Nordic Society Oikos

Post-Dispersal Predation on Isolated Seeds: A Comparative Study of 40 Tree Species in a

Southeast Asian Rainforest
Author(s): Geoffrey M. Blate, David R. Peart and Mark Leighton
Source: Oikos, Vol. 82, Fasc. 3 (Sep., 1998), pp. 522-538
Published by: Wiley on behalf of Nordic Society Oikos
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OIKOS 82: 522-538. Copenhagen1998

Post-dispersal
predationon isolatedseeds:a comparative
studyof
40 treespeciesin a SoutheastAsianrainforest

M. Blate, David R. Peart and Mark Leighton

Geoffrey

Blate,G. M., Peart,D. R. and Leighton, M. 1998.Post-dispersal

predationon
isolatedseeds:a comparative
studyof40 treespeciesina Southeast
Asianrainforest.
- Oikos 82: 522-538.

Manystudiesofpost-dispersal seedpredation havefocusedon density and distance

dependent mortality,whilerelatively fewhaveexamined thefatesof isolatedseeds.
Yet,scatter-dispersedseeds(sensuHowe)arecommonly deposited singlyor in small
groups.Furthermore, evenin specieswithhighly aggregated seeddistributions, the
fatesof themostwidelydispersed individualsmaybe criticalforrecruitment. We
comparedpredation rateson single,isolatedseeds,among40 speciesof treesin
lowlandtropicalrainforest at GunungPalung,WestKalimantan, Indonesia.Seeds
wereplacedalongfourreplicate transectsand monitored fordamagebypredators,
removaland germination in fourtrials,each lastingat least30 days.Tethering of
seedsdidnotaffect removal rates,indicating thatremovals wereattributable to seed
predatorsandnotmerely to physical disturbancebyanimalsor abioticfactors. After
30 days,mortality dueto seedpredation, averaged overspecies, wasmorethan50%;
amongspecies, predation lossesrangedfrom0 to 100%.Overtherangeofseedsizes
weexamined (0.1 g to 11.6g fresh weight)predation rateswerenegatively associated
withseedsizeandwiththethickness andhardness oftheseedcoat.Lowerpredation
on largerseeds is contrary to theoretical predictions and some priorempirical
findings,and maybe partially explainedby the scarcity of predators capableof
penetratingthephysical defenses oflargeseedswithhardseedcoats.Large,softseeds
withlowpredation ratesmayhavepoornutrition or maybe protected bychemical
defenses.Speciesdiffered greatlyin30-daygermination rates,ranging from0 to47%.
Somespecieswithlowpredation ratesalso had lowgermination rates;theimplica-
tionsfortheoverallriskofpredation duringtheseedstagearediscussed. Predation
rateswerenotassociated withspecies'natural dispersal mode(clumped vsscatter-dis-
persed),
contrary to theoretical predictions.Spinyrats(Maxomys spp.)werethemost
abundantseed eatingrodent.Caged spinyrats avoidedlarge,hard seeds and
preferredsoft,medium sizedseeds.The substantial ratesofpostdispersal predation
on isolatedseeds thatwe measuredmay be sufficient to influence strongly the
populationdynamics andlifehistory evolutionoftreesinthisrainforest community.

G. M. Blate, Yale School of Forestryand Environmental

Studies,New Haven, CT,
USA (presentaddress: TropicalForest Foundation,225 ReinekersLane, Suite 770,
Alexandria,VA 22314, USA [tff@igc.apc.orgj).- D. R. Peart, Dept of Biological
Sciences, DartmouthCollege, Hanover,NH 03755, USA. - M. Leighton,Dept of
Anthropology, Peabody Museum,Harvard Univ.,Cambridge,MA, USA.

Seed predationis a major source of mortalityin rain
forest trees. Pre-dispersal losses may reach 100%
(Janzen 1969) and post-dispersalseed mortalityoften
exceeds 75% (Howe et al. 1985, Schupp 1988a, b),
reaching 100% for some species (Chapman 1989).
Consequently,seed predationin tropical forestsmay
have an important role in population dynamics
(Harper 1977) and natural selection(Janzen 1971); it
may also influencecommunitystructure(Clark and
Clark 1984) and contributeto the maintenanceof
species diversity(Janzen 1970, Connell 1971, Grubb
1977).

Accepted5 January1998
Copyright?) OIKOS 1998
ISSN 0030-1299
Printedin Ireland - all rightsreserved

