Pollination of Bactris by Phyllotrox and Epurea.

Implications of the Palm Breeding Beetles on

Pollination at the Community Level
Author(s): Christian Listabarth
Source: Biotropica, Vol. 28, No. 1 (Mar., 1996), pp. 69-81
Published by: Association for Tropical Biology and Conservation
Stable URL: http://www.jstor.org/stable/2388772
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BIOTROPICA 28(1): 69-81 1996

Pollinationof Bactris by Phyllotroxand Epurea.

Implicationsof the Palm Breeding Beetles on
Pollinationat the CommunityLevel1

ChristianListabarth2
Research CenterforBiosystematicsand Ecology,AustrianAcademy of Sciences, Kegelgasse 27, A- 1030
Vienna,Austria

ABSTRACT
The reproductive biologyofthreesyntopical palm species,Bactrisbifida,B. monticola,
and B. gasipaeswas investigated
to determinetheirpollinationstrategiesand pollinators,and to elucidatetheirimpact on pollinationforthe local
palm assemblage.
In PeruvianAmazonia,Bactrisis pollinatedmainlyby beetlesofthegeneraPhyllotrox (Curculionidae)and Epurea
(Nitidulidae),whichare attractedto the protogynous, heavilyscentedinflorescencesformatingand oviposition.In
experiments (N = 15), beetleswereconstantly raisedin thestaminateflowers,whichabsciseafteranthesis.Pollinator
activityis crepuscular-nocturnal
and the beetleschangefrommale phase inflorescences to femalephase inflorescences
duringtwilight.The non-overlapof sexualphases withinindividualslargelypromotesoutbreedingin Bactris.The
extensively cultivatedB. gasipaes is pollinatedby otherspecies of Phyllotroxand Epurea than the primaryforest
speciesB. bifidaand B. monticola. The lattertwo sharethe same pollinatorswith two speciesof Desmoncus. These
speciesconstitute an assemblageof reproductively similarpalms. The beetlepollinatorsare associatedwiththepalms
mainlyat and above thegenericlevel,althoughdevelopmentof theirlarvaein theabscisedflowers of thehostspecies
probablyleads to a chemicalpreference and thus "flowerconstancy"to thatspecies.At the end of the hostplant's
flowering periodbeetlesmay switchto anotherassemblagemember,because the palms providethe same resources.
The assemblagemembersare patchilydistributed,and populationdensityin such patchesis extremely high. They
show staggeredflowering and the most abundantspecieswithinthe assemblageflower2 or even 3 timesa year,
whileless abundantspeciesfloweronce a year.

Keywords: Bactris(Bactridinae);cantharophily; community;Epurea (Nitidulidae);Palmae (Arecaceae);palm assem-

blage; Phyllotrox
(Curculionidae);
pollination;pollinatorreproduction.

THERE ARE A CONSIDERABLE NUMBER of pollination all investigatedspeciesof Bactrisand cantharophily

studiesin Bactris comparedto otherneotropical
palms. Mora Urpi and Solis (1980) reviewedthe
observations on pollinationin Bactrisby Barbosa-
Rodrigues(1903) on B. gasipaesKunth,B. cary-
otaefoliaMart., B. conciunaMart. and B. setosa
Mart.,and by Rodrigues-Lima (1955) on B. gas-
ipaes,and presenteddetaileddata on pollinationin
Bactrisgasipaes. Other authorsprovidedata on
pollinationofB. guineensis(L.) Mooreand B. major
Jacqu. (Essig 1971), B. wendlandianaBurretand
B. longisetaWendl. (Bullock 1981), B. gasipaes
and B. porschianaBurret(Beach 1984) and B.
bidentulaSpruce(Moraes& Sarmiento1992). Gen-
eralcantharophilouscharacters(Baker& Hurd 1968,
Faegri& van derPijl 1978, Gottsberger 1977) like
protogyny, temperature elevationand strongodours
are reported.Floweringbehaviouris verysimilarin
I Received 27 June 1994; revisionaccepted20 January to draw a particularfocus to the community
1995.
2
Currentaddress:Zieglergasse15/28, A-1070 Vienna, speciessharingtheirpollinators;to obtainquanti-
Austria.
has generallybeenestablished.However,important
aspectsof the pollinationof Bactris viz. mating
activityof the visitingbeetlesduringtheirflower
visitsand ovipositionin staminateflowers, and re-
productionof the pollinatorsin the abscisedsta-
minateflowershas so farbeen overlooked(Lista-
barth1992). Pollinationin the relatedgenusDes-
moncusstillputs emphasison the stronginterde-
pendencebetweenpalmsand theirbeetlepollinators
in an identicalpollinationsystem(Listabarth1994).
Studiesat the communitylevel are our most
promisingapproachforinterpreting complexeco-
systems. The studyoftropicalrainforests necessarily
impliessynthetic work,combiningthescattered in-
formation availablewithnew and complementary
data. An inductiveattemptis made hereand the
goals of thispaper are to reportpollinationin B.
bifidaMart.,Bactrismonticola Barb. Rodr. and B.
gasipaesincomparison to otherspeciesofthatgenus;
of
Bactris and Desmoncusin EasternPeru, syntopic
tativeinsightinto this apparentlyclose plant-pol-
69

