Journal of Tropical Ecology Identifying keystone plant resources in an Amazonian forest using a long

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Identifying keystone plant resources in an Amazonian forest using a long-
term fruit-fall record
Zoë Diaz-Martin, Varun Swamy, John Terborgh, Patricia Alvarez-Loayza and Fernando Cornejo
Journal of Tropical Ecology / Volume 30 / Issue 04 / July 2014, pp 291 - 301
DOI: 10.1017/S0266467414000248, Published online: 23 June 2014
Link to this article: http://journals.cambridge.org/abstract_S0266467414000248
How to cite this article:
Zoë Diaz-Martin, Varun Swamy, John Terborgh, Patricia Alvarez-Loayza and Fernando Cornejo (2014). Identifying keystone
plant resources in an Amazonian forest using a long-term fruit-fall record . Journal of Tropical Ecology, 30, pp 291-301
doi:10.1017/S0266467414000248
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JournalofTropicalEcology(2014)30:291–301.©CambridgeUniversityPress2014
doi:10.1017/S0266467414000248
Identifying keystone plant resources in an Amazonian forest using
a long-term fruit-fall record
Zoe¨ Diaz-Martin∗,VarunSwamy†,‡,1,JohnTerborgh†,PatriciaAlvarez-Loayza†and
FernandoCornejo§
∗DepartmentofEnvironmentalStudies,ConnecticutCollege,270MoheganAve,NewLondon,CT06320,USA
†CenterforTropicalConservation,NicholasSchooloftheEnvironment,DukeUniversity,Box90328,Durham,NC27708,USA
‡HarvardForest,324NorthMainStreet,Petersham,MA01366,USA
§BotanicalResearchInstituteofTexas,509PecanStreet,FortWorth,TX76102,USA
(Received21October2013;revised10May2014;accepted11May2014)
Abstract: Thekeystoneplantresources(KPR)conceptdescribescertainplantspeciesintropicalforestsasvitalto
communitystabilityanddiversitybecausetheyprovidefoodresourcestovertebrateconsumersduringtheseasonof
scarcity.Here,weusean8-y,continuousrecordoffruitfallfroma1.44-hamatureforeststandtoidentifypotentialKPRs
inalowlandwesternAmazonianrainforest.KPRswereidentifiedbasedonfourcriteria:temporalnon-redundancy;
year-to-year reliability; abundance of reproductive-size individuals and inferred fruit crop size; and the variety of
vertebrateconsumersutilizingtheirfruit.Overall,sevenspecieswereconsideredexcellentKPRs:twoofthesebelongto
thegenusFicus,confirmingthatthistaxonisaKPRaspreviouslysuggested.Celtisiguanaea(Cannabaceae)–acanopy
liana–hasalsobeenpreviouslyclassifiedasaKPR;inaddition,Pseudomalmeadiclina(Annonaceae),Cissusulmifolia
(Vitaceae),Allophylusglabratus(Sapindaceae)andTrichiliaelegans(Meliaceae)arenewlyidentifiedKPRs.Ourresults
confirmthataverysmallfraction(<5%)oftheplantcommunityconsistentlyprovidesfruitforabroadsetofconsumers
duringtheperiodofresourcescarcity,whichhassignificantimplicationsfortheconservationandmanagementof
Amazonianforests.
KeyWords:Amazon,CochaCashu,Ficus,frugivory,keystoneplantresources,MadredeDios,Peru,primates
INTRODUCTION group of plants that bear fruit primarily during the
transitional period between the wet and dry seasons
The keystone species concept, a fundamental theory in when fruit availability is lowest. Twelve keystone plant
ecology,explainstheroleofcertainspeciesinmaintaining species that support the nutritional requirements of the
communitystabilitythroughtrophicinteractions(Bond frugivorecommunityduringtheseasonoffruitscarcity
1993, Kricher 2011, Paine 1969, Power et al. 1996). wereidentifiedatCochaCashuBiologicalStation(CCBS)
A keystone species is one that exerts disproportionate inManuNationalParkinsouth-easternPeru.However,
influence on the food web relative to its abundance the study focused primarily on the availability of the
(Kricher 2011, Power et al. 1996). The concept can be plant resources during the season of food scarcity and
extended to include certain plant species that provide lessontheirreliabilityandabundance.Furthermore,the
nutritional resources for animals during the period of availabilityofplantresourceswasdeterminedprimarily
food scarcity (Bond 1993, Kricher 2011, Peres 2000, through observations of primate foraging, resulting
Whitmore 1998). Terborgh (1986a) first framed the in an incomplete list of keystone plant resources in
concept of keystone plant resources (KPR) in tropical relationtotheentirecommunityofvertebratefrugivores.
forests, suggesting that the frugivore community of a SubsequenteffortshaveidentifiedKPRsinothertropical
neotropicalforestdependsdisproportionatelyonasmall forestecosystems(Lambert&Marshall1991,Leighton&
Leighton1983,Peres2000),andtheKPRconceptisnow
largelyaccepted.However,giventhewidevarietyinthe
rawdataandtestcriteriausedinpreviousstudies,theKPR
1Correspondingauthor.Email:[email protected] conceptremainsopentofurthercriticalconsiderationand
292 ZOE¨DIAZ-MARTINETAL.
refinement,particularlyinthemethodsandcriteriaused study,weusedeightcompletecalendaryearsofseedtrap
toidentifyKPRs. datafromJanuary2003toDecember2010.
