Oecologia (2003) 135:110-121 DOI 10.1007/s00442-002-1167-2

James A. Allen * Ken W. Krauss * Robert D. Hauff Factorslimiting the intertidaldistribution of the mangrovespecies Xylocarpusgranatum

Received: 28 October 2002 / Accepted: 27 November 2002 / Published online: 1 February2003 ? Springer-Verlag2003

Abstract The species granatum is com- important, especially relative to a potential contribution to monly described as occurring in the upper intertidal zone secondary stress mortality. Other factors may ultimately of forests, but mature are occasionally prove to be more critical, such as physiological effects of found at lower elevations. In the Utwe River basin, on the salinity on germination, effects of tides on seed Pacific island of Kosrae, we investigated the relative dispersal and rooting, or differential herbivory on importance of several biotic and abiotic factors that may seedlings. control the intertidal distribution of X. granatum. Factors we evaluated included differential seed predation across Keywords Kosrae Federated States of Micronesia the lower, mid, and upper intertidal zones and seedling Seed predation. Salinity tolerance Flood tolerance responses to salinity, tidal flooding, and shade. Seed predation was 22.4% over the first 34 days and varied little among zones or in gaps versus under the forest Introduction canopy. By day 161, there were still no differences in seed mortality, but a significant difference was found in Patterns of mangrove tree species zonation have been the seedling establishment, with much greater establishment subject of scientific interest for many decades (Watson in the upper intertidal plots. X. granatum seedlings in a 1928; Davis 1940; Egler 1950; Macnae 1968; Chapman greenhouse experiment exhibited greater growth in 1976). Numerous factors influencing species zonation freshwater than seedlings in 23 ppt salinity, which is patterns have been proposed, including physiological typical of salinity levels found in the mid intertidal zone adaptationsto flooding and salinity, differential propagule in our field study sites in Micronesia, where mature X. dispersal, differential propagule predation, interspecific granatum trees are generally absent. Seedlings grown in competition, forest succession following land building, 23 ppt salinity, however, exhibited few visible signs of and responses to geomorphological processes (Louda stress associated with patterns in growth. Seedlings grown 1989; Smith 1992). The relative importance of these in a simulated tidal flooding treatment (with 23 ppt factors, however, has been examined systematically for salinity) also showed few signs of stress. Growth declined only a few species (Smith 1992; Clarke and Myerscough dramatically under 80% shade cloths, but there were few 1993; McKee 1993; McGuinness 1997a). interactions of shading with either 23 ppt salinity or One of the proposed factors that has been the subject of simulated tidal flooding. Differential seed predation is not considerable recent attention is seed or propagule preda- likely to be the primary factor responsible for the tion and particularly how it varies across the intertidal intertidal distribution of X. granatum on Kosrae. Howev- zone, in gaps versus the forest canopy, and in relation to er, seedling tolerance of flooding or salinity may be more the dominant tree species in the forest canopy (Smith 1987a; Smith et al. 1989; Osborne and Smith 1990;

