seed dispersal, seedling establishment and gap partitioning ...keywords] dispersal limitation\...

$: Seed dispersal, seedling establishment and gap partitioning ...Keywords] dispersal limitation\ establishment limitation\ gap\ gap light environment\ seedling establishment Journal$
Journal ofEcology 0887\75\ 563Ð578

563

Seed dispersal\ seedling establishment and gappartitioning among tropical pioneer treesJ[W[ DALLING" \ STEPHEN P[ HUBBELL"$ and KATIA SILVERA%!Smithsonian Tropical Research Institute\ Apartado 1961\ Balboa\ Repu"blica de Panama"^ $Department ofEcology and Evolutionary Biology\ Princeton University\ Princeton\ NJ 97433\ USA^ and %Departamento deBota"nica\ Universidad de Panama"\ Repu"blica de Panama"

Summary

0 We examined the abundance and distribution patterns of pioneer seeds in the soilseed bank\ and of pioneer seedlings in 42 recently formed gaps\ in a 49!ha forestdynamics plot on Barro Colorado Island "BCI#\ Panama[ The aim was to assess theimportance of dispersal limitation "failure of seeds to arrive at all sites suitable fortheir germination# and establishment limitation "failure of seeds having reached a siteto germinate successfully and establish as seedlings# in determining patterns of gapoccupancy[1 The abundance of seeds in the soil seed bank was strongly negatively correlatedwith seed size\ but was not correlated with the abundance of reproductive!sized adulttrees in the plot[ In contrast\ the abundance of pioneer seedlings × 09 cm height innatural gaps was strongly correlated with adult abundance\ but was not correlatedwith seed size[2 Seedlings were non!randomly distributed among gaps\ but seedling abundance wasnot directly related to gap size\ and there was no evidence of partitioning of the lightenvironment of gaps by small seedlings[ Large di}erences in growth and mortalityrates among species were observed after 0 year\ and this may result in the gap sizepartitioning previously found in saplings of the same species[3 Seedlings of most species\ particularly those with large seeds\ were relatively moreabundant than expected in gaps close to their conspeci_c adults[ Proximity to repro!ductives\ and by inference dispersal limitation\ therefore exerts some e}ect on seedlingdistribution[ None the less\ large di}erences between seed and seedling abundancesfor some species\ and low seedling occupancy rates in some gaps close to adultconspeci_cs\ suggest that seedling emergence probabilities and species!speci_c estab!lishment requirements may also be important determinants of local abundance[

Keywords] dispersal limitation\ establishment limitation\ gap\ gap light environment\seedling establishment

Journal of Ecolo`y "0887# 75\ 563Ð578

Introduction

Attempts to understand the coexistence of tree speciesin tropical forests have focused on biotic interactionsand the specialized regeneration requirements of thespecies concerned "Grubb 0866^ Denslow 0879\ 0876#\and on how history and probabilistic processes canpredict the dynamic properties of plant communities"Hubbell + Foster 0875a#[ While chance and biologyare both undoubtedly important\ probabilistic and

Correspondence] Jim Dalling "fax 496 1612954^ e!mail] dal!lingjÝbci[si[edu#[

deterministic processes have rarely been compared[This is partly due to the complexity of scaling upfrom detailed autecological studies that emphasizethe interactions among a few species in species!richcommunities[ One approach to this problem is toexamine in detail mechanisms underlying the coexist!ence of a single functional group of species[ An advan!tage of this approach over selecting species at randomfrom the entire community is that it addresses subtledi}erences among apparently ecologically similarspecies[

Pioneer species "which are characterized by aninability to persist as seedlings in the forest under!

564J[W[ Dalling et al[

Þ 0887 BritishEcological Society\Journal of Ecology\75\ 563Ð578

storey# form a small functional group of tropical treesthat are attractive for study since their recruitmentsites can be de_ned andmeasured "e[g[ Brokaw 0871a^Popma et al[ 0877^ but see Lieberman et al[ 0878# andbecause processes of growth and mortality are playedout rapidly[ Extensive work carried out by Brokaw"0871b\ 0874a\b\ 0875\ 0876# has highlighted di}er!ences in regeneration requirements among a subset ofthe c[ 39 pioneer species on Barro Colorado Island"BCI#\ Panama#[ Much of Brokaw|s work concernedthe e}ects of gap size on pioneer abundance and spec!ies composition\ and he found convincing evidencefor di}erent gap size requirements for three pioneerspecies that were based on both mortality patternsand growth performance of saplings "Brokaw 0876#[He further argued that a performance hierarchy evi!dent across gaps of di}erent sizes should also bemani!fested across the gradient from the gap centre to thegap edge[ More recently\ Brown "0885# found someevidence for gap partitioning within a large gap forthree dipterocarp species[ However\ in contrast toBrokaw|s _ndings\ the relative growth performanceamong the species remained unchanged from the gapcentre to the forest edge\ and was instead due solelyto di}erential seedling mortality[

Other studies have stressed the importance ofwithin!gap heterogeneity for the maintenance of treespecies diversity[ On BCI\ pioneers in general appearto be most abundant on mineral soil and may be moreabundant in large gaps than in small gaps in partbecause large gaps are more likely to be caused bytreefalls that resulted in soil disturbance "Putz 0872#[In French Guyana\ some\ but not all\ pioneers aremore abundant on tip!up mounds of fallen trees"Riera 0874#\ and in lowland forest at La Selva\ CostaRica\ Brandani et al[ "0877# found that many treespecies were associated with di}erent zones "root\ boleand crown# within gaps\ and suggested that theseassociation patterns resulted from non!random mor!tality of seedlings\ rather than the di}erential ger!mination patterns observed by other workers "Raich+ Gong 0889#[