522 OIKOS 82:3 (1998)

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 Some seed predationstudiesin the tropicshave fo-
cused on pre-dispersalpredation (e.g. Janzen 1969,
Grieg 1993). Many more(e.g. Wilson and Janzen1972,
Augspurger1981, 1983, Clark and Clark 1984, Becker
and Wong 1985, Coates-Estrada and Estrada 1988,
Schupp and Frost 1989, Schupp 1992, Bustamanteet
al. 1993,Howe 1993,Terborghet al. 1993,Forgetet al.
1994) have been promptedby the Janzen-Connellhy-
pothesis(Janzen 1970, Connell 1971), which proposes
thatpredationriskincreaseswithnonspecific seed den-
sityand/orthe proximityto parenttrees.Tests of the
Janzen-Connellhypothesishave naturallyfocused on
evaluatingthe relationshipbetweenpredationriskand
eitherthe local densityof seeds or the distance from
adult plants. However, the extremecase of very low
density,effectively isolated seeds has been largelyig-
nored.Accordingto Janzen'searly(1970) formulation,
theriskof predationwas assumedto fallalmostto zero
for the most widelydispersedseeds, i.e. those at the
fringesof the seed distribution.
Speciesdifferin thespatialpatternsof theirdispersed
seeds. Far fromthe parentplant, the densityof wind-
dispersedseeds declinescontinuouslywithdistance.In
contrast,some animal-dispersed seeds may be scattered
individuallyor depositedin clumps,generallyfarfrom
the parenttree (Howe 1989). Patternsof mortalityfor
scatteredseeds may be quite different fromthose dis-
persedin largerclumps(Whelan et al. 1991), especially
if densitydependentpost-dispersalseed predationis a
major source of mortality.We suggestthat assessing
predationriskforisolatedseeds maybe veryimportant,
both for seeds in the outer parts of distributions that
are aggregatedaround parenttrees,and forthose that
are normallyscatter-dispersed.
If the Janzen-Connell
hypothesisholds, so thatmost
recruitmentoriginatesfrom relativelyisolated seeds,
this does not imply that seed predation on isolated
seeds is inconsequential.On the contrary,if isolated
seeds are themain sourceof recruits, it becomesimpor-
tantto evaluatethefactorsthatinfluencetheirsurvival.
Seeds of scatter-dispersed taxa may occur singlyon the
forestfloor.This can resultfrombeingregurgitated or
defecatedone seed at a time,as occurs withtoucan or
hornbillregurgitationof several taxa in the Myristi-
caceae (Leighton1982,Howe 1989). Alternatively, defe-
cations containingseveral seeds of a taxon may be
scatteredby successivelayersof vegetationas theyfall
from high in the canopy, e.g. gibbon defecations
(Thomas 1995). The fate of isolated seeds is clearlyof
centralimportanceto the populationdynamicsand life
historyof scatter-dispersed species.Speciesdispersedby
animalsin clumps(e.g. seeds consumedby orang-utans
and deposited in large, multi-seededdefecations)are
intermediatebetweenthe extremesof scatteredseeds
and seed shadowsconcentratedheavilyaround parents.
Even orang-utandefecationsmay sometimesinclude
only one or a fewnonspecific seeds when the disperser
has been feedingon a diversityof species.
OIKOS 82:3 (1998)
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Studies on individuallyplaced seeds are demanding,
because manyseeds mustbe monitoredoverlargeareas
in orderto obtainestimatesof predationrates.But they
are necessaryto investigatethe seed dynamicsof the
many scatter-dispersed taxa that occur in rain forest
communities(Howe 1989), as well as to quantifythe
predationriskto isolated seeds in the "tails" of highly
aggregated distributions.Three studies in Panama
(Sork 1987, Schupp 1988a, b, Forget and Milleron
1991) examinedthe effectsof post-dispersalpredation
by vertebrates on isolated seeds of a singletreespecies,
i.e. at controlledor measured densitiesof < 1 m-2.
Hammond (1995) measuredpredationrateson seeds of
fourspeciesof treesin Mexico, and foundlowerpreda-
tionrateson singlyplaced seeds thanon seeds placed in
groups of 5 or 10, in matureor late secondaryforest.
However,to our knowledge,therehas been no commu-
nity-levelassessmentof predationon isolated seeds for
any plant community.A community-level approach
allows us to evaluate the patternsof seed predation
among species withwidelyvaryingseed morphologies
and sizes, and among larger taxonomic groupings
above the species level. Such comparisonsare more
whenthe speciesco-occur,are subject
easilyinterpreted
to predationfromthe same fauna,and evaluatedusing
the same methods of experimentation and
measurement.
Rain forestsin SoutheastAsia are characterizedby
interspecificallysynchronizedfruitingevents (masts),
occurringat intervalsof ca 5-7 yr (Whitmore1984).
Most of the time, i.e. between masts, the seed rain
includesmanytaxa of treesand lianas thatgenerallydo
not participatein the major mastingevents.Our study
was conductedduringa 10-month, non-masting period.
We quantifiedthe rates of loss of dispersedseeds to
vertebrateseed predatorson experimentally placed, iso-
lated seeds for 40 species of seeds that were available
duringthe studyperiod. The fatesof seeds weremoni-
tored for damage or removal by predators,and for
germination.Germinationstatuswas includedbecause
germinatedseeds are no longer susceptibleto seed
predation.Time to germinationinfluencesseed preda-
tion riskover the seed stage of the lifecyclesimplyby
influencingthe time that seeds are available to
predators.
The experiments includedboth scatter-dispersed and
clump-dispersed taxa. We also measuredseed size and
aspectsof seed morphologyforeach species,and exam-
ined the relationshipbetween seed morphologyand
predationrisk.
Optimal foragingtheory (Charnov 1976) predicts
thatpredatorsshould preferseeds withthe greatestnet
reward.Gross returnsto predatorsincreasewith seed
size. However,net rewardfor a givenseed is likelyto
vary widely among potentialpredator species, which
have differenthandling abilities,dependingon their
size, strengthand typesof mouthparts.Whiletheverte-
523
brate fauna at the studysite is documented(Blundell basins, and were thereforeconsideredspatiallyinde-
1996),the relativecontributions of vertebratespeciesto pendentwith respectto predationeffects.Seeds were
seed predationlosses are unknown.Consequently,we placed singly,and well spaced (see below), to assess
do not propose specifichypothesesfor relationships the predationrisk for isolated seeds. Between 8 and
betweenseed size and the predationrate imposed by 15 species were used on each transectfor each trial.
the predator community.However, for a given seed The specificseed taxa used varied over trialsbecause
size, it is logical to expect that predationrate would of phonological differencesamong the tree species.
decreasewithincreasingthicknessand hardnessof the Only three seed species were available, and used, in
seed coat (i.e. testa plus adherentendocarp). more than one trial. Differencesin crop size among
In addition to the field trials, where seeds were fruitingtrees and lianas also limitedthe number of
exposed to all seed predatorsin the community,we seeds available for each species. Consequently,the
conductedseparate experimentswhere seeds were ex-
numberof seeds per transectfor each species ranged
posed only to the most obvious potentialpredatorsin
from4 to 15 (mean n = 9.1). However,the numberof
the vertebratefauna at the studysite,spinyrats (Max-
species,species identities,and numberof seeds of any
omysspp.); theseseed eatingrodentsare locally abun-
given species, were always the same among the four
dant. Because of their potential importance as
replicate transectswithin any field trial. A total of
predators,we assessed the preferences of spinyrats for
seeds of varying size and morphologies, in cage 1499 seeds was placed in the fourfieldtrials.
experiments.
In summary,we addressedthe followingspecificre- Seed collectionand treatment
search questions: 1. What are the predationrates on All taxa used in theexperiments wereanimal dispersed,
isolated seeds due to terrestrial vertebrateseed preda-and all but one (Lithocarpussp.) had fleshyfruits.Seeds
tors,in the naturalhabitatat the timeof naturalseed werecollectedmainlyin the alluvialbenchand lowland
dispersal?2. What are the relationshipsbetweenpreda- sandstonehabitats,in two ways. First,some seeds were
tion risk and seed morphologicaltraits(seed weight, collectedfromthe forestfloor afternatural dispersal.
and thicknessand hardnessof the seed coat). 3. How Especially in the case of scatter-dispersed seeds, this
do seed morphologicaltraitsinfluencethepreference ofmethodwas ofteninefficient, because of thedifficultyof
the most abundantpotentialpredators,spinyrats? findingsingle seeds. Therefore,many taxa were col-
lected predominantlyfrom fruitsthat had not been
consumedby frugivores, but had fallenbelow fruiting
trees.We ensuredthat the fruitswere ripe and seeds
Methods were mature.Seeds were cleaned, wherenecessary,by
Studysite removingthe arils or pulp with a knife.Those with
signsof damage by invertebrates or fungiwerenot used
The studywas conductedin lowlandtropicalrainforest in the fieldtrials.
at the 15-km2Cabang Panti Research Site, ?13'S,
10007'E,in West Kalimantan,Indonesia in the900-km2 Seed morphological traits
Gunung Palung National Park. Annual rainfallis ca The wet weight(seed plus seed coat) and seed coat
4.5 m, but distinctdry periods occur duringFebruary thicknesswere recordedfor a subsampleof at least 5
and July-August.Several distincthabitat typesoccur randomly selected seeds of each seed taxon. Seed
withinCabang Panti (Leighton 1990); our studysites weight was determinedby
dividing the combined
werelocated on alluvial benchand adjacentsandstone-
weightof all seeds in the subsample(measuredto 0.01
derivedsoils, at 10-100 m elevationa.s.l. These habi-
g) by the numberof seeds. Seed coat thicknesswas
tats support the highestdiversityof tree species at
measuredto 0.05 mm usingVerniercalipers.If all seeds
Cabang Panti (M. Leightonand C. Cannon unpubl.).
in the subsamplecontainedan embryoand endosperm,
the seeds in the sample of that taxon were considered
viable. Seed coat hardnesswas recordedas "soft" if it
Predationrate trials could be penetratedeasily by a fingernail, "hard" if it
Experimentaldesign could not, and "veryhard" if it was difficult to pene-
Four field trials, each lasting a minimumof 30 d, trate with a knife.Seeds and fruitswere drawn and
were conducted between 11 September,1992 and 27 described,and a reference collectionof seeds,fruitsand
June, 1993. In each trial, "seeds" (i.e. the dispersal leaves was made forlateridentificationof thetaxa used
units, including the embryo, endosperm, testa and in the experiments. None of the seeds in the fieldtrials
sometimes adherent endocarp; see Table 1) were had spinesor otherunusual physicaldefense,although
placed along each of four replicatetransects.Tran- seeds of one specieswerecoveredwithdense hairs(see
sects ran along ridge trails separated by drainage Discussion).