J. A. Allen * K. W. Krauss (E) . R. D. Hauff McKee 1995; McGuinness 1997a, 1997b; Patterson et al. USDA Forest Service, Pacific Southwest Research Station, 1997; Sousa and Mitchell 1999). Most mangrove species Institute of Pacific Islands Forestry, produce propagules that are effective at dispersing at least 1151 Punchbowl St., Rm. 323, Honolulu, HI 96813, USA locally, so predation might be regarded as the first e-mail: [email protected] potentially critical post-dispersal factor affecting the Tel.: +1-337-2668882 ability of a species to establish itself across the whole Present address: intertidal range of a given river basin or estuary. K. W. Krauss, U.S. Geological Survey, Assuming that a species can disperse its propagules National Wetlands Research Center, effectively across the whole intertidal zone and that 700 CajundomeBlvd., Lafayette, LA 70506, USA III predationacross that range is <100%, the next factors Seed predationexperiment affecting a species' ability to establish across the entire Seed predation was examined experimentally using methods intertidal zone would be the species' physiological similar to those originally employed for by Smith toleranceto the rangeof tidal flooding, salinity,and light (1987a). Mature fruits were collected directly from trees in April conditionsencountered. 1999 and air-dried until the pericarps began to split open. In this study, we examined the importanceof these were then extracted and inspected for insect or other damage. Apparently undamaged seeds were selected and weighed to the potentialfactors: differential seed predationand tolerance nearest0.1 g. Individualseeds were tetheredwith a 1/0 fishhook to of flooding, salinity, and shade, as they affected the 1r-mlengths of line consisting of a 30-cm wire leader, 70 cm of intertidaldistribution of Xylocarpusgranatum Konig, a nylon twine, and a plastic numberedtag. The lines were tied to prop mangrovespecies rangingfrom East Africa to islands in roots, pneumatophores,or seedlings. Fifteen seeds were tetheredin the central Pacific Ocean et al. each of 18 plots, with six plots each in the lower, mid, and upper (Mabberley 1995). intertidalzones. Within each zone, three of the plots were located Specifically, our objectives were to determine:(1) the under the forest canopy and three were located in adjacent forest level of seed predationon X. granatumacross a rangeof gaps (?98 m2 in area). Seeds were laid out in three rows, with 2-m intertidalpositions and light levels, and (2) the survival spacing between rows and 1.5 m between seeds within rows to and growth responses of X. granatum seedlings to minimize entanglement of the lines. The canopy coverage in all plots was estimated by taking four spherical densiometer readings, combinationsof tidal flooding, salinity,and shade. facing in cardinal directions from the plot center. Xylocarpus Ourinterest in X. granatumstems fromour experience granatum seeds and seedlings already present in the plots were working in the Federated States of Micronesia. The subsampled with 1-mr2quadrants, and the length and width of the species is of considerableeconomic importanceon some gap plots were measured. Seeds were monitored 5 times over the is first 34 days, and any damage, mortality, and root or shoot Micronesianislands, where it commonlyused for wood development were noted. Seeds were considered dead if >25% of carvingsand occasionallyused for furnitureand interior their biomass was removed. Although other studies have used 50% construction.Also, althoughthe species is often described removal as criteria for mortality in dealing with propagules (cf., as occurringon the landwardedge, or upper intertidal Smith et al. 1989), 25% seemed to be a better criterion for X. zone, of mangroveforests (Macnae 1969; Percival and granatum seeds. On not a single occasion did a seed with >25% damage during the first 34 days become established by the end of Womersley 1975; Wells 1982), there are a numberof the experiment. Seeds were monitored twice more, at 73 and intriguingsituations in Micronesiaand elsewhere (e.g., 161 days after tethering,to check for seed survival and evidence of Chapman 1976; Bunt et al. 1982; Wells 1982) where seedling establishment. maturetrees of this species are found growing at lower Mean amounts of predation, expressed as percentages, were analyzed following a square root transformationusing a split-plot elevationsor at highersalinities than might be expectedof ANOVA with a nested errorstructure. Intertidal zone served as the a landwardedge species. These types of observations main plot while light level served as the subplot effect; the error suggest that the distributionof X. granatumcannot be structureincluded light level nested within intertidalposition. Since explained simply by physiological limitations such as predationwas low throughoutand most of the percent data fell at a toleranceof tidal flooding or range <20%, it was appropriateto use a squareroot transformation salinity. as opposed to an arc sine transformation(Lantican and Baldwin 1994). Results, however, differed little regardlessof transformation used. Materialsand methods Seed chemical composition was evaluatedfor a sample of ten X. granatumseeds selected from the same batch used in the predation The Study site experiment. seeds were dried at 70?C to a constant mass and submitted to the University of Hawaii's AgriculturalDiagnostics The field portion of this study was conducted on the island of Laboratoryfor analysis of ash, crude protein,crude fat, crude fiber, Kosrae (5?19'N, 163?00'E) in the Federated States of Micronesia. and total carbohydrates. A second batch of eight seeds were collected in September 1999 and submittedto Kosrae is a small (1 12 km2) volcanic island, with relatively evenly the same laboratory distributedannual rainfall of 5,000-6,000 mm. Typhoons and other for the same analyses, with the exception that the tough, fibrous large-scale natural disturbancesare rare in the region (Ray 1999; seed coat was first removed and discarded. Allen et al. 2001). The high rainfalland flat topographyof Kosrae's coastal plain allow for the development of extensive mangrove forests, which cover approximately 14% of the land area and two- Greenhouse experiment thirdsof the coastline (Whitesell et al. 1986). Eleven mangrovetree species, including one hybrid, are present on the island (Duke Mature X. granatum fruits were collected directly from trees on 1999), of which Sonneratia alba J. Smith, Bruguiera gymnorrhiza Kosrae in April 1998 and transportedto a greenhouse facility in (L.) Lamk, and Rhizophora apiculata BL are the most common Waimanalo, Hawaii. Fruits were air-drieduntil the pericarpsbegan to (MacLeanet al. 1988; Ewel et al. 1998a). All of the field work was split open; seeds were extracted, inspected for insect or other conducted within the Utwe River Basin, located on the southern damage, treatedwith powdered Sevin (Carbaryl),and sown directly end of the island. The Utwe River is about 2 km long and drains an into 2.8-1 plastic pots (Tall One, Stuewe and Son, Corvallis, Ore.) area of 600 ha; the intertidal zone containing mangroves is containing a commercial potting mix (Sunshine 1 Mix, SunGro approximately500 m wide from the landwardedge to the bay. The , Bellevue, Wash.). Many seeds germinated quickly tidal regime in the area is semidiurnal, with an average range of and were maintainedfor approximately8 weeks after sowing in a with approximately I m (Nautical Software 1996). Large X. granatum greenhouse screened sides and a roof of translucentfiberglass, trees and saplings are common in the upperreaches of the intertidal which allowed transmittance of approximately one-third of full zone, and seedlings are occasionally encountered at lower eleva- sunlight. Seedlings were maintained in the same greenhouse tions within the basin. throughoutthe pre-experimentalas well as the experimentalgrowth phases. Seedlings were fertilized initially with 3.6 g L-'pot volume of a controlled-release 14-14-14 NPK fertilizer (Graviota, Brewer 112 EnvironmentalIndustries, Honolulu, Hi.), and starting46 days