Phenology and floral synchrony of Rhizophora mangle along a natural salinity gradient

Rhizophora mangle is the most common species of mangrove within its range and a major component of coastal ecosystems in the tropics and subtropics. Its phenology is affected by seasonal variations in temperature, salinity, and precipitation, all of which may be altered by impending climate change. In this work, the monthly leaf, flower, and fruit phenology of R. mangle was assessed at three sites, along a natural salinity gradient for 12 months. We assessed phenological states using litter traps installed in mangrove stands, and by direct observation of leaf production at two sites, and flower, and fruit production at a single site. Phenological events were compared with seasonal climatic variations (in wind, rain, and temperature) to explore potential abiotic controls on the phenology of this species. Leaf shedding was lowest at the low salinity site. Leaf and stipule production showed a seasonal trend, decreasing during the cool and dry winter months. Flowering was highly seasonal and synchronous and peaked during the rainy season. Flowering was correlated with average temperature (r = 0.82; p < 0.05) at all three study sites, but was not correlated with precipitation. At the high‐salinity site, flowering was restricted to the rainy season. Fruit abortion was associated with wind speed (r = 0.79; p < 0.05). Flowering of R. mangle is induced by increasing temperatures and the onset of rains. Rising temperatures, drier summers, and more frequent and intense storms, due to climate change, may influence mangrove productivity, population dynamics, and floral synchrony.     

Polymorphic microsatellites in a mangrove species,Rhizophora mangle L. (Rhizophoraceae)

Twenty‐six microsatellite loci were isolated and characterized from the mangrove species Rhizophora mangle using (GT)_n and (CT)_n repeats. Eighty‐four per cent of the clones contained microsatellite sequences; the most common dinucleotides were the (GA/CT) and (CA/GT) repeats. Ten primers were selected to investigate the polymorphism among individuals of R. mangle from two natural populations of the Colombian Pacific Coast. The observed heterozygosity per locus varied from 0.20 to 0.80, the power of discrimination was 0.32–0.84 and the power of exclusion was 0.03–0.75. This set of microsatellites offers an efficient tool for population genetics studies on this species.     

Resistance of red mangrove (Rhizophora mangle L.) seedlings to deflection and extraction

Red mangrove (Rhizhophora mangle L.) is the dominant tree species in the intertidal zone of ecosystems on the Atlantic shores of the Caribbean and tropical western Atlantic. The propagules of this species are initially buoyant, becoming negatively buoyant before rooting in a variety of substrates. After establishment, these seedlings form aerial roots, leading to communities of plants with complex networks of stems and aerial roots. While established mangrove communities assist in stabilizing coastlines, seedlings are susceptible to wave, current and wind energy and this limits the habitats that they can successfully colonize. In this experiment, the mechanical resistance of seedlings growing at five locations with different substrate and canopy conditions was tested. The 78 seedlings tested ranged in height from 27 to 47 cm, had between one and ten pairs of leaves but had not yet formed aerial roots. Seedlings were pulled horizontally. The reaction force at 20° deflection in four cardinal directions and then force to failure in the landward direction was measured. Seventy-five percent of the seedlings failed in the root system. The remainder failed near the base of the stem. Larger seedlings were more likely to fail at the roots. Seedlings growing outside of mangrove overstory on coral rubble were 3.5 times more strongly anchored than those growing within the mangrove overstory on sand. In spite of directional loading by waves and on-shore breezes, the deflection resistance did not vary systematically with pulling direction. Seedling anchorage varies among locations with different overstory and substrate conditions, likely due to differences in competition and acclimation to wind and wave energy along with differences in rooting among substrates.     

Isolation and characterization of microsatellite loci in the red mangrove Rhizophora mangle (Rhizophoraceae) and its related species

Fourteen microsatellite markers were isolated from the red mangrove Rhizophora mangle (Rhizophoraceae), a widely distributed mangrove plant in the New World and West Africa. The range of expected heterozygosity of these markers was 0.000–0.672 in the two populations of R. mangle. Cross-species testing was examined for five other species of Rhizophora, and Kandelia candel and Bruguiera gymnorrhiza. All 14 markers could be amplified in R. samoensis, thirteen in R. racemosa, and six markers in all other species of Rhizophora. Our findings greatly increase the utility of these markers.     

