An Advantage of Large Seed Size: Tolerating Rather than Succumbing to Seed Predators

Author(s): Andrew L. Mack

Source: Biotropica, Vol. 30, No. 4 (Dec., 1998), pp. 604-608
Published by: Association for Tropical Biology and Conservation
Stable URL: http://www.jstor.org/stable/2388830
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BIOTROPICA30(4): 604-608 1998

An Advantageof Large Seed Size: ToleratingRatherthan

Succumbingto Seed Predators1

Andrew L. Mack2
Suite 200, 2501 M St., N. W., Washington,DC 20037, U.S.A.
ConservationInternational,

ABSTRACT
Althoughlargeseeds mightbe moreattractive and apparentto seed predators,
largeseed size could enable tolerance
of seed predators.If seeds are largeenough to sustaindamage thatwould kill smallerseeds yetstillproduceviable
seedlings,investment above the minimumby the maternalplant could be advantageous.I testedthishypothesis by
removing0-80 percentof the cotyledonsof fourlarge-seeded(4-180 g) treespeciesfromPapua New Guinea and
monitoringgermination and seedlinggrowthforeightmonths.All speciesshowedlittlenegativeeffecton seedling
size with up to 50 percentremovalof cotyledonsand the largerspeciesshoweda less seriouseffecton growththan
smaller-seeded speciesabove 50 percentremoval.Large-seededspeciesclearlyhave morethanthe minimum-required
cotyledonary reserves.Observationsof viable seedlingswith heavilydamaged cotyledonssuggestthat thesespecies
withstandattackby rodentsand beetlesby virtueof theirlargesize.

Keywords: cotyledons;
germination;
herbivory;
maternalinvestment; seedpredation;
Papua New Guinea;rodents; seedsize;
tolerance.

TYPICALLY, PLANTS PRODUCE MANY MORE SEEDS THAN METHODS

GERMINATE; mortality is highat the seed stageof a
plant'slifehistory. Hence, thereis thepotentialfor Freshly-fallen seeds were randomlycollectedfrom
selectionon seed traits.Seed size is one such trait, fourtreespeciesat theCraterMountainBiological
affecting severalfitnesscomponentssuch as seed ResearchStation,Chimbu Province,Papua New
dispersal,nutrient reserves,and seed numbers(Ma- Guinea. With thesespecies,fruitpulp was easily
zer 1989; Westobyet a!. 1992). Large seed size removedby hand withoutaffectinggermination
could have a detrimental effecton plant fitnessif (Mack, pers. obs.). All fourspecies exhibitrapid
it increasedseed predationUanzen 1969, Mittel- germinationand have thick,heavystoragecotyle-
bach & Gross 1984, Kelricket aL 1986). Because dons.All specieshavesofttestasthatareeasilypen-
of this,largeseed size mightbe viewedas a poten- etratedby ratsand insects.
tialliability(e.g.,easierto findand moreattractive It was not possibleto obtain adequate sample
to seed predators)thatmustbe offsetby otherad- sizesof freshseedsfroma singletree,so seedswere
vantagessuch as greaterreservesforthe embryo. collectedfrom2-4 treesforeach speciesand mixed
Here I suggestthe hypothesisthat largeseed beforetreatment. Afterseedswereweighed,differ-
size can presentanadvantageif it satiatespotential ent amountsof thecotyledonswereablatedwitha
seed predatorsbeforetheydamagetheembryo:that scalpel.I visuallyattemptedto removeamountsof
largeseed size actsas a buffer, allowingtheseed to cotyledonthatwould span 10-80 percentremoval
be damagedwhilethe embryogrowsand becomes while takingcare to avoid damagingor cutting
a self-sufficientseedling.A maternalinvestment in close to the embryo.Then the seeds were re-
endospermor cotyledonary tissuesabove themin- weighedand the actual amount of cotyledonre-
imum requiredforsustenanceof a vigorousseed- moved was estimatedby the weight difference.
ling mightact as a tolerancetrait(Rosenthal& Seeds were thenpottedin a shadehousein a ran-
Kotanen 1994), or insuranceagainsttheravagesof dom organization;pot positionswereperiodically
potentialseed predators.I make a simple testof rotatedduringthe studyto further minimizeany
thishypothesis withfourspeciesof treesand make potential position effects.Seedling growthwas
suggestions forfurther investigation. monitoredforeightmonths.
The speciesand seeds used in the experiment
are listedbelowwithseed measurements fromthis
1 Received19 June1995; revisionaccepted2 June1997. studyand noteson seed dispersers and seed pred-
2 Mailing address:P.O. Box 15, Weikert,Pennsylvania ators based on three years of fieldwork(Mack
17885, U.S.A. Email: a.mack@conservation.org 1995a, 1995b). Voucherspecimensare deposited