after separated into roots, stems, and . Total area was the experiment began, seedlings were fertilized approximately measured for each seedling using a Li-Cor Model 3100 leaf area every 15 days with a water-soluble 20-20-20 NPK fertilizer with meter (Li-Cor, Lincoln, Neb.), after which roots, stems, and leaves micronutrients(Peters Professional, United Industries, St. Louis, were dried at approximately70?C to a constant mass and weighed Mo.) at an average rate of 0.13 g 1-1pot volume. Both before and on an analytical balance. Several additional variables were after initiation of the treatments, the seedlings were periodically calculated from harvest data, including individual leaf area (cm2), sprayed with Dursban 50 W (Chlorpyrifos) and treated with specific leaf area (cm2 g'1), leaf weight ratio, stem weight ratio, and Marathon (Imidacloprid; a systemic granular) to control insect root:stemratio. Leaf and stem weight ratios were calculated as the infestations, particularlyby black twig borers (Xylosandruscom- biomass proportionof either leaves or stem to the biomass of the pactus), a common greenhouse,nursery, and orchardpest in Hawaii entire seedling. (cf., Solomon 1995). After biomass was determined,all leaves from one seedling in Seedlings were then randomlyassigned to one of six treatment each treatmentcombination and replication(n= 18) were submitted combinations of light and tidal flooding/salinity as follows: (1) to the University of Hawaii's AgriculturalDiagnostics Laboratory unshaded, <0.5 ppt salinity; (2) unshaded, 23 ppt salinity; (3) for foliar nutrientanalysis. There, macronutrientconcentrations of unshaded, 23 ppt salinity plus tidal simulation; (4) 80% shade, N, P, K, Ca, Mg, and Na as well as micronutrientconcentrations of <0.5 ppt salinity; (5) 80% shade, 23 ppt salinity; and (6) 80% shade, Mn, Fe, Cu, Zn, and B were determined. 23 ppt salinity plus tidal simulation.The salinity level of 23 ppt was Data for growth parameterswere analyzed using analysis of chosen to approximatethe mean salinity levels found in the interior covariance, with a split-plot design (light level being the main plot and riverine mangroves (i.e., lower and middle intertidalzones) of treatment,and salinity or tidal flooding being the subplot). Initial Kosrae (Krauss and Allen, in press; Ewel et al. 1998a). height was used as the covariantexcept for final diameterand leaf Salinity treatments were created with a commercial seawater count in which case their respective initial measurements were mix that closely approximates the true ionic composition of used. Significant relationshipswere found between measurements seawater (Forty Fathoms Marine Mix, Marine Enterprises,Balti- for all variables at harvest and assigned covariants, except for more, Md.). Seedlings were acclimated to the 23 ppt salinity specific leaf area. ANOVA procedureswere used for analysis of treatments gradually with an initial 3-day freshwater (<0.5 ppt) specific leaf area and foliar nutrientdata. All growthdata were first flood, followed by a rise in salinity to 5 ppt for 4 days, a rise in square-root transformed to improve homogeneity of variances. salinity to 13 ppt for 11 days, and, finally, a rise in salinity to 23 ppt. Salinity effects were evaluated by comparing the <0.5 ppt and Pots were flooded to 14 cm below the soil surface, which, due to 23 ppt soil water treatments only. Tidal flooding effects were capillary movement of water, ensured that the entire soil volume evaluatedby comparingthe 23 ppt soil water salinity treatmentand remained saturated.In the tidal simulation treatment,water levels the tidal simulationtreatment only, which also had water of 23 ppt. were maintainedto simulate a semidiurnaltide, which is common throughoutMicronesia. Each flood cycle was approximately2 h in durationwith flow simulationstaking approximately5 min to reach maximum tidal heights and ebb simulations taking approximately Resufts 15 min to drain tanks. At high tide, seedlings were flooded to approximately 4 cm above the soil surface and were drained to Seed predation approximately28 cm below the soil surface at low tide. Flooding regimes were not of sufficient duration to induce permanent underthe forestcanopy were fairly well anaerobic conditions to any of the hydrologic treatments.Average Plots established pH-unadjustedredox potential of the soil matrices across all three shaded,with an averageof only 3.3% (?0.56%SE) open hydrologic treatmentsat 7 cm below the surface was +316 mV. canopy across all intertidallocations. Gap plots were Shading was created artificially using 80% neutral density, establishedwithin gaps rangingin size from98.1 to 209.1 black knitted shade cloths (DeWitt Company, Sikeston, Mo.). mi2, which correspondedto between 12.2 and 60.8%open Photosynthetic photon flux density (PPFD) in the unshaded treatmentswithin the greenhouseattained maximum levels between canopy,depending upon not only gap area,but also stand 700 and 800 pmol m2 s- , whereas shaded treatments attained height. Stand heights in the lower intertidalzones were maximum levels around 100 pmol m-2 s-1. Measurements of shorterand thereforemore sunlightcould reach tethered maximum midday PPFD from an open site on Kosrae indicated a seeds for a given gap size. Vegetation in the lower light level of 2,223?221 (SE) /imol m-2 s-1. Assuming that 1.8- Rhi- 3.4% above canopy light reaches the mangrove understory(c.f., intertidal zone was dominated by short-statured Sherman et al. 2001), approximately40-76 pmol m 2 s-I of light zophora stylosa Griff., R. apiculata, B. gymnorrhiza, and would be expected for Kosrae. Smith (1987b), on the other hand, S. alba. In the mid and upper intertidal zones, the reported 100-350 imol m-2 s-1 of light under an Australian canopies were taller;therefore, gaps of comparablesize mangrove canopy, which may be more representativeof sites in allowed less light to reachthe tetheredseeds (21.1?2.9% Kosrae owing to similar species assemblages. The temperatureof the water in the unshaded and shade treatmentsaveraged 25.3?C open canopyvs. 43.7+12.6%for the lowerintertidal). The and 25.5?C, respectively, and did not differ significantly mid intertidalzone was dominatedmostly by B. gymnor- (P=0.773 1). rhiza, with some plots having S. alba and R. apiculata as Each individual treatment combination was imposed in a a co-dominant.The species composition of the upper separate 378-1 tank with a small submersible pump (circulation rate of 44 1 min-') on the bottom to keep the water well-mixed, intertidalzone differedfrom the other two zones in that though not aerated. Each treatment combination was replicated 26.9% was composed of X. granatumsaplings or trees. 3 times, with replicates consisting of a total of 54 seedlings - nine Both B. gymnorrhizaand S. alba as well as the occasional per salinity/shade combination. In all, we evaluated the growth R. apiculata and Barringtonia racemosa (L.) Spreng. response of a total of 162 seedlings. of the intertidalforest. Height and diametermeasurements were taken at the beginning composed the remainder upper of the experiment and at approximately bimonthly intervals. Only upperintertidal plots had matureX. granatumtrees, Numbers of leaves were also counted and observations were seeds, or seedlings, though occasional seedlings were recorded on leaf condition and the presence of black twig borer seen nearour mid intertidalplots. The averagenumber of damage at each measurementinterval. After a treatmentperiod of X. granatumseeds and seedlingsin upperintertidal zone approximately 25 weeks, lengths of the top five nodes of each seedling were measured, and seedlings were harvested and plots was 0.5 and 1.8 m-2, respectively. 113 60- (r2=0.042;P=0.4154), or gap size (r2=0.235;P=O.1869). Gap | Lower Intertidal -- Mid-Intertidal There was also no significant predictive relationship 50 . UpperIntertidal betweenseed mass and likelihoodof predation(r2=0.028; P=0.0090). 40 On most of the plots, the proportionof seeds consumed to 30 increasedrelatively steadily throughout the entire 34-day 0 period (Fig. 1). Although overall seed deterioration