524 OIKOS 82:3 (1998)

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 trialsat GunungPalung,West Kalimantan,Indonesia.Each ratwas
Table 2. Menus of seeds offeredto spinyratsin preference
offeredMenu A on the second night,and Menu B on the thirdnightaftercapture.For each menu,fourseeds of each taxon
were offeredtogether,at dusk. Each genus was representedby a singlespecies. See textand Table 1 fordetails.
Menu A
Genus Size Hardness
Friesodelsia small hard
Rourea small soft
Aglaia medium soft
Knema medium hard
Diospyros large hard
Elaeocarpus large v. hard
Seed dispersalsyndromes
Seed taxa were classed as scatter-dispersed
or clump-
dispersed,based on (1) theirpatternof occurrenceas
dispersedseed as observedin thisstudy,(2) theirusual
patternof occurrencein 1-M2 seed traps in the same
studysiteover severalyears(M. Leightonunpubl.) and
(3) the usual dispersalagent,as recordedin fieldcen-
suses of vertebratevisits to fruitingtrees (Leighton
1990). Taxa occurringmainlyas singleseeds afterdis-
persal and known to be dispersed by birds were
classifiedas scatter-dispersed,while those occurring
mainly in clumps and known to be mainly primate
dispersed were classified as clump-dispersed.Taxa
which did not clearlybelong to eithergroup, or for
whichinsufficient informationwas available, were not
assignedto eithergroup (Table 1).
Seed placement
For each transect,seeds were placed at 5-m intervals
along each of two lines that ran parallel to, on either
side, and 5 m away fromthe main transectline. Thus,
for example,a 500-m trail segmenthad 200 potential
seed locations (2 linesx 500 m lengthwith 5-m spac-
ing). Only slopes greaterthan 400 and very densely
vegetatedgaps were excluded fromthe potentialseed
placementlocations.
The total densityof seed rain at the researchsite
duringnon-mastingperiods is quite low, ca 0.25 seeds
m- 2 yr- l (Leighton1990),so thattheadditionof even
a few seeds can increase local densitiessubstantially.
However,placementof thewell spaced,individualseeds
in theexperimental trialsincreasedtotalseed densityby
only ca 16% above this natural level, in local areas
along each transect(ca 200 seeds added per 500 x 10-m
area).
Seeds were assigned randomlyto locations within
each transect,and each seed was droppedfroma height
of 50 cm, to simulatenaturalseed fall.In the fewcases
where it was necessary,a small amount of litterwas
moved to relocate the seed. The exact location was
markedby 2 stakes(ca 15 cm long and 3 mmdiameter),
insertedintothe ground10 cm on each side of theseed.
Stakes were untreatedwooden skewersthat had been
exposed to the air at the fieldsite for severalmonths
OIKOS 82:3 (1998)
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Menu B
Genus Size Hardness
Adenanthera small hard
Artocarpus small soft
Syzygium medium soft
Santiria medium hard
Lithocarpus large hard
Dracontomelon large v. hard
beforeplacement.Flagging was placed > 1 m above
each seed location. Singleseeds at 5 m x 10 m spacing
did not provide unusual, concentratedresourcesfor
predators,and the smallstakesused forrelocationwere
of natural materials.Thus, these seed placementand
markingprocedureswere unlikelyto resultin the at-
tractionof seed predatorsto the placementlocations.
Although seeds with signs of damage by fungi or
invertebrateswerenot placed in thefield,all seeds were
open to attackby theseagentsafterplacement.
Monitoring
All seeds used on a given transectwere placed in the
fieldon the same day (i.e. theyformeda "cohort",for
the purposesof measuringremovalrates). For the first
two weeks, seeds were checkedevery2 d for signs of
predation.Subsequently,remainingseeds werechecked
every4-7 d for at least 1 monthin each of the four
trials.At each check date, we recordedseed presence,
conditionand germination status.Seeds wereexamined
for signs of animal activity(e.g. toothmarksor seed
fragments)and placed in the followingcategories:nib-
bled (<half-eaten), mostly-eaten(>half consumed)
and eaten (if only fragmentsof the seed or seed coat
could be found).Seeds thatwere absent,but forwhich
there was no visual evidence of predation, were
classifiedas removed.
A tethering experiment(see below and Results)indi-
cated thatremovalof seeds could be reliablyattributed
to seed predators.The above classes were then aggre-
gated into two categoriesforanalysis.Seeds thatwere
intactor less thanhalfeaten wereclassed as remaining;
those that were more than half eaten or missingwere
classed as lost to predation.
Tethering experiment
In trial4, some seeds of each of the 12 speciesin that
trialwere tethered,to determinewhetherseed removal
could reliablybe attributedto seed predation,rather
than othercauses (e.g. water,litterfallor passing ani-
mals). Equal numbersof seeds of each species were
tethered,or left untetheredas controls.Seeds in the
controlgroup were treatedas in trials 1-3.
Tethered seeds were attached by a small drop of
epoxy glue (Araldite Rapid epoxy adhesive;
527
Table3. Predation ratesandmeanmorphological traits
fortheplantfamilies
trialson 40 speciesofrainforesttreesat GunungPalung,WestKalimantan, Indonesia.Familiesarelistedinorderofincreasing
predation rates.Predation ratecalculated rateindex(MRI, see text).Hardnesswas a classvariableat thespecies
as mortality
levelwith1 = soft,2 = hard,and 3 = veryhard.All meansand standard errorsat thefamilylevelwereobtainedfromspecies
meanvalues.
Family No. species Totalno. Mean seed
tested seeds weight(g)
Burseraceae 3 94 6.64 + 1.25
Lauraceae 3 119 4.5+ 0.51
Annonaceae 6 217 0.49+ 0.06
Myrtaceae 5 174 1.84 + 0.14
Connaraceae 3 101 0.36+ 0.06
Ciba-Geigy) to 2 m of finegauge monofilament nylon
line,followingthe methodsof Schupp (1988a; see also
Whelan et al. 1991). Glue was allowed to dryat least 6
h beforeplacementin the field.Tetheredseeds were
placed in the same way as controls,exceptthata tether
line was tied to a 20-30 cm x 1 cm ironwood stake
drivencompletelyinto the ground.
Data analysis
Two measures of predationrate were used for each
species.The first,the cumulativeprobabilityof mortal-
ity(CPM) was calculatedas theproportionof the total
seeds (those initiallyplaced) that had been lost to
predation by day n of each trial. CPM provides a
simple,intuitivemeasureof the amountof seed preda-
tion that had occurredfor each species,at each sam-
plingdate. Because of therelativelylow samplesizes on
each transect,data were pooled across the four repli-
cate transectsto betterestimateCPM on each sampling
date. While suitable for descriptiveresults,CPM is
unsuitable for statisticalcomparisons,which require
replicateestimatesof predationrates.
The secondmeasure,the'mortalityrateindex'(MRI)
allows forreplicateestimatesof predationrate (one for
each transect),but sacrificesthe abilityto followtime
trends in the cumulative probability of predation
(whichis possiblewithCPM). For each transect,MRI
providesa singleestimateof the mean rate of seed loss
to predationover the first30 d, duringwhichmost of
the seed losses occurred.
For each species,MRI was obtainedby firstcomput-
ing the logarithm(base 10) of one plus the proportion
of seeds remaining,foreach day over the 30-d period.
Then, the slope of the line formedby plottingthese
transformedproportionsagainst time was obtained,
using linear regression.A separateslope was obtained
for each transectsample,i.e. therewere fourreplicate
values foreach species.Finallytheseslopes werescaled
by multiplyingby - 100 to obtain the estimatesof
MRI for that species. Thus, MRI is an index of the
mean rate of predationloss per day over 30 d, but it is
not a true probabilityof predation.Because it can be
calculatedas a singlenumberforeach species on each
528
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by3 ormorespeciesinseedpredation
represented
Mean seedcoat Mean seed Meanpredation
(mm)
thickness coat hardness rate(MRI)
2.72 + 0.50 2.67 + 0.50 0.15 + 0.06
0.68+ 0.12 1.33+ 0.14 0.28+ 0.05
0.13+ 0.01 1.83+ 0.08 0.53+ 0.07
0.34 + 0.03 1.00 + 0.00 0.62 + 0.17
0.20+ 0.00 1.00+ 0.00 1.22+ 0.26
replicatetransect,theMRI providesmoreopportunities
for statisticalcomparisonsthan does the CPM.
Use of linear regressionon a logarithmicscale to
calculate the MRI assumes the daily probabilitythat
any remainingseed will be attackeddoes not varyover
the course of a trial. This is equivalentto assuming
negativeexponentialdeclinein the numbersof surviv-
ing seeds. In addition, using transectsas replicates
requiresthat therebe no consistentdifferences among
transectsfor seeds of a given species. Plots of the
transformed proportionsvs time were examinedvisu-
ally for time trends, and for consistentdifferences
among the trailsused as transects;theseplots indicated
no consistenttrendsin eithercase.
Because we foundno significant differencesbetween
MRI values fortetheredand untethered seeds,thedata
fromtrial4 werepooled withthe data fromtrials1-3
in overall analyses.Finally,because seeds fromonly a
fewspeciesoccurredin morethan one trial,we did not
compareindividualspecies'predationratesstatistically.
Rather,statisticalanalyses focusedon comparisonsof
predation rates (MRI) according to morphological
characteristics:seed weight,seed coat thicknessand
hardness.In the threecases (see above) wherea species
was used in more than one trial, mean values were
obtainedforthose species(over trials)beforestatistical
analyseswere done. Statisticalanalyseswere run using
SYSTAT software(SYSTAT Inc. 1992).
Feedingtrials
Experimentaldesign
To determinewhetherthe most common seed eating
rodentshave preferencesfor particularmorphological
characteristicsof seeds,feedingtrialswereconductedin
June 1993 with five spiny rats (Maxomys spp.; see
below). Rats wereofferedtwelveseed species(fromthe
40 used in thefieldtrials),chosento representthreesize
classes and two hardness classes. The six resulting
categories were (a) small-soft,(b) small-hard, (c)
medium-soft, (d) medium-hard,(e) large-hard,and (f)
large-very hard. The last categorywas alteredfromthe
OIKOS 82:3 (1998)
Table 4. Germinationand morphologicaltraitsof seeds of 15 rain foresttree taxa at Gunung Palung, West Kalimantan,
Indonesia 30 d afterplacementin the field.Only genericnames are listed;one species per genus was tested(see Table 1 for
details).Only thosespecieswithsome germinationafter30 d are included;no germination occurredforthe remaining25 species
in the fieldtrials.