Genetic and morphological variation of Rhizophora mangle (red mangrove) along the northern Pacific coast of Nicaragua

Red mangrove (Rhizophora mangle) dominates in tidally active areas of neotropical mangrove forests. Despite the ecological and economic importance of this species, we still know little about the genetic structure and diversity of its natural populations. In particular, Nicaraguan populations have not yet been investigated although they could be important for a better understanding of the evolutionary history of R. mangle in Mesoamerica. The aim of this study was to estimate the genetic and morphological variability of 4 populations sampled along the northwestern coast of Nicaragua. Microsatellite analysis showed higher levels of allelic diversity (30 alleles and a mean number of allele per locus per population = 6.42) than reported for the same species in other sites of tropical America. This variability could be attributed to the existence of a glacial refugium in the studied area and/or to repeated introgression among closely related species. Analysis of molecular variance (AMOVA) revealed that there was little but significant variation among the sampled sites suggesting that the studied populations cannot be considered as a single panmictic group, although they are closely related. This result was confirmed by the Bayesian analysis and UPGMA dendrogram showing three genetically distinct clusters. Bayesian analysis of migration rates showed that propagule dispersion associated with marine currents is an important factor shaping the observed genetic structure. The scatterplot from discriminant analysis indicated significant phenotypic differences between two groups, mainly related to specific leaf area variation. The morphological similarity between PR and PO was consistent with the results of molecular analysis, supporting the common origin of these two populations. Nevertheless, we did not find a significant statistical correlation between microsatellite and morphological data. In conclusion, the results reported here contribute to a better understanding of R. mangle genetic structure and would provide baseline information to guide land managers in implementing conservation initiatives in Nicaragua.     

Tension wood fibers are related to gravitropic movement of red mangrove (Rhizophora mangle) seedlings

Freshly collected viviparous seedlings (propagules) were collected from wild plants of Rhizophora mangle and planted in vertical or horizontal positions. A total of 80 seedlings were examined anatomically at various ages and orientations. After rooting, seedlings reoriented from horizontal to vertical by extreme bending in the hook region of the hypocotyl directly above the basal 1 cm where roots formed. Hypocotyl bending occurred over many months. Trends in position and relative abundance of tension fibers (also called gelatinous fibers) over time were followed. The erection of the seedling was related to increased secondary xylem and the number of tension wood fibers on the upper side of the hook region. However, linear regressions had low coefficient of determination (r ²) values, presumably related to seedlings with high variability. Received: June 18, 2001 / Accepted: October 2, 2001     

Tension wood fibers are related to gravitropic movement of red mangrove (Rhizophora mangle) seedlings

Freshly collected viviparous seedlings (propagules) were collected from wild plants of Rhizophora mangle and planted in vertical or horizontal positions. A total of 80 seedlings were examined anatomically at various ages and orientations. After rooting, seedlings reoriented from horizontal to vertical by extreme bending in the hook region of the hypocotyl directly above the basal 1 cm where roots formed. Hypocotyl bending occurred over many months. Trends in position and relative abundance of tension fibers (also called gelatinous fibers) over time were followed. The erection of the seedling was related to increased secondary xylem and the number of tension wood fibers on the upper side of the hook region. However, linear regressions had low coefficient of determination (r(2)) values, presumably related to seedlings with high variability.     

Photosynthetic characteristics of dwarf and fringe Rhizophora mangle L. in a Belizean mangrove