None the less\ gap size di}erences and within!gapheterogeneity appear to be insu.cient to explain thecoexistence of large numbers of apparently similargap!dependent species "Denslow 0884#[ Species dis!tribution patterns within and among gaps are knownto be clumped "Brokaw 0875\ 0876^ Brandani et al[0877# but the importance of limited seed dispersaland seed availability in the seed bank has not beenexamined[ These factors may reduce competitiveinteractions to only a subset of species present in eachgap[ Recent evidence indicates that the soil seed bankof pioneer species is much more dynamic than waspreviously thought "Alvarez!Buylla + Mart(#nez!Ramos 0889^ Chandrashekara + Ramakrishnan0882^ Dalling et al[ 0886\ 0887#\ with turnover ratesfor some species of little more than 0 year[ Similarly\while pioneers have traditionally been considered to

be capable of substantial long!distance seed dispersalof 649m or more "Holthuijzen + Boerboom 0871^Denslow+Gomez!Diaz 0889# these reports are basedon inferred rather than measured seed sources[ Seedshadows have rarely been measured directly for pion!eer species\ but in all cases examined seed densitiesdecline to low levels 29Ð59m beyond the crowns ofadult individuals "Alvarez!Buylla +Mart(#nez!Ramos0889^ Laman 0885^ Dalling et al[ 0886#[

Recent theoretical work has shown that strong dis!persal limitation can promote species richness by gre!atly slowing competitive exclusion "Tilman 0883^Hurtt + Pacala 0884#[ Under dispersal limitation\ gapsites are frequently not won by the best competitor inthe community but by the best competitor among therestricted set of species that arrives at the gap site[Although steady!state dispersal limitation has beenpostulated to be a widespread phenomenon amongchalk grassland perennials\ and large!seeded shade!tolerant tropical tree species "Grubb 0875^ Silman0885#\ the possibility that it is also strong in small!seeded\ highly dispersive pioneer species has not beenconsidered previously[ Nevertheless\ high dis!persability may actually be a sign that dispersal limi!tation has been a strong selective force during theevolution of pioneer life histories[

In this study we used the annual canopy heightsurvey carried out in the 49!ha forest dynamics ploton BCI to locate a large sample of newly formedcanopy gaps within a mapped forest stand[ Focusingon a group of 13 known pioneer taxa\ we looked forevidence of gap size partitioning\ and for dispersallimitation "strictly speaking\ seedling emergence lim!ited by the proximity of conspeci_c adults#[ Speci_!cally we asked]

0 What is the size distribution of gaps\ and how is theabundance of seedlings related to it<1 How does the abundance distribution of pioneerseedlings compare with that of seeds in the soil seedbank and adult trees<2 Do species show di}erential growth responses tolight availability<3 Are seedling dispersion patterns skewed towardsadult plants\ and does the proximity to adults explainany variation in seedling abundance among gaps<

Methods

STUDY AREA

The study was carried out in seasonally moist tropicalforest on Barro Colorado Island "BCI#\ Panama#"8>09?N\ 68>40?W#[ Rainfall on BCI averages1599mmyear−0\ with a pronounced dry season fromJanuary until April "Rand + Rand 0871#[ The ~oraand vegetation of BCI have been described by Croat"0867# and by Foster + Brokaw "0871#[ Geology andhydrology have been described by Dietrich et al[

565Gap colonizationby tropical trees


"0871#[ Investigations were carried out within the For!est Dynamics Project 49!ha plot\ on the central pla!teau of BCI[ The plot is described in detail by Hubbell+ Foster "0872#[ Nomenclature follows Croat "0867#[

SELECTION AND CENSUSING OF GAP SITES

To locate recent treefall gaps within the 49!ha plot\we used data from the canopy height census that hasbeen conducted annually "except for 0883# within theplot using the procedure described in detail by Hub!bell + Foster "0875b# and Welden et al[ "0880#[ Can!opy height was assessed using a range pole at theintersection point of each 4m× 4m subplot\ and themaximum canopy height was divided into the fol!lowing size classes] 9Ð1m\ 1Ð4m\ 4Ð09m\ 09Ð19m\19Ð29m and × 29m[ In March 0885 we identi_ed allthe potential new treefall gap sites "n& 69# as samplepoints that were ³ 4m height in 0884 but had been× 19m in 0882\ and that were at least 39m from theedge of the 49!ha plot[ Contiguous low canopy samplepoints were considered as single gaps\ and the area ofthe gap was estimated from the number of low canopypoints within it[ Hence an isolated low canopy pointwas considered to represent a gap³ 14m1\ and eachadditional low canopy point increased the gap size by14m1[At each low canopy site we recorded how the gap

had been formed "branch fall^ standing dead tree^ treesnapped^ tree uprooted^ multiple treefall#[ At sitesconsisting of a single low canopy sample point\ weestablished a grid of 25 0!m1 plots centred on thesample point[ We sampled more than the 14m1 pro!jection of the canopy opening on the forest ~oor\ sincethe e}ects of treefall gaps on seedling establishmentcan extend beyond the edge of the canopy opening"Popma et al[ 0877#[ For large gaps the grid size wasincremented by 29m1 for each additional contiguouslow canopy sample point[Within each 0!m1 subplot we searched for all seed!

lings from a list of 13 pioneer taxa that had beendrawn up prior to the study "see Species selectionbelow#[ All seedlings of these taxa × 09 cm in heightwere tagged and their height measured[ Additionallywe recorded\ but did not tag\ all seedlings of thesetaxa³ 09 cm in height[ Seedlings were treated as indi!viduals\ except for Cecropia in three adjacent 0!m1

plots in one gap that contained 29\ 39 and 49 seedlingsaggregated together in bird or bat faecal clumps[These clumps were counted as single individuals foranalyses[ All seedlings were recorded as either rootingin the soil or in elevated microsites "e[g[ on fallentrunks and roots#[ From previous studies "Dallinget al[ 0884\ 0886\ 0887^ Dalling + Denslow 0887# weare con_dent that we can identify these taxa even atthe cotyledonary stage[ InMarch 0886 we remeasuredthe height of all tagged seedlings and recordedwhether seedlings had been damaged and resprouted[

Estimates of seed abundances in the soil seed bank

for 06 pioneer tree species were based on 081 soilsamples of 9[14 l collected at 9Ð2 cm depth every 2months over a 0!year period along transects laid outaround eight reproductive!sized pioneer trees scat!tered throughout the 49!ha plot[ Correlations betweenseed bank density\ seed size and seedling abundancein the plot were performed using values for the highestseed bank density for each species over the year[Details of the sampling methodology for the seedbank study\ and of the seed bank dynamics of indi!vidual species\ are provided in Dalling et al[ "0886\0887#[ Data on seed size are from Dalling et al[ "0886#with additional collections made on BCI during 0885[