In this study, we reexamine the keystone plant
resourcesconceptinalowlandwesternAmazonianforest
using an 8-y record of year-round fruit production. We Dataanalysis
useaquantitativeapproachandacomprehensivesetof
criteriatoidentifypotentialKPRs,andtestthefollowing Community-wide fruiting phenology patterns. Before testing if
hypotheses: (1) community-wide fruiting phenology individual species fitted the KPR criteria based on their
reflects a distinct and consistent annual period of fruit fruitingphenology,wefirstdeterminedcommunity-level
scarcity,(2)averysmallfractionofspeciesconsistently periods of fruiting highs and lows, which correspond
produceall/mostoftheirannualfruitoutputduringthis to periods of resource abundance and scarcity for the
period, and (3) a subset of these species are sufficiently frugivorecommunity.Onlyspeciesthatproducefruitsor
abundantintheirfruitoutputandbroadlyconsumedto seedsconsumedbyvertebrates(personalobs.,Terborgh
serveaspotentialkeystoneplantresources(KPRs)forthe 1983, Terborgh et al. 2008) were analysed. All ripe
consumercommunity. fruitsandmatureseeds(withandwithoutadherentpulp)
recorded in the seed-trap collections were used in this
analysis since these categories indicate the presence of
METHODS fruitavailableforconsumption.
First,thetotalnumberofpropagulesrecordedinseed
Studysite trapsi.e.totalfruitoutputforeachspecieswastalliedfor
eachmonthofeachyear.Ifthetotalnumberofpropagules
CochaCashuBiologicalStation(CCBS)islocatedwithin recordedforaspeciesincludedbothseedsandfruit,seed
ManuNationalPark(11°54(cid:3)S,71°22(cid:3)W),atthewestern countswereconvertedtofruitcountsbydividingtheseed
marginoftheMadredeDiosriverbasininsouth-eastern count by the average number of seeds per fruit for that
Peru.Lessthan10cmofrainfallsduringthedryseason species,andthenaddingthatnumbertotheoriginalfruit
fromJunetoOctober,althoughthismayvaryannually counttoobtainthetotalfruitoutputforagivenmonth.For
(Terborgh1990).Community-widefruitingbeginsatthe speciescollectedonlyasseeds,noconversionwasneeded
onset of the rainy season, peaking once in November sincethedataweresubsequentlyrelativized.Dataonseeds
andagainbetweenJanuaryandMarch(Terborgh1990). perfruitwereobtainedfromAlvarez-Buylla&Mart´ınez-
Duringthisperiod,roughlybetweenSeptemberandApril, Ramos(1992),Cornejo&Janovec(2010),Gentry(1993),
an excess of fruit resources is available for frugivorous Kalko & Condon (1998), Russo (2003) and Stevenson
vertebrateconsumers(Terborgh1986b).Fruitresources etal.(2002).
arescarcebetweenMayandAugust,duringthetransition Analysisofwhole-communityfruitingphenologyand
fromtherainytotheearlydryseason(Terborgh1990). comparisonsbetweenindividualspeciesmustaccountfor
During this period, frugivores adjust their behaviour to substantialinterspecificdifferencesinfecundity,biomass
copewithlimitedresources(Terborgh1983,1986a;Van andnutritionalcontent.Sincedataonthesetraitswere
Schaiketal.1993). unavailable for several species, we instead relativized
the raw fruit output data for all species. Monthly fruit
outputsforeachindividualspeciesinagivenyearwere
Datacollection convertedtoproportionsoftotalannualoutputforthat
yearbydividingeachmonth’soutputbythatyear’stotal
Between2002and2011,year-roundquantitativedata output.Then,inordertoobtainthemonthlyproportion
onfruitandseedfallwerecollectedatCCBSwithina4-ha ofannualfruitoutputforthewholecommunity,monthly
(200×200m)long-termforestdynamicsplotsituated proportions for individual species in each month were
in mature floodplain forest habitat. A 17 × 17 array of summed and divided by the total number of species.
289evenlyspacedseed-falltrapswasinstalledwithinthe Finally, the monthly proportions of annual fruit output
central1.44ha(120×120m)oftheplotatthebeginning for each individual species and the whole community
ofthestudy.Seedtrapsconsistedof0.49m2(70×70cm) wereaveragedacrossall8ytoobtainthemeanmonthly
openbagsmadeof1-mmnylonmeshsewntowireframes relativizedoutputs,orMMROs.
with0.5-mmmonofilamentline.Cornersofthetrapswere Ifmonthlyfruitoutputwasuniformthroughtheyear,
attachedtonearbytreeswith1-mmmonofilamentlineso eachmonthwouldbeexpectedtoproduceanaverageof
thatthetrapsweresuspendedapproximately1mabove 8.33%ofthetotalannualoutput,andMay–Augustwould
theground.Thecontentsofthetrapswerecollectedevery produce,onaverage,33.3%oftheannualoutput,with
2wk,andallseeds,fruitandfruitparts(capsules,valves, 66.7%inSeptember–April.However,if,ashypothesized,
pods,etc.)wereidentifiedtospeciesandrecorded.Forthis the May–August dry season is, in fact, a period of fruit
KeystoneplantresourcesinanAmazonianforest 293
scarcity, the observed MMRO for each of these months was based on density of reproductive-sizeindividuals in
would be less than 8.33% of the yearly output, and two 4-ha forest dynamics plots at CCBS including the
significantly lower than the observed MMRO for the seed-fall monitoring site, and regional scale abundance
September–Aprilperiod. was based on density of reproductive-sizeindividuals in
four additional 4-ha plots of mature floodplain forest
spread across the Madre de Dios basin (BM: 12°15(cid:3)S,
KPR criteria. In a critical discussion of the keystone 70°55(cid:3)W;TRC:13°7(cid:3)S,69°36(cid:3)W;RA:12°32(cid:3)S,69°3(cid:3)W;
plant resource concept in the neotropics, Peres (2000) LA:12°34(cid:3)S, 70°4(cid:3)W). Species-specific size thresholds
describedfourcriteriatoidentifyspeciesofcommunity- for calculating density of reproductive individuals were
wideimportanceandevaluatetheirpotentialasaKPR: basedondbhofthesmallestobservedreproductivetrees
temporal redundancy, resource reliability, consumer within the long-term seed fall monitoring site at CCBS.