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70 Listabarth

linatorrelationship by assessmentof thephenology To testforapomixis5 inflorescences ofB. bifida

and structure of thispalm assemblage,and to per- werebaggedwithnets(mesh-width 0.1 mm).Tem-
formsuitableexperimental designin regardto pol- peratureelevationwas measuredwithan electronic
linatorreproduction. thermometer (ad 30th-1) on thebud's surfaceand
betweentheflowers and is expressedas thedifference
fromthe ambientair temperature.
MATERIAL AND METHODS The treatmentfor a community-wide assess-
Observationson pollinationwerecarriedout from mentwas as follows:thepalm assemblagewas de-
October, 1988 untilJanuary,1990, and data on finedas being constitutedof those specieswhich
thestructure ofthisparticular palm assemblagewere sharethe same pollinators.Therefore data of Des-
collectedinJanuary, 1993, bothinAmazonianPeru, moncus(Listabarth1994) are includedin the sec-
Dpto. Hu'anuco (9?37'S, 74?56'W). The natural tions"insectreproduction " and "phenology, " while
vegetationin the area is classifiedas tropicalmoist a separatestudywas conductedto assessassemblage
forest(sensuHoldridgeet a/., 1971). This is a terra structure,involvingthe speciesof bothgenera:the
firmelowlandrainforest, whichis locallydisturbed adultpalms of 12 randomlychosenplots(90-240
by selectiveloggingand partiallysurroundedby m2 in size) coveringa total area of 0.2 h were
secondaryforestor pasturebut havingan ample countedand mapped. Data wereanalysedin terms
connection to theprimaryforestareas.The climate ofoccurrences vs. non-occurrenceswithinindividual
showsa pronouncedseasonalitywitha wet season plots,and averagenumbersof individualsper m2
fromOctober to April (85% of the total annual are calculated.
precipitation) and a dryseason fromMay to Sep-
tember(only15% of theannualprecipitation). To-
RESULTS
tal annual precipitation in 1989 was 2280 mm.
The groundiswelldrained(whitesandsorpodzols), HABITAT, HABIT AND PHENOLOGY.-In thearea four
but locallythereare smallareaswithgleyicpodzols Bactrisoccur syntopically: The understory of the
thatbecometemporarily floodeddue to the heavy primaryforestcontainsthreespecies,B. monticola,
rainfallsduringthewet season. B. bifidaand B. macroacanthos. Bactrisgasipaesis
For floralbiology18 inflorescences of Bactris a subcanopy-canopypalm thatpresumably escaped
bifida,5 of B. monticola and 8 inflorescencesof B. fromcultivationand whichis rarelyfoundinside
gasipaeswerestudiedin detail,severalotherswere the forest.
observedas controls.Phenologicaldata of all flow- The slenderstemsof the caespitoseBactrisare
eringindividualsobservedwereplottedon thetime spiny(e.g., B. gasipaes,B. monticola)or may be
axis and represent the populationsbut not single completely unarmed(e.g., B. bifida,B. macroacan-
individuals. thos).Besidesthestemsotherorgansmaybe armed
Plant specimenare depositedat AAU, NY, suchas leafsheaths,petioleand rachisbut also the
USM and WU: Bactrismonticola Barb.Rodr.(C.L. marginsof thepinnae.The inflorescences are inter-
11-71188), B. bifidaMart. (C.L. 11-81188), B. foliarat anthesis(exceptforB. gasipaeswhereonly
macroacanthos Mart. (C.L. 11-3689) and B. gasi- the leafsheaths persist)but alwayssituatedbelow
paes Kunth(C.L. 11-20889). The palmswereiden- thecrownand thusexposedand at leastfunctionally
tifiedbyH. Rainer(Vienna).The beetleswereiden- infrafoliar. The inflorescences are sheathedby the
tifiedbyJ.-F.Voisinand R. Vincent(Paris)and C. prophylland one prominent peduncularbract.The
H. C. Lyal (London), and discriminated in sp.1, fleshyinnersurfaceof the bractis creamywhite
sp.2 etc.,becausethereis no applicablesystematic whilethegreenorbrownoutersideis usuallyspiny.
treatment. The beeswereidentified byD. W. Rou- The monoeciousinflorescences bear both pistillate
bik (STRI-Panama). and staminateflowers whichare basicallyarranged
To raise those insects,which ovipositedinto in triads(one centralpistillateflowerflankedbytwo
male flowersand apparently reproducedthere,ab- staminateones) but thedistalpartsof therachillae
scisedflowersof all Bactrisspecieswere put into arealwayspuremalewithpairedorsinglestaminate
Petri-dishes withsterilemoistsand. Different mois- flowers.
turewas offered to providedifferentqualitiesofthe Bactris bifida is a small (up to 2 m high)
substrate. In B. monticola and B. bifidaflowers were understory specieswhichformsclustersof usually
countedtoquantify thenumberofinsectsperflower. 2 or 3 stems.The individualsoccurirregularly in
The same treatment forraisinginsectswas made thewell drainedareasoftheforest.The population
fordroppedfemaleflowers. of B. bifidaappearsmorphologically veryhetero-

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 Pollinationat the CommunityLevel 71

TABLE 1. Comparison in Bactris.

offlowering

B. bifida B. monticola B. gasipaes

Bractopens-pistillateanthesis' 1545-1630 1800-1830 1600-1700
End of pistillateanthesis' 0000-0500 2300-0200 0050-0900
Staminateanthesisstarts' 1330-1425 1645-1700 1615-1735
Abscissionof staminateflowers' 1730-1900 1715-1730 1745-1815
End of staminateanthesis' 1900-2030 2030-2100 1845-1930
T-elevation2in bud 1.1-3.6 1.4-3.3 0.9-3.1
T-elevation2in pistillateanthesis 3.8-6.3 (7.2) 7.3-8.2 (8.7) 7.9-9.8 (12.9)
T-elevation2in staminateanthesis 3.6-5.0 (7.6) 8.4-9.7 (12.2) 3.3-3.8 (5.1)
1 Time ranges(local time).
2 Usual range(maximum)in 'C.