- 20 0 precludedthe collection of additionaldata on crab or insect damage at days 73 and 161, evidence of fresh 10 damage was noted for some seeds at both times, suggestingthat X. granatum seeds are subjectto predation 0 for an extendedtime period. By day 73, and especially by day 161, potentially importantdifferences in seedling establishmentamong the intertidalzones were apparent(Fig. 2). Althoughthe amountof seed mortalitywas not significantlydifferent amongthe threezones for day 73 (F2,2=11.96; P=0.0771) 10 or day 161 (F2,2=8.05; P=0. 1 105), a significantly greater *0 proportion of the surviving seeds had successfully anchoredtheir roots into the soil and developed shoots in the upper intertidal plots by day 161 (F2,2=21.68;

- P=0.0441). No statistical differences were found for 30 0 1 0 2 0 3 either seed mortality or seedling establishmentin gap versus canopy plots on days 73 and 161.

Seed chemicalcomposition Days Mean seed mass and crude chemical compositionof ten Fig. 1 Cumulative amnount of Xylocarpus granatum seeds with X. 25% or more biomass consumed by crabs at several contrasting granatum seeds selected from the same batch used in intertidal positions and two levels of canopy shading (full intact the predationexperiment were contrastedwith published canopy vs. gap) in the Utwe River basin over the first 34 days data on eight other mangrove species (Table 1). X. granatum seeds are highly variable in mass but are generally larger than propagules of the other species. Virtually 100% of the seeds had some evidence of crab Crudechemical composition also differedfrom the other (91.0%) and/or insect (66.7%) damage after 34 days; species, particularlyin crude fiber content. Although a however, the overall mean proportion of seeds killed by substantialportion of the crude fiber is in the tough seed predators, defined as seeds at least 25% consumed, was coat, a smaller sample of seeds submittedfor analysis only 22.4%. Differences in the proportion of seeds with theirseed coats removedalso had a high crudefiber consumed at day 34 were not significant for intertidal content(Table 1). zone (F2,2=2.68; P=0.2721), gap versus canopy plots (FI,2=0.06; P=0.8309), mean densiometer reading

Table 1 Propertiesof mangrove propagules used in past predationstudies as well as in the currentstudy Species Cumulative Physical and chemical properties(%, ?SD) Source

