Flower food tissues as reward for pollinating birds - Sociedad Argentina de Botánica

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Bol.Soc.Argent.Bot. 37(1-2):71

-

77.2002

FLOWER FOOD TISSUES

AS

REWARD

FOR

POLLINATING

BIRDS

G. G. ROITMAN' 3, A. N.SÉRSIC23,A.A.COCUCCI2andN. H.MONTALDO1

Summary: Nectar is the rewardregularly offered by flowersto their pollinating birds. Studieson

pollination bybirdshave focusedon nectar as areward while alternativereward systems have been

poorlystudied. Previous reviews have shown the presence offood tissuesthat serve as nutritive rewards todifferentclasses of pollinators.However,inarecentrevision of plant-birdinteractions,the existenceofa solid reward for birdshas beendisregarded.InSouthAmerica at leastthreecasesofthis

veryparticular bird-flowerInteraction have been recently studied. In this paper we describe thesyndrome features(flowermorphology, rewardproperties, position of the pollinationunit,flowercolordisplayand

common visitors),that deviate fromthetypicalornithophiloussyndrome,and its possibleorigin is discussed.

Key words:Flower, food reward, pollination,birds,syndrome,review.

Resumen:Tejidosalimenticios floralescomo recompensaparalasaves polinizadoras.El néctares la recompensa típicaquelas floresofrecena las avespolinizadoras.Losestudiossobreornitofiliase han

concentradoen elnéctarcomorecompensa, mientrasque otras retribuciones alternativas fueronesca¬ samenteanalizadas.Revisiones previashan mostrado que laproducciónde tejidos alimenticios puede servircomo recompensapara diferentes polinizadores,yalmenos tres casos deesta particularinteracción se estudiaron últimamenteen América del Sur.Sin embargo,unarevisiónreciente sobreinteracciones planta-ave descarta lapresenciaderecompensassólidas.En este trabajo describimoslascaracterís¬

ticas del síndromequelodiferenciandeltípicosíndromeornitófllo(morfologíafloral,propiedadesde la

recompensa,posiciónde launidad de polinización,color de la exhibiciónfloralyvisitantesmáscomu¬ nes), y también discutimos su posibleorigen.

Palabrasclave:Flor,alimentocomorecompensa, polinización,aves, síndrome,revisión

INTRODUCTION

themostcommonly found tubular, bilabiateor

brush-typearchitecturesarerelatedrespectivelytomodes ofpollen placement ontheback,the front of the head and the ventral bodyparts(Feinsinger, 1991).

Nectaristhe reward(primary attractant) regularly offered by flowerstotheir pollinatingbirds. In bird-flowersitspresenceis announcedexclusively by color (secondaryattractant),which is often vivid andnot infrequently scarlet red. Suchannouncement may

enable the birdstolocate andindividualize particular

typesof floweramongmany others.

Flowerpartshavemechanical functions normally involved either in adaptation tothe structure and behavior of the birdsorin thedeterring of pollina¬

tors other than birds. Such is thecaseofpendant inflorescences (coupledwithcapillary devices to avoid the dripping of nectar), mechanical deterrents (strong corollas), morphologies adjusted toensure

pollen placement on differentparts ofthe bird’s body,etc(Faegri &vanderPijl, 1979).Forexample,

Nectar-feedingbirds

Around the worldnearly twelve families ofbirds

are known as flower visitors (Armstrong, 1979; Stiles, 1981;Westerkamp,1990). Inthe Neotropics, themostnotorious bird pollinatorsareTrochilidae.

(hummingbirds). This family of300species hum¬ mingbirds, is considered the largest andmosthighly specialized group of flower-feeding birds (Stiles, 1981).Passerine pollination has been considereda very commoninteractioninthe OldWorld (Faegri &vanderPijl, 1979), but in the Neotropics the im¬

portanceof birds other than hummingbirdsaspol¬ linators has been stressed onlyrecently.Asanex¬

ample at least 17 species of the Neotropical Erythrina (Fabaceae)showadaptationstopollina¬ tion by perching birds(Bruneau,1997; Steiner, 1979). Incontrast tothe specialization of the hummingbird -flower interactions, those involving New World nectar-feedingpasserinesarerelativelyunspecialized

1

Laboratoriosde Botánica “L.R. Parodi”, Cátedrade Bo¬ tánicaAgrícola.Facultad deAgronomíadelaUniversidad

deBuenos Aires.Av.SanMartín 4453, RA-1417 Buenos

Aires,Argentina.