geneous:theleavesareusuallybifid,butin some Bactris macroacanthos is apparentlya habitat

individuals pinnateleaveswithup to 38 grouped specialistwhichis restricted to wetbut well drained
pinnaearedeveloped. Inflorescencesareeither spi- and indinedsitesnearcreeks.Only a fewclusters
cateorforked, andbothtypesofinflorescences may withup to 4 stems,2-4 m high,occurredin the
alternateonthestem.Theperianth ofthestaminate investigated area. Individualswerefoundwithin-
flowers is creamy whitebuttherearea fewindi- fructescences but did not flowerduringthe study
vidualswhichdeveloppinkish petals. period.
However,its biologyin termsof phenology,
flowering behaviour and insectvisitationis a well
FLOWERING AND POLLINATION
definedandconstant character.One inflorescenceis
produced perstemandflowering period.Flowering Bactrisbifida.-2 or 3 weeks beforeanthesisthe
periodis twicea year,inAprilandMay,andfrom inflorescence budsprotrude fromthesubtending leaf
Octoberto November. Flowering in 2 subsequent sheathand rapidlyincreasein lengthand diameter.
flowering periodswithin1 dusteris commonly ob- Already3 to 4 daysbeforeanthesis,thermogenesis
served,butsinglestemsusuallyflower onlyoncea occursin thebud (1-3.6?C above airtemperature).
year.Of 53 inflorescencesinvestigatedonly4 flow- As soon as the peduncularbractsplitsand the in-
eredoutsideof thenormalperiod.Fruitsmature florescence is released(ca. 1600 hr), the pistillate
within 6 months andchangecolourfromgreento flowersare at anthesisand stigmasare hyalineand
violetandfinallyblack.Ripefruits arefoundbefore coveredwith stigmaticliquid. Spicate and forked
and during thesubsequent floweringperiod. inflorescenceswere foundin a ratio of 1:2 (N =
Bactris monticola
forms dustersofupto6 stems. 53), and rachis(rachillae)are 4-6 cm long and
The clusters arepatchily distributedin theforest, typicallybear denselyarrangedtriads.The ratioof
sincethespeciesis essentially
restrictedto thetem- femaleto male flowers was 1:3.7 and 1:4.4 (counts
porarilyinundated areas.Inthosepatches numerous of2 inflorescences). The inflorescenceemitsa sweet-
clustersofB. monticolaarefound.Thesinglespiny ish, yeastyfragranceand thereis thermogenesis,
stemsareup to 5 m high.Usually2 inflorescences both reachinga maximumat ca. 1700 hr (Table
per stemare borneduringthe flowering period 1). Emissionof fragranceand thermogenesis de-
whichis oncea yearfromOctoberto November. creasesuccessively untilca. 2300 hr.Stigmasremain
In only1 caseflowering occurred extraperiodicallyreceptiveforsome 8-12 h (Table 1) untiltheydry
inJune.Thefruits areblack-violet
atmaturity (April, outand becomebrownish, whilethestaminate flow-
May). ersare stillclosed.
Clusters ofBactrisgasipaesbearseveral (up to Staminateanthesisbeginsin theearlyafternoon
8) densely armedstems,10-20 m high.According of thenextday (1330-1430 hr) and petalsspread.
to thesizeof thepalmup to 9 inflorescences are The anthersare stillclosed but soon dehisceand
subsequently borneperstemand flowering period releaseclumpedpacksofpollen.Thermogenesis and
(Augustto November). The fruits arebrick-red o; emissionof fragrance, however,less intensivethan
orangeat maturity (January & February) andhar- duringpistillateanthesis,reachmaximumvaluesat
vestedby birds(ifnotby man).B. gasipaeswas 1730 hr (Table 1). At thattime,singlestaminate
observed insecondary forestsitesorat theedgesof flowersalreadyabscisefromthe rachillae,but the
theprimary forest. massof theflowers is shedlater(untilca. 1900 hr;

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72 Listabarth

TABLE 2. InsectvisitorsofBactrisinflorescences.

B. bifida B. monticola B. gasipaes

Visitors female male female male female male

Heteroptera/Miridae - - (*) (*)

Hymenoptera/Apinae/Meliponini
guianae
Trigonafulviventris (*)
Trigonarecursa- (*)
Trigonaamazonensis ---
Trigonarufescens - -

Partamonacupira -- -
Hymenoptera/Halictidae/Megaloptasp (*) (*) * * * *
spl
Coleoptera/Staphilinidae * * * * *
sp2
Coleoptera/Staphilinidae (*) (*) (*) * *
Coleoptera/Scarabaeidae/Dynastinae (*) (*)
Coleoptera/Curculionidae/Barinae (*) (*) (*) (*) * *
Coleoptera/Curculioinidae/Derelomini
Phyllotrox spi *** *** *** ***
sp2
Phyllotrox *** ***
sp3
Phyllotrox *** ***
Coleoptera/Nitidulidae
Epurea spi *** *** *** ***
Epureasp2 *** ***
Diptera/Phoridae (*) * *
Diptera/Drosophilidae (*) (*) *

Otherinsects (Blattodea)diverse (Blattodea;Tettigon- (Blattodea;Tettigon-

Diptera idae; moths)-di- idae; Forficulidae;
verseDiptera moths)-Chalci-
didae; diverse
Diptera

found;* constant,rare;*** constant,verycommon.