(%p(%,?SE) Fresh Ash Crude Crude Crude Total mass (g) protein fat fiber carbohydrates Avicennia gertninansa 60.0?8.0 1.0?0.2 4.7?0.7 - McKee (1995) Rhizophora manglea 18.0?5.0 10.1?2.4 3.8?0.4 - - - - McKee (1995) Laguncularia racemosaa 28.0?9.0 0.3?0.1 8.6?2.1 - - - - McKee (1995) Avicennia marinaa 96.0?1.8 3.4?0.9 - 2.4?0.3 8.0?1.5 1.6?1.7 61.5?4.2 Smith (1987a) Bruguiera exaristataa 73.7?5.9 3.0?0.6 - 6.1?1.4 18.2?3.0 5.2?0.8 44.6?3.5 Smith (1987a) Bruguiera gymnorrhizaa 59.0?6.4 19.8?9.5 - 6.5?1.1 9.5?1.6 11.0?1.8 31.2?3.1 Smith (1987a) Ceriops tagala 71.7?4.3 1.4?0.3 - 5.6?1.1 7.7?2.3 19.4?6.5 22.8?4.3 Smith (1987a) Rhizophorastylosaa 50.4?10.9 30.3?10.4 - 5.3?0.5 5.3?1.3 21.4?2.0 38.2?3.8 Smith (1987a) Xylocarpus granatum 22.4?8.6 40.7?21.8 2.8?0.6 3.4?0.6 2.0?0.4 55.1?9.9 36.6?10.6 Present study (entire seed) X. granatum (cotyledon - - 3.0?0.8 5.1?0.7 4.1?0.9 42.9 ?5.1 45.0?6.6 Present study only) 114

Shoot development VZ1 Rooted, established I Rooted, not established .= oo--dB ^ N?? <55?. > ? O O O v Viable seed r -O-O O O O t-O N~~)C- +l +l +l Dead or buriedseed O ~~~+l+l +l +l +l +l +l +l +l +l +le ^- t o. 11 lt vn o) r- cl 'I ?1 C1 C1 1t It cn oo

A Gap Canopy Gap Canopy Gap Canopy 100- en X Cd qm _- _?^_en0Ct ,

80 - 'j . ~~ ~~+ +l +l +l +l +l +l +l +l +l +l +l~ -Ct r 0 oo? > =~~~~~~1 IC tn 1t-?o m mr- r 40

0) 60

40 O-O O-t--- +l +l 0) 4-4~ +1 O1 1 + + +l Ct ~~~~00?1 00 tf cl C-i- 11 cl 0006 0 0 20- O sQ m - - ~~~~~~~~t^ -

CIS 0

4 . +l +l +l +l +l +l +l +l +l +l +l O Nt = ? N ^ o-t ^ > m b t o eas wB Gap Canopy Gap Canopy Gap Canopy 4

4._ i0 oo j 80- 0 0 -0 60- e ~~~+i+l +l +i +i +l +i oo +l +l +l O r- - C U: = ~~~t) _ tt v) _) O' n 00oo oo cn IC U:~~~~C 6--4 0 0600-0- C 0006 0 0 (D 40 a) C)~~~~~0 O-4t nC

20- S ~~~~~~~~~~~+106 U~~~~~V 1^v) CS-O C) C-4 t C4

0 E ~~~~+l+l +l +l +l +l +l IC +l +l +l C4 r- 0e~~~C O. ,* * ,*t- 0,t ) ,*\o ( t en v) Lower Mid- Upper Ch- 00 o MN C O O kn cn Intertidal l ntertidal i ntertidal S~~~~~0 ,:- t f_

Fig. 2 Condition of X. granatum seeds tethered in the Utwe River basin after A 73 days and B 161 days. Seedlings with shoot 8 3 > N~~~~~~~~~~~~1- C1 development and rooted were considered to be successfully established within the respective intertidaland/or canopy locations w0 ._ ~~+1+1 +1 +1 +1 +1 +1 oo +1 +1 +1 C4, ?- r- * r- en "t - en 0 r- 1 I Ct~~ ~~v _ _ Seedling responsesto salinity,tidal flooding, and shade Survival of X. seedlings to the granatum subjected co t nn n wn e o salinity/flooding regime and shade treatmentsin the greenhousefor 25 weeks was 93%.Virtually all of theivi o 00 seedlings that died are believed to have been killed by black twig borers rather than by the effects of the treatmentsthemselves. Seedlings killed by the black twig borerall had similarpatterns of decline, characterizedby w 4 E w e b -U ' S =~~~~~~~~~~~C1 rapidwilting of the leaves and the presenceof bore holes on the stem. Approximately 28% of the surviving seedlings showed some evidence of attackby black twig borers; mainly, the presence of dried sap around a borehole indicated a successfully repelled attack. The growth of surviving seedlings appearedto be relatively unaffected, with some of the largest seedlings in the experimentbeing among those with signs of black twig borerattack. 115 100 Means for 14 response variables are presented by . o-Unshaded treatment in Table 2, and a 90 * Shade summary of statistical differencesis presentedin Table 3. When seedlings were 80 subjectedto 23 ppt salinity, stem diameterand biomass, root biomass, and total biomass were reduced(Tables 2, Z 70 / 3) as comparedwith <0.5 ppt controls,but therewere no