SPECIES SELECTION

Twenty!four species "henceforth called {focal species|^Table 0# were chosen for inclusion in the study\ basedupon patterns of seedling distribution we haveobserved on BCI\ regeneration requirements of spec!ies reported in the literature "Putz 0872^ Brokaw0874a\ 0876^ Garwood 0875#\ and on our capacityto identify very small seedlings[ We included threemultispecies taxa\ Cecropia\ Spondias and Zanthox!ylum\ because they are common in gaps on BCI eventhough we are unable to identify them to species assmall seedlings[ Analyses were carried out at the gen!eric level on the seedlings and adults of these taxa[Since a continuum of light requirements exists for treespecies growing on BCI\ we could not delineate ade_nitive pioneer guild^ however\ for all studied spec!ies for which data are available "n& 03# a high pro!portion of recruits reaching × 0 cmd[b[h[ are foundin gaps "Welden et al[ 0880# and have high scores inthe demographic index of Condit et al[ "0885#\ indi!cating high growth\ high mortality and a strong tend!ency to recruit into gaps[ We also included one shade!tolerant species\ Alseis blackiana[ Alseis was includedfor comparison since it is common in gaps\ commonin the soil seed bank "Dalling et al[ 0886# and appar!ently rare or absent in the forest understorey as a smallseedling despite the persistence of larger seedlings andsaplings in the shade "J[ Dalling\ personal obser!vation#[

LIGHT MEASUREMENTS

We assessed the light environment of gaps and ofindividual seedlings inOctoberÐNovember 0885 usinghemispherical "_sheye# photography[ To characterizegaps we took one photograph at each of the 4m× 4mgrid intersections within gaps\ at 0m above theground[ To characterize the light environment ofseedlings\ we randomly selected up to 39 seedlings ofeach species\ ranging between 09 cm and 39 cm inheight in the initial census in FebruaryÐMarch 0885[Actual sample sizes for individual species varied"range n& 01Ð24# since many seedlings initially rec!orded in March were dead or had resprouted by Nov!



Table 0 Demographic and life!history characteristics of the focal species[ Reprod[ d[b[h[& diameter at breast height at _rstreproduction[ Density measurement is for reproductive!sized individuals[ A& animal dispersed^ W&wind dispersed[ Abun!dance in the surface 2 cm of the seed bank ¦&³ 09 seeds mÐ1^ ¦¦³ 49 seeds mÐ1^ ¦¦¦× 49 seeds mÐ1 "data fromDalling et al[ 0886#

Reprod[ d[b[h[ Seed mass" Dispersal Recorded inTaxa "cm# "mg# agent seed bank<

Alchornea costaricensis Pax + Ho}m[ 19 27[49 A ¦Alseis blackiana Hemsl[ 19 9[01 W ¦¦¦Annona spraùei Sa}[ 7 39[39 A ÐApeiba membranacea Spruce ex Benth[ 29 03[19 A ¦Casearia arborea "L[ C[ Rich# Urban 19 0[54 A ¦Cecropia spp[ L[ 7Ð29 9[4Ð9[5 A ¦¦¦Ceiba pentandra "L[# Gaertn[ 59 54[99 W ÐCordia alliadora "R[ + P[# Cham[ 19 01[49 W ÐCroton billberìanus Mu( ll[ Arg[ 4 13[9 A ¦Ficus insipida Willd[ 39 0[59 A ¦¦Guazuma ulmifolia Lam[ 19 3[59 A ¦Jacaranda copaia "Aubl[# 29 3[69 W ¦¦Luehea seemannii Tr[ + Planch[ 29 0[89 W ¦¦Miconia arèntea "Sw[# DC 00 9[97 A ¦¦¦Ochroma pyramidale "Cav[# Urban 19 5[59 W ¦Palicourea ùianensis Aubl[ 0 03[29 A ¦Pseudobombax septenatum "Jacq[# Dug[ 39 77[29 W ÐSapium caudatum Pitt[ 19 53[99 A ÐSolanum hayesii Fern[ 3 1[39 A ¦Spondias spp[ L[ 29 635Ð0315 A ¦Terminalia amazonica "J[ F[ Gmel[# Exell 29 2[79 W ÐTrema micrantha "L[# Blume 19 2[89 A ¦¦Turpinia occidentalis Croat 19 39 A ÐZanthoxylum spp[ 19Ð29 00Ð25 A ¦¦

"Air!dry diaspore masses are given "without wings#[ For Spondias the diaspore is a _brous endocarp[ Seed mass for Turpiniais estimated from seed dimensions in Croat "0867#[

ember\ and we only report data for the 09 most com!mon species[ The height at which photographs weretaken depended on plant size\ but was always³ 4 cmfrom the shoot apex[

Photographs were taken with Kodak Tri!X panASA!399 black and white _lm "Eastman Kodak\Rochester\ NY# using a Nikkor 7!mm hemisphericallens and aNikon FM1 camera "Nikon\Melville\ NY#[Photographs were analysed using the video imageanalysis program CANOPY "Rich 0878^ Rich et al[0882#[ Images were input through a Sanyo CCDVDC2713 video camera _tted with a Nikkor 44mmMicro lens\ and the digitized video image "401× 379pixels# displayed on a Panasonic WV!4309 monitor[One of us "KS# was responsible for setting the thr!eshold image intensity value classifying the openingsand vegetation for all photographs[ Although thisdetermination involves subjectivity\ practised oper!ators can achieve a high degree of repeatability "Richet al[ 0882 and references therein#[

The indirect site factor "ISF#\ de_ned as the pro!portion of di}use skylight\ and the direct site factor"DSF#\ de_ned as the proportion of direct sunlightunder a canopy relative to that in the open\ were usedto calculate an estimated global site factor "GSF#[GSF is de_ned as the total proportion of global radi!ation under a plant canopy relative to that above it\

and is the weighted sum of ISF and DSF "Rich 0878^Canham et al[ 0889#[ ðGSFŁ& pitiðISFŁ¦ pdtdðDSFŁ\where pi is the proportion of di}use skylight\ pd isthe proportion of direct sunlight received above thecanopy\ and ti and td are the proportions of di}useskylight and direct sunlight that are transmittedthrough the canopy[ For our estimated GSF\ weassume that incident radiation was split evenlybetween di}use and direct radiation "i[e[ pd and piboth & 9[4^ Canham 0877#[

