REPRODUCTIVE BIOLOGY OF Bellucia (MELASTOMATACEAE).

(*)

Susanne S. Renner (**)

9UMMABY

Thz izpioduativz biology oi iivz 0(5 thz izven ipe.tU.ii BdUbxcÁa. lUzI.aitoma.ta-

czaz), a gznui o(( ihmbi and imalt tizzA, invzAtigatzdin Amazônia, Sacczii&ul iiait-

t>zt by Beltiuú/i ie.qiuA.to ^ioial viiitaXion by bzzA. Thz ^IOWZAA aiz pA.oda.zzd continuouity

alZ yeou, and atm viiitzd by a vlidz vaAizty iemaíz bzzi, thz piincÂpaí potii.natou

bzinq Xyloc.opa, Cen-fcfcci, Ptilotopui, EpichafUò, Eutazma, Bambai, and Oxaza. The £toiaZ

attiactjmti aiz colol and thz odoK pioduzzd by lhe, polZzn, itamzm, and p&taÍA; thz

wvxvidii poltífí. Thizz ipecÀZÂ o<$ BzXXucÂa aiz izli-incompatibiz. IndiiciiminatzvLiitoi

bzhaviol and tack o& phznotogicat, mon.phoioqic.al, oi gwztic banizAA tzad to hybiid-

ization bztuizin iympatAiz ipzcÁti o^ SzIZueÂa, and no moiz than taco ipzdzi occupy thz

iamz habitat at any oni localittj. Sc^Iucia pioduczA bzAiizi axtth numzAoui imatt izzdi,

and ti diipzAizd by biidi, bati, monkzyi, tapiu, tuitlei, andanti. Szzdling zitabtÀAh-

mznt izqailZA ^atí mnZight, and oczau on a vahizty o£ ioil typZi. Thz iz.ploduoXi.vz

itiatzgy ii int.ZApiZtzd ai tliat o^ a pionzzi ipzcÁiò.

I1ÍTR0DUCTI0H

As part o f a n effort to understand evolutionary re I a t i o n s h i ps i n a sitia 1 1 g r o u p o f

closely related species, thereproductive biology of Bellucia (Melastomataceae) was In-

vestigated, Thi s n e o t r o p i c a l g e n u s comprl s e s s e v e n s p e c i e s , four o f w h i c h a r e m e d ium-s ized

trees, a n dthe other three shrubs. T h e species differ from each other in i n f l o r e s c e n c e

position, pubescence, and morphology o f the calyx. A l i b u t t w oa r e corrmon, wide-ranging

species. T h eobject o f this study w a s to e s t a b l i s h whether these species have diversi-

fied in c r i t i c a i aspects o f phenology, pollination biology, breeding system, a n d seed

dispersai strategy,

Dlstribution

The d i s t r i b u t i o n o f t h e s e v e n s p e c i e s i s s h o w n in F i g u r e 1. Bellucia grossularioidcs

(*) Funded by grants from Deutscher Akademischer Austauschdienst, Deutsche Forschungs-

gemeinschaft, and Smithsonian Institution.

(**) Botanisk Institut; Aarhus Universitet; Nordlandsvej 8 8 ; DK-8240 Risskov; DENMARK,

ACTA AMAZÔNICA, 1 6 / 1 7 (n<? ú n i c o ) : 1 9 7 - 2 0 8 . 1986/87. 197

occurs from southern Mexico to Bolivia and Mato Grosso, Brazil; Β. pentamera covers

a similar latitudinal span but has a more western distribution and does not reach the

Guianas. Bellucia aequiloba occurs at the southwestern periphery of the Amazon basin,

in Brazil and northern Bolivia; B. dichotoma is found in the central and eastern Amazon

b a s i n , and one shrub species, B. a c u t a t a , is confined to the savannas of Brazilian Ama­

zonia, mainly along the Madeira river. A further two shrub species occur in Mato Grosso

and adjacent Bolivia, and Terr. Fed. Amazonas in Venezuela, respectively (Renner, in

press). Bellucia occurs on several islands in the Caribbean where it has been intro­

duced; it has also been introduced in Africa and Asia (Stone, 1972; van S t e e n i s , 1975)·

Three species occur at elevations from sea-level to between 800 and 1600 m e t e r s ; the other

four are lowland species.