not found;(*) facultatively

Table 1). The definiteend of staminateanthesis, stageinflorescences. Only pollencollecting bees

when the last flowershad abscisedand no more (Trigonafulviventrisguianae,T. recursa,Megalopta
pollenis available,is onlyat ca. 2000 hr. sp.)aresometimes attractedtothestaminate flowers
From the onset of pistillateanthesisDroso- (Table2).
philidae,Staphilinidaeand Phyllotrox sp.2 (Cur- Bactrismonticola, B. gasipaes.-Bothspecies
culionidae:Derelomini)are attracted.During twi- showa similar flowering behaviour compared to B.
lightseveralothervisitors(compareTable 2) arrive bifida.The finaldevelopment of theinflorescence
on the inflorescence,especiallyPhyllotrox sp.l and budsoccurs mostrapidly. In B. monticola thebuds
Epureasp.l (Nitidulidae).At ca. 1900 hr visitors protrude fromthesubtending leafsheathforthe
crowdtheinflorescence and mate,ovipositintothe firsttimeonlyaboutfourweeksbeforeopening,
staminateflowerbuds, and feedon floralexudates and stillincreaseconsiderably. In B. gasipaesbud
or petal tissue.As a resultof thisactivityfrequent development triggerstheabscission ofthesubtend-
contactswiththe protrusive stigmasare observed. ingleaf,whichbreaksat thebase of thepetiole.
Activityof thevisitorsdiminishes in thenightuntil Priortoanthesis thermogenesis occursinbud(Table
insectsbecomecompletelyinactivein the morning anthesis
1). Pistillate startsimmediately afterthe
and hide betweenthe staminatebuds (beetles)or peduncular bracthassplit,whichis in thelateaf-
leave(flies).One quantitativesampletakenat 1300 ternooninboth,B. monticola andB. gasipaes(Table
hr.yielded472 Phyllotrox sp.1, 229 Phyllotroxsp.2, 1). The inflorescencesarealwaysbranched to the
and 67 Mystrops sp.l. During staminateanthesis order.The inflorescences
first ofB. monticola bear
beetlescommenceactivityand feed on the abun- 16-19 spirally arranged whichareca. 17
rachillae,
dantlyreleasedpollen packs, althoughmatingis cmlong,andin B. gasipaes42-50 rachillae, each
stillobserved.At twilight, duringthe abscissionof 21-28 cmlong,werecounted The
perinflorescence.
thestaminateflowers thevisitorsdepartto another arrangement of theflowers differsfromthebasic
inflorescence.Thereis no arrivalof beetlesto male patternin thatthenumberof pistillate flowersis

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 Pollinationat the CommunityLevel 73

reduced.Perfect triadsare interspersed in thedom- workerswereobserved.In B. monticola, workersof

inantlymale flowers,and female-maleratios of Trigonarufescens and T. amazonensis wereattracted
1:10.4 in B. monticola, and even 1:72.5 in B. gas- to male phase inflorescences onlyin the late after-
ipaesarefound(countsof 1 inflorescence each). The noon. Some individualsof Megalopta,theonlybee
inflorescences
are fragrant (similarbut distinguish- observedalso on femalephase inflorescences, reg-
able odours with sweetish,yeastycompoundsin ularlyvisitedthe attractiveinflorescences. In late
eitherspecies)and showconsiderable thermogenesis afternoonthe meliponinebees leave, followedby
duringpistillateanthesis(Table 1), its intensity Megaloptaand the beetlesat twilight.
reachingmaximaat earlyanthesis,decliningduring
the night.The end of pistillateanthesisis charac-
terisedby the witheringand/or browningof the INSECT REPRODUCTION.-In all thespecies ofBactris
stigmas,eitherduringthe night(B. monticola)or variousinsectscould be raisedin theabscisedmale
in the morning(B. gasipaes) (Table 1). flowers.The insectsbreedinginside these flowers
Staminateanthesisstartsin the afternoon, and belong to the ordersColeopteraand Diptera and
theanthersdehiscesimultaneously whentheflowers are represented by curculionid,nitidulidand sta-
open. Also duringstaminateanthesisodour pro- phylinidbeetles,and phoridand drosophilidflies,
ductionand thermogenesis occurs.Thereis less in- respectively (Table 3). While in all the samples
tensityof fragrance than at pistillateanthesis,but Phyllotrox emerged,theNitidulidaewereraisedless
in B. monticolathermogenesis is evenhigher(Table constantly. Larvaefedon thetissueofthestaminate
1). Thermogenesis and odour productionshow a flowersand developedrapidly,maturelarvae left
peak fromthe onsetof anthesisuntilthe firststa- the flowers2-4 d afterthey had dropped and
minateflowers abscise.In bothB. monticola and B. changedto the groundand completedmetamor-
gasipaes,abscissionof staminateflowersis a dra- phosisthere(Fig. 1). The timebeetlesneeded for
maticeventwhichoccurswithinjusta fewminutes, metamorphosis was ca. 14 d forPhyllotrox butless,
and onlysomestaminate flowersremainon thedistal ca. 12 days,forEpurea.The beetleshatchedin the
parts of the rachillaeuntil the end of staminate lateafternoon (between1600 hr& 1800 hr).Quan-
anthesis(Table 1). titativedata forraisedPhyllotrox and Epureain the
Beforeand especiallyduringtwilight,visitors flowersof B. bifidaand B. monticolashow wide
arriveto thefemalephase inflorescences. The spec- rangesbetweenthe individualsamples(Fig. 2): in
trumresemblesthat of B. bifidawith minordif- 2-18 percentof the flowersPhyllotrox developed
ferencesand most of the constantand abundant and in 2-28 percentof the flowersEpureadid so.
visitors
differonlyat thespecieslevel,ifat all (Table The totalnumberof both beetlespecies,however,
2). The number of beetles surpassed several is much moreconstantand in everyfifthflowera
thousands, inB. gasipaes,due tothemuch beetledevelops(x = 0.18 ? 0.085, range:0.08-
especially
biggerinflorescences.Visitorsexhibitthe same be- 0.38; N = 11, includingdata of Desmoncus poly-
haviouras in B. bifidaand primarily mate,which acanthos[Listabarth19941).
involvesmuch activityand repeatedcontactswith Otherregularbreedersin theflowers of Bactris
the receptivestigmasprotruding fromthe mass of weredrosophilidflies,whichwereraisedin abun-
staminatebuds. Bugs (Miridae), which have not dant numbers.Metamorphosis lasts ca. 12 d and
been foundon B. bifidawerealwaysabundantat is completedin theuppermostsubstrate-layer. Un-
thefemalestagein theinflorescences ofB. monticola like the beetles, the imagines of Drosophilidae
and B. gasipaes.Theseinsectssuckon thestaminate emergedpreferably in themorning(700-1000 hr).
buds but disappearduringthe night.During the Besides the male flowersalso the femaleones
non-sexualphase of theinflorescences fliesare par- (or latertheyoungfruit)are breedingsites,at least
rare.The stillabundantbeetlevisitors
ticularly shel- in B. bifidaand B. gasipaes.One speciesofBarinae
ter themselvesbetweenthe rachillaeand the sta- (Curculionidae)in each was found to be a pre-
minatebuds and commenceactivityonly at sta- dispersal fruitpredator.The beedeswererarely found
minateanthesis.The exclusivelyattractedvisitors on theinflorescences duringanthesisbut werepres-
duringmale phaseswerethe pollen-collecting me- entup to 1 week after.The infestedfruitdropped
liponineand halictidbees (Table 2). In B. gasipaes, ca. 2 weeksafterovipositionand thelarvaemoved
some workersof Partamonacupira were waiting to thegroundforpupatingafterca. 1 moreweek.
sinceearlymorningand recruited abundantworkers The whole metamorphosis lasted for4-5 weeks.
immediatelyafterthe petals spread. During sta- Barinaeof B. gasipaesadditionallyhad a parasite,
minate anthesisalso numerousTrigona rufescens a chalcid wasp, which was even more abundant