DATA ANALYSIS

Seedling dispersion patterns of individual species wereexamined using a nearest neighbour analysis of pion!eer seedlings to conspeci_c "or congeneric# adult treesof reproductive size[ Data from both the 0889 and the0884 censuses of the 49!ha plot were used to _ndnearest adults\ since the exclusive use of the 0884census may have excluded individuals that died shor!tly before or after gap formation in 0882Ð83\ whereasexclusive use of the 0889 census may have excludedrapidly growing individuals of species that are repro!ductive at small diameters "e[g[ Palicourea andCroton#[ Reproductive sizes were estimated from fruitcensuses carried out in the 49!ha plot "J[ Dalling\unpublished data^ S[J[ Wright\ J[ Pavon + A[ Jara!



millo\ unpublished data#[ For most species\ adult cen!sus year "0889 vs[ 0884# and small changes in theestimated size!at!reproduction had only a very smalle}ect on the median distance between adult and seed!ling[

We used the KolmogorovÐSmirnov two!sampletest to test the null hypothesis that the distribution ofseedlings of a target species is identical to that of allfocal species with respect to the distribution of adultsof the target species[ In principle the analysis is similarto that described by Hamill + Wright "0875#[ Foreach target species we generated a cumulative fre!quency curve of distances of seedlings to the nearestreproductive!sized conspeci_c adult "or congenericadult for Cecropia spp[ and Zanthoxylum spp[# andcompared it to a cumulative frequency curve gen!erated from the distribution of seedlings of all 13focal species vs[ adults of the same target species[ Thestatistic for the two!sample KolmogorovÐSmirnovtest is de_ned by the module of the maximum di}er!ence between the cumulative distributions "Dmax# andthe sample sizes of the curves to be compared "n0\n1#[The level of signi_cance was calculated from theobserved value for Dmax using the expression]

P& 1e Ð ð"1 "n0n1# "Dmax#1#:"n0¦ n1#Ł

where P is the smallest level of signi_cance at whichthe null hypothesis is rejected "Pacheco + Henderson0885#[ Although our application of this test violatesthe assumption of mutual independence between thetwo populations being compared "seedlings of thetarget species are included in the sample of all focalspecies#\ this remains a conservative test of dispersiondi}erences since departures in the cumulative fre!quency distributions can only result from over orunder!representation by species other than the targetspecies[ We included the target species in the all!focalspecies curve since many plots contained only oneseedling "often that of the target species#[ Seedlingsthat were closer to the edge of the 49!ha plot thanto the nearest target adult were excluded from theanalysis\ hence the sample size for the all!speciesaccumulation curve varies slightly between species[To analyse e}ects of distance from the nearest adult

conspeci_c on within!gap seedling abundance we usedgeneralized linear modelling techniques "McCullagh+ Nelder 0878# implemented in the GLIM statisticalpackage "Crawley 0882#[ To avoid problems of incon!stant variance and negative seedling counts that mightbe predicted with a normal errors linear regressionmodel\ and to account for large di}erences in seedlingnumber between gaps "range 1Ð073#\ we carried out aweighted regression on the proportion of all focalseedlings in each gap belonging to the individual tar!get species[ The proportional response variable wasmodelled using binomial errors and a logit link func!tion\ with the total number of focal seedlings in eachgap as the binomial denominator[ Hypothesis testingwas carried out using the x1 test on di}erences in

deviance[ The appropriateness of the assumption ofbinomial errors was checked by comparing theresidual deviance with the residual degrees of freedomafter _tting the explanatory variable[

Results

GAP CHARACTERISTICS

We identi_ed 42 gap sites from 69 low!canopy sitesrecorded in the 0884 canopy height survey[ Most ofthese sites "72)# consisted of a single\ isolated lowcanopy point and were therefore considered as gapsof ³ 14m1 "Hubbell + Foster 0872#[ Few gaps con!sisted of two or more contiguous low canopy sites"two sites n& 3^ three sites n& 2^ four sites n& 0^ _vesites n& 0#[ While all the gaps × 14m1 containedseedlings of at least one of the focal species\ 06 "28)#gaps of the³ 14m1 lacked seedlings of the focal spec!ies[ Gap size was not related to seedling density foreither seedlings³ 09 cm height\× 09 cm height or allseedlings combined "d[f[0\22^ F& 0[4Ð2[0^ r1& 9[93Ð9[98#[

We could determine the origin of gap formation forall gaps occupied by focal species and for half thegaps unoccupied by any focal seedling[ Most gaps"37)# resulted from branch or crown fall[ Fewer gapsresulted from trees snapped at the base "04)#\uprooted trees "04)# or standing dead trees "08)#[Only 00) of gaps were clearly the result of multipletreefalls[ Microsite conditions within gaps re~ectedthese di}erent modes of formation\ with di}erentamounts of woody debris "mean cover& 02)\ range0Ð22)# and liana loads "S[ Schnitzer\ unpublisheddata# re~ecting di}erent amounts of crown materialdeposited into the gap[ Although we did not inves!tigate in detail association patterns between speciesand within gap microsites\ some species establishedmore or less frequently than expected in elevated siteson fallen debris "Table 1#[ After 0 year such seedlingswere equally likely to survive as those established inthe soil "Yates!corrected x1& 1[18\ d[f[& 0\ NS#[

SPECIES DIVERSITY AND SEEDLING

ABUNDANCE PATTERNS

We found seedlings ³ 09 cm height for all of our 13focal species except Ceiba\ Pseudobombax andSapium\ and seedlings × 09 cm height for all speciesexcept Trema and Ochroma[ Species varied greatly inabundance "Fig[ 0 and Table 1#\ ranging from threespecies represented by single individuals up to Cec!ropia representing 18) of all seedlings ³ 09 cmheight[ Relative abundance plots for seedlings³ 09 cm and× 09 cm in height were very similar\ andthere was greater evenness of relative abundance ofseedlings than of seeds in the soil seed bank "Fig[ 0^this was also true comparing only the 06 taxa presentboth in the seed bank and seedling census#[



Table 1 Number of occupied gaps\ number of seedlings ³ 09 cm height and × 09 cm height\ and a comparison of seedlingnumbers recruiting in terrestrial vs[ elevated microsites in 25 gap sites[ P!values refer to under "Ð# or over!representation "¦#of elevated seedlings compared with the expected seedling number based on all species combined[ Species with no observedelevated seedlings were given a value of 0 for calculation of G statistics

