maintained similar capacities for A at 10 and 40？g？L？1 salinity and during both permanent and tidal hydroperiod treatments. Hydroperiod alone had no detectable effect on leaf gas exchange. However, PWUE increased and PNUE decreased for both species at 40？g？L？1 salinity compared to 10？g？L？1. At 40？g？L？1 salinity, PNUE was higher for L. racemosa than R. mangle with tidal flooding. These treatments indicated that salinity influences gas exchange efficiency, might affect how gases are apportioned intercellularly, and accentuates different strategies for distributing leaf nitrogen to photosynthesis for these two species while growing competitively. 1. Introduction Mangroves are forested wetland habitats characterized by individual tree species that can segregate along rather diffuse environmental gradients. Salinity and hydroperiod (i.e., frequency, depth, and duration of flooding) are considered two of the more important factors that control the local distribution of mangrove species [1–5], and both factors have the potential to interact strongly along spatial and temporal scales in many floodplains [6–9]. Indeed, interactions between salinity and hydroperiod have been implicated in the regulation of survival, growth, physiological proficiency, and zonation of individual seedlings, saplings, and trees that colonize mangrove wetlands [10, 11]. Through repetitive experimentation, we are progressively gaining a better understanding of the interactive nature of these environmental drivers on seedling establishment and competitive
References
[1]
J. G. Watson, “Mangrove forests of the Malay Peninsula,” Malayan Forest Records, vol. 6, pp. 1–275, 1928.
[2]
W. Macnae, “A general account of the flora and fauna of mangrove swamps and forest of the Indo-West Pacific region,” Advances in Marine Biology, vol. 6, pp. 73–270, 1969.
[3]
A. E. Lugo and S. C. Snedaker, “The ecology of mangroves,” Annual Review of Ecology and Systematics, vol. 5, pp. 39–64, 1974.
[4]
P. B. Tomlinson, The Botany of Mangroves, Cambridge University Press, Cambridge, UK, 1986.
[5]
P. A. Hutchings and P. Saenger, Ecology of Mangroves, University of Queensland Press, St. Lucia, Australia, 1987.
[6]
V. J. Chapman, Mangrove Vegetation, Lubrecht and Cramer, Vaduz, Liechtenstein, 1976.
[7]
A. E. Lugo, “Mangrove ecosystems: successional or steady state?” Biotropica, vol. 12, pp. 65–72, 1980.
[8]
R. R. Twilley, “Mangrove wetlands,” in Southern Forested Wetlands Ecology and Management, M. G. Messina and W. H. Conner, Eds., pp. 445–473, Lewis Publishers, Boca Raton, Fla, USA, 1998.
[9]
D. M. Alongi, The Energetics of Mangrove Forests, Springer, New York, NY, USA, 2009.
[10]
M. C. Ball, “Ecophysiology of mangroves,” Trees, vol. 2, no. 3, pp. 129–142, 1988.
[11]
N. C. Duke, M. C. Ball, and J. C. Ellison, “Factors influencing biodiversity and distributional gradients in mangroves,” Global Ecology and Biogeography Letters, vol. 7, no. 1, pp. 27–47, 1998.
[12]
K. W. Krauss, C. E. Lovelock, K. L. McKee, L. López-Hoffman, S. M. L. Ewe, and W. P. Sousa, “Environmental drivers in mangrove establishment and early development: a review,” Aquatic Botany, vol. 89, no. 2, pp. 105–127, 2008.
[13]
W. E. Odum, C. C. McIvor, T. J. Smith III, et al., “The Ecology of the Mangroves of South Florida: A Community Profile,” Tech. Rep. FWS/OBS-81/24, U.S. Fish and Wildlife Service, Office of Biological Service, Washington, DC, USA, 1982.
[14]
Y. Schaeffer-Novelli, G. Cintrón-Molero, R. R. Adaime, and T. M. de Camargo, “Variability of mangrove ecosystems along the Brazilian coast,” Estuaries, vol. 13, no. 2, pp. 204–218, 1990.
[15]
P. Delgado, P. F. Hensel, J. A. Jiménez, and J. W. Day Jr., “The importance of propagule establishment and physical factors in mangrove distributional patterns in a Costa Rican estuary,” Aquatic Botany, vol. 71, no. 3, pp. 157–178, 2001.