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74 Listabarth

TABLE 3. in Bactris:Quantitativeresults.
Breedingexperiments

B. bifida B. monticola B. gasipaes

No. of samples(male flowers) 4 4 7
Insectsraised(foundin x samples) spl (4)
Phyllotrox Phyllotroxspi (4) Phyllotroxsp3 (7)
Epureaspi (3) Epureaspi (3) Epureasp2 (5)
Staphilinidaespi (1) Staphilinidaespi (2)
Drosophilidae (4) Drosophilidae (4) Drosophilidae (7)
Phoridae (1)
emergedafterx days
Phyllotrox (1O)-13-15-(17) 13-15-(16) (11)-12-14-(17)
Epureaemergedafterx days (10)-11-12-(15) 11-12-(13) (11)-12-14-(15)
No. of samples(youngfruits) 5 3 6
Barinaespi (4) Barinaesp2 (6)
Insectsraised(foundin x samples) Chalcididae (5)
Insectsemergedafterx days 27-34-(48) 24-31

thanthebeetleitselfin thesamples(ratioBarinae: DISCUSSION

Chalcididae= 1:0.8/1:1/1:1.3/1:1.5/1:17).
POLLINATION.-Pollination in Bactrishas received
COMMUNITY.-Bactris monticola,B. bifida, Des- repeatedattention(Beach 1984, Bullock 1981, Es-
moncus mitisand D. polyacanthos constitutea palm sig 1971, Listabarth1992, Moraes & Sarmiento
assemblagesharingthe same speciesof Phyllotrox 1992, Mora Urpi 1982, Mora Urpi & Solis 1980),
and Epurea, but also Megalopta,as pollinators. partiallydue to the economicimportanceand ex-
Therefore, all thosepalms are induded in the as- tensivecultivation ofBactrisgasipaes.Thereis good
sessmentofstructure and populationdensityofthis evidencethatin somepalms relatedgeneraor con-
assemblage.Phenologicaldata of Desmoncusare genericspeciesdo not necessarily show the same
takenfromListabarth(1994). pollinationstrategy(Fisher& Moore 1977; Hen-
Twelve plotswereanalysedforoccurrences vs. derson1985; Listabarth1993a, b; Schmid1970a,
non-occurrences and 3 categoriesare distinguished: b). A uniformstrategy,however,is foundin Bactris
category1, forthoseplotsthatdid not containany and the majortrendin pollinationis towardscan-
of thespecies(4 plots= 33%), and category2, for tharophily. Amongthemostcomprehensive studies
thosethatcontainedonly1 species(2 plots= 17%). arethoseofBeach (1984) and Mora Urpi and Solis
Six of the plots (50%) contained2 or 3 of the (1980). Theydescribea protogynous, 24-hourflow-
assemblagespeciesand are subsumedundercate- eringcyde and crepuscular-nocturnalflowering,
gory3 (Table 4). Althoughthe plotswerenot all thermogenesis and strongodor productionduring
same-sized,the categories1-3 are recognizedalso anthesis,and visitationby beetles (Scarabaeidae,
in absolutesizes of the total area (2000 m2), and Nitidulidae,Curculionidae),drosophilidflies,and
the same patternsare also found in numbersof bees. Beach (1984) concludes,thatBactrisgasipaes
clustersand stemsper area. and B. porschianawere pollinatedby the scarab
The populationsof theindividualspeciesshow beetles,thesmallweevilsand nitidulidbeetlesbeing
staggeredfloweringduringthe earlywet season; co-pollinators, while Mora Urpi and Solis (1980)
thus,fromOctoberuntilFebruaryconstantflow- considerweevilsto be most importantpollinators
eringof any of the assemblagespeciesoccurs.Ad- in B. gasipaes.The latterviewis strongly supported
ditionally,B. bifidaand D. mitisshow twiceand by thepresentstudy.
even tripleperiodsof flowering. During the year Constancyand abundance of the curculionid
1989 therewere only shortperiodsin which no and nitidulidbeetlesfound on Bactris,and also
flowering withinthe assemblageoccurred(Fig. 3). recordsfroma numberof otherpalm genera(An-
Conspicuously, thosespecieswhichare foundmost dersonet al. 1988; Barfodet a/. 1987; Henderson
regularlyand abundantlyin theplots,B. bifidaand 1984, 1985, 1986; Kiichmeister et al. 1993; Lis-
D. mitis,show twiceand even tripleflowering pe- .tabarth1992, 1994; Scariotet al. 1991) strongly
riods,whilespeciesthatoccurmostrarely(D. po- emphasizetheirdominantroleforpollination.Lar-
lyacanthos)or whichare pedologicallylimited(B. val utilizationof abscisedflowersstresstheirmost
monticola)have a singleand quite shortflowering directadaptationtowardsthe host plant. Scarabs
period(Table 4, Fig. 3). aremostrarelyfoundon B. bifidaand B. monticola

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 Pollinationat the CommunityLevel 75

FIGURE 1. Scanning electron

micrographs
ofthemetamorphosis
of Phyllotrox:
(a) apod larva,(b) pupa libera,
and(c) imago.Bars:1 mmeach.

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FIGURE 2. Number of Phyllotrox sp1 and Epurea sp 1 raisedper staminateflowers.Data are based on either4
samplesof Bactrisbifida(Bb) and B. monticola(Bm), and 3 samples of Desmoncus polyacanthos (Dp [Listabarth
19941).

and not evenconstantly presentin B. gasipaes,and quite limited.Meliponinebees are only foundon
thus may hardlyplay a major role in pollination. inflorescences at male stage. Megalopta,however,
Also, theimpactof drosophilidfliesforpollination may have impacton pollinationand is partof the
seemsto be of low importance, if at all, sincetheir communityconcept,as the bee is also found on
presenceduringstaminateanthesisis restricted and Desmoncus(Listabarth1994).
thusthe transferof pollen to femaleinflorescences Bactris bifida,B. monticolaand B. gasipaes

TABLE 4. Occurrences
and frequencies specieswithin12 plots.
ofassemblage

Category1 Category2 Category3

Plot Plot Plot Plot Plot Plot Plot Plot Plot Plot Plot Plot
1 2 3 4 5 6 7 8 9 10 11 12
Plot size in m2 200 160 120 120 210 180 180 240 240 160 90 100
Area size per category 600 m2 (=30%) 390 m2 1010 m2 (=50.5%)
(=19.5%)
B. monticola* 4/13 1/2
B. bifida* 2/5 1/2 1/2 3/5 2/5 2/3 1/2 1/2
D. mitis* 2/8 5/25 4/23 1/4 3/17 1/3
D. polyacanthos* 1/4
Assemblage* 2/5 1/2 3/10 8/30 6/28 7/20 5/21 3/9
No. of clustersper
100 m2 0.95 0.56 1.67 3.33 2.50 4.38 5.56 3.00
No. of stemsper
100 m2 2.38 1.11 5.56 12.50 11.67 12.50 23.33 9.00

* Number of clusters/stems
per plot.

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 Pollinationat the CommunityLevel 77

Desmoncus mitis

Desmoncus polyacanthos

Bactris bifida

Bactris monticola

Assemblage -

co co co 0) 0) 0) 0) 0) 0) 0) 0) 0) 0) 0) 0) a
O CO O CO co co co co co co co co co co co 0)
0) 0) 0) 0) 0) 0) 0) 0) 0) 0) 0) 0 0) 0) 0) 0

? z a X
U. <: 5 n co ? z a X

FIGURE 3. Floweringphenology(in 10-day intervals)of the assemblagespecies Bactrismonticola,B. bifida,

and D. mitisduringthe studyperiod (October 1988-January1990).
polyacanthos,
Desmoncus

sharea limitedspectrumofvisitors, whichdoes not The sexualsystemof Bactris,whichis basically