specificity and resource abundance. This set of criteria Because scandent and hemiepiphytic species are not
providesacomprehensiveframeworktoevaluateaspecies systematically censused in the forest dynamics plots,
and determine its importance at the community level. theirabundanceswereestimatedaseither‘abundant’or
Thesecriteriawereadaptedandappliedtothe8-yrecord ‘present’fromreviewingtheavailableliteratureforthese
ofseedfallasdescribedbelow. specieslocallyatCCBS(McManus2003)andregionally
withintheAmazonBasin(Burnham2002,Nabe-Nielsen
2001).Inordertocompareabundancesbetweenlianas
Temporal non-redundancy (TNR). Peres (2000) defined
andtreespecies,treeswereconsideredeither‘abundant’
temporal redundancy as ‘the degree to which the
((cid:2)1indiv.ha−1)or‘present’(<1indiv.ha−1)bothlocally
availability of a potential KPR synchronizes with that
andregionally.Anothermeasureofresourceabundance
of the combined pool of alternative food resources
was based on the total and average number of fruits
used by a consumer assemblage’. Therefore, the
recordedinseedtrapsduringtheseasonoffruitscarcity
relative fruit output of a putative KPR should be
(May–August)forallyearsthataspeciesshowedtemporal
disproportionately greater during the period of fruit
non-redundancy.
scarcityandcorrespondinglylowerduringtherestofthe
yearinordertobeconsideredtemporallynon-redundant.
Weconsideredaspeciesastemporallynon-redundantif
Consumergeneralization. Consumerspecificitywasdefined
itsproportionofannualfruitoutput(asinferredfromseed
byPeres(2000)as‘aninversefunctionofthepercentage
trapdata)duringMay–Augustwassignificantlygreater
of frugivorous species in a local vertebrate assemblage
than the expected percentage of 33.3% if fruit output
... that were reported to exploit a putative KPR’. In
wasuniformthroughtheyear.Basedonthiscriterion,a
thiscontext,thelocalfrugivorousvertebrateassemblage
specieswhoseobservedpercentageofannualfruitoutput
consistsof‘allbirdandmammalspeciesoccurringatany
in May–August was >42.5% (χ2 = 3.82, df = 1, P =
one site including at least 50% of fruit in their diet’. If
0.05)wasconsideredtemporallynon-redundantforthat
anabundantresourceregularlyprovidesfoodresources
year.
duringtheseasonoffruitscarcity,butisonlyconsumedby
asmallportionofthefrugivoreassemblage,itcannotbe
Resource reliability. Peres (2000) defined resource reli- consideredavaluableresourcetotheentirecommunity
ability as ‘the degree to which a potential KPR at a (Peres 2000). Therefore, an ideal KPR should also be
given site will predictably become available every year highlygeneralized,i.e.consumedbyspeciesfromatleast
to sustain vertebrate consumers, and in the case of 50%ormoreoftheconsumercategoriesdescribedbelow.
low-redundancy resources, through annual periods of Frugivorous vertebrate species were assigned to one
scarcity’. We interpreted the reliability criterion for a of 10 consumer categories based on foraging habits
potential KPR in our study as being temporally non- and body size. For example, diurnal primates were
redundant (based on our TNR criterion) in at least half categorizedaslarge(6–10kg),medium-sized(1–6kg)and
ofallyearsconsidered,i.e.4ormoreof8y. small((cid:3)1kg).Sakimonkeys(Pitheciasp.),marmosets,
coatis (Nasua nasua) and marsupials were not included
because sufficient diet information was lacking. Based
Resource abundance. This criterion is defined by Peres onacomprehensiveliteraturesurveycompiledforCCBS
(2000)as‘thecrudeabundanceofapotentialKPRata (Andresen 2008, Bunce 2009, Castro 1991, Galetti
givensite,onthebasisoftheapproximatepatchdensityof 2000, Gibson 2008, Julliot 1996, Kays 1999, Meluk &
agivenresource,andwhenavailable,someindicationof Rodriguez1999,Mitchell1999,Podolsky1985,Ramirez
patchsize’.Inthisstudy,abundanceoftemporallynon- 1989, Romo 1996, Sherman 1991, Symington 1987,
redundant and reliable tree species was calculated at a Van Roosmalen 1985, Wehncke et al. 2003, 2004;
local scale as well as a regional scale. Local abundance Wright 1985) as well as other published literature
294 ZOE¨DIAZ-MARTINETAL.
Figure1. Whole-communitymeanmonthlyrelativizedfruitoutput(MMRO)atCochaCashuBiologicalStation(CCBS),MadredeDios,Peru,based
onyear-roundfruitfalldatarecordedwithinalong-termforestdynamicsplotoveran8-ystudyperiodfrom2003–2010.Errorbarsare±1SE.