Family Genus No. of No. Percent Seed coat Seed coat Seed
seeds germinating germinating thickness(mm) hardness weight(g)

Lauraceae Cryptocarya 94 44 46.8 0.4 1 4

Connaraceae Rourea 41 13 31.7 0.2 1 0.5
Sapotaceae Palaquium 26 8 30.8 0.15 2 1.2
Leguminosae Fordia 40 11 27.5 0.1 1 0.5
Meliaceae Dysoxylum 57 13 22.8 0.1 1 6.3
Sterculiaceae Sterculia 36 7 19.4 0.1 1 0.3
Gnetaceae Gnetum 23 4 17.4 0.3 2 0.8
Myrtaceae Syzygium 174 28 16.1 0.34 1 1.8
Guttiferae Calophylluin 39 4 10.3 0.2 2 1
Annonaceae Friesodelsia 76 6 7.9 0.1 2 0.2
Leguminosae Adenanthera 60 4 6.7 0.1 2 0.2
Burseraceae Santiria 31 2 6.5 0.6 2 0.8
Connaraceae Agalea 27 1 3.7 0.2 1 0.5
Annonaceae Xylopia 31 1 3.2 0.15 2 0.7
Myristicaceae Knema 46 1 2.2 0.1 2 1.7

Sub-total 801 147 18.4 0.2 1.5 1.4

Others 698 0 0
Total 1499 147 9.8 0.2 1.5 1.4

originallyplannedlarge-soft to large-very
hard,because
no speciesof large-softseeds wereavailable in the field
at the time. "Small" seeds were <0.7 g, "medium"
seeds were between0.7 g and 3.0 g and "large" seeds
were > 3.0 g (freshweights,includingseed coat).
The 12 seed specieswererandomlyassignedto one of
two menus(Table 2). Each ratwas offeredbothmenus,
one on each of two consecutivenights.Withineach
menu,fourseeds of each morphologicalcategory(e.g.
small-hard)were offered.Thus, over two nights,each
rat was offered48 seeds (2 menusx 6 morphological
classes x fourseeds in each class).
Trials
On the firstnightof capture,ratsweregiventwo seeds
of each of the 12 species (Table 2) so theywould be
familiarwitheveryspeciesused in the trialsto follow.
On thesecondnight,each ratwas givenmenuA and on
thethirdnight,menuB. Seeds wereplaced haphazardly
on the papered sides of the tank floors,beforedusk.
Uneaten and partlyeaten seeds, as well as the seed
coats of consumedseeds,were removedand talliedthe
followingmorning.Betweenthe two feedingtrialsthe
rats were given 6-12 peanuts and ca 25 ml of water;
thesewere generallypartiallyconsumed.