differ in majorcategories withintheindividualspe- monoecious,needs to be explainedin functional
cies (Table 2). Most of thevisitorsare crepuscular- terms.The pronounceddichogamouspalmsdisplay
nocturnal(beetles& the bee Megalopta)and thus a threefoldnon-overlapof sexual phases: thereis
of thesame activity rangeas theirhostplants.The neitheroverlapwithinnorbetweeninflorescences of
odourdrivensystem(Pellmyr& Thien 1986, Schatz the same stem,and hardlyany betweeninflores-
1990), coupledwithprotogyny, thermogenesis and cencesof one cluster.This functionalexplanation
creamycoloured flowersare virtuallytypicalfor maygenerally be appliedto mostextantmonoecious
cantharophily (Gottsberger1977, Irvine& Arm- palms, which have developed heterodichogamy
strong1990, Prance& Arias 1975). Bactris,how- (Cruden& Hermann-Parker 1977, but fortermi-
ever,whichbasicallyshowsthe same characters as nologysee Renner& Feil 1993). A spatial sepa-
a numberofothercantharophilous speciesintropical rationoffunctional genderis thusachievedbytem-
lowland rain forest(reviewedin Schatz 1990), is poral separationof the sexualphaseswithinan in-
among the most sophisticatedbeetle-pollinated florescence and successiveproductionof inflores-
plantswe know. cences(Andersonet al. 1988, Bawa et al. 1985,
A commonquestionabout beetlepollinationis Henderson 1986, Listabarth1993b). Therefore,
the so-calledprimitivism of beetles,comparedto speciesofBactrisaremainlyoutbreeding, and there
advancedgroupsof pollinatorslike bees. The dis- is no need forthe evolutionof self-incompatibility
tinctionofprimitivism, however,is highlyarbitrary mechanisms (Bawa & Beach 1981). However,Mora
and usuallybased on morphologicalnon-special- Urpiand Solis(1980) reportself-sterility as a quan-
izationand/orthesystematic positionof taxa. In a titativecharacterin B. gasipaes,whileClementand
functional contextBactrisis extremely specialized, Arkcoll(1984) provedself-compatibility in some
sincebeetlespollinatethe plantsand reproducein clonesof B. gasipaes.Sexualreproduction maythen
it,whiletheplantmaintains providing occuralso by geitonogamy,
itspollinators viz. inbreedingwithin
larvalfood.Pollenand ovulesaregenerally protected the same plant. Because of the veryfewopportu-
byraphidesand tannins (Uhl & Moore1973, 1977), nities,whenoverlapbetweeninflorescences occurs,
and thus destruction of flowersby the visitorsis occasionalinbreedingwould not limit gene flow
avoided. Male flowersof B. gasipaes contain .2 significantly. Apomicticfruit-set, testedat leastfor
percentprotein,2.8 percentfats and 15 percent Bactrisbifida,did not occur.
carbohydrates (Aguiar& Clements1984), actually In contrast to sexualreproduction, dusteringin
enoughto feedthe larvaeand virtuallyconfirmed Bactriseffects a strongvegetativepropagation which
by the successfulbreedingexperiments. may not onlycompensateforfacultative failingof

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78 Listabarth

but whichhas a drasticimpacton pop-

fruit-set, enon (Beach 1984, Gottsberger& Silberbauer-
ulationstructureby providinga multiplenumber Gottsberger 1991).
is thusan important
ofmates(Table 4). Clustering The beetlelarvaeprobablyare manipulatedby
of Bactrisspecies,
catalystforsexual reproduction the specificodors of the host plant duringtheir
whereit occurs. developmentto preferthe host species over the
others.Providedthatplantsinducethisspecificity
INSECT REPRODUCTION.-Reproduction of pollina- (Simpson& Neff1981, Pellmyr& Thien 1986),
torsis a specialconsideration in pollinationbiology theywillattracta selectsubsetof "flowerconstant"
sincethe mutualisticinterdependencies are intensi- visitorsaccording
to theirlarvalprovenience.
Further
fied(Norstoget al. 1986, Simpson& Neff1981). likelihoodforvisitsto a preferred speciesof host
An excellentexampleis demonstrated forSiparuna plant is hatchingbelow thatplant at a convenient