(Romoetal.2004,Swamy2008,Terborgh1986a),the abundance were also assigned based on the yearly
number and per cent of frugivore categories for each average of fruit output of each species recorded in the
potentialKPRspeciesweretallied. seedtraps:>100(excellent),<100and(cid:2)10(good),<10
and (cid:2)5 (fair), <5 (poor). The final ranking of overall
potential as a KPR for each species was determined by
combiningitsrankingforeachindividualcriterion,e.g.
OverallpotentialasaKPR. AputativeKPRspeciesneedsto
speciesrankedas‘excellent’forconsumergeneralization
havefirstsatisfiedthetemporalnon-redundancycriterion
and‘good’/‘excellent’foreitherabundancecriterionwere
because only those species that bear the majority of
considered overall ‘excellent’ potential KPRs, whereas
their fruit during the season of maximum overall fruit
species ranked as ‘fair’/‘poor’ in either abundance
scarcity are potentially ‘entirely indispensable’ to the
criterionand‘good’/‘excellent’forgeneralizationreceived
frugivorouscommunity(Peres2000).Next,onlyspecies
anoverallrankof‘good’.Allspecieswererankedinterms
thatconsistentlyexhibittemporalnon-redundancyi.e.in
of their overall potential as a KPR as either ‘excellent’,
atleastfourormoreyearswereconsideredtohavemet
‘good’,‘fair’or‘poor’.
the reliability criterion. Species that made the shortlist
of reliable temporal non-redundancy were then ranked
separately for the reliability, consumer generalization
andabundancecriteria.Ranksforreliabilitywerebased RESULTS
on the per cent of study years (out of 8 y total) a
species exhibited temporal non-redundancy, as follows: Community-widefruitingphenologypatterns
>87.5% (excellent), 75% (good), 62.5% (fair) and 50%
(poor).Ranksforconsumergeneralizationwerebasedon Thedistributionofwhole-communityMMROs(Figure1)
thepercentageofthefrugivorecommunitythatforaged indicates a pronounced seasonal variation in fruit
uponeach species: (cid:2)50% (excellent),40% (good),30% availability, with an annual peak during January and
(fair) and <30% (poor). Ranks for resource abundance FebruaryandatroughfromMay–August.Only26.0%of
wereassignedbasedonthelocaldensityofreproductive- annual fruit output is produced from May–August and
size individuals: (cid:2)1 indiv. ha−1 (excellent), <1 and the remaining 74.0% is produced between September
(cid:2)0.5indiv.ha−1 (good),<0.5and>0.125indiv.ha−1 andApril,versustheexpectedratioof33.3%and66.7%
(fair) and <0.125 indiv. ha−1 (poor). Scandent and (Figure2a).Themeanmonthlyproportionofannualfruit
hemiepiphytic species were also assigned abundance output (Figure2b) between May–August (6.7% mo−1),
ranks based on estimates of local abundance from is significantly lower than between September–April
availableliterature(McManus2003).Ranksforresource (9.4%mo−1,t=−4.68,P<0.001).
KeystoneplantresourcesinanAmazonianforest 295
Figure2. Observed(whitebars)vs.expected(blackbars)proportionsofwhole-communityannualfruitoutputatCochaCashuBiologicalStation
(CCBS),MadredeDios,Peru,basedonyear-roundfruit-falldatarecordedwithinalong-termforestdynamicsplotoveran8-ystudyperiodfrom
2003–2010.MeancumulativeproportionofannualoutputoverthemonthsofSeptember–AprilandMay–Augustcomparedwiththeexpectation
ofuniformfruitoutputyear-round(a).MeanmonthlyproportionofannualfruitoutputforSeptember–Aprilvs.May–Augustcomparedwiththe
expectationofuniformfruitoutputinanygivenmonth(b).Errorbarsare±1SEcalculatedforsamplesizesof16(a)and94(b).
Temporalnon-redundancyandresourcereliability ‘present’ on a regional scale (Table2). No information
wasavailableontheabundanceofCayaponiamacrocalyx,
Out of a total of 453 species analysed, 222 species had anon-woodyclimber.
temporallynon-redundantfruitingpatternsforatleast1
y.However,only21species(<5%ofallspeciesanalysed),
weretemporallynon-redundantfor50%ormoreofthe Consumergeneralization
8 y, representing a yearly average of 13.9 species or
(cid:4)3% of all species (Table1). Of these 21 temporally Fruits of nine of 21 temporally non-redundant and
non-redundant and reliable species, 12 species showed reliable species were consumed by 50% or more of
temporal non-redundancy in 4 y (50%); four species all frugivore categories and therefore considered as
showed temporal non-redundancy in 5 y (62.5%); one generalizedresources(Table3).
species was temporally non-redundant in 6 y (75%);
threespeciesweretemporallynon-redundantin7of8y
(87.5%)andonespecies–Celtisiguanaea(Cannabaceae)
OverallpotentialasaKPR
–wastemporallynon-redundantinall8y(Table1).