2

InstitutoMultidisciplinariode Biología Vegetal,Universi¬ dadNacionaldeCórdoba,CONICET,Argentina.

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Bol.Soc.Argent. Bot. 37(1-2) 2002

and similartothe interaction between theOldWorld theintroducedwhite-eye,and alsobyrats.F. perchingbirds and their flowers (Stiles, 1981). The reineckeiis visited by flying foxes(Bats,Pteropidae), “dogma” that NewWorld bird-flowersareexploited the starling Aplonis

_atrifuscus

and the pigeon by hovering birds while OldWorld flowersaregener- Columbavitiensis(Cox, 1984).

allyvisitedby perching birds (van derPijl,1961)has

been recently dismissed (Westerkamp, 1990). The ticular bird-flower interactionhas beenrecently studied. presence of the already mentionedpasserine perch¬

ingbirds that visit flowers in the New World and the isnectarlessthroughout,ismainlypollinated by spe-reportedcasesof hoveringvisitors in the Old World cialized oil-collectingbees (Vogel,1974;Molau,1988;

suggest that neither geographical distributionnor Sérsic, 1994). Thereareabout 50species of thegenus,

systematic affiliationaredirect indication of the kind which lack oil-producing glands (elaiophores).As al-of flower-birdinteractions (Westerkamp.op.cit.).

Studies ofpollination by birds have focusedon present.Inmany casesCalceolariaspeciesmayrely nectaras areward while alternative rewardsystems on autogamy orpollinationby pollen collecting-bees. have hardly been noticed. In thispaper wedescribe Butatleastinonespecies,C.uniflora,aparticular the syndrome features (flower morphology, reward kind of birdpollinationwith food tissuesasreward, properties, position of the pollinationunit,flower has evolved (Sérsic & Cocucci,. 1996) (Fig.

1).

This color display andcommonvisitors),that deviate from species grows within the low vegetation of the thetypicalomithophilous syndrome.

In South Americaatleast threecasesofavery

par-InScrophulariaceae, the genus Calceolaria, which

temativetooil-flowersotherpollination strategiesare

patagoniansteppeandforms perennial cushions of

no morethan 10cmheight. The flowersaremarkedly zygomorphic andtwo-lipped, thesaccatelower lip

showinganotoriouslapfoldedtothe outside of the Plant

_food

tissuesasreward

Simpson&Neff(1981)reviewed thepresenceof flower.This thick andsharplybounded lap is white,

foodtissues thatserve asnutritive rewardstodiffer- andcontrastsoptically against the yellow and redor entclasses ofpollinators.Beetles,batsorbirdscon- brownish redspotted lower lip. This juicy appendage

sumedifferent floralorextra-floralpartswhilepolli- iseatenby the fruit- andseed-eatingbird, Thinocorus

nating species ofNymphdea (Nymphaeaceae), rumitivorus, member of the family Thinocoridae,

Bactris(Arecaceae)orFreycinetia (Pandanaceae). (Sérsic & Cocucci, 1996). This family doesnotinclude These authors confirmedthat foodtissuesarealso flower-birds of any kind, since they don’t show spe-analternative reward that flowers offertobirds. How- cialized morphologicaladaptations andthey forage

ever,whenreviewingplant-bird interactionsProctor for foodonthe ground by walking rapidlyacrossthe etal. (1996), disregarded theimportance of solidre- lowvegetation. Calceolaria fothergillii, endemic of the MalvinasIslands,is the only species in the genus thatshares the striking floral features of C.

uniflora,

Individualcases

_of

birdpollination with

_food

tis- suggesting that it could also be similarly bird

polli-sues asreward

wardstothis kind of pollinators.

nated(Vogel, 1974; Sérsic & Cocucci, 1996).

In Myrtaceaetwo caseshave been described in In the OldWorldsomeobservations have been tworelatedgeneraofsmalltrees(Fig. 2).Acca (Feijoa) reported: Osmoxylon (Araliaceae) fromMalaysiaat- sellowianaproduces flowers with 4 fleshysweet pet-tractsbirds (pigeons) bymeansoffruitimitations, als,andnumerousstamens.Theyarevisitedby pollen whichconsistonsterile flowers placedbetweennor- foraginginsects and bybirds, which feedonpetals.