(Monimiaceae)and gall midges (Feil 1992), and time(late afternoon),when new inflorescences are
in dipterocarps the breedingof pollinators(thrips) produced.Nonetheless,beetlesmayswitchto other
isoffundamental importance (Appanah1993). Most plantswithsimilarodours.
importantbreedersin Bactris are Phyllotrox and
Epurea.The numberof emerginginsects,and the COMMUNITY, A SCENARIO.-Commonpatternsin
timedevelopment takes,differed substantially(Ta- the fewbut exemplarystudieson plant-pollinator
ble 3, Fig. 2), apparently due to the differentcon- communities arestaggeredfloweringwithintheplant
ditions(overallhumidity)insidethe Petri-dishes. assemblagethat provideresourcesfor pollinators
The breedingexperiments give some insightin overtheyear(Ashtonet al. 1988, Heithauset al.
thebiologyof thepollinators.In Bactrisbeetlesdo 1975, Stiles1975, 1978), shortindividualdistances
not competeforovipositionsites on the inflores- betweenthe plants,or distancesbeingeasilyman-
cences,nordo theyexcludeeach other.Competitive aged by thatindividualguild ofpollinators(Haber
interactions seemconfinedto thelarvae,whichfeed & Frankie1989, Heithausetal. 1975, Stiles1978),
on theremainsofstaminateflowers, and thevelocity a similarfloraldisplayoftheassemblagebeingserv-
of developmenthas likelythe main impactforef- iced (Armbruster 1986, Haber & Frankie1989),
fective reproduction. The reproductive cycleofEpu- and a usuallyquite close systematic relationshipof
rea is two days less thanthatof Phyllotrox, which the assemblagespecies (Armbruster1986, Stiles
may explainthe higherratesof emergingnitidulid 1975).
beetles.However,the averagepercentageof total Presentdata providea similarperspectivefor
beetlesper flowersis relativelyconstant.Data of Bactrisand Desmoncus and theirbeetlepollinators.
Desmoncus polyacanthos (Listabarth1994) corrob- Floweringofeachspecieswas typically seasonal(De
orate this evaluationand simultaneously demon- Stevenet al. 1987). Duringrainyseasonthe pop-
strate,that in the absenceof the nitidulidbeetles ulationsfloweredsuccessively with broad overlap.
therateofweevilsis considerably increased.Overall Two of the fourspecieshad a second (and third)
beetle reproduction is highlyefficient, as an esti- floweringperiodduringthe dryseason. The sum-
mated outputof two generations per monthsug- marisedfloweravailabilityof thepalm populations
gests. thus shows only relativelyshortperiods without
Recapitulating thetrendsin insectreproduction flowersduringthe whole year(Fig. 3). Assuming
we findthat the numberof emergingbeetlesper beetlesto have a potentiallife period of several
flowersis relatively constantand everyfifthflower weeks,and providedthatbeetles(or larvae)with-
will produceone beetle,nitidulidbeetlesdevelop standtheseperiodsof non-flowering of any of the
quickerthantheweevils,but weevilsare morecon- assemblagespecies,thereis a continuousmainte-
stantbreedersthantheNitidulidae,and maycom- nanceof the pollinatorsby the palms.
pensate for a constantnumberof beetles in the The individuals,lumped to "assemblage-spe-
absenceof the latter(Fig. 2). cies",showpatchiness evenamongeachother,prob-
Thermogenesis appearsto be an important fac- ablydue to birddispersalof theredor black-violet
tor forthe feedinglarvae,whichhave to develop fruits(Zona & Henderson1989). In plots of cat-
rapidly.Within 2-4 days the flowersdecompose egory3, representing halftheareasize,an extremely
and larvaehave to be readyforpupation.Thus, the highdensityof individualsperarea is found(Table
elevationof temperature mayincreasetheirmetab- 4). In termsofreproductive units(stems),thisden-
olismin the decisivefirsthoursof life.Thermoge- sityis stillincreased.
nesis as a mean of volatilisationof the attracting The individualspeciesthusjointhecommunity
odor is stillanotherexplanationforthatphenom- in providingshortdistancesbetweeneach otherand