Total seedlingsSpecies Gaps occupied ³ 09 cm × 09 cm Terrestrial Elevated G P

Alchornea 19 02 21 34 9 1[3 NSAlseis 18 060 028 299 09 9[5 NSAnnona 02 2 04 07 9 1[0 NSApeiba 05 49 20 70 9 2[8 "UnderCasearia 6 13 09 23 9 1[0 NSCecropia 14 234 69 276 17 6[0 ""OverCeiba 0 9 1 1 9 Ð ÐCordia 6 03 07 21 9 1[0 NSCroton 7 08 86 004 0 3[1 "UnderFicus 3 00 3 03 0 9[1 NSGuazuma 5 1 7 09 9 1[6 NSJacaranda 11 61 23 89 05 19[6 """OverLuehea 08 12 68 090 0 2[3 NSMiconia 12 46 020 068 8 9[2 NSOchroma 0 0 9 0 9 Ð ÐPalicourea 14 14 001 026 9 6[6 ""UnderPseudobombax 0 9 0 0 9 Ð ÐSolanum 3 00 3 04 9 1[2 NSSapium 0 9 0 0 9 Ð ÐSpondias 09 4 05 10 9 1[0 NSTerminalia 1 02 5 08 9 1[0 NSTrema 0 1 9 1 9 Ð ÐTurpinia 1 3 4 8 9 2[5 NSZanthoxylum 03 12 13 34 1 9[9 NS

Total 777 728 0548 57

Fig[ 0 Rank abundance plots for pioneer tree species present in the soil seed bank "data from Dalling et al[\ 0886#\ present asseedlings ³ 09 cm height in gaps\ and present as seedlings × 09 cm height in gaps on Barro Colorado Island\ Panama[ Sevenspecies occurred as seedlings but were not present in the seed bank[

Changes in the rank order of abundance of species\and its relationship to seed size\ were analysed usingSpearman|s rank correlations "Table 2#[ Whereasrank abundance of seeds in the soil was negativelycorrelated with seed size but not correlated with adultabundance\ rank abundance of seedlings ³ 09 cmheight was negatively correlated with seed size\ andpositively correlated with both seed bank rank abun!dance and adult rank abundance[ Although cor!related with seedlings ³ 09 cm height\ the only otherrank correlation for seedlings× 09 cm was with adult

abundance "rs& 9[89#\ indicating that the relativeabundances of pioneer species are mostly set duringemergence and early establishment[ Some of thesechanges in relative abundance appear to result frompoor establishment success of small!seeded species[Excluding the shade!tolerant species Alseis\ there wasalso a signi_cant positive correlation between themagnitude of change in relative abundance from theseed bank to the seedling layer "× 09 cm height# andseed size "rs& 9[41\ n& 05\ P³ 9[94#[Seedlings of individual species were not evenly dis!



Table 2 Spearman|s rank correlation tests among rank abun!dance of seeds in the soil seed bank "Dalling et al[ 0886#\seedling abundances and adult abundances[ Sample sizes aresmaller for comparisons with the soil seed bank since only06 of the seedling taxa germinated from the soil "n] numberof species\ rs] correlation coe.cient\ P] level of signi_cance\NS if P× 9[94#

n rs P

Seed size vs]Seed bank density 06 Ð 9[63 ³ 9[90Seedlings ³ 09 cm 13 Ð 9[47 ³ 9[90Seedlings × 09 cm 13 Ð 9[21 NSAdults 13 Ð 9[08 NS

Seed bank density vs]Seedlings ³ 09 cm 06 9[43 ³ 9[94Seedlings × 09 cm 06 9[15 NSAdults 06 9[97 NS

Seedlings ³ 09 cm vs]Seedlings × 09 cm 13 9[75 ³ 9[90Adults 13 9[72 ³ 9[90

Seedlings × 09 cm vs]Adults 13 9[89 ³ 9[90

tributed among the gaps[ This clumped distributionpattern was indicated by comparison of the species|accumulation rates in sequentially sampled gaps\which were lower than expected when compared withcurves from a null!model "similar results were foundconsidering only seedlings ³ 09 cm or× 09 cmheight#[ The null curve was generated by allocatingseedlings randomly to gaps\ but with the overall seed!ling abundance distribution across gaps maintained"Fig[ 1^ n& 49 randomizations#[ For all seedlingscombined\ an average of 09 gaps would need to besampled to encounter 64) of the focal species\whereas only six gaps would have been needed if theseedling population was randomly distributed[

Fig[ 1 Observed "closed circles# and null!model "open circles#species accumulation curves for pioneer tree species presentin successively sampled gaps on BCI[ Data are for all seed!lings "³ 09 cm and × 09 cm#[ Null!model species accumu!lation curves were generated by randomly assigning seedlingsto gaps while maintaining the observed abundance distri!bution[ Error bars are 84) con_dence intervals "n& 49randomizations#[

GAP LIGHT ENVIRONMENTS

Gap size effects

Single hemispherical photographs taken at the canopyheight survey points did not reveal any relationshipsbetween seedling abundance and the light regime[Most surprisingly\ there was no signi_cant di}erencein the measured light conditions of gap sites lackingany individuals of our target species "n& 06^ meanGSF& 9[051\ SE 2 9[91# and light conditions ofoccupied gap sites "n& 23^ mean GSF& 9[061\SE2 9[90^ d[f[0\38\ F& 9[12\ NS#[ For occupied gaps\there was no relationship between seedling densityand light conditions for seedlings ³ 09 cmheight\× 09 cm height\ or all seedlings combined"r1& 9[99Ð9[90#[

Species responses to light conditions

In contrast to gap!level light measurements\ lightmeasurements made at the individual seedling levelrevealed signi_cant e}ects on growth for most specieseven though sample sizes were often small "Fig[ 2 andTable 3#[ Two species for which light e}ects on growthwere undetectable were Alseis and Cordia[ ManyAlseis seedlings were in relatively dark microsites andgrew very little over the year[ In contrast to all otherfocal species\ Cordia seedlings appeared not torespond to higher light microsites by growth[ Thismay have been the result of very heavy herbivoryof all Cordia seedlings in the census by a specialistcassidine chrysomelid beetle Ischnocodia annulus "J[Dalling\ personal observation^ D[ Windsor\ personalcommunication#[ Excluding Alseis and Cordia\ wefound no evidence that the remaining speciesresponded di}erentially to light "ANOVA test of hom!ogeneity of slopes\ d[f[0\6\ F& 0[68\ NS#[

