Responses of neotropical mangrove seedlings grown in monoculture and mixedculture under treatments of hydroperiod and salinity

Pablo Cardona-Olarte1,4, Robert R. Twilley2,*, Ken W. Krauss3 & Victor Rivera-Monroy21Department of Biology, Center for Ecology and Environmental Technology, University of Louisiana at Lafayette,Lafayette, LA 70504, USA2Department of Oceanography and Coastal Science, Wetland Biogeochemistry Institute, Louisiana State University, BatonRouge, LA 70803, USA3U.S. Geological Survey, National Wetlands Research Center, Lafayette, LA 70506, USA4Apartado aereo 402450, Cali, Colombia(*Author for correspondence: Tel.: +1-225-578-8806; E-mail: rtwilley@lsu.edu)

Key words: wetland competition, mangrove traits, flooding, Laguncularia racemosa, biomass allocation, Rhizophoramangle

Abstract

We investigated the combined e!ects of salinity and hydroperiod on seedlings of Rhizophora mangle andLaguncularia racemosa grown under experimental conditions of monoculture and mixed culture by using asimulated tidal system. The objective was to test hypotheses relative to species interactions to either tidal orpermanent flooding at salinities of 10 or 40 g/l. Four-month-old seedlings were experimentally manipulatedunder these environmental conditions in two types of species interactions: (1) seedlings of the same specieswere grown separately in containers from September 2000 to August 2001 to evaluate intraspecific responseand (2) seedlings of each species were mixed in containers to evaluate interspecific, competitive responsesfrom August 2002 to April 2003. Overall, L. racemosa was strongly sensitive to treatment combinationswhile R. mangle showed little e!ect. Most plant responses of L. racemosa were a!ected by both salinity andhydroperiod, with hydroperiod inducing more e!ects than salinity. Compared to R. mangle, L. racemosa inall treatment combinations had higher relative growth rate, leaf area ratio, specific leaf area, stem elon-gation, total length of branches, net primary production, and stem height. Rhizophora mangle had higherbiomass allocation to roots. Species growth di!erentiation was more pronounced at low salinity, with fewspecies di!erences at high salinity under permanent flooding. These results suggest that under low to mildstress by hydroperiod and salinity, L. racemosa exhibits responses that favor its competitive dominanceover R. mangle. This advantage, however, is strongly reduced as stress from salinity and hydroperiodincrease.

Introduction

Forest structural attributes in neotropical man-grove forests are a!ected by several factorsincluding propagule dispersal (Rabinowitz, 1978;Sousa et al., 2003), propagule predation (McKee,1993a, b), seedling and sapling establishment(Ellison & Farnsworth, 1993; McKee, 1995a), andsimultaneous death of adult trees from lightning

strikes (Smith et al., 1994). Among these factors,the establishment of seedlings and saplings is oneof the most important processes in forest regen-eration (Grubb, 1977; Harper, 1977). In man-groves in particular, the establishment of newindividuals is not only controlled by ecologicalprocesses such as herbivory (Onuf et al., 1977;Robertson et al., 1990), but also by the response ofmangroves to physiological stress caused by

Hydrobiologia (2006) 569:325–341 ! Springer 2006J.C. Trexler, E.E. Gaiser & D.L. Childers (eds), Interaction of Hydrology and Nutrients in Controlling Ecosystem Function inOligotrophic Coastal Environments of South FloridaDOI 10.1007/s10750-006-0140-1

resource shortages and regulator excess (Huston &Smith, 1987) in intertidal habitats (Ball, 1988a,1996).

While vegetative responses to regulators aremediated by the species-specific tolerances, theresponses to resource levels are also mediated bycompetitive interactions with other seedlings oradult neighbors (Huston & Smith, 1987; Leish-man, 1999). In both cases, the seedling responsesmay depend on plastic adjustments of plant traitsto the prevailing environmental conditions, whichcan dictate overall seedling performance. Becauseof energetic and physiological constraints onresource acquisition, trade-o!s among morpho-logical, life history, and physiological traits arealso important (Smith & Huston, 1989). Forinstance, an increase in leaf biomass allocationrelative to roots can lead to enhanced plant growthby enhanced acquisition of light resources, butmay also restrict the species’ ability to exploit low-nutrient habitats (Chapin, 1980; Bloom et al.,1985; Chapin et al., 1987, 1990).

Species-specific traits, such as growth rate,shade tolerance, photosynthetic performance,antiherbivore defenses, nutrient use e"ciency, andbiomass allocation are important mechanismsdriving the outcome of plant–plant interactions(Gaudet & Keddy, 1988; Koike, 2001). Plant traitscan be used to model complex species interactions,whose study in the field would require complicatedexperimental designs of long duration (Smith &Huston, 1989). Plant traits also are used as indi-cators of ecological restoration success (Pywellet al., 2003).