Seven species were considered as ‘excellent’ potential
KPRs (Table4). Two of these belong to the genus Ficus
Resourceabundance and are consumed by 80% of the frugivore consumer
categories. Two liana species (Celtis iguanaea and Cissus
In terms of fruit output recorded in seed traps during ulmifolia) and three tree species (Pseudomalmea diclina,
the period of fruit scarcity, four out of the 21 reliably Trichilia elegans and Allophylus glabratus) were also
temporallynon-redundantspeciesaveraged>100fruits considered‘excellent’potentialKPRs.Threespecieswere
perseason,eightspeciesaveragedbetween10–100fruits classified as ‘good’ potential KPRs, five species were
per season, three species between 5–10 fruits and six considered ‘fair’ and six species were considered ‘poor’
speciesaveraged<5fruitsperseason(Table1).Interms (Table4).
ofdensityofreproductive-sizeindividualsforthe14tree
species,fivewere‘abundant’((cid:2)1indiv.ha−1)andnine
were‘present’(<1indiv.ha−1)onalocalscale;sixspecies DISCUSSION
were ‘abundant’ and eight were ‘present’ on a regional
scale (Table2). Nine of the 21 potential KPR species Theobservedpatternsoffruitingphenologyforthewhole
are lianas. Based on a literature review of the diversity community confirmed that the months of May–August
and dominance of liana species locally as well as in the encompass the season of fruit scarcity while the rest of
Amazon basin (Ecuador and Peru), four liana species theyearistheseasonofrelativefruitabundance.These
wereconsidered‘abundant’andthree‘present’onalocal resultssupportpaststudiesoffruitingphenologyatCocha
scale; two species were considered ‘abundant’ and two Cashu Biological Station (CCBS) that found the annual
296 ZOE¨DIAZ-MARTINETAL.
Table1. Specieswithtemporallynon-redundant(TNR)fruitingpatternsin(cid:2)4yoveran8-yperiod(2003–2010)ofyear-roundfruit-fall
datacollectionwithinalong-termforestdynamicsplotatCochaCashuBiologicalStation(CCBS),MadredeDios,Peru.Totalandaverage
fruitoutput(TFOandAFO)recordedinseedtrapsduringtheseasonoffruitscarcity(May–August)weretalliedforTNRyearsonly.
∗Scandentorhemiepiphyticgrowthform.
Species TNR(y) TFO AFO
Abutagrandifolia(Mart.)Sandwith(Menispermaceae) 4 8 2
AgonandrabrasiliensisMiers(Opiliaceae) 5 23 4.6
AllophylusglabratusRadlk.(Sapindaceae) 5 280 56
Cayaponiamacrocalyx∗Harms(Cucurbitaceae) 4 9 2.3
Celtisiguanaea∗(Jacq.)Sarg.(Cannabaceae) 8 857 107.2
Cissusulmifolia∗(Baker)Planch(Vitaceae) 7 134 19.1
DipteryxmicranthaHarms(Fabaceae) 7 88 12.6
DiospyrosartanthifoliaHiern(Ebenaceae) 5 3 0.5
Doliocarpusdentatus∗(Vahl)Standl.(Dilleniaceae) 4 290 72.6
Drypetescf.amazonicaSteyerm.(Gentry43655)(Putranjivaceae) 4 119 29.8
Fevilleacordifolia∗L.(Cucurbitaceae) 4 4 1
FicuspallidaVahl(Moraceae) 4 4663 1166
Ficuscf.trigonaL.f.(Foster12567)(Moraceae) 4 1029 257
Haydeniaurbaniana(Loes.)M.P.Simmons(Celastraceae) 7 46 6.6
HuerteaglandulosaRuiz&Pav.(Tapisciaceae) 4 16 4
Leretiacordata∗Vell.(Icacinaceae) 6 57 9.5
Paulliniaelegans∗Cambess(Sapindaceae) 4 3 0.8
PrunusdebilisKoehne(Rosaceae) 4 23 5.8
Pseudomalmeadiclina(R.E.Fr.)Chatrou(Annonaceae) 4 112 28
TrichiliaelegansA.Juss(Meliaceae) 5 125 25
Xylosmaintermedia(Seem.)Triana&Planch.(Salicaceae) 4 2152 538
Table2. Localandregionalabundancesofreliablytemporallynon-redundantspeciesatCochaCashuBiologicalStation(CCBS),Madrede
Dios,Peru,basedonsteminventorydata(sixsitesand24hatotalforregionalestimates).Speciesdesignatedas‘Present’and‘Abundant’
have<1and(cid:2)1indiv.ha−1,respectively.∗Scandentorhemiepiphyticgrowthformandthereforenotincludedinsteminventorydata;
abundanceestimatesarebasedonpublishedliterature.ˆUnderestimatedabundance.