I 60 significanteffects on any other morphologicalvariables measured.Compared to the 23 ppt salinitysoil saturation 50 treatment,seedlings in the tidal simulationtreatment (i.e., periodicflooding with 23 ppt salinity water) - differedby 40 . maintainingslightly greater 0 20 40 60 80 100 120 140 160 180 mean root, stem, and total biomass as well as a highermean stem weight ratio. Days Shadinghad far greatereffects on seedlinggrowth and Fig. 3 Stem height growth (cm) of X. granatumseedlings subjected morphology than 23 ppt salinity or simulated tidal to different light environmentsfor 25 weeks flooding. Unshaded seedlings were on average 52% taller, had 32 (171%) more leaves, and had >4 times as

Table 3 Significance values (Pt>F) from analysis of covariancefor X. granatumseedlings subjectedto differentcombinations of sunlight, salinity, and tidal flooding

Variable Light Salinity Tidal flooding Lightxsalinity Lightxtidal flooding Height (cm) ** NS NS NS NS Diameter (mm) * NS NS NS Leaves (no.) ** NS NS NS NS Leaf biomass (g dry wt) NS NS NS NS Stem biomass (g dry wt) * * NS NS Root biomass (g dry wt) ** * * NS Total biomass (g dry wt) * * NS NS Leaf area (cm2) ** NS NS NS NS Individualleaf area (cm2) * NS NS NS NS Mean internode length (cm) ** NS NS * * Specific leaf area (cm2g2-)a NS NS NS NS Leaf weight ratio NS NS NS NS NS Stem weight ratio * NS * NS * Root:stem ratio NS NS ** NS Significant variables (at a=0.05) 13 4 4 3 2 NS P>0.05, *0.01

Table 4 Means for foliar micro- and macronutrientconcentrations (?SE) of X. granatumseedlings subjectedto different combinationsof sunlight, salinity, and tidal flooding. For abbreviations,see Table 2 Unshaded 80% shade FS SS TS Mean FS SS TS Mean Macronutrient(%) N 1.32?0.37 2.16?0.16 2.53?0.02 2.01?0.21 2.46?0.26 2.69?0.18 2.35?0.13 2.50?0.11 P 0.17?0.02 0.13?0.02 0.16?0.01 0.15?0.01 0.18?0.04 0.17?0.02 0.19?0.02 0.18?0.01 K 1.73?0.13 1.47?0.24 1.61?0.14 1.60?0.10 1.77?0.13 2.31?0.19 2.40+0.30 2.16_0.15 Ca 3.53?0.31 3.28?0.11 3.37?0.17 3.39?0.11 3.87?0.11 3.65+0.30 3.65?0.18 3.72?0.11 Mg 0.33?0.03 0.20?0.04 0.24?0.01 0.26?0.02 0.42?0.08 0.35?0.02 0.33?0.04 0.37?0.03 Na 0.27?0.02 0.74?0.16 0.94?0. 12 0.65?0. 11 0.23?0.03 0.74?0.15 0.93?0.18 0.63+0.12 Micronutrient(pg g-1) Mn 36.7?3.2 58.3?2.9 85.0?18.6 60.0?8.9 41.0?7.0 48.0?3.2 53.0?14.1 47.3?5.0 Fe 43.3?7.0 77.0?21.5 42.7?5.8 54.3?8.8 45.3?1.8 53.0+4.0 37.7?1.3 45.3?2.6 Cu 4.7?1.5 4.7?0.3 4.3?0.9 4.6?0.5 4.0?0.6 7.7?0.7 7.0?1.5 6.2?0.8 Zn 4.0?0.6 7.0?1.0 8.3?0.9 6.4?0.8 9.0?1.0 8.3?0.9 10.0?1.5 9.1?0.6 B 27.0?4.7 121.0?10.4 212.3?35.5 120.1?28.8 50.3?4.7 103.7?15.3 240.7?21.3 131.6t29.4 Ratio Na/K 0.16?0.02 0.54?0.14 0.61?0.13 0.43?0.09 0.13?0.01 0.33?0.07 0.39?0.05 0.28?0.05 Na/Ca 0.08?0.01 0.22?0.04 0.28?0.04 0.19?0.03 0.06+0.01 0.20?0.04 0.26?0.06 0.17?0.04 116 Table 5 Significance values (Pr>F) from ANOVA comparisons for foliar nutrientconcentrations of Xylocarpus granatum seedlings subjected to different combinations of sunlight, salinity, and tidal flooding Variable Light Salinity Tidal flooding Lightxsalinity Lightxtidal flooding

N NS * NS NS NS P NS NS NS NS NS K * NS NS NS NS Ca NS NS NS NS NS Mg NS * NS NS NS Na NS ** NS NS NS Mn NS * NS NS NS Fe NS NS * NS NS Cu * NS NS NS NS Zn NS NS NS NS NS B NS ** ** NS NS Na/K ** * NS NS NS Na/Ca NS ** NS NS NS Significant variables (at a=0.05) 3 7 2 0 0 NS P>0.05, *0.01