With the exception of the relatively shade!tolerantspecies Alseis\ there was no evidence that seedlings ofthe focal species partitioned the light environment"Fig[ 3#[ In a pair!wise comparison of light conditionsexperienced by seedlings of di}erent species\ the onlysigni_cant di}erence found was between Alseis andCecropia seedlings "Bonferroni adjusted posthoc com!parison\ P³ 9[94#[ None the less\ some partitioningof the light environment may appear as seedlings con!tinue to grow and die[ After 0 year therewere dramaticdi}erences in both growth and mortality ratesbetween species[ Annual mortality "{m| of Sheil et al[0884# varied between 8) "Casearia and Alseis# and74) "Jacaranda#\ and relative height growth variedfrom 6[4× 09Ð3 cm cmÐ0day−0 forAlseis to 2[5× 09Ð2

cm cmÐ0day−0 for Cecropia[ Furthermore\ for speciesthat had× 09 individuals in the initial census therewas a trend of increasing mortality with growth rate"Pearson correlation\ r& 9[36\ n& 03\ P& 9[98^ Fig[4#[



Fig[ 2 Relationships between light measured as the estimated global site factor using hemispherical photo analysis and therelative height growth for pioneer tree species on BCI measured after 6months for 09 species growing in 24 gaps[ Regressionequations are given in Table 3[



Table 3 Regression equations and probabilities for signi_cant relationships "Fig[ 2# between seedling relative height growth"cm cm−0 day−0# and the above!plant estimated global site factor "GSF# light measurement taken with a hemispherical lens inNovember 0885

Species Regression equation r1 n P

Annona y& 9[903x Ð 9[9991 9[50 01 9[9915Cecropia y& 9[905x Ð 9[9998 9[44 03 9[9913Croton y& 9[900x Ð 9[9991 9[16 24 9[9904Jacaranda y& 9[915x Ð 9[9917 9[24 03 9[9159Luehea y& 9[909x Ð 9[9995 9[28 15 9[9996Miconia y& 9[900x Ð 9[9995 9[08 12 9[9281Palicourea y& 9[919x Ð 9[9997 9[61 12 9[9990Zanthoxylum y& 9[919x Ð 9[9993 9[38 09 9[9149

Fig[ 3 Estimated global site factor "2 84) con_dence inter!vals# for seedlings of 09 species of pioneer trees on BCIranked by their mean values[ Sample sizes are given in brack!ets above each species[

Fig[ 4 Correlation between annual mortality rate and height!growth rate for the 03 species of pioneer trees on BCI with× 09 individuals in the initial census[

EVIDENCE FOR DISPERSAL AND EMERGENCE

LIMITATION

Seedlin` dispersion relative to adults

Distributions of the seedlings of most species weresigni_cantly skewed towards their conspeci_c adultswhen compared to the distribution of seedlings of all

focal species to the same adult trees "Fig[ 5 shows the09 most common species#[ The most marked e}ectswere found for the understorey shrub Palicourea\ themid!story treeCroton\ and the canopy trees Jacarandaand Zanthoxylum spp[ None the less\ even seedlingsof the very small!seeded and very abundant canopytree Alseis\ and of the very small!seeded pioneer treeMiconia\ were signi_cantly skewed towards adults[Seedlings ofAlchornea\ the least abundant of the spec!ies tested\ did not di}er from expected in their dis!tribution pattern\ and Luehea seedlings were sig!ni_cantly skewed away from adults "Fig[ 5#[Excluding Alchornea\ Dmax "the maximum di}erencebetween cumulative distributions# was positively cor!related with seed size "Spearman|s rank correlation\rs& 9[66\ n& 8\ P³ 9[94#[

Between gap seedling abundance patterns

Comparisons of species abundance on a per!gap basis\and expressed as the proportion of all focal seedlingspresent in the gap "Fig[ 6#\ reveal some di}erencescompared with the seedling dispersion patternsdescribed above[ While Alseis and Cecropia showedno apparent e}ect of distance on the proportion ofseedlings in the gap\ most species had wedge!shapeddistributions with both high and low occupancy ratesin gaps close to adults\ but only low rates in distantgaps[ For three species\ Apeiba\ Croton and Jacar!anda\ there were signi_cant negative relationshipsbetween the proportion of seedlings in the gap anddistance from the nearest conspeci_c adult "binomialregression^ Fig[ 6#[

Discussion

ABUNDANCE PATTERNS OF PIONEER SPECIES

Species| relative abundances changed markedly fromthe soil seed bank community to the seedling com!munity\ but relative abundances of seedlings werevery similar to relative abundances of adults[ Seed



Fig[ 5 Distribution of seedlings relative to adults for the 09 most common species[ Upper panels] cumulative distribution ofrelative frequencies of distance from the nearest reproductive!sized adult of a target species "i# for seedlings of the target species"thick broken line#\ and "ii# for all focal species "thin solid line#[ Note] the all!species distribution represents the expecteddistribution pattern of the target species assuming no dispersal limitation\ and no distance or density!dependent e}ects on itsrecruitment[ Lower panels] relative frequencies of the target species and all species taken at four classes of distance from adultsof the target species[ Note di}erences in scale between species[

germination\ seedling emergence and early estab!lishment probabilities therefore appear to be veryimportant determinants of abundance for pioneers[Whereas the rank abundance of seeds in the soil seedbankwas strongly negatively correlatedwith seed size\the strength of the relationship with seed size declinedafter seedling emergence\ and for seedlings × 09 cmhigh seed size was uncorrelated with abundance[ The

declining importance of seed size results\ in part\because some relatively large!seeded species\ such asPalicourea and Croton\ that were very rare in theseed bank became common as seedlings\ whereas therelative abundance of small!seeded species droppedfrom the seed bank to the seedling layer "e[g[ from32) to 05) for Miconia\ and from 17) to 7) forCecropia#[



Fig[ 5 continued

Di}erences between seed bank and seedling relativeabundances may re~ect variation in the relativeimportance of direct dispersal into gaps vs[ emergencefrom the soil as recruitment pathways for di}erentspecies[ However\ direct seeding into existing gaps isprobably important for very few pioneers on BCI]fruit production is limited to a few months per yearfor all the species in this study "Foster 0871#\ andalmost all show some seed dormancy "Table 0#[