Species Localabundance(indiv.ha−1) Regionalabundance(indiv.ha−1)
Abutagrandifoliaˆ Present(0.125) Present(0.042)
Agonandrabrasiliensis Present(0.625) Present(0.208)
Allophylusglabratus Present(0.5) Present(0.417)
Cayaponiamacrocalyx∗ – –
Celtisiguanaea∗ Likelyabundant Likelyabundant
Cissusulmifolia∗ Likelyabundant –
Dipteryxmicrantha Abundant(1.75) Abundant(1.25)
Diospyrosartanthifolia Abundant(3.75) Abundant(1.292)
Doliocarpusdentatus∗ Present Present
Drypetescf.amazonica Abundant(6.5) Abundant(3.917)
Fevilleacordifolia∗ Likelyabundant –
Ficuspallida Present(0.125) Present(0.042)
Ficuscf.trigona Present(0.25) Present(0.083)
Haydeniaurbaniana Present(0.625) Abundant(2.292)
Huerteaglandulosa Abundant(1.875) Abundant(1.5)
Leretiacordata∗ Likelyabundant Likelyabundant
Paulliniaelegans∗ Present Present
Prunusdebilis Present(0.125) Present(0.042)
Pseudomalmeadiclina Abundant(13.5) Abundant(7.083)
Trichiliaelegansˆ Present(0.75) Present(0.75)
Xylosmaintermedia Present(0.375) Present(0.125)
lows in fruit production to be during the transitional fruit output as well as seasonal patterns can change
months between the rainy season and the early dry markedlyfromyeartoyear.Forexample,insomeyears,
season from May–August, and the season of high fruit fruit output was lowest in September and/or October
productionbetweenJanuary–March(Janson&Emmons whereas in other years, fruit output peaked in these
1990,Terborgh1983,1986a,b,1990).However,overall months.Fruitingphenologyintropicalforestsoftenvaries
KeystoneplantresourcesinanAmazonianforest 297
Table3. Categoriesoffrugivoresthatfeedonreliablytemporallynon-redundantplantspecies,andthepercentageofallfrugivorecategories
theyrepresentatCochaCashuBiologicalStation(CCBS),MadredeDios,Peru.Frugivorecategories:LP–Large-bodieddiurnalprimates:
blackspidermonkey(Ateleschamek(Humboldt,1812)),redhowlermonkey(Alouattaseniculus(Linnaeus,1766));MP–Medium-bodied
diurnalprimates:browncapuchin(Cebusapella(Linnaeus,1758)),white-frontedcapuchin(Cebusalbifrons(Humboldt,1812));SP–Small
diurnalprimates:duskytitimonkey(Callicebusmoloch(Hoffmannsegg,1807)),emperortamarin(Saguinusimperator(Goeldi,1907)),
saddle-backtamarin(Saguinusfuscicollis(Spix,1823)),squirrelmonkey(Saimirisciureus(Linnaeus,1758));NAM–Nocturnalarboreal
mammals:kinkajou(Potosflavus(Schreber,1774)),nightmonkey(Aotustrivirgatus(Humboldt,1812));R–Rodents:agoutis(Dasyprocta
spp.),acouchis(Myoproctaspp.);LTM–Largeterrestrialmammals:SouthAmericantapir(Tapirusterrestris(Linnaeus,1758)),collared
peccary(Pecaritajacu(Linnaeus,1758)),white-lippedpeccary(Tayassupecari(Link,1795));Ba–Bats:fruitbats(Artibeusspp.);LAB–
Largearborealbirds:guans(Penelopespp.,Aburriaspp.,Pipilespp.),toucans(Ramphastidae),macaws(Araspp.),parrots(Amazonaspp.);
LTB–Largeterrestrialbirds:pale-wingedtrumpeter(PsophialeucopteraSpix,1825),curassows(Craxspp.,Mituspp.);SB–Smallbirds:
tanagers(Thraupidae),manakins(Pipridae).
Species Frugivorecategories %categoriesrepresented
Ficuspallida LP,MP,SP,NAM,LAB,LTB,SB,LTM 80%
Ficuscf.trigona LP,MP,SP,NAM,LAB,LTB,SB,LTM 80%
Allophylusglabratus LP,MP,SP,NAM,LTB 50%
Trichiliaelegans MP,SP,LAB,LTB,SB 50%
Pseudomalmeadiclina LP,MP,SP,NAM 50%
Cissusulmifolia LP,MP,SP,NAM,SB 50%
Celtisiguanaea Ba,LAB,LP,MP,SP 50%
Abutagrandifolia LP,MP,SP,NAM 40%
Dipteryxmicrantha Ba,R,LP,NAM 40%
Diospyrosartanthifolia LP,MP,SP,NAM 40%
Cayaponiamacrocalyx NAM,MP,SB 30%
Doliocarpusdentatus SP,NAM,SB 30%
Haydeniaurbaniana MP,SP,SB 30%
Paulliniaelegans SP,SB 20%
Leretiacordata LP,SP 20%
Xylosmaintermedia NAM,SB 20%
Agonandrabrasiliensis LP 10%
Huerteaglandulosa SB 10%
Prunusdebilis LP 10%
Drypetescf.amazonica LP 10%
Fevilleacordifolia LTM 10%
Table4. Overallpotentialof21specieswithtemporallynon-redundantfruitingpatternsatCochaCashuBiological
Station(CCBS),MadredeDios,Perutofunctionaskeystoneplantresourcesbasedonthreeadditionalcriteria.
∗Scandentorhemiepiphyticgrowthform.
Overallpotential Species Generalizedresource Abundance(Adults/Output) Reliability
Excellent Celtisiguanaea∗ Excellent Excellent/Excellent Excellent
Pseudomalmeadiclina Excellent Excellent/Good Poor
Trichiliaelegans Excellent Good/Good Fair
Cissusulmifolia∗ Excellent Good/Good Poor
Allophylusglabratus Excellent Good/Good Fair
Ficuscf.trigona Excellent Fair/Excellent Poor
Ficuspallida Excellent Poor/Excellent Poor
Good Diospyrosartanthifolia Good Excellent/Poor Fair
Dipteryxmicrantha Good Excellent/Fair Excellent
Haydeniaurbaniana Good Excellent/Fair Excellent
Fair Xylosmaintermedia Fair Fair/Excellent Poor
Doliocarpusdentatus∗ Fair Fair/Good Poor
Drypetescf.amazonica Fair Excellent/Good Poor
Leretiacordata∗ Poor Excellent/Fair Good
Abutagrandifolia∗ Good Fair/Poor Poor
Poor Agonandrabrasiliensis Poor Good/Poor Fair
Cayaponiamacrocalyx∗ Poor Poor/Poor Poor
Paulliniaelegans∗ Poor Fair/Poor Poor
Prunusdebilis Fair Poor/Poor Poor
Huerteaglandulosa Poor Excellent/Poor Poor
Fevilleacordifolia∗ Unknown Excellent/Poor Poor
298 ZOE¨DIAZ-MARTINETAL.
annually in response to variation in biotic and abiotic glabaratus, Prunus debilis and Ficus pallida, were present
factors;rainfallandirradianceareparticularlyimportant both locally and regionally but only locally abundant
sincetheymediatewaterstressandalsoaffectleafingand (based on stem density or fruit output), suggesting
flowering(vanSchaiketal.1993,Wright&vanSchaik that their potential as KPRs is restricted to the mature
1994).Therefore,theobservedinterannualvariationin floodplainforesthabitatthatcharacterizesCCBS.