Twin Cays (Belize) is a highly oligotrophic mangrove archipelago dominated by Rhizophora mangle L. Ocean‐fringing trees are 3–7 m tall with a leaf area index (LAI) of 2.3, whereas in the interior, dwarf zone, trees are 1.5 m or less, and the LAI is 0.7. P‐fertilization of dwarf trees dramatically increases growth. As a partial explanation of these characteristics, it was hypothesized that differences in stature and growth rates would reflect differences in leaf photosynthetic capacity, as determined by the photochemical and biochemical characteristics at the chloroplast level. Gas exchange and chlorophyll fluorescence were used to compare photosynthesis of dwarf, fringe and fertilized trees. Regardless of zonation or treatment, net CO₂ exchange (A) and photosynthetic electron transport were light saturated at less than 500 µmol photons m^?2 s^?1, and low‐light quantum efficiencies were typical for healthy C₃ plants. On the other hand, light‐saturated A was linearly related to stomatal conductance (g_s), with seasonal, zonal and treatment differences in photosynthesis corresponding linearly to differences in the mean g_s. Overall, photosynthetic capacity appeared to be co‐regulated with stomatal conductance, minimizing the variability of C_i at ambient CO₂ (and hence, C_i/C_a). Based on the results of in vitro assays, regulation of photosynthesis in R. mangle appeared to be accomplished, at least in part, by regulation of Rubisco activity.     

Influence of a salinity gradient on the vessel characters of the mangrove species Rhizophora mucronata

BACKGROUND AND AIMS: Although mangroves have been extensively studied, little is known about their ecological wood anatomy. This investigation examined the potential use of vessel density as a proxy for soil water salinity in the mangrove species Rhizophora mucronata (Rhizophoraceae) from Kenya. METHODS: In a time-standardized approach, 50 wood discs from trees growing in six salinity categories were investigated. Vessel densities, and tangential and radial diameters of rainy and dry season wood of one distinct year, at three positions on the stem discs, were measured. A repeated-measures ANOVA with the prevailing salinity was performed. KEY RESULTS: Vessel density showed a significant increase with salinity, supporting its use as a prospective measure of salinity. Interestingly, the negative salinity response of the radial diameter of vessels was less striking, and tangential diameter was constant under the varying environmental conditions. An effect of age or growth rate or the presence of vessel dimorphism could be excluded as the cause of the absence of any ecological trend. CONCLUSIONS: The clear trend in vessel density with salinity, together with the absence of a growth rate and age effect, validates the potential of vessel density as an environmental proxy. However, it can only be used as a relative measure of salinity given that other environmental variables such as inundation frequency have an additional influence on vessel density. With view to a reliable, absolute proxy, future research should focus on finding wood anatomical features correlated exclusively with soil water salinity or inundation frequency. The plasticity in vessel density with differing salinity suggests a role in the establishment of a safe water transport system. To confirm this hypothesis, the role of inter-vessel pits, their relationship to the rather constant vessel diameter and the underlying physiology and cell biology needs to be examined.     

Effect of environment and gibberellins on the early growth and development of the red mangrove, Rhizophora mangle L.

Seedlings of the red mangrove, Rhizophora mangle L., were subjected to a variety of salinity, light, and plant growth regulator treatments to examine the influence of these factors on early development. Stem, leaf, and root growth were significantly enhanced in both low salinity seawater and under reduced intensities of solar radiation. Semi-quantitative analyses of GAs by enzyme-linked immunoabsorbant assays (ELISA) suggest that under these conditions the early 3/13 hydroxylation GA₁ biosynthetic pathway is predominant in R. mangle. Concentrations of GA₁ and GA₁₉-like substances were highest in propagules exhibiting enhanced development. Attempts to identify the endogenous GAs by GC-MS were unsuccessful, most likely due to undetermined impurities present in mangroves. Exogenous applications of GA₃ to R. mangle were moderately successful in alleviating shoot growth inhibitions observed at higher salinities and light levels. The role of gibberellins is discussed in terms of metabolic responses to the external environment and possible impacts upon the distribution of this species.     

Biosorption of Pb2+ from aqueous solution by waste biomass of aerial roots of Rhizophora mangle (red mangrove)

The processing waste of the aerial roots of Rhizophora mangle was used in both its unmodified or mercaptoacetic acid (MAA) modified form for the sorption of Pb2+ from aqueous solution. The biomass rapidly and strongly sorbed Pb2+ at pH 5.0, which indicated chemisorption. A significant increase in Pb2+ sorption resulted from MAA treatment of the biomass, indicating that sorption occurs through an ion-exchange process. From sorption-capacity experiments, the unmodified and modified materials extracted, at pH 5, 31.3 and 85.5 mg of Pb2+ per gram of biomass, respectively, from aqueous solutions. Our studies may contribute to an innovative method for the economical and ecologically save removal and recovery of heavy-atom metal ions from contaminated waters through biosorption.     