Investigations of two of the more importantenvironmental regulators in intertidal settings,salinity and hydroperiod, have focused on assess-ing physiological strain (e.g., Kylin & Gee, 1970;McKee, 1996; Smith & Snedaker, 2000) andseedling-level growth (e.g., McKee, 1995a, b, c;Delgado et al., 2001; Krauss & Allen, 2003; Sousaet al., 2003) under either field or laboratory con-ditions without assessing competitive neighbore!ects. More experimental e!orts are needed toquantify plant competitive responses undermanipulations of salinity and hydroperiod.Accordingly, in our e!orts to model ecosystem-level processes (cf., Chen & Twilley, 1998; Twilleyet al., 1998), sensitivity analysis indicates the needto address specific factors that likely control

recruitment of seedlings to the sapling stage inmangrove forests. Most studies have focused onresources (nutrients, light) and regulators (salinityand sulfide); there are few studies that include thethird physical factor that controls mangrovezonation, hydroperiod (Twilley & Rivera-Monroy,2005). The three-axis conceptual model by Twilleyand Rivera-Monroy requires an understanding ofhow these three factors (resources, regulatorsand hydroperiod) on plant traits can improvesimulation models and restoration monitoringprograms.

Rhizophora mangle L. and Laguncularia race-mosa (L.) Gaertn. f. are two of the dominantmangrove species in the neotropics. Both specieshave been observed as initial recruits in earlystages of mangrove forests regenerating from dif-ferent types of disturbance. Yet recruitmentpotential incorporating combined e!ects of mul-tiple environmental stressors along with ecological(competing) constraints limits the ability of exist-ing models to predict their spatial and temporaldynamics (Huston & Smith, 1987). Some short-term observations of mangrove seedling responsesto salinity (Pezeshki et al., 1990; McKee, 1993a)and flooding (McKee & Mendelssohn, 1987;McKee, 1996) have been performed in the absenceof plant–plant interactions and have indicated thatR. mangle and L. racemosa seedlings start showingdi!erent growth patterns at higher salinity. Inaddition, under field conditions plants are sub-jected to the e!ects of their neighbors, which canchange resource levels and interactions for suc-cessful acquisition of these resources (Tilman,1982; Bazzaz, 1990). In this study design, weincluded competition between seedlings of R. mangleand L. racemosa under both monoculture and mixedculture under experimental combinations of eithertidal flooding or permanent flooding together witheither mesohaline (10 g/l) or hypersaline (40 g/l)salinity. From accounts in the literature and ourown modeling e!orts (Chen & Twilley, 1998;Twilley et al., 1998; Twilley & Rivera-Monroy2005), we developed three directional hypothesesto test (1) L. racemosa shows higher growth rateand productivity than R. mangle in response toexperimental combinations of salinity and tidalflooding just described, (2) plant traits a!ectingincreased growth are more responsive to theseexperimental treatments in L. racemosa than in

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R. mangle, and (3) L. racemosa seedlings growfaster in mixed culture than in monoculture.

Materials and methods

Experimental design

We performed two separate experiments thatcompared mangrove seedling responses to salinityand flooding by using a substitutive design(monoculture and mixed culture experiments,Inouye 2001) in moderation (density of only fourseedlings). In both experiments, we controlled thesalinity concentrations of seawater circulating ineach experimental unit, as well as three compo-nents of hydroperiod (amplitude, duration and

frequency) by using a simulated tidal system withina greenhouse at the University of Louisiana atLafayette, Center for Ecology and EnvironmentalTechnology, Louisiana, USA (30 "N, 92 "W).

In both monoculture and mixed culture exper-iments, we used split-plot designs where salinitytreatment was the main plot, and hydroperiod andspecies were included as sub-plot e!ects. For bothexperiments, there were 12 tables assigned to 1 of 2salinity treatments (10 g/l, 40 g/l), which includedrepeated patterns of six experimental replicatesdistributed as duplicate blocks across the green-house area (Figs. 1 and 2). Each table contained aset of 6 plastic buckets (48 cm height and 15 cm indiameter) with a 190-l plastic reservoir under-neath, for a total of 72 buckets in each experiment.Salt water at the appropriate salinity made by

Lr

Rm

RmRm Lr

Lr Lr

PF

TF

Rm

(a)

(c)

(b)(d)

Figure 1. Layout of the monoculture experiment with the experimental tables and buckets: (a) spatial distribution of tables (mainplots); (b) magnification of a table showing the distribution of experimental buckets (circles), continuous line-circles are bucketssubjected to permanently flooded hydroperiod (PF) and dotted-line circles are buckets subjected to tidal flooding hydroperiod (TF); (c)and (d) lateral view of an experimental bucket containing seedlings of either Rhizophora mangle or Laguncularia racemosa.

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either diluting natural seawater (30 g/l) or addingartificial seasalts was pumped from the reservoirinto each experimental bucket separately. Threebuckets on each table were assigned to tidalflooding and three were assigned to permanentflooding. Tidal floods consisted of 6 h cycles to adepth of 20 cm.

Soil in each bucket consisted of a 1:1 mixture ofriver sand and commercial potting soil (Sta-Green,Spectrum Brands, St. Louis, MO, USA), which isenriched in both macro and micronutrients.Buckets were filled to half-volume with this mix-ture. Temperature inside the greenhouse duringboth experiments ranged between 8 and 37 "C(average about 22 "C), and light was 53% ofambient. The monoculture experiment was con-ducted from August 12, 2000 through August 14,2001, and the mixed culture experiment was con-ducted from August 2, 2002 through May 5, 2003.To avoid build-up of substances inhibiting plant

growth, the water in each tidal unit was replacedevery 2.5 months.