[16]
E. J. Farnsworth and A. M. Ellison, “Sun-shade adaptability of the red mangrove, Rhizophora mangle (Rhizophoraceae): changes through ontogeny at several levels of biological organization,” American Journal of Botany, vol. 83, no. 9, pp. 1131–1143, 1996.
[17]
M. S. Koch, Resource Availability and Abiotic Effects on Rhizophora mangle L. (Red Mangrove) Development in South Florida [Ph.D. dissertation], University of Miami, 1996.
[18]
C. E. Lovelock and I. C. Feller, “Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest,” Oecologia, vol. 134, no. 4, pp. 455–462, 2003.
[19]
J. H. Davis, The Ecology and Geologic Role of Mangroves in Florida, vol. 32, Publication no. 517, Papers from Tortugas Lab, Carnegie Institute of Washington, pp. 304–412, 1940.
[20]
G. Cintrón, A. E. Lugo, D. J. Pool, and G. Morris, “Mangroves of arid environments in Puerto Rico and adjacent islands,” Biotropica, vol. 10, pp. 110–121, 1978.
[21]
K. L. McKee, “Soil physicochemical patterns and mangrove species distribution—reciprocal effects?” Journal of Ecology, vol. 81, no. 3, pp. 477–487, 1993.
[22]
R. Chen and R. R. Twilley, “Patterns of mangrove forest structure and soil nutrient dynamics along the Shark River estuary, Florida,” Estuaries, vol. 22, no. 4, pp. 955–970, 1999.
[23]
K. W. Krauss, T. W. Doyle, R. R. Twilley, V. H. Rivera-Monroy, and J. K. Sullivan, “Evaluating the relative contributions of hydroperiod and soil fertility on growth of south Florida mangroves,” Hydrobiologia, vol. 569, no. 1, pp. 311–324, 2006.
[24]
R. Chen and R. R. Twilley, “A gap dynamic model of mangrove forest development along gradients of soil salinity and nutrient resources,” Journal of Ecology, vol. 86, no. 1, pp. 37–51, 1998.
[25]
R. E. Sherman, T. J. Fahey, and R. W. Howarth, “Soil-plant interactions in a neotropical mangrove forest: iron, phosphorus and sulfur dynamics,” Oecologia, vol. 115, no. 4, pp. 553–563, 1998.
[26]
I. C. Feller, K. L. McKee, D. F. Whigham, and J. P. O'Neill, “Nitrogen versus phosphorus limitation across an ecotonal gradient in a mangrove forest,” Biogeochemistry, vol. 62, no. 2, pp. 145–175, 2003.
[27]
H. A. Mooney and S. L. Gulmon, “The determinants of plant productivity-natural versus man-modified communities,” in Disturbance and Ecosystems, H. A. Mooney and M. Gordon, Eds., pp. 146–158, Springer, New York, NY, USA, 1983.
[28]
M. C. Ball and J. B. Passioura, “Carbon gain in relation to water use: photosynthesis in mangroves,” in Ecophysiology of Photosynthesis, E.-D. Schulze and M. M. Caldwell, Eds., pp. 247–259, Springer, New York, NY, USA, 1994.
[29]
M. C. Ball, “Comparative ecophysiology of mangrove forests and tropical lowland moist rainforest,” in Tropical Forest Plant Ecophysiology, S. S. Mulkey, R. L. Chazdon, and A. P. Smith, Eds., pp. 461–496, Chapman and Hall, New York, NY, USA, 1996.
[30]
K. W. Krauss and J. A. Allen, “Influences of salinity and shade on seedling photosynthesis and growth of two mangrove species, Rhizophora mangle and Bruguiera sexangula, introduced to Hawaii,” Aquatic Botany, vol. 77, no. 4, pp. 311–324, 2003.
[31]
K. W. Krauss, R. R. Twilley, T. W. Doyle, and E. S. Gardiner, “Leaf gas exchange characteristics of three neotropical mangrove species in response to varying hydroperiod,” Tree Physiology, vol. 26, no. 7, pp. 959–968, 2006.
[32]
P. Cardona-Olarte, R. R. Twilley, K. W. Krauss, and V. Rivera-Monroy, “Responses of neotropical mangrove seedlings grown in monoculture and mixed culture under treatments of hydroperiod and salinity,” Hydrobiologia, vol. 569, no. 1, pp. 325–341, 2006.