fruitingpatternsatCCBSislikelyinfluencedbyvariation Seven species are either scandent or hemiepiphytic
inthetiming,distributionandamountofannualrainfall andwerethereforenotaccountedforintreeinventories.
aswellastheamountofmonthlyirradiance.Adetailed One liana species Abuta grandifolia that frequently
analysis of the interaction between fruiting phenology attains a diameter >10 cm is occasionally but not
and rainfall patterns is beyond the scope of this study systematically censused in tree inventories, resulting
since complete rainfall records for the study region are in an underestimation of its local as well as regional
unavailableforlargeportionsofthestudyperiod(2003– abundance. Both Celtis iguanaea and Leretia cordata are
2010).Nevertheless,theoveralltrendoverthe8-ystudy dominant liana species contributing to the oligarchy
period confirmed that May–August was typically the of lianas in Ecuador (Burnham 2002), which confirms
periodoffruitscarcityatCCBS. their regional and likely local importance as well.
Over450specieswereanalysedinthisstudyandonly Paullinia elegans and Doliocarpus dentatus have been
21 of those species exhibited temporal non-redundancy documentedinEcuador(Nabe-Nielsen2001),indicating
for 50% or more of the study years, emphasizing their thattheyaredistributedregionally.Cissusulmifoliaand
importance during the season of fruit scarcity. Several FevilleacordifoliaarelocallyabundantatCCBS(McManus
specieswereconsideredtemporallynon-redundantinat 2003); information on their regional distribution was
leastone,butlessthanfour,oftheeightstudyyears.It unavailable.Totalandaveragefruitoutputsrecordedin
is possible that frugivores opportunistically utilize these seed traps indicate if a reliably TNR species is fecund
species in addition to more reliable potential keystone enough to serve as a likely KPR. Nine species that
plantresources(KPRs)tosustaintheirpopulationsduring recorded<5fruitsperseasononaverageoverthe8yof
the season of fruit scarcity when food resources are analysisarethereforepoorcandidatesforKPRs.However,
limited(Leighton&Leighton1983,Peres2000,Terborgh this observation is misleading, given the relatively
1986a). However, our evaluation of the reliability small sample area, which limits the presence/density
criterionandinterpretationofresultsareconstrainedby of reproductive individuals of less common species and
the relatively small size of the sample area (1.44 ha), therefore does not provide an accurate estimate of
whichislikelynotlargeenoughtocapturefruitingevents fruit output for these species. Additionally, inherent
onanannualbasisforlessabundantspecies.Giventhat differences in biomass and nutritional content of fruit
not all reproductive-size individuals of any species fruit were beyond the scope of, and not accounted for, in
every year, the sample area may not include sufficient this study, thus limiting the qualitative comparison of
fruiting individuals of these species to register annual fruit output between species. Furthermore, the passive
records of fruiting, even if the fruiting period for these sampling design (an evenly spaced grid of seed traps)
speciesisconsistentfromyeartoyear. used in this study unavoidably underestimates the true
Unlike the other criteria, resource abundance does fruit crop size of most species, particularly for species
not ‘make or break’ a species’ potential as a KPR but with distinct morphologies and architectures, such as
a putative KPR should be sufficiently abundant that unbranchedpalmsandcauliflorousspecies.Thepassive
its removal would have a significant impact on the sampling design could also substantially underestimate
consumercommunity(Peres2000).Althoughonlylocal the fecundity and true fruit crop size of certain highly
abundance was used in ranking the overall potential valuedfruitresources(e.g.Diospyrosartanthifolia,Dipteryx
of putative KPRs, information on regional abundance, micrantha) whose output is consumed almost entirely
when available, enhances the scope of this study by by arboreal frugivores, resulting in scant fruit-fall data
indicating whether potential KPRs identified at this consistingprimarily/entirelyofdispersedseeds.
study site are important at a regional scale as well. Determining consumer generalization was hampered
Therefore, reliably temporally non-redundant species by the high floristic diversity of the study site (and of
that are abundant both regionally and locally, such as the neotropics in general) and the paucity of available
Pseudomalmea diclina, Drypetes cf. amazonica, Diospyros literature,especiallyforlesscommonspecies.Someplant
artanthifolia, Huertea glandulosa and Dipteryx micrantha, species may be more generalized and therefore more
are excellent candidates for KPRs at a regional scale. important than indicated by this study since the 50%
Dipteryxmicranthaisacommonandwell-studiedspecies cut-off was based only on available information in the
atCCBSaswellasinotherregionsoftheneotropics(Cintra literature. Thus, it is probable that more consumer
1997). Species such as Xylosma intermedia, Ficus cf. categoriesthanwereportfeedonthelesscommonspecies.