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C) EO tI v- C' ,6 rN N "C O: 2c rt | 119 pericarpwere much less likely to survive and grow well occur in some mid to lower intertidalhabitats) did not than seeds with fewer boreholes.Only 3.3% of the seeds exceed the physiologicaltolerance of the species. Wells in our study had more thantwo boreholesand, overall, it (1982) reported that X. granatum can withstand consid- appearsthat crabs were responsiblefor greaterdamage erable periods of inundationby freshwaterbut occurs and more seed mortalitythan insects. most frequentlyon brackishsites flooded infrequentlyby seawater. Our results, coupled with field observations, suggest X. granatum can also withstand regular flooding Toleranceof salinity,tidal flooding, and shade similar to that experiencedin areas with semi- diurnal tidal regimeswith waterof two-thirdsthe salinityof full- Seedlings growing in the 23 ppt salinity treatments strengthseawater. survivedas well as seedlings in freshwater,and, though Shadingclearly reducesX. granatum seedling growth growth was reduced significantly in some cases, there and thereforemight limit the capabilityof X. granatum to were no indicationsthat 23 ppt salinityis enoughto cause becomeestablished under forest canopies. Gaps, however, severe physiological stress. Leaf Na:K ratios in the are not uncommonin any of the intertidalzones (Ewel et presenceof 23 ppt salinity,for example,averaged 0.61 or al. 1998b) and thereforeshading alone should not be a less, which is below the 1.0 level often associatedwith factor limiting the intertidaldistribution of the species. severe stress in glycophytes(Wyn Jones et al. 1979) and Shading interacted significantly with salinity or tidal well below the levels reportedfor some other mangrove floodingfor only a few growthvariables (Table 3), which species (Downton1982; Ball and Farquhar1984; Naidoo might be furtherevidence that the salinity and flooding 1985; Popp et al. 1985). The increase in Na associated regimesexamined were not nearthe limits of X. granatum with 23 ppt salinity apparently does not interfere physiologicaltolerance. substantiallywith the uptakeof either K or Ca, which is believed to occur with many other species (Marschner1986; Grattanand Grieve 1999). LoweredK Implicationsfor furtherresearch concentrationswith high light, however, suggests that there may be a more substantialion imbalanceat high Of the factorsexamined in this study,limitations imposed light levels. This might explain why Popp et al. (1985) on seedling growthby salinityor tidal flooding appearto reportedthat X. granatum leaves collected from mature exert a slightly greater influence on the intertidal trees (presumablyexposed to light levels in excess of distributionof X. granatum than seed predation,but none those in our greenhouse experiment)had Na:K ratios of the factors tested clearly control the species distribu- >1.0. tion. Physiologicaleffects of salinityor flooding on seed Unfortunately,limitations on available greenhouse germination,the influenceof tides and freshwaterloading space preventedus from testing seedlings over a wider on dispersal, or leaf herbivory on seedlings might rangeof salinitylevels, such as an optimallevel of around ultimatelyprove to be more importantfactors than those 8 ppt (Hutchingsand Saenger 1987; Smith 1992), a full- tested in this study and could be fruitfultopics for future strength seawater treatment,and a fluctuating salinity research. treatment.We believe, however, that the 25-week expo- One phenomenonwe observedin the mid and lower sure to 23 ppt salinity effectively demonstratesthat X. intertidalhabitats was that seeds that escaped predation granatum seedlings are capable of surviving on sites still largely failed to become rooted in the substrate.In representativeof at the least mid intertidalzones, where many such cases, the radiclehad emergedfrom the seed, matureX. granatum trees are generally absent or quite but the seed remainedloose on the soil surface.We do not rare.Our design does not allow us to rule out the possible know whether this failure to establish is due to the detrimentaleffects of occasional higher salinity pulses, frequentmovement of the seed by tidal action (which butX. granatum reportedlygrows on sites with maximum might break fine roots beginning to enter the soil), a salinitylevels of 34 ppt (Wells 1982; Smith 1992), a level physiological limitation on root development,or some rarelyexceeded in mid intertidalhabitats on Kosrae(Ewel othercause. et al. 1998a). Also, Bunt et al. (1982), in their study of It is possiblethat a variantof Rabinowitz's(1978) tidal mangrovespecies distributionalong five rivers in north- sorting hypothesis might apply to X. granatum, even ern Queensland,singled out X. granatum as a species though the original form of the hypothesis has been whose distributionis poorly correlatedwith river water largely rejected(Tomlinson 1986; Smith 1992). Seeds of salinity, which suggests that it can grow over almost the Xylocarpus species float well (Hutchings and Saenger completesalinity range from freshwater to seawater.Seed 1987), and althoughmost are believed to be nonviableby productionand periodicity,on the other hand, may be then, they are frequentlyfound on Pacific islandsfar from influenced by salinity, potentially having a significant where they are naturally established (Degener and effect on the overall propensityfor