Sun-shade adaptability of the red mangrove,Rhizophora mangle (Rhizophoraceae): Changes through ontogeny at several levels of biological organization

Rhizophora mangle L., the predominant neotropical mangrove species, occupies a gradient from low intertidal swamp margins with high insolation, to shaded sites at highest high water. Across a light gradient, R. mangle shows properties of both “light-demanding” and “shade-tolerant” species, and defies designation according to existing successional paradigms for rain forest trees. The mode and magnitude of its adaptability to light also change through ontogeny as it grows into the canopy. We characterized and compared phenotypic flexibility of R. mangle seedlings, saplings, and tree modules across changing light environments, from the level of leaf anatomy and photosynthesis, through stem and whole-plant architecture. We also examined growth and mortality differences among sun and shade populations of seedlings over 3 yr. Sun and shade seedling populations diverged in terms of four of six leaf anatomy traits (relative thickness of tissue layers and stomatal density), as well as leaf size and shape, specific leaf area (SLA), leaf internode distances, disparity in blade–petiole angles, canopy spread: height ratios, standing leaf numbers, summer (July) photosynthetic light curve shapes, and growth rates. Saplings showed significant sun/shade differences in fewer characters: leaf thickness, SLA, leaf overlap, disparity in bladepetiole angles, standing leaf numbers, stem volume and branching angle (first-order branches only), and summer photosynthesis. In trees, leaf anatomy was insensitive to light environment, but leaf length, width, and SLA, disparities in bladepetiole angles, and summer maximal photosynthetic rates varied among sun and shade leaf populations. Seedling and sapling photosynthetic rates were significantly depressed in winter (December), while photosynthetic rates in tree leaves did not differ in winter and summer. Seasonal and ontogenetic changes in response to light environment are apparent at several levels of biological organization in R. mangle, within constraints of its architectural baiiplan. Such variation has implications for models of stand carbon gain, and suggest that response flexibility may change with plant age.     

Colonization of a dynamic substrate: factors influencing recruitment of the wood-boring isopod, Sphaeroma terebrans, onto red mangrove (Rhizophora mangle) prop roots.

The isopod Sphaeroma terebrans, which bores into the prop roots of the red mangrove, Rhizophora mangle, can cause death and subsequent breakage of the inhabited root and, debatably, may reduce the support system of the tree. We examined whether different characteristics of a root or its physical setting, both of which may relate to habitat quality, influence the colonization of S. terebrans. A series of in situ experimental manipulations were conducted over 2 years. The first experimental protocol examined colonization of intact root substratum. Free-hanging aerial prop roots which were previously unsubmerged were bent down and anchored underwater at high tide after which the colonization of S. terebrans was monitored. A second manipulation was performed to evaluate the relative roles of submergence depth and plant anatomy in isopod colonization preference. Detached aerial prop roots were oriented either with the root tip directed downward, or upside down with the root tip directed upward but at a constant water depth. Additionally, detached aerial prop roots were oriented so that their tips were in contact with the sediment surface in order to investigate whether colonization on grounded roots was prevented by benthic predators. For all experiments, colonization began within 24 h; juveniles were the predominant colonizers. The submergence depth of a prop root, a characteristic of a root's physical setting, was consistently the strongest component correlated with the abundance of colonizing S. terebrans. The root-quality feature of root diameter was also found to play a significant role in colonization. Biotic influences, such as predation, however, did not influence recruitment of the isopod onto a root. Additionally, the absence of burrowing on grounded roots appeared to be related to intrinsic plant features. Along a root there was a strong preference by S. terebrans to colonize the root tip region (i.e., youngest part of the root) especially when these roots were also the deepest. The results of our experimental manipulation using natural root substratum are the first to identify physical setting as an important feature of habitat suitability for S. terebrans.     

Elevated CO2 alters anatomy,physiology, growth,and reproduction of red mangrove (Rhizophora mangle L.)