Acclimation procedures

Mangrove seedlings from a nursery in Florida wereacclimated to 3-month-old seedlings in our green-house to near equal heights and then four seedlingswere planted in each experimental bucket. Two ofthe four seedlings were placed in a second smallercontainer, grown together, and removed before theonset of experimental treatments. In the mono-culture experiment these four seedlings were ofeither R. mangle or L. racemosa. In the mixedculture experiment, these four seedlings includedboth R. mangle and L. racemosa. Forty of theseseedlings per species were harvested for eachexperiment, and their height, diameter, freshmass, and dry mass were recorded to estimate theinitial dry mass of the unharvested, experimental

PF

LR

TF

(a)

(c) (b)

Figure 2. Layout of the mixed culture experiment with the experimental tables and buckets: (a) spatial distribution of tables(main plots); (b) magnification of a table showing the distribution of experimental buckets (circles), continuous line-circles arebuckets subjected to permanently flooded hydroperiod (PF) and dotted-line circle are buckets subjected to tidal floodinghydroperiod (TF); (c) lateral view of an experimental bucket containing seedlings of both Rhizophora mangle and Lagunculariaracemosa.

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seedlings. For the remaining experimental seed-lings, water level was kept at 10 cm and salinity waskept at 10 g/l in all buckets initially, then thesalinity level for half the seedlings was graduallyraised to 40 g/l over 20 days. Tidal floods (to adepth of 20 cm) were then initiated, and permanentfloods were raised from 10 to 20 cm.

Acclimation procedures were nearly identicalfor both monoculture and mixed culture experi-ments, with the exception that water level in per-manently flooded treatments for the mixed cultureexperiment was raised from 10 to 20 cm by anincrement of 1.5 cm/d. A total of 144 seedlings (72per species) were assigned to 72 experimentalbuckets at the onset of each experiment.

Pore water measurements

Pore waters were sampled quarterly for determi-nations of soluble reactive phosphorus (SRP),ammonium, sulfide, nitrite+nitrate (N+N), andsalinity. Ammonium, SRP, and N+N weredetermined by standard methods (Parsons et al.,1984). Sulfide was determined after an antioxidantbu!er solution was added to an aliquot of pore-water sample (McKee et al., 1988). This samplewas then analyzed with a sulfide electrode, andreadings were converted to sulfide concentrationby using standard curves prepared from Na2Ssolutions in antioxidant bu!er. Porewater salinitywas determined from another sample aliquot byusing a conductivity meter (Model 30, YSI Cor-poration, Yellow Springs, OH, USA). Also, redoxpotentials were measured at 10 cm depth with apH meter (Model 250A, Orion Research, Inc.)after platinum electrodes were standardized withquinhydrone solution.

Growth and biomass variables

Plants were measured initially and monthly forheight, diameter, leaf count, and number of leafscars. The number of nodes and length of brancheswas assessed bi-monthly. At the end of theexperiment, plants were harvested and separatedinto roots, stems, and leaves. Roots and stemswere oven-dried to constant weight at 60 "C fordeterminations of dry mass. Leaf area of all har-vested leaves was measured with a leaf area meter(Li-3000A, Li-Cor, Inc., Lincoln, NE, USA) and

oven-dried at 60 "C for elemental analysis. Fromthese data, calculations were made for root/shootmass ratio (g/g) and leaf area ratio (total leaf area/total plant mass, cm2/g). In addition, a represen-tative sample of 10 leaves per plant was measuredfor leaf area and dry mass for determinations ofspecific leaf area (leaf area/leaf mass, cm2/g). Netprimary production was estimated as the di!erencebetween biomass at harvest plus senescent leafmass, minus the estimated initial plant mass. Rel-ative growth rate was calculated as the di!erencein the natural logarithm of initial and final(at harvest) seedling dry mass divided by time inmonths (Pattison et al., 1998). Cumulative branchlength was calculated by summing the lengths ofall branches on each plant.

Statistical analyses

Data were analyzed as a split–split plot design forboth the monoculture experiment and the mixedculture experiment. In both experiments the mainplot (salinity) contained both hydroperiods (tidalflooding, permanent flooding), and in the mixedculture experiment, both species were containedinside each bucket. Therefore, both experimentstested salinity over the variance componentresulting from the table e!ect and generated dif-ferent error degrees of freedom for mixed modelanalyses. Hydroperiod and species in the mono-culture experiment were tested over the variancecomponent associated with the interactions amongtable, salinity, hydroperiod, and species. In themixed culture experiment, hydroperiod was testedas in the other experiment, and species was testedover the variance component resulting from theinteraction among table, salinity, hydroperiod,bucket, and species. Error terms are assigned byProc Mixed, including the variance componentssuggested by the analysis (Table 2).

Implicit to split plot-designs is the randomnature of the main plots, and the analyses were runas mixed models. In so doing, restricted maximumlikelihood (REML) methods were used to test fortreatment significance. This methodology requiresa di!erent approach than the traditional meansquare methods to calculate the degrees of freedomand estimate treatment e!ects (Kenward & Roger,1997). Plants were uneven in size when the treat-ments started. To account for this size e!ect, initial

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biomass estimates were used as a covariate for allanalyses. Where e!ects were significant for spe-cies by salinity or species by hydroperiod inter-actions, species-level groupings by salinity andhydroperiod were reported in figures. All datawere either normal and homoscedastick, or theywere transformed prior to analyses. Raw valuesof means and standard errors are presented ingraphs, and data transformations are indicatedin captions when necessary. Posthoc comparisonswere made with a Bonferroni adjustment. Allanalyses were performed by using the ProcMixed of SAS version 8.02 (SAS Institute, Cary,NC, USA).