[33]
G. Lin and L. D. S. L. Sternberg, “Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L,” Oecologia, vol. 90, no. 3, pp. 399–403, 1992.
[34]
G. Lin and L. Da S. L. Sternberg, “Effects of salinity fluctuation on photosynthetic gas exchange and plant growth of the red mangrove (Rhizophora mangle L.),” Journal of Experimental Botany, vol. 44, no. 1, pp. 9–16, 1993.
[35]
E. J. Farnsworth, A. M. Ellison, and W. K. Gong, “Elevated CO2 alters anatomy, physiology, growth, and reproduction of red mangrove (Rhizophora mangle L.),” Oecologia, vol. 108, no. 4, pp. 599–609, 1996.
[36]
G. Lin and L. da S.L. Sternberg, “Differences in morphology, carbon isotope ratios, and photosynthesis between scrub and fringe mangroves in Florida, USA,” Aquatic Botany, vol. 42, no. 4, pp. 303–313, 1992.
[37]
G. L. Guanghui Lin and L. D. S. L. Sternberg, “Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.),” Australian Journal of Plant Physiology, vol. 19, no. 5, pp. 509–517, 1992.
[38]
S. C. Snedaker and R. J. Araújo, “Stomatal conductance and gas exchange in four species of Caribbean mangroves exposed to ambient and increased CO2,” Marine and Freshwater Research, vol. 49, no. 4, pp. 325–327, 1998.
[39]
T. J. Andrews, B. F. Clough, and G. J. Muller, “Photosynthesis gas exchange properties and carbon isotope ratios of some mangroves in North Queensland,” in Physiology and Management of Mangroves, H. J. Teas, Ed., pp. 15–23, W. Junk Publishers, The Hague, The Netherlands, 1984.
[40]
H. A. Mooney and S. L. Gulmon, “Environmental and evolutionary constraints on the photosynthetic characteristics of higher plants,” in Topics in Plant Population Biology, O. T. Solbrig, S. Jain, G. B. Johnson, and P. H. Raven, Eds., pp. 316–374, Columbia University Press, New York, NY, USA, 1979.
[41]
S. von Caemmerer and G. D. Farquhar, “Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves,” Planta, vol. 153, no. 4, pp. 376–387, 1981.
[42]
G. D. Farquhar and T. D. Sharkey, “Stomatal conductance and photosynthesis,” Annual Review of Plant Physiology, vol. 33, pp. 317–345, 1982.
[43]
J. A. Berry and W. J. Downtown, “Environmental regulation of photosynthesis,” in Photosynthesis: Development, Carbon Metabolism and Plant Productivity, D. E. Buetow, G. M. Padilla, I. L. Cameron, and A. M. Zimmerman, Eds., pp. 263–343, Academic Press, New York, NY, USA, 1982.
[44]
W. Wang, Z. Yan, S. You, Y. Zhang, L. Chen, and G. Lin, “Mangroves: obligate or facultative halophytes? A review,” Trees Structure and Function, vol. 25, no. 6, pp. 953–963, 2011.
[45]
K. W. Krauss and M. C. Ball, “On the halophytic nature of mangroves,” Trees Structure and Function, vol. 27, pp. 7–11, 2013.
[46]
U. Zimmermann, J. J. Zhu, F. C. Meinzer et al., “High molecular weight organic compounds in the xylem sap of mangroves: implications for long-distance water transport,” Botanica Acta, vol. 107, no. 4, pp. 218–229, 1994.
[47]
K. W. Krauss, K. L. McKee, and M. W. Hester, “Water use characteristics of black mangrove (Avicennia germinans) communities along an ecotone with marsh at a northern geographic limit,” Ecohydrology, 2013.
[48]
K. W. Krauss, P. J. Young, J. L. Chambers, T. W. Doyle, and R. R. Twilley, “Sap flow characteristics of neotropical mangroves in flooded and drained soils,” Tree Physiology, vol. 27, no. 5, pp. 775–783, 2007.
[49]
M. C. Ball and G. D. Farquhar, “Photosynthetic and stomatal responses of two mangrove species, Aegiceras corniculatum and Avicennia marina, to long term-salinity and humidity conditions,” Plant Physiology, vol. 74, pp. 1–6, 1984.