Changes in abundance may result instead from atrade!o} between dispersal and establishment or fromdi}erences in the habitat requirements of pioneer

species[ Here we _nd some evidence suggesting sucha trade!o} because the change in relative abundancefrom the seed bank to the seedling layer was positivelycorrelated with seed size[ Both emergence and estab!lishment probabilities may be important componentsof this trade!o}[ In a growth chamber experiment\species varied considerably in the burial depth fromwhich they emerged successfully[ Whereas larger!seeded species such as Apeiba and Solanum suc!cessfully emerged from 4!cm burial\ the small!seededpioneers Miconia and Cecropia were only capable ofemerging from the surface few millimetres of soil "J[



Fig[ 5 continued

Dalling\ unpublished data#[ Similarly\ the presence ofsurface litter has a strong inhibitory e}ect on seedgermination and emergence\ with the smallest seededspecies being most susceptible "Va#zquez!Yanes et al[0889\ Guzma#n!Grajales + Walker 0880^ Molofsky +Augspurger 0881^ Dalling 0884^ Metcalfe + Grubb0884#[ Once emerged\ small seedlings from small seedsmay also be more susceptible to damage and herbi!vory\ uprooting by birds and mammals\ and des!iccation during the dry season "e[g[ Clark + Clark0878^ Grubb 0885^ Harms + Dalling 0886#[

EVIDENCE FOR HABITAT SPECIALIZATION

Although seedling abundance varied enormouslywithin gaps\ we failed to _nd an e}ect of gap size onseedling density\ either when gap size was expressedas the number of contiguous low canopy sites\ orusing the estimated GSF index of light taken at eachgap sample centre point[ This is in contrast to thestrong correlation found by Brokaw "0871b# in thesame patch of forest for saplings × 0m height[ Thisdi}erence may be because most gaps in our studywere small "14m1 on our scale^³ 099m1 by Brokaw|s"0871a# de_nition#\ whereas Brokaw|s study includednumerous gaps × 299m1[ Seedling density may beunresponsive to small changes in canopy openness invery small gaps "see Fig[ 0 in Brokaw 0871b#\ or per!haps the di}erence results from greatly reduced lightavailability in the seedling layer as opposed to thesapling layer of gaps[

In examining how habitat requirements for seedlingestablishment and early growth di}ered among spec!ies\ we focused on potential partitioning of the light

environment and on one extreme comparison of thepotential conditions for seedling emergence "use ofthe terrestrial vs[ elevated sites#[ Hemispherical photo!graphs have been used successfully in previous studiesto characterize the light environment of individualplants "Pearcy 0872^ Newell et al[ 0882^ Rich et al[0882^ Olesen 0883# and in this study we found a posi!tive relationship between seedling relative heightgrowth and light availability "as estimated GSF# foreight out of 09 species[

None the less\ we failed to _nd species!speci_cresponses to light[ With the exception of the relativelyshade!tolerant species Alseis\ neither the mean lightenvironments of seedlings nor the growth responsesto light were signi_cantly di}erent between species[While this may be because sample sizes were small\di}erences in growth rates among gap!dependentspecies with di}erent carbon allocation patterns maybe counteracted by di}erences in herbivore loadsamong well and less well defended plants "Coley +Barone 0885#[

After 0 year\ however\ di}erences in growth ratesand mortality rates among species were clear\ andthere was a tendency for growth and mortality to bepositively correlated[ In a greenhouse study on BCI\Kitajima "0883# found comparable results for 02mostly shade!intolerant species[ She found that thespecies with the highest relative growth rates "RGR#in sun also had the highest RGR in shade\ and thatmortality rates in shade were positively correlatedwith RGR in both sun and shade[ She interpretedthese results as consistent with a growth!mortalitytrade!o} acting through species!speci_c allocationpatterns either to leaf area or to other morphological



Fig[ 6 Relationship between distance of a gap to the nearest reproductive!sized individual of a target species\ and the proportionof all focal seedlings within that gap belonging to the target species[ Data were analysed by weighted binomial regression andsigni_cance tested against the x1 distribution "0 d[f[#[

traits that confer resistance to pathogens and herbi!vores[ The large di}erences in growth and mortalityamong pioneers we report here suggest that a similartrade!o} may be at work\ and that this might explain

the di}erent distribution patterns of saplings of threepioneer species found by Brokaw "0876#[ Assumingthat RGR rankings among species remain the samethroughout early growth\ then pioneers with the high!



est RGR would be increasingly limited to sites withthe highest light availability if\ in lower light sites\rates of carbon assimilation were too low to replacetissue lost to herbivores and pathogens[ In contrast\species with lower RGR would have lower rates oftissue loss because of greater allocation to defensivetraits and would have lower mortality rates in moreshaded sites[

The e}ect of within!gap heterogeneity in recruit!ment sites on pioneer distributions onBCI has alreadybeen highlighted "Putz 0872#\ and the di}erentialestablishment success in elevated vs[ terrestrial sitesfound here provides further evidence[ The role of fac!tors other than light in determining establishment suc!cess in gaps "e[g[ root competition and nutrient avail!ability\ litter\ damage from falling debris# requiresmore attention for their importance to be assessed[

IMPORTANCE OF DISPERSAL LIMITATION

Seed distribution patterns in relation to adults suggestthat some dispersal limitation operates for most com!mon pioneer species on BCI "Fig[ 5#[ As expected froma seed size vs[ seed number trade!o}\ the e}ects ofdispersal limitation for small!seeded pioneers wereslight\ but the degree to which seedling distributionswere skewed towards conspeci_c adults was positivelycorrelated with seed size[ On a presenceÐabsence per!gap basis\ however\ the e}ect of dispersal on gapoccupancy is less clear\ and few species were so dis!persal limited as to be completely absent from distantgaps[ Instead\ most species showed triangular dis!tributions of seedling relative abundances with respectto distance to reproductive!sized conspeci_cs "Fig[ 6#[This may suggest that dispersal limitation providesan upper boundary to the potential number of seed!lings able to colonize a site\ and that other factorsin~uence seedling abundances within individual sites\or it may re~ect the importance of making moredetailed assessments of the fruit production and dis!persal parameters of individual species[ In our analy!sis\ the only parameter for dispersal limitation was thedistance to a reproductive!sized individual[ In reality\seed shadows of wind!dispersed species are unlikelyto be symmetrical\ seed crops presumably increasewith tree diameter and not all trees fruit annually[