Results

Porewater and nutrient conditions of the soil

Porewater sulfide concentrations and redoxpotentials indicated that much of the soil was

anaerobic with redox potentials ranging from)180 to )17 mV under permanent flooding vs. )48to 167 mV under tidal flooding for both experi-ments (Table 1). This pattern indicates a greateroverall aerobic state for diurnally flushed tidaltreatments. Porewater salinity also varied aroundthe target levels but was often slightly higher thantarget levels under permanent flooding thanporewater salinity in tidal flooding. Overall,salinity was maintained within 6 g/l of the targetedvalues of 10 and 40 g/l treatments throughoutboth experiments (Table 1).

Concentrations of the major nutrients (SRP,ammonium, and N+N) indicated generallyenriched soil conditions. Porewater sulfide con-centrations ranged from undetectable to 0.87 lM,ammonium ranged from 0.2 to 29.8 lM, soil totalnitrogen ranged from 0.53 to 0.69 mg/g, and SRPranged from 46.2 to 123.4 lM (Table 1). Pore-water ammonium tended to be low (3.7–4.3 lM)for both permanently flooded and tidally floodedseedlings in the mixed culture experiment at 10 g/l

Table 1. Pore water and nutrient conditions of the soil under experimental salinity and hydroperiod manipulations determined at theinitial (month A) and final (month B) sampling dates for each experiment

Experiment Salinity

treatment

Month Hydroperiod

treatment

Redox

potential

(mV)

Porewater

sulfides

(lM)

Porewater

salinity

(g/l)

Porewater

ammonium

(lM)

Total

soil

nitrogen

(mg/g)

Soluble

reactive

phosphorus

(lM)

Mean±SD Mean±SD Mean±SD Mean±SD Mean±SD Mean±SD

Monoculture 10 g/l A PF )149±39 0.15±0.18 11.9±1.1 21.8±10.7 0.60±0.26 88.7±35.3

B PF )180±33 0.17±0.15 11.7±1.3 29.8±38.9 76.8±18.2

A TF 167±97 bdl 9.7±0.6 18.0±4.9 0.69±0.12 46.2±17.1

B TF )16±68 bdl 10.3±0.5 19.7±25.4 58.9±16.8

40 g/l A PF )123±43 0.02±0.02 45.1±1.3 17.3±6.0 0.59±0.13 97.4±31.0

B PF )135±45 0.01±0.02 43.0±2.4 13.5±21.2 80.3±21.7

A TF 136±80 bdl 40.9±1.2 17.1±5.7 0.69±0.10 69.7±24.7

B TF 38±74 bdl 39.8±0.9 11.1±9.0 49.7±4.2

Mixed culture 10 g/l A PF )17±36 0.52±0.22 12.6±7.3 4.3±4.8 0.63±0.19 120.4±55.0

B PF )112±62 0.87±0.52 16.0±8.8 4.4±4.2 123.4±52.9

A TF 149±41 0.04±0.06 10.0±0.7 4.0±5.4 0.65±0.13 107.6±21.3

B TF )48±115 0.16±0.21 9.7±0.6 3.7±5.2 110.0±22.6

40 g/l A TF )31±37 0.07±0.06 41.3±1.5 0.2±0.5 0.53±0.16 84.1±12.1

B PF )72±79 0.18±0.17 45.2±4.3 15.9±13.9 84.7±12.5

A TF 149±29 bdl 36.8±6.7 14.4±8.5 0.66±0.20 86.0±11.1

B TF )31±96 bdl 37.3±7.1 5.2±3.6 86.4±11.0

PF=permanent flooding; TF=tidal flooding; bdl=below detection limits.

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salinity, but SRP tended to be high (108–123 lM)for these same treatments.

Relative growth rate and net primary production

Substantial species di!erences in relative growthrate were detected for monoculture and mixedculture experiments (Table 2). Species by salinityand species by hydroperiod interactions weresignificant for the e!ects of relative growth rate,indicating, as for many growth and biomassvariables reported for these experiments, thattreatment combinations should be analyzed sepa-rately. Laguncularia racemosa, for example, hadsubstantially higher relative growth rates in bothexperiments under all treatment combinations(Table 2, Fig. 3). The e!ects of the treatment onseedling relative growth rates were di!erent foreach species under both experiments. While tidalflooding and lower salinity induced growth in bothexperiments for L. racemosa, R. mangle experi-enced no changes. Relative growth rate for mixedcultured, L. racemosa was 30% lower under per-manently flooded treatments relative to tidal

treatments under low salinity and 23% lower forthe same comparisons at high salinity. Relativegrowth rate of L. racemosa declined 19.4 % withincreasing salinity under tidal flooding. Similartreatment e!ects on relative growth rate wereobserved for both the monoculture and mixedculture experiment.