Thiscaseis known sincelong (Müller, 1886) and has Freycinetia

_funicularis

{Pandanaceae) fromAsia repeatedly appeared in the literature (Popenoe, 1920; provides fleshy,sugarybractssurroundingthe flow- Sick, 1986). (Though,vanderPijl, 1961) dismissed the

,ers. These are eatenparticularly by bulbuls presence ofediblepetals inthis species, Stewart (1986) (Pycnonotidae) whichactaspollinators, (Proctor & and Stewart & Craig(1989) showedthatbirdsare more

Yeo, 1973). Cox (1983) showed

that

thebird-polli- important than insectsaspollinatorsòf Acca under natedF. arbórea from Hawaiiwasoriginallyvisited culture inNewZealand,USAandJapan. A similar

syn-by the endemic, andnow almost extinct birds drome has been hypothesizedby Landrum (1986) and Psittirostrapsittacea, Loxiodes kona and Corvus Nic Lughadha& Proença(1996) andrecently described

tropicus,andinrecentyears byZosteropsjapónica, for Myrrhiniumatropurpureum(Roitmanetal.,1997). malones(Faegri &vander Pijl, 1979).

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i

B

A

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wm

_i

¿¿a

KM

t

i

1

).5cm,

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Fig.l: A-CCalceolaria_uniflora.A:cushionofplantswithintactflowers;B: one flowerwith the food tissuepartiallypecked.

C:cushion of plantswherealmostall flowers show theappendage completelyremoved. D.Thinocorus rumicivorus (female). Theflowers ofMyrrhinium bearalsofleshypetals but reward. Sugar concentration is 14 %inthepetals of thereductionin the number ofstamensandconse- Myrrhinium (Roitmanetal.,1997), 2.14 %inthe

ap-quentlyin theamountofpollen offeredseems afurther pendage ofCalceolaria (Sérsic & Cocucci, 1996) and

steptowardsspecialization, because pollenismoreef- 0.23- % and 1.35%,respectivelyinthe bracts of the ficiently transferred. Fourteenspeciesoffruit-orseed carpellate and staminateinflorescences ofFreycinetia eatingbirds includingMimidae,Tyrannidae,Turdidae, _reineckei_{(Cox, 1983).}_These_{concentration values}are Thraupidae, Emberizidae,Parulidae,and Icteridae _coincident_with_those_{ofgenerally low food-value fruits} have been observed removing the sweetpetals

(Roitmanetal.,1997). _&or nectar_{Denslow, 1985;}offeredby_{Herrera, 1987; Cox, 1983; Dafiii,}bird-pollinatedplants (Moermond 1994).

Syndrome _Position

of

the pollinationunit:In all cases

known flowers are not pendulous for this ornithophilous category. They are exposedin omithophilouspollination differor arecompletely _branches_{and open in}_an_upright_position_allowing

absentinthis special category ofbird pollination

añ

accesstopollinators from differentangles. The

withfoodtissuesasreward. These traits could help two-lipped flowersof Calceolaria

_uniflora

makean torecognize asyndrome by identifyingconver- exception, since flowersareexposedatgroundlevel gences betweenunrelatedtaxa.Followingarethe allowingtheaccessonlyfromonedirection. moresalientconvergenttraits found:

Reward: There’sno nectar.Instead,fleshy and

inS

grouPs

oí

birds.Moreoversomespecies belong sweet partsofafloweror aninflorescence functionas t0familiesapparentlyneverreportedasflower

feed-Some ofthe features already mentionedfor

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eat-Bol. Soc. Argent. Bot. 37 (1-2) 2002

C

A

150 cm 3 cm

D

B

1

G

30 cm

u

i

E

-..«r

_'

•

S

***•

i

1 _{_5cm}

Fig.2:A-B.tecasellowicma.A:Intactflowers. B: flowershowingtwopetals partiallyremoved (arrows). C-E:Myrrhinium

atropurpureum.C:aspectofthetree.D: flowering branch. E: flowers. F:Saltatoraurantiirostris, arrows show theplaceswhere

pollenwereplaced.G:Turdus

_ruflventris

a commonvisitortoboth Acca and Myrrhinium. ingbirds,likeThinocoridae, Turdidae andMirtiidae.