Rat captureand caging

Rats were capturedusing heavy duty wire mesh live-
traps, of a type commonlyused by rural villagersin
West Kalimantan.The trapswerebaitedwitha mixture
of peanutbutterand dryoats and placed in thefieldat
dusk. Two verysimilarspinyrat specieswerecaughtin
the traps,M. rajah and M. whiteheadi.We decided to
include these species in the trialsin the proportionin
whichtheywere trapped.The fiveanimals used in the
preferencetrialscomprisedfour M. rajah and one M.
whiteheadi.Each rat was weighed,sexed, identifiedto
species (Payne et al. 1985) and placed in a tank (either
glass or wire mesh) measuring1 m x 50 cm x 40 cm.
Half the floorwas coveredwithleaves and the remain-
der coveredwithpaper. A metal can was providedfor
shelter.Walls werecoveredwithwhitepaper to produce
uniformilluminationwithinthetanks;lids wereof 1-cm
wiremesh. For the feedingtrials,tankswere placed in
an open air hut at the fieldstation.
Results
Overall rates of seed predationon isolatedseeds
These rateswerecalculatedas the cumulativeprobabil-
ity of mortality(CPM).- Of the 1499 seeds placed, 2%
were removedon the firstday, 21% by day 5, 35% by
day 10,47% by day 20 and 53% by day 30. The average
removalrate over all species (based on species-specific
means) was 51% after30 d. In each trial,therewas a
wide range among the species,in both the progressive
ratesof seed removaland in the final(30-d) proportion
of seeds remaining.At the extremes,for some species,
no seeds were removedin 30 d, while for others,all
seeds were removed(Table 1). Clear physicalevidence
of consumption(i.e. partiallyeaten seeds or the seed
coat residue from seeds completelyconsumed) was
noted in 26% of seed removal events.Removal rates
were not significantlydifferent betweentetheredand

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 a) untetheredseeds in trial 4 of the field experiment
12 (Friedman'stest,blockedby species,df = 1, P = 0.39).
Evidence of attack by invertebrates was seen on 40 of
10 - the 1499 seeds over the first30 d. Of these40 seeds, 18
had been removedfromtheirplacementlocations by
8 day 30.
Of the familiesrepresentedby 3 or more species,
Burseraceaehad thelowestpredationrate(measuredas
a 4 MRI) and Connaraceae thehighest(Table 3). MRI was
not significantlydifferentbetween scatter-dispersed
2 .. taxa (mean 0.60, n = 23) and clump-dispersedtaxa
(mean 0.57, n = 10; t-test.P > 0.05).
0
0 1 2 3 4 5
Seed coatthickness(mm)
Germination
b)
Some germinationoccurredby day 30 for 15 species
(38% of all species; Table 4). Among these 15 species,
8- the percentageof seeds germinating by day 30 ranged
from2% to 47%. For all 40 species combined,only
9.8% of the seeds placed germinatedby day 30 (Table
6-
4). Afterday 30, germination continued,but at an even
slowerrate. By day 40, overallgerminationwas 10.2%
4 (in the threetrialswhereseeds were monitoredfor at
a) least 40 d), and by day 80, 20.6% of seeds had germi-
nated (in theone trialwhereseeds werefollowedfor80
d).
0-
Soft Hard V. Hard
Relationsamongseed morphological
traits
Seed coathardness
c) There were severalstatisticalrelationshipsamong seed
morphologicaltraits. First, seed coat thicknesswas
positivelycorrelatedwithseed weight(Spearman'srank
4. correlationr = 0.62, P < 0.01; Fig. la). Second, seed
weight differedsignificantly among hardness classes,
withveryhard seeds beingmuchlargerthaneitherhard
or soft seeds (ANOVA, df= 2,37, F= 7.0, P = 0.003;
Tukey's test;Fig. lb). Finally,seed coat thicknesswas
2- greatestin veryhard seeds, intermediate in hard seeds
and lowestin softseeds (ANOVA, df= 2,37, F = 56.6,
P < 0.0001; Tukey's test;Fig. lc).
0

Relationbetweenseed morphological
traitsand
Soft Hard V. Hard
predationrate
Seed coathardness
The effectsof seed morphologicaltraitson the rate of
Fig. 1. Relationsamongmorphological characters
for40 spe-
cies of seedsof rainforesttreesat GunungPalung,West seed loss to predatorswereanalyzedin a linearstatisti-
Kalimantan, Indonesia.(a) Seedweight vs seedcoatthickness cal model, with MRI as the dependentvariable and
(n= 40). Seed weight includestheseedcoat. Seedcoat thick- weight,hardnessand seed coat thicknessas indepen-
nesswas positively correlated withseed weight(Spearman's dent variables, plus all interactionterms. Backward
rankcorrelation r= 0.62,P < 0.01). (b) Seed weightvs seed
coat hardness.Values are means+ 1 S.E. n = 19 for soft, stepwiseregressionwas used to eliminatethose vari-
n = 17forhardandn =4 forveryhardseeds.Seedweight was ables contributing minimallyto total explainedvaria-
different
significantly amonghardness classes(ANOVA,df= tion in MRI. The distributionof residuals indicated
2,37,F= 7.0,P = 0.003).See textfordescription of hardness
classes.(c) Seed coat thicknessvs seed coat hardness.Seed that assumptionsof linear models were not seriously
coat thickness differed amonghardnessclasses violated.The resulting
significantly model retainedall threeindepen-
(ANOVA,df= 2,37,F= 56.6, P < 0.0001). dent variablesand the interactiontermsweightx seed

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Table5. Analysis rateindex(MRI, seetext)as thedependent
tableforthelinearmodelwithseedmortality
ofvariance variable,
as theindependent
seedweightand seedcoat thickness
and seedcoat hardness, variables.
Source Sum-ofsquares DF Mean-square F P
Hardness 0.00131 2 0.00066 4.51010 0.01236
Weight 0.00107 1 0.00107 7.36131 0.00736
Thickness 0.00064 1 0.00064 4.38787 0.03770
Hardnessx Weight 0.00156 2 0.00078 5.3627 0.00552
ThicknessxWeight 0.00115 1 0.00115 7.91951 0.00547
Error 0.02448 168 0.00115