[50]
M. C. Ball, “Salinity tolerance in the mangroves Aegiceras corniculatum and Avicennia marina—I. Water use in relation to growth, carbon partitioning, and salt balance,” Australian Journal of Plant Physiology, vol. 15, no. 3, pp. 447–464, 1988.
[51]
B. F. Clough and R. G. Sim, “Changes in gas exchange characteristics and water use efficiency of mangroves in response to salinity and vapour pressure deficit,” Oecologia, vol. 79, no. 1, pp. 38–44, 1989.
[52]
R. Reef, I. C. Feller, and C. E. Lovelock, “Nutrition of mangroves,” Tree Physiology, vol. 30, no. 9, pp. 1148–1160, 2010.
[53]
R. Chen and R. R. Twilley, “A simulation model of organic matter and nutrient accumulation in mangrove wetland soils,” Biogeochemistry, vol. 44, no. 1, pp. 93–118, 1999.
[54]
S. R. Pezeshki, “Plant response to flooding,” in Plant-Environment Interactions, R. E. Wilkinson, Ed., pp. 289–321, Marcel Dekker, New York, NY, USA, 1994.
[55]
T. T. Kozlowski, “Plant responses to flooding of soil,” BioScience, vol. 34, pp. 162–167, 1984.
[56]
T. T. Kozlowski, “Responses of woody plants to flooding and salinity,” Tree Physiology Monographs, vol. 1, pp. 1–29, 1997.
[57]
G. Naidoo, “Effects of flooding on leaf water potential and stomatal resistance in Bruguiera gymnorrhiza (L.) Lam,” New Phytologist, vol. 93, pp. 369–376, 1983.
[58]
G. Naidoo, “Effects of waterlogging and salinity on plant-water relations and on the accumulation of solutes in three mangrove species,” Aquatic Botany, vol. 22, no. 2, pp. 133–143, 1985.
[59]
S. R. Pezeshki, R. D. DeLaune, and J. F. Meeder, “Carbon assimilation and biomass partitioning in Avicennia germinans and Rhizophora mangle seedlings in response to soil redox conditions,” Environmental and Experimental Botany, vol. 37, no. 2-3, pp. 161–171, 1997.
[60]
S. R. Pezeshki, R. D. Delaune, and W. H. Patrick Jr., “Differential response of selected mangroves to soil flooding and salinity: gas exchange and biomass partitioning,” Canadian Journal of Forest Research, vol. 20, no. 7, pp. 869–874, 1990.
[61]
Y. Ye, N. F. Y. Tam, Y. S. Wong, and C. Y. Lu, “Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging,” Environmental and Experimental Botany, vol. 49, no. 3, pp. 209–221, 2003.
[62]
Y. Ye, N. F. Y. Tam, Y. S. Wong, and C. Y. Lu, “Does sea level rise influence propagule establishment, early growth and physiology of Kandelia candel and Bruguiera gymnorrhiza?” Journal of Experimental Marine Biology and Ecology, vol. 306, no. 2, pp. 197–215, 2004.
[63]
K. G. Boto and J. T. Wellington, “Soil characteristics and nutrient status in a Northern Australian mangrove forest,” Estuaries, vol. 7, no. 1, pp. 61–69, 1984.
[64]
K. L. McKee, I. A. Mendelssohn, and M. W. Hester, “Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans,” American Journal of Botany, vol. 75, pp. 1352–1359, 1988.
[65]
K. C. Ewel, J. A. Bourgeois, T. G. Cole, and S. Zheng, “Variation in environmental characteristics and vegetation in high-rainfall mangrove forests, Kosrae, Micronesia,” Global Ecology and Biogeography Letters, vol. 7, no. 1, pp. 49–56, 1998.
[66]
G. Naidoo, “Factors contributing to dwarfing in the mangrove Avicennia manna,” Annals of Botany, vol. 97, no. 6, pp. 1095–1101, 2006.
[67]
K. L. McKee, I. C. Feller, M. Popp, and W. Wanek, “Mangrove isotopic (δ15N and δ13C) fractionation across a nitrogen versus phosphorus limitation gradient,” Ecology, vol. 83, no. 4, pp. 1065–1075, 2002.