Color: The rewardis self-announcing,unlikenec¬ tar, the presence of which needstoberevealed by coloration of other flowerparts(nectarguides). The foodtissue normally resemblesafruitwithavividand contrasting coloration within the flower. The presence ofacontrastingbicoloreddisplay,like that occurring bothinMyrtaceaeand Calceolaria, enhances avian visits for fruit removalinPrunas serótina and Phytolaccaamericana(Willson & Melampy, 1983).

In Calceolaria

_uniflora

the food tissue maintains itswhite color during the wholeanthesis,simulating ajuicy fruit.Atthe site where theseplantsgrow, a

variety of fleshy omithocorous diaspores arealso

recognizable at groundlevel,suchasthose from Berberís empetrifolia, Empetrum rubrum,Ephedra

frustillata

and Pernettya mucronata.

InMyrrhinium and Acca colorchanges ofthe petals arevery peculiar.Petalsare first dark red (Myrrhinium)orpale pink withadark redcenter (Acca)andturn togray andcompletely whitere¬

spectively (Roitmanetal., 1997). One trait that

usu-2 cm

allyinvolves animal learning isfloralcolor change (Weiss,

1991).

Inmost cases(ca. 220 genera of 74

familiesof flowering plants) insects learntodistin¬ guishand visitpre-change flowers (wherethere¬

ward isavailable),instead of post-change flowers (rewardless)that only increase theplant attractive¬

nesstopollinatorsat adistance(Weiss, 1991). In these Myrtaceae the reward ispresentinthepost¬

change flowers, while pre-change flowers may in-the attractiveness. These features resemble

crease

those present in omithochorous interactions where color signals may be usedtoindicate which fruits

areripe (post-change) and ready for dispersal

(Willson &Melampy,1983). Sincepartoftheperi¬ anth isremoved,the attractivenessoftheflowerdi¬ minishes whenexploited, thusreducing theprob¬

abilityofsuccessivevisits.

Floralconstruction (architecture):

Ornitho-philousflowerswith food tissuesasrewards show the bilabiate and the brush type architectures. Instead, tubularflowers, verywidespreadinthenec¬ taromithophilousones, arenotrepresented.

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natedgroups.

The

family Colletidae (Hymenoptera) is considered the mostprimitive amongbees, and

Cox (1991) suggested that vertebrate pollination Euryglossinaethemostprimitive subfamily among and dioecyareancestralconditionsinPandanaceae, them. Members of this subfamilyarerestrictedto aprimitivegroupofLiliopsidathat may have lacked Australian Myrtaceaeonwhich they principally col-nectaries “abinitio'”,whileanemophilyand entomoph- lect pollen, (Michener,,1965). Australia and South ilyarederivedinthe family.

Althoughpollinationefficiencyand effectiveness by Antarctica,thoughthe effectivenessas afaunal

ofbees and birdsmayvarygreatly4

,

manycasesof bridgewaslimitedinearlyTertiarytoorganismsable omithophilyhave demonstrated that they evolved totolerate cooltemperateclimates (Michener, 1979). frombee-pollinatedgroups,seeGottsberger (1993). Thereare noEuryglossinaeoutofAustraliaand,

co-Myrrhinium, Acca and Calceolariaseemtobe ex- incidentally,theMyrtaceaearepoorly diversifiedelse-amples of this kind of origin.

The geographic distribution of the oilsecreting subtropical regions of Central and South America, Calceolariaspecies and their oil bees overlap. Myrtaceaespeciesaremainly pollinated byApidae,

About 22 % of the total Calceolaria species have Anthophoridae andHalictidae(Proença& Gibbs, 1994; developed no elaiophores, theproportion of Nic Lughadha & Proença, Í996). AccordingtoNic elaiophorelessspecies increasingathigherlatitudes Lughadha& Proença(1996), the presence ofnectarin tothe North and South (Sérsic, 1994). Thereare no theflowersofthe Myrtaceae isbasal,while the nu-collectionsofoilbeesover43° S,althoughtherange merouspollen-flowergeneraoftheMyrtoideaelost ofCalceolariaisbroader. The harsh patagonian cli- theirnectarysecondarily.

mate attheselatitudes,with low temperatures and Origin

Americawere neverindirectcontactbutwerejoined

where,exceptin SouthAmerica. Inthetropical and

extremelystrongwinds,mayhave limited the distri- Concludingremarks bution of the oilcollecting bees,whicharenormally

adaptedtomoremoderate climates.