Net primary production was higher forL. racemosa than for R. mangle across all treat-ments (Table 2, Fig. 4). While L. racemosa showedstrong treatment e!ects in the monocultureexperiment, R. mangle showed no change in themonoculture experiment and only minimal changein the mixed culture experiment (Fig. 4). Produc-tion of L. racemosa under monoculture was higherrelative to mixed culture under higher salinitiesindicating that interactions between L. racemosaand R. mangle may reduce productivity athigher salinities for L. racemosa (Fig. 4). Salinitysignificantly a!ected net primary production ofL. racemosa only under permanent flooding,whereas the hydroperiod e!ect was independentfrom salinity and caused a much stronger e!ectthan salinity.

Table 2. ANOVA table describing experimental growth and response variables for seedlings of R. mangle and L. racemosa grown inmonoculture and in mixed culture experiments

Source of variation DF,

DFerror

Relative

growth

rate

Net

primary

prod.

Total

leaf

area

Cumulative

branch

length

Stem

height

Leaf

area

ratio

Specific

leaf

area

Root/Shoot

Monoculture experiment

Species 1, 63 *** *** *** *** *** *** ** *

Salinity 1, 63 *** *** *** * *** *** *** **

Hydroperiod 1, 63 *** ** * *** ns ns ns *

Species! salinity 1, 63 * ** ns *** ns *** * ns

Species!hydroperiod 1, 63 *** *** ** *** *** ns ns ***

Salinity!hydroperiod 1, 63 ns ns ns ns ns ns ns *

Covariate (plant mass at t0) 1 *** ** ** * ** *** ns ns

Mixed culture experiment

Species 1, 122 *** *** *** *** *** *** *** ns

Salinity 1, 11.9 ** *** *** *** *** ns *** **

Hydroperiod 1, 61.1 *** *** *** *** ns *** ns **

Species!salinity 1, 69.8 *** * ** *** ** *** * **

Species!hydroperiod 1, 72.7 *** ** *** *** *** ns ns ns

Salinity!hydroperiod 1, 55.2 ns ns *** ns ns ns ns ns

Covariate (plant mass at t0) 1 ** ** *** *** *** ns ns ns

ns: Not significant at the 0.05 level; *: Significant at 0.01–0.05 level; **: Significant at 0.01–0.001 level; ***: Significant at <0.001 level.

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Total leaf area

Laguncularia racemosa had greater plant leaf areathan R. mangle in all treatments for both experi-ments (Table 2; Fig. 5). Leaf area for R. mangletended to di!erentiate among treatment combi-nations in the monoculture experiment but not inthe mixed culture experiment, indicating that per-haps the larger L. racemosa seedlings shaded R.mangle under mixed culture. By the end of bothexperiments, the height of L. racemosa averaged40–50 cm greater than R. mangle. In the mono-culture experiment, hydroperiod had an e!ect on

plant leaf area at higher but not at lower salinity(Fig. 5).

Branch and stem attributes

Laguncularia racemosa had significantly highercumulative branch length in all treatment com-binations from both experiments, but theenhancement was most pronounced with tidalflooding at high salinity in monoculture (Ta-ble 2). Permanently flooded conditions reduced

Figure 3. Relative growth rate (RGR) of Laguncularia race-mosa (L) and Rhizophora mangle (R) seedlings in response toeither tidal flooding (TF) or permanent flooding (PF) hydro-period and 10 g/l (10S) or 40 g/l (40S) salinity under experi-mental monoculture (a) and mixed culture (b). Error bars are±1SE.

Figure 4. Net primary productivity (NPP) of Lagunculariaracemosa (L) and Rhizophora mangle (R) seedlings in responseto either tidal flooding (TF) or permanent flooding (PF)hydroperiod and 10 g/l (10S) or 40 g/l (40S) salinity underexperimental monoculture (a) and mixed culture (b). Error barsare ±1SE. Data for the mixed culture experiment were log-transformed for the analysis.

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branch growth by nearly 50% in both salinitytreatments. Otherwise, results for cumulativebranch length response under mixed culture wereidentical to those for plant leaf area (see Fig. 5).There was very little e!ect of salinity and hy-droperiod on cumulative branch length of R.mangle, which had only 33% of the maximumvalues reported for L. racemosa.

Stem height was greatest for L. racemosagrowing in low salinity tidal treatments underboth monoculture and mixed culture (Fig. 6).Height growth di!erentiation paralleled results

for total leaf area in demonstrating that compe-tition e!ects forced greater mean separationamong seedlings growing in mixed culture than inmonoculture for both species. Salinity a!ected L.racemosa under tidal but not permanently floodedconditions in both experiments (Fig. 6). Lag-uncularia racemosa growth based on stem heightwas nearly twice that of R. mangle under lowsalinities in the mixed culture experiment. Thereduction in growth of L. racemosa in the mixedculture experiment compared to more consistentresponse of R. mangle across all treatments

Figure 5. Plant leaf area of Laguncularia racemosa (L) andRhizophora mangle (R) seedlings in response to either tidalflooding (TF) or permanent flooding (PF) and 10 g/l (10S) or40 g/l (40S) salinity under experimental monoculture and mixedculture. Error bars are ±1SE. Data were rank-transformed forthe analysis of (a) and squared root-transformed for the anal-ysis of (b).