coat thicknessand weightx hardness(Table 5). Over-
all, predationrate(measuredas MRI) decreasedsignifi-
cantlyas seed weight,hardnessand seed coat thickness
increased.Small seeds withsoftand thinseed coats had
the highestremovalratesof all seeds in thetrials,while
large seeds with extremelyhard and thick seed coats
were least commonlytaken (Fig. 2).
The interactionsof seed coat hardnessand thickness
withseed weightindicatethatpredatorsresponddiffer-
entlyto thephysicalimpediments of seed coat hardness
and thickness,for seeds of different sizes. The main
effectsand the interactionsare apparentin Fig. 2a, 2b,
and 2c. Relativelyfew large seeds were removed,irre-
spectiveof hardnessand seed coat thickness.Although
seeds withthinand/orsoftseed coats were,on average,
taken rapidly,predationon the seeds withthesemor-
phological attributeswas concentratedin the small
seeds. In contrastto larger seeds, small seeds had a
wide range of removal rates, and that variationwas
associated withseed coat thicknessand hardness(Fig.
2a, 2b). Small seeds with hard seed coats generally
experiencedlowerpredationratesthansmall seeds with
softseed coats (Fig. 2a).
Feedingtrials
In the experiments withcaptiverats,no large seeds (of
eitherthe hard or very hard categories)were eaten;
large seeds were thereforeexcludedfromthe statistical
analysis.There was a significantdifferenceamong the
proportionof seeds eaten in the remainingfour mor-
phologicalclasses (Friedman'stest,blockedby ratindi-
vidual, df= 3, P = 0.039; Table 6). The percenteaten
was similar for soft seeds (both small and medium
sized) and medium sized hard seeds, but small hard
seeds were eaten in much lower proportions.
Discussion
Role of predatorsin seed removal
The tetheringexperimentindicatedthat the seeds that
were moved afterplacementin the fieldwere actively (seed coat thickness,hardnessand size) werenot totally
removedby animals,ratherthan incidentally disturbed predictablefrom one another, and each contributed
by animal activityor by abiotic factorssuch as rain or significantlyto thestatisticalmodelrelatingmorpholog-
litterfall.Alternativeexplanations of the similar re-
moval ratesbetweentetheredand untethered seeds (e.g.
thatattractionof predatorsto theglue or monofilament
lines balanced higher removals of untetheredseeds)
seem implausible.We conclude that tetheringwas not
necessaryto obtain good estimatesof removalrates.It
remainspossible that some of the seeds removedby
predatorswerenot immediately killedor consumed,but
rathercached forfutureuse, in whichcase some could
ultimatelyescape predation.However,seeds cached by
rodentsare generallylarge and hard, and such seeds
had verylow removalrates(e.g. two speciesof Canar-
ium,with0% and 0.05% of seeds removedafter30 d;
Table 1, Fig. 3b, 3c). Thus, seed caching probably
contributednegligiblyto the removal of seeds in the
fieldtrials.In a substantialfraction( > 1/4)of thecases
where seeds were taken, visible evidenceof predation
(parts of seeds or seed coats) was foundat the marked
locations. In the remainingcases, we inferthat seeds
wereeitherconsumedentirely, moved beforeconsump-
tion,or leftresiduesthat were not easily recognized.
Relativelyfew seeds showed evidence of attack by
invertebrate seed predatorsover a 30-d period(only40,
or 2.6% of seeds placed). Of these 40 seeds, 18 (45%)
wereremovedby day 30, similarto the overallremoval
rate of 53% of all seeds placed. Thus, it appears that
attackby invertebrates may not have a major effecton
the likelihoodof removalby vertebratepredators.
traits
Seed size and morphological
The strongrelationsamong the morphologicalcharac-
teristicsof the seeds were not surprising.From normal
allometricrelationships, large seeds would be expected
to have thickerseed coats. Seeds combiningthesetraits
(e.g. Canariumspp., Elaeocarpussp., Table 1) shouldbe
mechanicallymost difficult fora seed predatorto con-
sume.Such speciesdid have low removalrates(Table 1,
Fig. 2). Finally, very hard seed coats were also very
thick,and wererestricted to the largestspeciesof seeds
(Fig. 2a, 2c).
Althoughcorrelated,the threemorphologicaltraits

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ical traits to removal rate in the field experiments Table 6. Resultsof seed predatorpreference trialsat Gunung
(Table 5, see also Fig. 2). Some large seeds (e.g. Palung, West Kalimantan, Indonesia. Data are numbersof
seeds in each hardnessand size class eatenby individualspiny
Dysoxlum) had thin,softseed coats while some small rats (Maxomys spp.) over 2 nights.Each rat was provided
seeds (e.g. Santiria) had thick,hard seed coats. Only with 8 seeds of each categoryon each night.Rat no. 5 was
Maxomys whiteheadi.the remainingrats were M. rajah. See
Table 2 forseed speciesoffered.Hard seeds weresignificantly
a) less preferredthan soft seeds (Friedman's test,df= 3, P=
0.039).
2.5 -
0 soft
0 0 ~~~~hard Rat individual Small Medium
_ 1.0- 0. v. hard
- 0 X Microcus Soft Hard Soft Hard
1.5- 3 2 6 6
0
0~~~~~ 2 8 5 8 5
1.0 3 4 0 6 4
4 1 0 1 4
c 0.5 ja 5 8 0 5 4

0.0 I I Totals 24 7 26 23
-1.2 -0.6 0.0 0.6 1.2 Mean 4.8 1.4 5.2 4.6
Log seed weight

one species (Microcus sp.) had unusual structuralfea-

b)
turesof the seed coat (otherthan thicknessand hard-
2.5-
Athin
ness) that appeared likelyto influenceseed predators.
Microcusseeds were covered in dense coarse hairs ca
2.0- 0 thick
A ~~ ~~00 v. thick 1.5 cm long. Predationrate (MRI) for Microcus was
1.5- X Microcus low comparedto the othersmall, softseeds (Fig. 2a);
only 18% of Microcus seeds had been removed by
0~~~~~~~~~~~
1.0 A predators30 d afterplacementin the field(Table 1).
In some cases, the morphologicalcharacteristics af-
fectingpredationrates were consistentat the family
level.Burseraceaeseedsweregenerallylarge,withthick,
C) ~-1.0 A -0.6 hard seed coats (Table 3), traitsassociated with low
0.0 0.6
seed mortalityrate. In contrast,Connaraceae seeds
a
were small,withthin,softseed coats, traitsassociated
1 .5 A withhighmortalityrate (Tables 3 and 5, Fig. 2).

AX AA
Log seed
coaeticknes
Fi.2.0Rlto-n ewenpeainrt
variablesfor40 speciesof seeds of rainforesttreesat Gunung
Palung,West Kalimantan,Indonesia.Predationratemeasured
as mean 30-d mortalityrate index (MRI, see text) over four
replicatetransects.See Table I for sample sizes, Table 5 for
statistical tests. (a) Predation rate vs seed weight, symbols
coded by seed coat hardness.(b) Predationratevs seed weight,
symbolscoded by seed coat thickness.(c) Predationrate vs
seed coat thickness,symbolscoded by seed weight.Microcus
sp. was the only species withunusual morphologicalfeatures
likelyto affectpredators;its seeds were covered with dense
coarse hairs (see text).
Influenceof seed size and morphology
on
predationrate
It has been argued several times that larger seeds
should be more susceptibleto vertebratepredation.
Harper et al. (1970) suggestedthat large seeds should
harphlgia be preferentiallytaken,because of the higherrewards
for seed predators.Similarly,the more formalmodels
of optimalforagingtheory(Charnov 1976) predictthat
large seeds should be preferredover small ones, given
equal handlingtime. Sork (1987) noted that although
large seed size facilitatesestablishmentof seedlings
underlow lightconditions,it may also increasethe risk
of vertebratepredation.Putz and Appanah (1987) fur-
thersuggestthat large seeds are less likelythan small
seeds to be hiddenby surfacelitterand soil, and thus
more apparent to visuallyorientedpredators.Boman
and Casper (1995) found higherpredation rates on
larger seeds (> 1 cm length)than on seeds < 1 cm
lengthin hardwoodforestin the northeastern USA. In
cage experiments,Adler (1995) found that Central

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 a)

1.0I

0.9

0.8

0.7

E 0.6
-5-ficrocus
0.5 - ] \
c +~~~~~~~~~~~~~~~~~~~Gnetum
o -A- ~~~~~~~~~~~~~~~~~~~~~~
-x Dysoxylum
t:04
: 0.4 -+- ad, > ^ * * * ffi Ternstromia mag.
--SyZy gum1
0.3 -o-riesdelsia 2
X Agalea
-

0.2

1 13
0.1
0. I I I I I I

0 1 2 4 5 6 8 10 12 14 16 18 22 24 26 28 30
Timeelapsed
(days)
Fig. 3.