604

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 Advantages of Large Seed Size 605

sp 1
Cryptocarya sp2
Cryptocarya
,= 100' . 100
,= 80 , * 80
60 *60
4O 40
20 20

0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0

Aglaia mackiana Endiandrasp

,=1004 100'
0 I IL-o
.(D 80 L * .80'F

0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0

tissueremoved
proportion tissueremoved
proportion
FIGURE 1. Plotsof percent of maximum heightof seedlings of cotyledon
againstproportion removed priorto
Alllinearregressions
germination. shownweresignificant(P < 0.001).The regression foreachspeciesare:
equations
sp. I y = -72x + 67, R2 = 0.33; Cryptocarya
Cryptocarya sp. 2 y = -48x + 52, R2 = 0.15;Aglaia y = -50x +
76, R2 = 0.40; Endiandrasp. y = -28x + 66, R2= 0. 11.

at the Harvard UniversityHerbaria (Cambridge, wellas batsand hornbills(Rhyticerosplicatus). Some

Massachussetts), Universityof Papua New Guinea seeds are attackedby ratsand beetlesbut less so
(Port Moresby,PNG), and ForestResearchInsti- than the previousspecies.Initialseeds:x = 8.8 g,
tute (Lae, PNG). SD-= 2.5, range= 5.1-13.5 g, N = 31.
Aglaia mackiana Meliaceae (voucherAM # Based upon growthrates,color of leaves,and
256; see Pannell 1997). This speciesis primarily sizeand textureofthecotyledons, thedifferent
spe-
cassowary-dispersed. Seed mortalityis low but cies werejudged to have depletedcotyledonary re-
seeds are commonlyminedby unidentified beetles servesand to be fullyself-sufficient at approxi-
and gnawedbyrats(mostlyRattusverecundus). Ini- mately185 days forAglaia, 230 days forEndian-
tial seeds:x = 116.6 g, SD = 26.6, range= 61- dra, 165 daysforCryptocarya sp. 2, and 145 days
169 g, N = 28. forCryptocaryasp. 1. I used theheightofthetallest
Endiandra sp. Lauraceae (voucher D. D. seedlingof each speciesat thesetimesto represent
Wright# 71). This speciesis dispersedby casso- the observedmaximumheight and divided the
waries and flyingfoxes (Dobsonia moluccensis). heightof each seedlingby thisvalue to yieldthe
Seeds are gnawedby rodentsand beetles(Ontho- percentof maximumheightfor each individual
phagusnearlatenasutus ArrowScarabenae)[voucher (Fig. 1). This value enablesacross-species compar-
depositedAcademyof NaturalSciences]thatchew isonsbecausethemaximumheightof thefourspe-
1 cm diametertunnelsthroughthecotyledons. (99 cm forEndiandra,62 cm forAgla-
Ini- cies differed
tial seeds:x = 126.1 g, SD = 30.4, range= 58- ia, 22 cm for Cryptocaryasp. 1, and 25 cm for
184, N = 32. Cryptocarya sp. 2). Analysisof othermeasures(e.g.,
Cryptocaryasp. 1 Lauraceae (voucherAM # actualheightsor growthratesat different censuses)
13). This, thesmallestspeciesstudied,is dispersed did not cause substantivechangesin theresultsre-
in largenumbersby cassowaries,but otherfrugiv- portedhere.
orous birdsalso disperseseeds.Seeds are not com-
monlyattackedby insectsor rats.Initialseeds:x-
RESULTS
5.3 g, SD = 1.0, range= 3.3-7.5, N = 26.
Cyptocaryasp. 2 Lauraceae (voucherAM # I had predictedthat the two smallerCryptocarya
277). This species is dispersedby cassowariesas specieswould show a more pronouncednegative

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606 Mack

150
evidentin the lowerrightportionof the contour
*
125 - surface(Fig. 3).