Figure 6. Stem height of Laguncularia racemosa (L) and Rhizo-phoramangle (R) seedlings in response to either tidal flooding (TF)orpermanent flooding (PF) and 10 g/l (10S) or 40 g/l (40S) salinityunder experimental monoculture (a) and mixed culture (b). Errorbars are ±1SE. Data were log-transformed for the analysis.

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resulted in less interspecific di!erentiation at thehigher salinity.

Leaf area and biomass allocation

Leaf area ratio, the amount of photosynthetic areaper unit plant mass, generally decreased forR. mangle at high salinities in monoculture andincreased in mixed cultures, while L. racemosa leafarea decreased in mixed culture as salinity andflooding increased (Table 2, Fig. 7). In the

monoculture experiment, leaf area ratio forL. racemosa did not change with treatments. InR. mangle the e!ect of hydroperiod was significantfor low salinity but not significant for high salinity.Salinity induced stronger e!ects than hydroperiodon leaf area ratio of L. racemosa than R. mangle.Specific leaf area was a!ected less among alltreatments than the leaf area ratio; however,L. racemosa tended to have a greater specific leafarea of approximately 71 cm2/g for all treatmentsthan R. mangle ("55 cm2/g).

Laguncularia racemosa allocated proportion-ally more biomass to leaves and to stems than didR. mangle in all treatments (Table 2, Fig. 8). Thishigher biomass allocation to shoots allowedL. racemosa to accumulate more biomass thanR. mangle in all treatments (especially at lowsalinity or tidal conditions), thus a!ecting theroot/shoot ratio significantly greater in monocul-ture for both species than in mixed culture. Thesame general trend was observed for reduced leafarea (Fig. 5) and height (Fig. 6), indicating thee!ect of mixed culture conditions, especially forL. racemosa. But there was no correspondingchanges to root biomass allocation across mono-culture and mixed culture conditions, indicatingthat below ground resources were not as sensitiveto these interactions.

Discussion

Soil environment

Soil nutrient concentrations were comparable tofield data reported for mangrove forests (Boto,1983; Koch & Snedaker, 1997; Duarte et al., 1998;Sherman et al., 1998; Chen & Twilley, 1999;Gleason et al., 2003), which indicates that SRPlevels range from undetectable to 20 lM, andammonium levels range from undetectable to ashigh as 760 lM in Florida Bay (USA) (Rosenfeld,1979). We are puzzled by the lower levels ofporewater ammonium for 10 g/l treatments undermixed culture (Table 1). Perhaps these levelsreflect a greater uptake by both species during thesummer of the mixed culture experiment that wasnot present during the monoculture experiment.Such competition would be inherent in the mixedculture experiment and may have prompted higher

Figure 7. Leaf area ratio (LAR) of Laguncularia racemosa (L)and Rhizophora mangle (R) seedlings in response to either tidalflooding (TF) or permanent flooding (PF) and 10 g/l (10S) or40 g/l (40S) salinity under experimental monoculture (a) andmixed culture (b). Error bars are ±1SE. Data for both exper-iments were rank-transformed for the analysis.

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growth rates in L. racemosa than those inR. mangle through resource competition (Tilman,1982).

Growth di!erentiation between species

Laguncularia racemosa and R. mangle respondeddi!erently to the combined e!ects of salinity andhydroperiod in both monoculture and mixedculture, with overall greater plant growth byL. racemosa. Enhanced growth for L. racemosarelative to R. mangle is a general characteristicof the species under low stress (cf., Wadsworth,1959; McKee, 1995c; Krauss et al., 2006).Accordingly, the greatest interspecific di!erences

typically occurred under low salinity and tidalflooding in our study. Most L. racemosaresponses were significantly a!ected by salinityand hydroperiod, with stronger response to hy-droperiod, whereas R. mangle experienced littleor no change with treatments. These patternsdenote the higher plasticity and greater growthpotential in L. racemosa than in R. mangle basedon reduced growth and productivity as salinityand/or flooding increased to those of the exper-imental conditions. In contrast, R. manglemaintained more constant growth and produc-tivity across all salinity and hydroperiod treat-ments. This consistency in mass-based growth ofR. mangle in both experiments suggests that

Figure 8. Biomass allocation to above- and below-ground components of Laguncularia racemosa (L) and Rhizophora mangle (R)seedlings in response to either tidal flooding (TF) or permanent flooding (PF) hydroperiod and 10 g/l (10S) or 40 g/l (40S) salinityunder experimental monoculture (a) and mixed culture (b). Plant standing biomass (g) is depicted in parentheses.

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interspecific competition did not a!ect R. man-gle’s overall growth in the range of the experi-mental conditions examined in our study. Theexception for R. mangle was leaf area, which didappear to be a!ected at high salinity and ex-tended flooding when in competition withL. racemosa (Fig. 5). Salinity up to 32 g/l had noe!ect on the leaf area of R. mangle in Hawaii(Krauss & Allen, 2003), but salinity tended toincrease leaf area relative to flooding alone(Pezeshki et al., 1990) and to exert slower overallgrowth on R. mangle propagules (Smith &Snedaker, 1995). Laguncularia racemosa, on theother hand, exhibited more sensitive traits toexperimental conditions such as reduced height,leaf area, and biomass at higher salinities andincreased flooding in mixed culture throughoutour study.