Mangroves, woody halophytes restricted to protected tropical coasts, form some of the most productive ecosystems in the world, but their capacity to act as a carbon source or sink under climate change is unknown. Their ability to adjust growth or to function as potential carbon sinks under conditions of rising atmospheric CO₂ during global change may affect global carbon cycling, but as yet has not been investigated experimentally. Halophyte responses to CO₂ doubling may be constrained by the need to use carbon conservatively under water-limited conditions, but data are lacking to issue general predictions. We describe the growth, architecture, biomass allocation, anatomy, and photosynthetic physiology of the predominant neotropical mangrove tree, Rhizophora mangle L., grown solitarily in ambient (350 ll^–1) and double-ambient (700 ll^–1) CO₂ concentrations for over 1 year. Mangrove seedlings exhibited significantly increased biomass, total stem length, branching activity, and total leaf area in elevated CO₂. Enhanced total plant biomass under high CO₂ was associated with higher root:shoot ratios, relative growth rates, and net assimilation rates, but few allometric shifts were attributable to CO₂ treatment independent of plant size. Maximal photosynthetic rates were enhanced among high-CO₂ plants while stomatal conductances were lower, but the magnitude of the treatment difference declined over time, and high-CO₂ seedlings showed a lower P_max at 700 ll^–1 CO₂ than low-CO₂ plants transferred to 700 ll^–1 CO₂: possible evidence of downregulation. The relative thicknesses of leaf cell layers were not affected by treatment. Stomatal density decreased as epidermal cells enlarged in elevated CO₂. Foliar chlorophyll, nitrogen, and sodium concentrations were lower in high CO₂. Mangroves grown in high CO₂ were reproductive after only 1 year of growth (fully 2 years before they typically reproduce in the field), produced aerial roots, and showed extensive lignification of the main stem; hence, elevated CO₂ appeared to accelerate maturation as well as growth. Data from this long-term study suggest that certain mangrove growth characters will change flexibly as atmospheric CO₂ increases, and accord with responses previously shown in Rhizophora apiculata. Such results must be integrated with data from sea-level rise studies to yield predictions of mangrove performance under changing climate.     

Simulated sea level change alters anatomy, physiology, growth, and reproduction of red mangrove (Rhizophora mangle L.)

Tropical coastal forests – mangroves – will be one of the first ecosystems to be affected by altered sea levels accompanying global climate change. Responses of mangrove forests to changing sea levels depend on reactions of individual plants, yet such responses have not been addressed experimentally. We report data from a long-term greenhouse study that assessed physiological and individual growth responses of the dominant neotropical mangrove, Rhizophora mangle, to levels of inundation expected to occur in the Caribbean within 50–100 years. In this study, we grew potted plants in tanks with simulated semidiurnal (twice daily) high tides that approximated current conditions (MW plants), a 16-cm increase in sea level (LW plants), and a 16-cm decrease in sea level (HW plants). The experiment lasted 2½ years, beginning with mangrove seedlings and terminating after plants began to reproduce. Environmental (air temperature, relative humidity, photosynthetically active radiation) and edaphic conditions (pH, redox, soil sulfide) approximated field conditions in Belize, the source locale for the seedlings. HW plants were shorter and narrower, and produced fewer branches and leaves, responses correlated with the development of acid-sulfide soils in their pots. LW plants initially grew more rapidly than MW plants. However, the growth of LW plants slowed dramatically once they reached the sapling stage, and by the end of the experiment, MW plants were 10–20% larger in all measured growth parameters. Plants did not exhibit differences in allometric growth as a function of inundation. Anatomical characteristics of leaves did not differ among treatments. Both foliar C:N and root porosity decreased from LW through MW to HW. Relative to LW and HW plants, MW plants had 1–7% fewer stomata/mm², 6–21% greater maximum photosynthetic rates, 3–23% greater absolute relative growth rates (RGRs), and a 30% higher RGR for a given increase in net assimilation rate. Reduced growth of R. mangle under realistic conditions approximating future inundation depths likely will temper projected increased growth of this species under concomitant increases in the atmospheric concentration of CO₂.     

Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl

Abstract. Propagules of the mangrove, Rhizophora mangle L., were precultivated for 9 months in a greenhouse. The young plants were transferred into unaerated nutrient solutions without and with 200 mol m ³ NaCl and subsequently their growth, their water relations and the photosynthetic properties of their leaves were studied. Growth of the salttreated plants was significantly increased, while the control plants gradually died off after finishing the experiments. The shoot water potential and the stomatal resistance of the leaves were lowered while the chlorophyll contents and the chlorophyll a/b ratio in the leaves of salt-treated plants were increased by NaCl, the net result being an enhanced rate of CO₂ assimilation. The leaves of both sets of plants showed diurnal fluctuations in malic acid concentration which were more pronounced in the leaves of salt treated plants which, additionally, were more succulent. However, the plants showed no net CO₂ fixation at night, indicating that Rhizophora mangle is a CAM-cycling plant. After 200 d of cultivation without or with NaCl, the Na⁺, Cl and K⁺ concentrations in tissues and vacuoles were measured. Energy-dispersive X-ray microprobe analyses on root vacuoles of control plants reveal Na⁺ preference, on those of salt treated plants a strong K⁺ preference. Vacuolar K⁺ concentrations are neither affected by NaCl nor do they vary across the root radius. High vacuolar Na⁺ and Cl concentrations are found in the hypodermis followed by a stepwise decrease towards the inner root cortex cells. Ion concentrations of the photosynthetically active leaf tissues seem to be regulated by (1) radial filtration across the root cortex: (2) ion exchange of the xlem parenchyma cells: and (3) sequestration of Na⁺ and Cl in the hypodermal water storage tissue of the leaves.     

Abundance and richness of mollusks and crustaceans associated to the submerged roots of red mangrove (Rhizophora mangle) at Bocaripo Lagoon, Sucre, Venezuela

Mangrove roots are important habitats for many species. The abundance and richness of mollusks and crustaceans associated with the roots demerged of Rhizophora mangle was studied. The samples were gathered between February 2005 and January 2006, in Bocaripo lagoon, north coast of Sucre state, Venezuela. Five stations were established inside the lagoon; on every station two roots were chosen at random, put in plastic bags and scraped. The associated organisms were separated by taxa and fixed in 10% formaldehyde. One thousand ninety two specimens of mollusks, distributed in two classes: Bivalve and Gastropod were collected. Bivalve was the most abundant with 943 individuals. The most representative family was Mytilidae with 6 species, being Musculus lateralis the dominant species. The crustaceans were represented by 372 organisms, belonging to the class Malacostraca, where Panopeus herbstii (169 ind.) was the most abundant species. The families Panopeidae, Porcellanidae and Majidae had the highest number of species. Maximum abundance was in February (224 ind.), with a richness of 25 species and the minimums in November (45 ind.) and a richness of 12 species. The stations 1 and 5 presented the major abundance and richness of organisms, which could be related to environmental conditions favorable, as the major availability of microhabitats and nourishing offer; on the contrary the station 4, presented a more inhospitable environment, due to the high values in the salinity and temperature, which contributes with the minor abundance and richness of the present species.     

Primary Phloem Development in the Shoot Apex of Rhizophora mangle L. (Rhizophoraceae)

The primary phloem in the shoot apex of the mangrove Rhizophora mangle L. is largely confined to the comparatively condensed area between the first three leaf pairs. The main extension zone, surrounded by the stipular sheath of the third leaf pair, contains vascular bundles arranged in a procambial ring and characterized by a well-developed primary phloem and a less advanced xylem. The phloem consists of a great number of sieve elements, an equal number of associated companion cells, and a few phloem-parenchyma cells. The differentiation of the sieve-element protoplast (with e.g., chromatolytic nuclear degeneration, loss of the vacuole and most organelles) proceeds largely according to a well-known pattern. Their P-type plastids, however, form their protein crystals rather late and therefore cannot be used as an early cell marker. Lateral sieve-element walls are distinct from other wall parts and walls of other cells by their heavy nacreous thickenings, the formation of which is shown to be strictly correlated with the occurrence and orderly arrangement of cortical microtubules.