75- DISCUSSION
50
Studies of seed predationhave sometimesfound
25-
-s
ioo that rodentsprefer"large" seeds (Mittelbach&
Gross 1984, Westobyet a!. 1992). Alternatively,
-25
large seeds could preventpredationby smallseed
predatorssuch as ants (Thompson 1987, Wes-
0 - 25 -50 -75 > 75 tobyeta!. 1992). Studies of the benefitsof large
oftissueremoved
Percentage seeds have focused on the size and vigor of re-
sulting seedlings (e.g., Zhang & Maun 1993).
FIGURE 2. Hi-lo plots of percentof maximumseed- However, the literatureon this topic (reviewed
ling heightamong seedlingswith different amountsof
theircotyledonsablated.The centralhorizontalline rep-
by Westobyet al. 1992) mostlydeals with tem-
resentsthe mean, the box represents? 2 SE and the peratefloraswherevirtuallyall specieshave seeds
whiskerrepresents + 2 SD. Those categorieswithiden- weighing less than 5 grams (e.g., Baker 1972,
tical symbols(* or #) did not differsignificantly
(SNK Mazer 1989, Westobyet a!. 1992, Juradoet a!.
test;see Results). 1991). Little attentionhas been devoted to the
possibilitythat large seeds enable plants to tol-
erate damage (Rosenthal & Kotanen 1994),
effectdue to cotyledonablation.The effectofpro- probablybecause fewstudieshave examinedflo-
portionremovedon seedlingheightwas stronger ras wheretrulylarge seeds occur.
in the smallest-seeded species(the largestnegative Largecotyledonsor endospermcan protectthe
regressioncoefficient) but the othersmall Crypto- embryobysatiatingpotentialseed predatorsbefore
caryaspecieshad a regression coefficient similarto theseagentsdamage the embryo."Satiation"here
thatof themuchlargerAglaiaseeds(Fig. 1). How- includesboth physically fillingthe rodent'sgut or
ever, removal of large amounts of cotyledon reachingsome maximumtolerableamountoftoxic
(>50%) caused greatermortality in thetwo small- secondarycompoundscontainedin the consumed
er-seededCryptocarya speciesthanin thetwolarge- tissues.In the largestspeciesstudied,up to 141 g
seededspecies(x2 = 11.25, df = 1, P < 0.00 1; Fig. of cotyledonscould be removedwithoutkillingthe
1). seed. This amount could certainlysatiate most
I pooled thedata forall speciesand dividedthe seed-gnawing rodentsat thestudysite.Elevenspe-
seedsintofiveclasses:thosewith0, > 0 and ? 25, cies of rodenthave been recordedat the site (D.
> 25 and ? 50, > 50 and ? 75, and > 75 percent D. Wright,pers. comm.). Nine of thesetypically
removal.A one-wayANOVA revealedthat there weighless than 120 g, one speciesaverages212 g,
was a significant effecton the dependentvariable, and one species weighs over 500 g on average
relativegrowth,due to amount of removal(F = (Flannery1995). Viable,partially-gnawed seedsare
6.48, SS = 1.97, df = 4, P < 0.0001). Student- commonlyfound (Mack, pers. obs.). Likewise,
Newman-Keuls tests showed that the relative largeseed size makesit unlikelythatrodentswill
growthamong all seeds with0-50 percentof the carryseeds to a cache site. In an Australianrain
cotyledonremoveddid not differ but forest,verylargeseeds are less likelyto be moved
significantly,
thatthosewith > 50 percentremovalhad signifi- by rodentsthan smallerseeds (Osunkoya et a!.
cantlysmallerseedlingsthanthosewith< 50 per- 1994). Aftergrazingon a seed,it is likelya rodent
cent (P < 0.01; Fig. 2). will abandon it. Establishedseedlingsof the tWo
The overallpatternis evidentin a three-dimen- largestspeciesin this studyare commonlyfound
sionalplot of thedata (Fig. 3). A surfacewas fitted growingfrompartially-gnawed seeds (Mack, pers.
to the plot using the distance-weightedleast obs.).
squaresmethodwithtensionrelaxedto 0.15 (SYS- The situationis similarwherebeetlesminethe
TAT, Wilkinson1990). The upturnedsurfacefor storagetissue.If the storagetissueis largein vol-
large seeds indicatesthat the effectof cotyledon ume, tunnellingscarabbeetlescan extensively feed
ablationon largeseedsis less pronouncedthanfor and tunnelthroughthistissuewithoutlethallyen-
small seeds and the drop in growthand survivor- counteringthe seed embryo.Heavily-mined coty-
ship occurringaround 50 percentremovalis also ledons were commonlyobservedon young seed-