trigona,Trichiliaelegans,Agonandrabrasiliensis,Allophylus Inaddition,duringtheperiodoffruitscarcity,frugivores
KeystoneplantresourcesinanAmazonianforest 299
may consume certain less-palatable species that are beconsideredaspotentialKPRsandonlyabout2%can
availableyear-roundbutnotconsumedduringperiodsof be considered ‘excellent’ potential KPRs. Because KPRs
highfruitavailabilityofpreferredspecies(Terborgh1983, maysetthecarryingcapacityofafrugivorecommunity
1986a, b; van Schaik et al. 1993). Consequently, the (Terborgh 1983, 1986a), it is essential to keep this
numberofconsumercategoriesmaybeunderestimated smallalbeitcriticallyimportantgroupofspeciesinmind
forsomespecies,whereasthereisgreatercertaintyinthe whenselectingareastoprotect,monitoringforecosystem
number of consumer categories for the more common health or attempting habitat restoration. For example,
plantspecies. designationofPseudomalmeadiclinaasaKPRwouldraise
Only seven species of more than 450 analysed in its conservation profile since this species is commonly
thisstudymettherequirementstoqualifyas‘excellent’ harvestedfortimberintheMadredeDiosbasin(Alvarez-
potentialKPRs.TwoofthesebelongtothegenusFicus, Loayzaetal.2008).ProvidingprotectiontoKPRspecies
confirming the importance of this genus as a KPR incurrentlyunprotected,fragmentedordisturbedforests
in the tropics (Lambert & Marshall 1991, Leighton & couldboostnutritiveresourcesforfrugivores,whichoften
Leighton1983,Mabberley1992,Terborgh1986b,van expand their home ranges in search for food during
Schaik et al. 1993). Terborgh (1986a) even speculated seasonsoffruitscarcity(Terborgh1983,vanSchaiketal.
that the removal of Ficus from the flora at CCBS 1993). Prior information on the KPRs of a disturbed or
would result in ecosystem collapse. Celtis iguanaea, an degraded forest habitat could also help in reforestation
abundant liana species across the Amazon Basin was efforts by making the restored forest more hospitable
also previously identified as a potential KPR at CCBS; for animal species to recolonize. Finally, because of the
this was the only species in our study that displayed mutualistic relationship between plants and their seed
temporal non-redundancy in all 8 y, which further dispersers, it is imperative to maintain healthy and
enhancesitspotentialasaKPR.Allophylusglabratusisa abundant populations of frugivores that will inevitably
commonunderstoreytreelet,whosecongenerAllophylus facilitateforestregeneration.
scrobiculatus, was previously identified as a potential
KPRatCCBS,suggestingthatthegenusAllophylusmay
serve as an important KPR during the season of fruit
ACKNOWLEDGEMENTS
scarcity.Cissusulmifolia,anewlyidentifiedpotentialKPR
atCCBS,isadominantlianainearlysuccessionalhabitats
Financial support for this research was provided by the
alongtheManuRiverinPeru(McManus2003).Trichilia
Andrew Mellon Foundation and the National Science
elegans, a common midstorey tree, and Pseudomalmea
Foundation (DEB 0742830). Z. D-M. was supported
diclina, a common (sub-) canopy species have also not
by a grant from the Goodwin-Niering Center for the
previouslybeenidentifiedaspotentialKPRs;thesespecies
EnvironmentatConnecticutCollege.V.S.wassupported
are therefore significant additions to the literature on
by a 2012–13 Bullard Fellowship in Forest Research
KPRs.
from Harvard Forest. Seed fall data collection received
Certainspeciesclassifiedashavingintermediate(‘good’
assistancefromAmadorTapia,AngelicaGarcia,Antonio
and‘fair’)overallpotentialasKPRscateredtospecialized
Guerra,BethPringle,CeciliaRamirez,ClaraRojas,Jenifer
consumersand/orhadlowoutput.Forexample,canopy
Alvarez, Juan Kapeshi, Julian Huarancasi, Kyle Dexter,
bats as well as rodents forage heavily on Dipteryx
Luis Delgado, Nancy Suarez, Nadir Pallqui, Natalia
micrantha,alargeemergenttree(Cintra1997,Romoetal.
Quinteros, Nohemi Huanca, Victor Chama and Yuri
2004). These species are vital plant resources for their
Huillca. We thank the Instituto Nacional de Recursos
specificfrugivorousconsumersbutnotforthefrugivore
Naturales (INRENA) and Servicios Nacionales a Areas
communityasawhole.Otherspeciesthatrankedpoorly
Naturales Protejidas (SERNANP), Peru for providing
overall as potential KPRs were either uncommon or
authorizationtoconductresearchinManuNationalPark.
had low fecundity or were eaten only by specialized
CommentsandsuggestionsfromMercedesFosterandtwo
consumers.Ingeneral,specieswithlocalizedoccurrence
anonymousreviewersgreatlyenhancedthequalityofthis
and/or abundance are likely important KPRs for the
manuscript.
communities where they occur but not important on a
larger scale. This concurs with past studies suggesting
thattherelativeimportanceofdifferentKPRsmaydepend
onthespatialscaleoftheanalysis(Peres2000,Terborgh LITERATURECITED
1986b).
Our findings have significant implications for the ALVAREZ-BUYLLA,E.R.&MART´INEZ-RAMOS,M.1992.Demography
conservationandmanagementofneotropicalforests.Itis andallometryofCecropiaobtusifolia,aneotropicalpioneertree–an
importanttoemphasizethataverysmallportion,about evaluationoftheclimax-pioneerparadigmfortropicalrainforests.
5%,ofthetotalfleshyfruit-bearingplantcommunitycan JournalofEcology80:275–290.