General patterns of plant interspecific responses

The spatial distribution of mangrove species inthe intertidal zone can be a!ected by severalfactors that can cause changes in the functionaltraits that control growth potential in mangrovetrees (Ellison & Farnsworth, 1997; Ellison, 2002).It is clear that certain functional traits of man-grove trees, such as those quantified in our study,can explain patterns of vegetation dynamics inmangrove wetlands. When gaps form in a forest,for example, changes in plant height haveimportant consequences for capturing above-ground light resources (Canham & Marks, 1985;Caldwell, 1987; Stevens & Carson, 1999). Whileoptimum growth of L. racemosa in our study wasmuch greater than were those of R. mangle, severalof the functional traits of L. racemosa were alsomore sensitive to changes in hydroperiod andsalinity than R. mangle. Two traits in particular,net primary production and leaf area, appearedto a!ect relative growth rate of L. racemosa andR. mangle and varied under conditions ofmonoculture vs. mixed culture. A greater leafarea, for example, may benefit seedlings in amangrove understory that are limited by light;understory light can be attenuated to 1.8–3.4 % ofambient levels (Sherman et al., 2001). Under suchconditions, enhanced leaf ratio would allowcompetitive growth responses to light gaps thatmay form from small-scale disturbances such as

lightning. Recruitment of mangrove saplings,which is dependent on seedling vigor under amangrove canopy, dominate gap regenerationprocesses after such a disturbance (Chen &Twilley, 1998). Based on our past study, en-hanced vigor of seedlings growing at high salinityand long flood durations prior to a disturbancemay also benefit species’ success. Indeed, basedon model simulations, L. racemosa and R. mangletend to dominate the composition of gaps orhurricane-devastated forests initially, while Avi-cennia germinans (L.) Stearn tends to dominate ata later successional sere (>100 years: Chen &Twilley, 1998; Doyle et al., 2003).

Results from this study are consistent withmany field observations (e.g., Chapman, 1976;Koch, 1996) which have found that R. mangletrees tend to occupy locations where more per-manent flooding occurs and where soil salinitiesare similar to seawater (35 g/l). In the neotropics,the fringe zone is usually dominated by R. mangle,and L. racemosa is generally low in abundancewithin the first 10 m of the fringe but more com-mon to interior locations. Laguncularia racemosais also common on sand or mud flats in riverswhere flooding can be deep at times (Delgadoet al., 2001).

Responses to salinity and hydroperiod e!ects

Except for the leaf area ratio at low salinity,R. mangle exhibited few changes in plant traitswith hydroperiod treatments. Hydroperiod dida!ect many plant responses in L. racemosa. Formost of the other traits, the response to hydro-period by R. mangle depended on salinity and/orcompetitive interactions. This pattern is impor-tant to note because it indicates the more sensi-tive response of L. racemosa to flooding than tochanges in salinity. One consequence of this dif-ference in species response to flooding andsalinity is that L. racemosa tends to be con-strained in its spatial distribution towards areaslacking constant flooding where its growth ispurportedly optimum and much higher than thatof R. mangle. Greater branch elongation andheight of L. racemosa is a strategy that increasescapture of aboveground resources (Caldwell,1987; Schulze & Chapin, 1987), thus increasing itscompetitive advantage on R. mangle. Evidence

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that L. racemosa is actually quite tolerant to longflood durations (Delgado et al., 2001; Krausset al., 2006) may explain why L. racemosa oftendominates early successional seres that are lightsaturated (Chen & Twilley, 1998) but can lagbehind occurrence of R. mangle in early regen-eration of lightning gaps that are more lightlimited (Sherman et al., 2000).

Mangroves produce morphological and phys-iological adaptations to cope with flooding(Scholander et al., 1955; Hutchings & Saenger,1987; Ball, 1996), yet di!erent patterns of growthcan occur across hydroperiod and salinity gradi-ents (Ball, 1988a, 1996; Delgado et al., 2001). Ourstudy documents significant plant growth reduc-tions under permanent flooded conditions; hence,morphological adaptations are not completelyameliorative. There are other examples such asBruguiera sexangula (Loir.) Poir, that had ahigher e"ciency in leaf-level carbon gain underincreased salinity and reduced shade, but therewas reduced plant growth even with a higher leafarea plasticity (Krauss & Allen, 2003). Relative toL. racemosa in our study, R. mangle appears tohave a similar strategy of less overall growthsensitivity across a wide range of treatments asreported by Krauss & Allen (2003). Mechanismsassociated with reduced growth of mangrovesacross these gradients are less understood thanmechanisms of salt tolerance (McKee, 1996) butare undoubtedly linked to propagule retention inR. mangle (Smith & Snedaker, 2000). Explana-tions for reduced growth caused by flooding in-clude reduced water absorption (Naidoo, 1985),inhibition of nitrogen uptake by H2S (Kochet al., 1990), and reduced root oxygen tensioninhibiting metabolic functions in the roots(McKee, 1996).