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 Pollinationat the CommunityLevel 79

ina permanent flower viz.resource

availability, for to theareaas a cultivate.Itspollinators aredifferent
foodandreproduction ofpollinating beetlesduring fromall otherBactrisspeciesinvestigated and con-
theyear.Floraldisplay andthepollination strategysequentlyalso fromthoseof Desmoncus.The long
oftherelatedgeneraBactrisand Desmoncus (Uhl flowering periodcould have an excellentimpacton
& Dransfield 1987) is indistinguishable in all as- the stability of the communitybut definitely has
pects(Listabarth 1994). not.
Distribution and flowering of the individual In summary, it appearsthatadaptationsof the
species,however, is of coursea function of their beetles to the palms are mainlyfoundabove the
individual lifestrategies. Bactrismonticola forms generic level,due to themeshingoftheirsexuallife
densepopulations withmanyindividuals, and a cydes. Adaptationsof beetlestowardsone species
short,synchronous flowering periodis a guarantee of host plant remainsto be proved,however,it
foroutbreeding. Bactris andDesmoncus
bifida mitis, seems likelythat specificodors serveas chemical
whosepopulations areformed by abundantindi- cues generatingtemporalhostspecifity. The func-
vidualswhichshowmultiple floweringperiods, def- tionalassemblagestudiedis a fragment ofa complex
arethemostindependent
initely specieswithin this community,and no unequivocaldecisionmay be
assemblage andwouldalsodo their own,butequal- drawn,whetherstillotherplantspeciesareinvolved.
lybenefitfrom eachotherandfromthepollinatorsThere are, however,otherplants whichprobably
generatedbyother assemblage members. Finally D. have impacton thiscommunity:stillotherpalms
polyacanthos, a rarespecies,whichflowers in be- (pers. observ.),cyclanths(Gottsberger1991), and
tweentheflowering periodsof the otherspecies Zamia (Norstoget al. 1986).
whilstpollinators are abundantis probably most
dependent on thecommunity, but nevertheless is ACKNOWLEDGMENTS
an important generator ofpollinators.
Doubtful andnon-community members among I amgrateful toC. H. C. Lyal,H. Rainer,D. W. Roubik,
R. Vincentand J.-F.Voisinforidentifications, to E.
BactrisareB. macroacanthos and B. gasipaes: the Adisa-Svoma forassistanceontheSEM,andtoW. Mor-
absenceofflowers in B. macroacanthos duringthe awetzforworking areduetoM.
Specialthanks
facilities.
studyperiodindicates a non-annual flowering pat- Gillman,A. Henderson, and D. W. Roubikfortheir
tern.Bactrismacroacanthos maysupport thecom- critical comments on an earlierdraftofthemanuscript.
I am indepted toM. E. Roithmair forpermanent support
munity, sinceeven rare specieswillhave impact on study.Permission for
duringall phasesof thepresent
themaintenance ofthepollinator populations which fieldwork in PerufromtheMinisterio de Agriculturay
wouldbe increased again,ifwe expectpollination Alimentaci6n, andfinancial supportprovidedbytheFWF
andreproduction ofthesamebeetlespeciesalsoin (P-9664-BIO),theBMfWF(GZ55.442/245-19/88),
and theTheodorKornerFondsaregratefully acknowl-
B. macroacanthos.
edged.
Bactrisgasipaesis a widelydistributed species
intropicalAmerica (Clement 1991)andintroduced

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