Americanspinyrats (Proechimyssemispinosus)prefer- seeds of different sizes in our cage experiments (Table

entiallyate large seeded species. Empirical studies in
old fields(Mittelbachand Gross 1984) and in deserts
(Podolsky and Price 1990) also supportthe contention
that rodentsgenerallypreferrelativelylarge seeds.
However, despite theoreticalargumentsand many
empiricalresultsto the contrary,seed predatorsin our
fieldexperimentpreferredrelativelysmall seeds (seed
weight < 0.5 g freshweight),at least withinthe range
of seed weightsrepresentedby the 40 species studied
(0.1 g to 11.6 g freshweight).Similarresults,i.e. higher
predationrates on small and mediumsized seeds than
on largeseeds,wereobtainedby Osunkoya(1994), in a
rain foreststudyin northeastern Australia,whereseeds
of 12 species rangingin mean size from0.06 g to 35.2
g (freshweight) were placed in the field. However,
Osunkoya's (1994) study differedfrom ours in that
seeds of all specieswereplaced together,so thatpreda-
tors were presentedwithmany more seeds, and many
alternativeseed sizes to choose among, at each loca-
tion. The preferenceof seed predatorsfor small and
medium sized seeds found by Osunkoya (1994) also
matches the preferenceof spiny rats for small and
medium sized seeds, when they were presentedwith
6).
It is not surprisingthat large seeds withthick,hard
seed coats would generallybe leftby seed predators,
because of the difficulty or impossibilityof handling
them.For example,Terborghet al. (1993) foundthat
theverylarge(25-30 g), physicallywell-protected seeds
of Calatola venezuelana(Icacinaceae), sufferedno pre-
dation at all. Our observationssuggestthatthe animals
that eat such seeds are specialistscapable of dealing
with veryhard seed coats. The tuftedgroundsquirrel
(Rheithrosciurus macrotis), a large squirrel with ex-
tremelypowerfuljaws, readily eats the large, hard
Canariumseeds; almost ail recorded observationsof
tuftedground squirrelsat the researchsite are in or
below the canopy of fruitingCanariumtrees(G. Blate
and M. Leightonpers. obs.). Yet, even such specialist
seed predatorsdo not impose a highmortalityrate on
the taxa with large,hard seeds (Table 1, Fig. 2), per-
haps because such specialistpredatorsdo not occur at
high abundances.
In contrast,thelow removalratesof largeseeds with
soft,thin seed coats cannot be attributedto physical
defenses. Furthermore,it seems unlikely that large

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 b)
1.0

0.9

0.8 A I

0.7 -
Cananiucf. apertum

g 0.6 -x+ A denanthera

-\- Knerma
O 0.5 - - Cryptocarya
1
0 \ -\-i-Palaguium
.0 - Co\b-ryntocarya
2
C). o --x--Dysoxvlum
Aft\ x
0

_ o
-a---TeT-t ama
A
0.3 - Fissistigma
- Syzygium 2
0.2

Id
0.t
0.0 -|Ht- -l1-1--
0 2 4 7 8 9 10 11 12 13 14 16 18 20 22 24 26 28 30
Timeinfield(days)
Fig. 3.

seeds would, in general,be visuallymore cryptic,or to be taken by invertebratethan by vertebrateseed

provide less effectivechemical cues than small seeds.
The fact that some fairlylarge seeds withno physical
protection(e.g. Stemonurussp. 2, Cryptocaryaspp.)
wereremovedat quite low ratessuggeststhatthesetaxa
may be eitherunrewardingnutritionally, or protected
by effectivechemicaldefenses.Grubb (1996) presents
data fromrain forestspecies indicatingthat nitrogen
concentrationdoes generallydecline with increasing
embryo size. Grubb (1996) also found that nitrogen
concentrationtendedto increasewiththe thicknessof
the seed coat, suggestingthat more nutritionallyre-
wardingseeds may be betterprotectedphysicallyfrom
the attacksof seed predators.
Generalizationsabout theeffectsof seed size mustbe
qualifiedbecause the range of seed sizes we examined,
althoughit coverstwo ordersof magnitude,spans only
part of the potentialrange.Metcalfeand Grubb (1995)
reportedseeds rangingin dryweightfrom5 x 10-6 g
to 50 g (i.e. coveringsevenordersof magnitude)in rain
forestin Singaporeand Malaysia, exclusiveof orchids
and parasiticplants. It is possible that predationrates
may eventuallydecline with decreasingseed size, for
verysmall seeds. Verysmall seeds are also more likely
predators.Anotherqualificationrelatesto the focusof
this study on isolated seeds. It is possible that the
trendswe found in predationrates,accordingto seed
size and morphology,and accordingto plant family,
may be differentwhenseeds occur at highdensities,for
example near the parent plant in species with highly
aggregatedseed distributions.
Germination
When exploringthe implicationsof seed predationfor
population dynamics,it is importantto considernot
only the predator-inducedmortalityrate of seeds, but
also the lengthof time that seeds are vulnerableto
predators.Seeds of differentspecieshave verydifferent
germinationrates (Table 4). For the seed stage of the
lifecycle,both the predationrate and the durationof
the seed stage contributeto the likelihood of seed
predation.Ng (1978) notedthatthe seeds of rainforest
canopy trees that germinatedwithin 12 weeks after
dispersalweremorelikelyto escape seed predationthan
those with more delayed germination. Similarly,

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 c)

1.0

0.9

0.8 1- * * * . . * * * * *
-u-~~~~~~~~~~~~~~~Canariu
Elacarus
0.7 XX\ aa Adenanthera
-.-Syzygium 4
0.6 Kx Stemonurus mal.
E
-o- Santiri'a
-a-Syz;ygium 3
O
0.5
\*
XXX
(4oV;
Gymnacranthera
X
Stemonurusumb.
t 0.4 -+ Ternstroemia
sp.
- Roureopsis
0.3 - Baccaurea

0.2

0.1

0.0 -
0 1 2 4 5 6 8 10 12 14 16 18 20 22 23 24 25 26 27 28 29 30
Timeinfield(days)
Fig. 3.