Links between relative growth rateand other plant traits

Relative growth rate was reduced by L. racemosaacross gradients in hydroperiod and salinity indi!erent ways than those of the other plant traitsassessed. Reduction in the values of some traitssuch as plant leaf area, stem height, and cumula-tive branch length, were observed with changes inhydroperiod at low salinity but were not observedat high salinity. In other cases, the change

depended on either salinity or competition treat-ment. Most of the traits assessed, except for rootto shoot ratio, were positively correlated to rela-tive growth rate. Thus, higher relative growth ratesoccurred when plants exhibited higher values ofleaf area ratio, specific leaf area, and cumulativelength of branches. In most cases higher values ofthese traits occurred for L. racemosa thanR. mangle. Indeed, frequently high values of leafarea ratio and specific leaf area are associated withplants exhibiting high growth rates (Poorter &Remkes, 1990; Lambers & Poorter, 1992; Reichet al., 1992), which are commonly found in pro-ductive habitats (Grime & Hunt, 1975; Grime &Campbell, 1991). These leaf traits and the highrelative growth rates give L. racemosa a competi-tive advantage to rapidly colonize open areas insheltered intertidal zones. When L. racemosa andR. mangle share the same habitat conditions sim-ulated in this study, L. racemosa possesses traitsfor growth that may confer a competitive advan-tage over R. mangle. This situation is particularlyimportant in early rather than later stages of forestregeneration because these traits also are linked tofaster rates of tissue loss and generally low toler-ance to shading (Welden et al., 1991; Burslemet al., 1995).

Models and theories of plant growth indicatethat in response to resource variation plants par-tition photosynthates to optimize resource captureand consequently maximize growth rate (Bloomet al., 1985; Hirose, 1987; Shipley & Meziane,2002). Implicit in these ideas is the prediction thatplants will adjust their allocation in above- andbelowground mass to compensate for thatresource which is in short supply (Bazzaz et al.,1987; Tilman, 1988; Chapin et al., 1990; Gleeson& Tilman, 1992). The increased cost of carbonacquisition per unit of water and nutrient uptakein saline habitats (Ball, 1988a, b) suggest thatmangroves exhibit an increased biomass allocationto roots with increasing salinity (Ball, 1988b). Inour study both species reduced their allocation toroots with increasing salinity. Biomass allocationby individual plants can be adjusted to the specificsets of local conditions (Bazzaz et al., 1987) andcan also be controlled by ontogenic or size-dependent e!ects (Coleman & McConnaughay,1995; Gedroc et al., 1996; McConnaughay &Coleman, 1999). It is possible that factors not

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tightly controlled in our experiment, such asnutrients, could have had important influence onthe root to shoot ratio. We referenced among-treatment anomalies in ammonium and SRPabove, but making specific links to growthcharacteristics is not supported on patternsobserved. Furthermore, it is likely that di!erencesin biomass allocation from past studies were con-founded by ontogenic e!ects since plants canchange allocation patterns throughout their stagesof development (Coleman & McConnaughay,1995; Gedroc et al., 1996; McConnaughay &Coleman, 1999).

Conclusions

Our study documented species-specific di!erencesin plant morphological traits that make L. race-mosa and R. mangle respond di!erently to changesin salinity and hydroperiod. As a consequence ofplasticity in plant morphological traits, therefore,L. racemosa has higher growth potential for sev-eral plant traits, reaches greater abovegroundstature, and attains higher productivity than doesR. mangle at low salinity with tidal conditions,thus accepting our first two study hypotheses. Thesuperior performance of L. racemosa relative toR. mangle changes with either increased salinity ormore permanent flooding, such that at 40 g/L andlong flood duration, performance of L. racemosaand R. mangle was similar.

Finally, competition with L. racemosa mayhave reduced stem growth and cumulative lengthof branches in R. mangle, thus also accepting ourthird study hypothesis that L. racemosa generallygrew faster in mixed culture than in monoculture.Competition has been implicated as an importantfactor a!ecting species distribution in mangroves(Ball, 1980, 1988b; Smith, 1988; Clarke &Myerscough, 1993; McGuinness, 1997). Di!eren-tial competition can result from phenotypic dif-ferentiation in expression of plant traits indi!erent environments (Leishman, 1999). Ourstudy indicates that higher relative growth rate inL. racemosa a!ects plant height and branchextension, which makes this species able to ex-ploit more e"ciently above ground resourcesthan R. mangle.

Acknowledgements

We would like to thank Patty Higgins, RogerHolland, Steve Coats, J. Ernesto Mancera, andEdward Castaneda for assistance with fieldlogistics, research ideas, and maintenance ofgreenhouse experiments. James B. Grace, SusanMopper, Karl H. Hasenstein, John A. Nyman,Donald Cahoon, Barry Moser, and Jarita Davisprovided helpful peer, statistical, or editorialreviews. Experiments were supported by theNational Science Foundation under CooperativeAgreement #DEB-9910514 (Florida CoastalEverglades, Long-Term Ecological Research).Instituto Colombiano para el Desarrollo de laCiencia y Tecnologia (Colciencias) provided ascholarship to the first author. Funding fromDepartment of Energy (DE-FG02-97ER12220)provided greenhouse research facility at theCenter for Ecology and Environmental Technol-ogy at UL Lafayette. This is contribution #303 ofthe Southeast Environmental Research Center atFlorida International University. Any opin-ions, findings, conclusions, or recommendationsexpressed in the material are those of the authorsand do not necessarily reflect the views of theNational Science Foundation. Mention of tradenames does not constitute endorsement by theU.S. Government.

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