Hamill + Wright "0875# examined how juveniledistribution patterns can di}er from cumulative fre!quency distributions representing a null model of ran!domly distributed juveniles[ Simulations based onlimited seed dispersal and a consequent clumping ofjuveniles close to conspeci_c adults yielded similarresults to those found here for themajority of pioneers"Fig[ 5#\ but so did an alternative scenario in whichadults and juveniles both show a preference for par!ticular underlying patch types within the forest[ Sucha result might be expected if individual species di}erin their ability to colonize di}erent edaphic or topo!graphic sites within the 49!ha plot[ However\ little

evidence exists for such habitat preferences amongpioneers[ Harms "0886# used a Monte!Carlo simu!lation to generate comparative null distributions ofstems × 0 cmd[b[h[ across _ve di}erent habitat types"high plateau\ low plateau\ slope\ stream and swamp#within the 49!ha plot[ Of the 13 focal species we exam!ined in this study\ only _ve showed habitat associ!ations^ Alseis stem density was negatively associatedwith the small swamp site in the plot\ and Cordia\Miconia\ Palicourea and Terminalia were negativelyassociated with slope sites[

Seedling dispersion patterns relative to seed dis!persion patternsmay also be strongly a}ected by post!dispersal seed predation\ and it is important to pointout that what we have examined is\ strictly speaking\emergence limitation rather than dispersal limitation[If seed predation is positively density!dependent\ asoccurs forMiconia "Dalling et al[ 0887#\ then seedlingdensities close to adults may be lower than expected[However\ if dispersal limitation is strong enough\ withmost seeds aggregated around adults\ then quitestrong density!dependence may not greatly a}ect theshape of the dispersal curve\ and density dependenceitself may go undetected "Hubbell 0868#[ In the caseof Luehea\ the seedling dispersion pattern suggeststhat density!dependent e}ects can overcome those ofdispersal limitation[Luehea seedling abundances werelower than expected up to 39m from the nearest adult"Fig[ 5#[ This is consistent with observations ofLueheaseed rain and seed abundance in the soil seed bank]while seed rain densities decline logarithmically withdistance from adults\ germinable seed densities fromthe soil seed bank are low and independent of distancefrom adults "J[ Dalling\ unpublished data#[

Uniform or patchy density!independent seed pre!dation and low seedling emergence probabilities mayalso a}ect seedling dispersion patterns[ Strong den!sity!independent seed mortality has been found forboth pioneer and non!pioneer species "Gryj + Dom!(#nguez 0885^ Dalling et al[ 0887#\ and may accentuateapparent dispersal limitation by reducing the prob!ability of seedling emergence at the tail of the seeddispersal curve[ The extent to which di}erential seed!ling emergence probabilities among species might alsomodulate the e}ects of dispersal limitation isunknown[ In the two studies we are aware of\ less than09) of the estimated seed pool emerged as seedlingsunder gap conditions "Williams!Linera 0889^ Ken!nedy + Swaine 0881#\ but species!speci_c emergencerates have not been measured[

MAINTENANCE OF DIVERSITY OF GAP!

DEPENDENT SPECIES

Seed dispersal\ seed germination and early estab!lishment\ as well as seedling growth and mortality\ allseem to play a role in determining the patterns ofpioneer abundance and distribution[ Seed dispersaland dormancy parameters ultimately determinewhich



gap sites are reached by individual species\ and appearto have most in~uence on the larger seeded specieswith small seed crops[ In contrast\ small!seeded spec!ies may be most constrained by their seed germinationand seedling emergence probabilities\ as suggested bytheir decline in relative abundances from the soil seedbank to the seedling layer[ Finally\ di}erences ingrowth and mortality rates among species withdi}erent carbon allocation patterns may explainobserved patterns of gap partitioning observed in sap!ling size classes "Brokaw 0876#\ but not observed forseedlings[

Acknowledgements

This research was funded by NSF grant DEB8498915[ We thank the Smithsonian TropicalResearch Institute "STRI# for providing facilities\Felix Matias and Arturo Morris for assistance in the_eld\ and Joe Wright and Milton Garcia for the useof the photo analysis system[ Rick Condit and RobinFoster generously provided census data from the 49!ha plot data and canopy height data collected byAndres Hernandez and Arturo Morris[ N[ Brokaw\R[ Condit\ J[ Denslow\ P[ Grubb\ K[ Harms\ E[ A[Herre\ C[ Lovelock\ and S[ J[ Wright provided helpfulcomments on earlier drafts[ This article is a con!tribution from the Center for Tropical Forest Science\supported by the John D[ and Catherine T[ Mac!Arthur Foundation[

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Sheil\ D[\ Burslem\ D[F[R[P[ + Alder\ D[ "0884# Theinterpretation and misinterpretation of mortality ratemeasures[ Journal of Ecolo`y\ 72\ 220Ð222[

Silman\ M[R[ "0885# Reèneration from seed in a neotropicalrain forest[ PhD dissertation\ Duke University[ Raleigh\NC[

Tilman\ D[ "0883# Competition and biodiversity in spatiallystructured habitats[ Ecolo`y\ 64\ 1Ð05[

Va#zquez!Yanes\ C[\ Orozco!Segovia\ A[\ Rinco#n\ E[\ Sa#n!chez!Coronado\ M[E[\ Huante\ P[\ Toledo\ J[R[ + Bar!radas\ V[L[ "0889# Light beneath the litter in a tropicalforest] e}ect on seed germination[ Ecolo`y\ 60\ 0841Ð0847[

Welden\ C[W[\ Hewett\ S[W[\ Hubbell\ S[P[ + Foster\ R[B["0880# Sapling survival\ growth\ and recruitment]relationship to canopy height in a neotropical forest[Ecolo`y\ 61\ 24Ð49[

Williams!Linera\ G[ "0889# Origin and early development offorest edge vegetation in Panama[ Biotropica\ 11\ 124Ð130[

Received 04 September 0886revision accepted 8 February 0887

seed dispersal, seedling establishment and gap partitioning ...keywords] dispersal limitation\...

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