Theabsenceoftherequired bees and thenatu- israreinthe Angiosperms andappeared

indepen-raltendencyofsomebirdstopractice flower preda- dentlyinonly few species of three families of the

tion5 probablypromoted the origin of this interac- Magnoliopsida andoneoftheLiliopsida. tionbetweenbirds and Calceolaria (Sérsic &

The presence offoodtissuesasreward for birds

Thisparticular pollinationstrategyevidently has Cocucci, 1996). Althoughmembers ofonlyone spe- notevolvedfromtrueomithophilousflowers with cies of birds have been observedvisitingthe flow- nectarasrewardbut probably derived frominsect ersof Calceolaria, the possibility that other birds pollinatedancestors.It isnoteworthy thatmostcases

with similar habits alsopollinatethemisnotdis-

-

mentioned of flowerswith food tissuesasreward for carded. Seed-eatingbirds like the Emberizidaemem- birdsarephilogeneticallyrelatedtonectarlesstaxa.

bers Melanodera melanodera and M. xantho- Freycinetiais included in the familyPandanaceae grammaand Turdus

_falklandii

(Turdidae)arealso withthe anemophilous genus PandanUs and the frequentlypresentintheareaand appearas poten- pollen-rewarding beetlepollinatedSararanga (Cox, 1990). Theclosest relatives of the Myrrhinium-Accd Thebiogeographyand the mainpollinatorsofthe complexhavepollenflowersexploitedbybees (Ñic twoomithophilous Myrtaceae speciesmaygivea Lughadha & Proença, 1996), and finally

,

Calceolaria

possible explanationoftheir evolution frombeepolli-

_uniflora

is includedinamainly oil-rewarding

bee-pollinatedgenus (Sérsic,1994).Onlyfewmorpho¬ logicalchangeswere necessaryinthese flowersor

inflorescencestoproduceprofoundchanges intheir tial pollinators.

4For

example,bumblebeesdeposited 10times more pollen

per visitthan hummingbirds in Delphinium neisonii flowers, butwithin apopulationhummingbird visitation ratesare 10

timeshigher than those of bumble bees Waser&Price (1990). pollination strategies. Althoughthepollinationunits.

5ln

fact,Musisaxicola alpina (Tyrannidae) wasobserved here involvedarewelladapted forvisitationbybirds, eating corollas of theoil-bearing and normally bee- _thereare noevident adaptations of the birdstothe pollinated Calceolaria brunellifolia in Mendoza (Argenti¬

na);also many passerinebird’swereobserved taking nectaras wellas eating the corollas of Anarthrophyllum

desideratum (Papilionaceae) which occurs together with concluded that selection favored theelaborationofa C. uniflora (Sérsic,unpübl.).

plants andthey feed opportunisticallyonfoodtissues

aswellas on avarietyof fruits.Simpson&Neff(1981)

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Bol.Soc. Argent. Bot.37 (1-2)2002

COX, P. A. 1983. Extinction of the Hawaiian avifaunare¬ sulted inachange ofpollinatorsforthe ieie, Freycinetia arbórea. Oikos 41: 195-199.

COX, P. A. 1984. Chiropterophily and ornithophily in Freycinetia (Pandanaceae)inSamoa.Plant Syst. Evol. 144: 277-290.

COX, P. A. 1990. Pollination and the evolution ofbreedingsys¬ temsinPandanaceae. Ann.MissouriBot.Gard. 77: 816-840. COX, P. A. 1991. Abioticpollination:anevolutionaryes¬ capefor animal-pollinatedangiosperms. Phil. Trans. Royal Soc. London. Series B 333:217-224.

DAFNI, A. 1994. Pollinationecology:Apracticalapproach. IRLPress, Oxford.

FAEGRI, K. & L.vander PIJL. 1979. Theprinciples of

pollinationecology. Pergamon Press, Oxford. FEINSINGER, P. 1991. Interaccionesentreplantas y colibríes

enselvastropicales.Bol. Acad.Nac.Ciencias. Cordoba. 59: 29-54.