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 Advantages of Large Seed Size 607

0' N

IV 0'3

-o

FIGURE 3. Three-dimensional plot of initialseed size (z axis), proportionof seed ablated (x axis) and percentof
maximumheightof seedlings(y axis). Data forall fourspeciesare pooled (N = 117) and a contoursurfacefitted
leastsquaresprocedure.
witha distance-weighted

lings of the two largestspecies. This advantage metabolism)sig-

and otherfactors(e.g.,dessication,
would onlyapplyto speciesthatexhibitrapidger- affect
nificantly weightchangeoverlongertimepe-
minationand do not remaindormantlongerthan riodsthanthemanipulation. Such analyseswere
it would take fora lethalamount of tissueto be beyondthescopeof thisstudybutshouldbe in-
damaged. corporated intofurther Lastly,
examinations. only
In all fourspeciesstudied,seedlinggrowthwas a fewspecieswerestudiedhere.Futurestudies
not significantly amongseedsthathad 0-
different shouldexaminea largenumberof unrelated spe-
50 percentof the cotyledonremoved(Fig. 3), sug- cies;ideally, ofa plotsuchas Figure3
thecontour
gestingthereis greatermaternalinvestment in the shouldbe derived frommeanvaluesfordifferent-
cotyledonsamongthesespeciesthantheminimum sized species.
necessaryto produce a healthyseedling.Despite Thisstudyaddsa potentialadvantage to large-
heavy damage, seeds still yield viable seedlings to thosedescribed
seededness byFoster(1986) in
(Figs. 1 and 3). oflarge-seeded
a review tropicaltrees.Maternalin-
There are severalcaveats.Seedlinggrowthwas vestmentin storagetissuemightincreasefitness
measuredin a shadehouse,not under true field through ofotherwise
tolerance lethallevelsofher-
conditions;and the effectof cotyledonremovalin in smallerseedsas wellas the
bivory(predation)
thefieldcould differ. However,numerousfieldob- recognizedadvantagesto seedlingvigor.A large
servations(pers. obs.) of healthyseedlingswith numberof studieshaveaddressed thevariety of
heavilydamagedcotyledonsindicatethatthesespe- thatcanaffect
factors theevolutionofseedsizeand
cies can thrivedespitelevelsof damagecomparable in maternal
thetrade-offs investment in seedsize
to thoseof the manipulatedseeds in thisstudy.I versusseed number(reviewedby Shaankeret al.
did not measurenaturally-occurring levelsof dam- 1988). Thesedataarenotintended to claimthat
age. This would have meantweighingfreshseeds largeseedshaveevolvedin thesespeciessolelydue
and re-weighing them later (losses due to boring to a selective
benefit dam-
to largeseedssurviving
beetles are otherwisedifficultto measure) after age. However, thispotential
benefitof large-seed-
weeks in the field.This createscomplicationsbe- ednessmeritsfurther study.Many experiments
cause germinating seedswould need to be uprooted measuring seedsizeversusnumber havebeencon-

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608 Mack

ducted in controlledgreenhouse environments ACKNOWLEDGMENTS

whereseedpredatorsareexcluded.Wherethere are I thankthe Universityof Papua New
Guinea forspon-
seed "predators"
thatrejectseedsupon satiation, soringmy residencyin PNG and the WildlifeConser-
therecouldbe significant
selection
infavorofseeds vationSociety,theDouroucouliFoundation,and theNa-
thatexceedthesatiation Futurestudies tional Science Foundation(BSR 89-0399) as principal
threshold.
financialsupporters.
I thankK. Ickesand J. H. Jessenfor
of maternaltrade-offs
in seedsizeversusnumber help in the field,Ronda J. Green,S. J. Mazer and D. D.
shouldexaminethisaspect,particularly
withvery Wrightforcommentson themanuscript,and B. D. Gill
large-seeded
species. foridentifyinga beetlespecimen.

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FLANNERY, T. F. 1995. Mammalsof New Guinea. CornellUniversity Press,Ithaca,New York.
FOSTER, S. A. 1986. On the adaptivevalue of largeseeds fortropicalmoistforesttrees:a reviewand synthesis. Bot.
Rev. 52: 260-299.
JANZEN, D. H. 1969. Seed-eaters versusseed size, number,toxicityand dispersal.Evolution23: 1-27
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