regenerationin X. Degener 1974; Nakanishi 1981, 1983; Hacker 1990). granatum. Highlymobile seeds fromebbing/flowing tides Could it be that their ability to float so well, combined and uplandrunoff likely decreasesthis effect on Kosrae. with their relatively slow germination and rooting, Likewise, our tidal flooding treatment(albeit with effectively sort most X. granatum seeds out of lower shallowerflooding and less reducedconditions than might intertidalzones that flood essentiallyevery day? 120 Anotherobservation we have made in the field is that Dahdouh-GuebasF (2001) Mangrove vegetation structuredynam- X. granatum seedlings are relatively common in some ics and regeneration. PhD dissertation. Vrije Universiteit Brussel, Brussels areas where maturetrees are absent.No other mangrove Dahdouh-GuebasF, VerneirtM, Tack JF, SpeybroechDV, Koedam species on Kosraeexhibits a similarpattern. In virtually N (1998) Propagulepredators in Kenyan mangroves and their every case, we have observedthat X. granatum seedlings possible effects on regeneration.Mar FreshwaterRes 49:345- are heavily attacked by leaf herbivores (as of yet 350 Davis JH (1940) The and geologic role of mangroves in unidentified).Differential herbivory across the intertidal Florida. Publications of the Carnegie Institute, no. 517. zone, or on sites dominatedby matureX. granatum trees Washington,D.C. versusthose thatare not, thereforemight be an important Degener 0, Degener I (1974) Flotsam and jetsam of Canton Atoll, factor. This could prove to be a variation of the South Pacific. Phytologia 28:405-413 proposedfor man- Downton WJS (1982) Growth and osmotic relations of the dominance-predationmodel originally mangrove Avicennia marina,as influenced by salinity. Aust J groves by Smith (1987a), in which seed predationis Plant Physiol 9:519-528 expected to be relativelylow undercanopies dominated Duke NC (1999) The 1998 survey of Rhizophora species in by conspecifics and relatively high under canopies Micronesia. Unpublished report to the USDA Forest Service, by other species. In the case of X. granatum, Institute of Pacific Islands Forestry, Honolulu, Hi. Marine dominated Group, Botany Department,University of Queensland, it might be better regardedas a dominance-herbivory St. Lucia, Queensland model. Egler FA (1950) Southeast saline Everglades vegetation, Florida, Smith (1987a) noted that no single factor is likely to and its management.Vegetatio 3:213-265 account for the distributionpatterns of all 45 woody Ewel KC, Bourgeois JA, Cole TG, Zheng S (1998a) Variation in environmental characteristicsand vegetation in high-rainfall species thenknown to occurin Australianmangroves. We mangrove forests, Kosrae, Micronesia. Global Ecol Biogeogr agree and furtherbelieve that even for a single species, Lett 7:49-56 observedpatterns of distributionwill rarelybe tracedto Ewel KC, Zheng S, Pinz6n ZS, Bourgeois JA (1998b) Environ- only one factor. Instead, they will be explained much mental effects of canopy gap formation in high-rainfall the interactionsof severalbiotic and mangrove forests. Biotropica 30:510-518 more effectively by GrattanSR, Grieve CM (1999) Salinity-mineralnutrient relations in abiotic factors. horticulturalcrops. Sci Hortic 78:127-157 Hacker JB (1990) Drift seeds and fruit on Raine Island, northern Acknowledgements The authorsthank Jason Jack, Erick Waguk, Great BarrierReef, Australia.J Biogeogr 17:19-24 Tara Tara, and Robert Cabin for their assistance with the field Hutchings P, Saenger P (1987) Ecology of mangroves. University portions of this project and Cheyenne H. Perry, Thomas G. Cole, of QueenslandPress, St. Lucia, Queensland and David Fujii for helping with the greenhouse experiment. Krauss KW, Allen JA (in press) Factors influencing the regener- Katherine C. Ewel, Ernesto Medina, Ram Oren, James Baldwin, ation of the mangrove Bruguieragymnorrhiza (L.) Lamk. on a Tammy Charron,and two anonymous referees provided excellent tropical Pacific island. For Ecol Manage technical, statistical, and editorial reviews of this manuscript. Lantican CB, Baldwin JA (1994) Training notes on design and Gratitudeis extended to Wayne P. Sousa, Farid Dahdouh-Guebas, analysis of forestry experiments. Forestry Research Support and Todd E. Minchintonfor providing ideas and/or additionaldata Programmefor Asia and the Pacific, and South Pacific Forestry for incorporationinto Table 6. Finally, the authors would like to Development Programme,field document no. 4, RAS/92/361 thank the Kosrae State Development Review Commission for their Louda SM (1989) Differential predation pressure: a general supportof work in Kosrae and Jim Brewbakerfor providingaccess mechanism for structuringplant communities along complex to the University of Hawaii greenhouse facility at Waimanalo, environmentalgradients? Trends Ecol Evol 4:158-159 Hawaii. Mention of trade names does not constitute endorsement MabberleyDJ, Pannell CM, Sing AM (1995) , Fl Mal I, by the U.S. Government. 12/1:1-407 MacLean CD, Whitesell CD, Cole TG, McDuffie KE (1988) Timberresources of Kosrae,Pohnpei, Truk, and Yap, Federated States of Micronesia.Resource bulletin PSW-24. USDA Forest References Service, Berkeley, Calif. Macnae W (1968) A general account of the fauna and flora of the Allen JA, Ewel KC, Jack J (2001) Patterns of natural and mangrove swamps and forests in the Indo-Pacific region. 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