GOTTSBERGER,G, 1993. Floral ecology: F. Special Top¬ ics. I. Progr. Bot. 54: 461-504.Springer VerlagBerlin,

Heidelberg.

HERRERA,C.M. 1987.Vertebrate-dispersed plantsofthe Iberian Peninsula:astudy of fruits characteristics. Ecol.

Monog. 57:305-331.

JANZEN, D. H. 1980. When is it coevolution?. Evolution 34: 611-612.

JORDANO,P.Í987. Patterns ofmutualisticinteractions

inpollinationand seed dispersal:connectance, depen-dence,asymmetries,and coevolution. Amer. Nat. 129: 657-677.

KRESS, W. J. & D. E. STONE. 1993. Morphology and floral biologyof Phenakospermum(Strelitziaceae),anarbores¬ centherb of the Neotropics. Biotropica 25: 290-300. LANDRUM, L.R. 1986. Monograph 45. Campomenesia,

Pimienta,Blepharacolyx,Legrandia,- Acca,Myrrhinium

and Luma (Myrtaceae). FloraNeotropica,The New York BotanicalGarden,New York.

MICHENER, C. D. 1965. A classification of the bees of the Australianand South Pacific regions. Bull. Am. Nat. Hist. 130:1-362.

MICHENER,C.D.- 1979. Biogeography of bees: Ann. Mis¬ souriBot. Gard. 66:277-347.

MOERMOND T. C. & J. S.DENSLOW.1985.Neotropical

avian frugivores:patternsof behavior, morphology and

nutrition,withconsequences for fruit selection. In: P. A. BUCKLEY, M. S. FOSTER, E. S. MORTON, R. S. RIDGELY &F. G. BUCKLEY (eds.). Neotropical Orni¬

thology:pp. 865-897. Ornithological Monographs 36. American Ornithologists’Union, Washington.-MOLAU, U. 1988. Scrophulariaceae. Part i. Calceolarieae.

Bòt.Gard. Bronx, New York.

MÜLLER, F. 1886. Feijoa, einBaumder Võgelm Seiner Blumenblãtter ais Lockspeise bietet. Kosmos 1: 93-98.

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pollinatorcommunitynotusedby other plantsor to achievegreaterpollinatorconstancy.Thesechanges usuallypromoteaone-to-onerelationship and /ora moreexpensivereward. However, in both Acca and Myrrhinium, their relationshiptobirdsis still diffuse, sincemanybirdspecies visitthem,andthereward qual¬ ityhasnotbeen increased,incomparisonto thatof nectarorfruits. Nevertheless, the production of “fruit-like”petals enables these plantsto attracta newkind of pollinators (birds) different from thoseprevalentinmost

Myrtaceae and Calceolaria (bees). The Acca and Myrrhinium plant-bird interactionseems tobean unspecializedoneanditwould be theoutcomeof dif¬ fusecoevolution (Janzen, 1980, Jordano, 1987). These characteristicscontrast with the highly coevolved oligotropic omithophilous systemsfrequently found

inthe Neotropics, butaresimilartothepaleotropical

allotropicFreycinetia reineckie. The latter ispollinated

by bats and birds in Samoa in which the rewardare

fleshy bracts,(Cox,1990).

The origin and explosive diversification of flower¬ ingplants during Cretaceous is often attributedtoa

simultaneous evolutionary radiation of insects, which servedascriticalpollenvectors.Vertebratesarethought tohaveplayedaninsubstantial role in early evolution of angiosperms because the maingroups,whichare

importantpollinatorsofextantplantstaxa(birds and bats), originatednoearlier thanthe Eocene, (Kress & Stone, 1993).Insectpollinationwasprobably thepre¬ cursorof hummingbird pollination,notonlybecause insectswerefirston scenebut also becauseintermedi¬ ateprocessesarevisible nowadays (Stiles, 1981).

ACKNOWLEDGMENTS

We aregratefultoD. Medan and J. J. Valla forcon¬

structivecriticismto anearlierdraft. To L. Galetto for

comments onthemanuscript. Partial financialsupport wasprovided by the National Research Council (CONICET)towhichANSand AACaremembers.

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Recibido el 07 de Noviembre de 2001,aceptadoel 06 de Mayo de 2002.