Geldenhuys(1993) foundthat the seeds of Podocarpus
facaltus,whose hard sclerotestadelayedgermination by
up to one year,sufferedmore post-dispersalpredation
than the rapidlygerminatingseeds of P. latifolius,a
relativewitha thin,leatheryseed coat.
Althoughlong dormancyis more common in very
small than in large seeds (Harper et al. 1970,Putz and
Appanah 1987,Swaine and Whitmore1988),thisgener-
alization does not apply to the shorttermgermination
rates found in our study.The large seeds at Gunung
Palung withthick,hard seed coats (e.g. Canariumspp.,
Ternstroemia spp., Lithocarpusspp.), wereactuallyslow
to germinate(Table 4, G. Blate pers.obs.). No seeds of
thesetaxa germinatedin the presentstudy(afterup to
80 d in thefield),eventhoughfewhad been removedby
predators.In contrast,the seeds that did germinate
(Table 4) were mostlyfromtaxa with smaller,softer
seeds,whichalso tendedto have higherpredationrates.
Thus, differencesin germinationrates may tend to
reduce differencesin the lifetimeprobabilityof seed
predationbetweenthe taxa with large,physicallywell
protectedseeds and those with smaller,less protected
seeds.
Clearly, then, germinationrates (and the specific
conditionsforgermination) interactwithseed predation
rates to influencethe population dynamicsof plant
species. Similarly,in the process of natural selection,
traitsthat influencegerminationare likelyto interact
withthosethatinfluence to seed predation.
susceptibility
These issueshave apparentlynotbeenexploredin depth,
eithertheoretically A comparativestudy,
or empirically.
monitoringthe fateof seeds of manyspeciesup to the
germinationstage, and includingseedlingmortalityof
the early germinantswould be informative in this re-
spect. At the population level, studies of individual
variationin germination behavior,losses to seed preda-
tion and earlyseedlingsurvivalwould shed lighton the
trade-offs involvedin earlyvs late germination.
Dispersalmode,anti-predator
defensesand
predationrates
Howe (1989) predicted that scatter-dispersedseeds
would tend to germinatein relative isolation from
thusreducingdensity-dependent
conspecifics, predation

OIKOS 82:3 (1998) 535

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 d)
1.0

0.9

0.8 -u--
~~~~~~~~~~~~~~~~~~~~O
0.7
~ ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~-Lithocarpus
to ~~~~~~~~~~~~~~~~~~~~~~~~~~
Lansium,
S ---- Coscinium,
g 06 -
Diospyr
71 <--A-, Polyalthia
0.5 -x- $y mygium
5
o -+
Xylopia
0.4 -9-Fordia
X < _ 8 <
0
;, ~~~~~~~~~~~~~~~~~~~Rourea
-0 Friesodelsia 1
0.3 - Sterculia

Artocarpus
0.2

0.1
I

0.0 .-- .. ...--- I I I - I i 1

0 1 2 3 5 7 9 1l 13 17 21 30
Timeinfield(days)

Fig. 3. Survivorshipof seeds in fieldpredationtrialsfor40 species of rain foresttreesat Gunung Palung, West Kalimantan,
Indonesia.Values are proportionsof seeds remainingafter30 d in thefield.Data aggregatedfrom4 replicatetransectsforeach
fieldtrial.See Table 1 forsample sizes and fullspeciesnames. Species listedon figuresare in increasingorderof proportionof
seeds taken by day 30. (a) Trial 1, (b) Trial 2, (c) Trial 3, (d) Trial 4.

risk,and consequentlylesseningselectionpressurefor Conclusion

the evolutionof chemicalor physicaldefenses.Scatter-
The fieldexperiment showedconclusively thatverte-
dispersedseeds should thereforebe poorly protected,
brateseed predators do findand take isolatedseeds
and consequentlydependenton good dispersal (and undernaturalconditions, at thetimeof naturalseed
thus escape fromdensitydependentpredation)to sur- fall.Less thanhalfof theplacedseedsremained after
vive. In contrast,clump-dispersed species(mostlyseeds 30 d. Thus,post-dispersal vertebrateseed predators,
defecatedby primates)would generallygerminatein actingafterdissemination of seedsby animalvectors,
close proximityto conspecifics,resultingin density-de- probablyaccountforsubstantial mortality of isolated
pendentpredationpressure,naturalselectionfordefen- seedsin thisrainforest habitat.The levelsofpost-dis-
sive traits, and thus better developed physical or persalseedpredation we havedocumented forisolated
chemicaldefenses. seedsmaybe sufficient to exerta stronginfluence on
In thisstudy,we did findthatsmall,scatter-dispersed both the population dynamics of trees and natural
seeds that were poorlyprotectedphysically(e.g. all of selection actingon seedtraits.
the Connaraceae, Baccaurea stipulate,and Sterculia The measured predation ratesapplybothto scatter-
dispersedspeciesand to the moreisolatedseeds of
stipulate)had the highestpredationrates.But Artocar-
clump-dispersedspecies.Our resultsdo not fitneatly
pus cf. nitidus,Friesodelsiaspp. and Fissistigmasp., all
withthepatterns predictedbyHowe (1989),suggesting
small clump-dispersedspecies, also lacked significant thatgeneralizations abouttheevolveddefenses ofscat-
physical defensesand sufferedsimilar,high levels of tervs clump-dispersed speciesmaystillbe premature.
mortality. Moreover, both Canarium spp. and Predationrateswere more relatedto the size and
Elaeocarpus stipularis,despite being scatter-dispersed,morphological characteristics
ofseedsthanto theusual
were the most physicallywell-protectedseeds in our dispersalmode (scattervs clumped),forthe 40 seed
trialsand had the lowestpredationrates. taxawe examined.

536 OIKOS 82:3 (1998)

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 Whetherthe trendof lower predationrate with in- Charnov, E. J. 1976. Optimal foraging:the marginalvalue
theorem.- Theor. Popul. Biol. 9: 129-136.
creasingseed size holds across a wider range of seed Clark, D. A. and Clark, D. B. 1984. Spacing dynamicsof a
sizes,or forseeds at highdensity,remainsto be tested. tropicalrain foresttree:evaluationof the Janzen-Connell
However, in communitieswhere seed predationrates model. - Am. Nat. 124: 769-788.
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dispersal in Cymbopetalum baillonii(Annonaceae) at Los
spectiveof seed density,theremay be interesting impli- Tuxtlas,Mexico. - J. Trop. Ecol. 4: 157-172.
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largeseeded and smallseeded speciesmaybe somewhat dispersalby rodentsin Panama. - Oecologia 87: 596-599.
attenuatedby the time the progenyreach the seedling Forget,P.-M., Munoz, E. and Leigh, E. G., Jr. 1994. Preda-
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Acknowledgements - We thanktheCenterforResearchand Grubb, P. J. 1977. The maintenanceof species-richnessin
in
Development Biology,IndonesianInstituteof Science plant communities:the importanceof the regeneration
(LIPI) and the Subdirectorate of Nature Conservation niche. - Biol. Rev. 52: 107-145.
(PHPA) oftheMinistry ofForestry, forpermission toconduct Grubb, P. J. 1996. Rainforestdynamics:the need for new
researchat GunungPalung,and fortheircooperation and paradigms.- In: Edwards,D. S., Booth, W. E. and Choy,
assistance.A. G. Blundell,D. G. Gavin,G. D. PaoliandC. 0. S. C. (eds), Tropical rainforestresearch:currentissues.
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thankP. J.Grubb,V. L. Sorkand C. 0. Webbforcomments Hammond,D. S. 1995. Post-dispersalseed and seedlingmor-
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