Flora Neotropica base map no ι

Fig.1. Distribution of Bellucia. Two additional species occur in Mato Grosso and adjacent
Bolivia and in T e r r . Fed. Amazonas in Venezuela, respectively.

The four arborescent species grow iηundisturbed and disturbed vegetation, and are

tolerant of a range from sandy, well drained to waterlogged (at least for part of the

year) soils. The shrubs grow in savannas which are submitted to regular burning and

flooding. Logging, road-bui1 ding, and pasturing have provided excellent habitats for the

light-demanding species of Bellucia. B. dichotoma and B . grossularioides are amongst

the most important pioneer species in terms of numbers of individuals per area in cen­

tral Amazonia, (n extra Amazonian regions, B. pentamera is often found invading newly

deforested land.

The species' ranges often overiap but no more than two species occupy the same
Susanne S. Renner
habitat at any one locality.

Phenology

The flowering periods of B . d i c h o t o m a , B . g r o s s u l a r i o i d e s , and B . acutata in the

vicinity of Manaus were determined by per iodic observations from October 1980 to November

I982 and April 1982 to November 1984. In addi t ion , col laborators of the "Minimal cri­

tical size o f e c o s y s t e m s " INPA-WWF project (Lovejoy et a l . , 1984) collected phenological

data for B . dichotoma and B. grossularioides in the same area from 1981 to 1984.

These three species flowered for lengthy periods or continuously throughout the

year. During the beginning of the rainy season from about October to January there was

a high abundance of new flower buds but some flowering occur red i η a 11 months of the year.

Some individual trees of B . dichotoma flowered continuously for at least five y e a r s ;

others paused for several months at irregular intervals. Flowering within the species

was thus partly asynchronous. In other parts of the range of B . grossularioides this

spec ies ei ther prefers the ra i ny season (Croat, 1 9 7 8 ; Cavalcante, 1979) or shows no clearcut

flowering period (Roosmalen, pers. c o m m . ) . According to local residents B . pentamera,

and B . aequiloba flower all year round near Rio Branco and Cruzeiro do Sul (Acre, Bra­

zil). T h e fruiting phenology is the same as the flowering phenology.

Near Manaus an average tree or shrub o f Bellucia d i c h o t o m a , B. g r o s s u l a r i o i d e s , or

B. acutata puts out ten to twenty-five fresh flowers per d a y .

Floral Morphology and Floral Cycle

All six species have very similar flowers (comp. Fig. 2 A , B ) . The flowers have

five to eight pure white (in Bellucia dichotoma) or external 1y ρ ink-flushed petals which

vary slightly in length between the species. The tree species have flowers six to eight
1
centimeters a c r o s s , w h i 1 e the shrub spec i es flowers are three to four cent irneters indiame-

ter. The buds begin to spl it open in the evening and by sunrise the petals spread horizontal ly.

Upon opening of the flowers, the ten to sixteen stamens form a compact ring around the

style which then bends to the lower (i.e., closest to the ground) side of the flower and

comes to lie between two stamens with the st igma protrud ing from the r ing of stamens (Fig.

2 A , B ) . The stigma is large (about 3~5 mm diam.) and sticky. The stamens are thick and

have the anthers turned inward with the two minute apical anther pores pointed slightly

inward, too. The stamens are white except for a yellow area externally at the base of

the connective. In all species, the petals change color from white to brown on the sec­

ond day of anthesis. The flowers do not close during the night and the flower parts are

shed on the third day.

Fragance is produced by the p e t a l s , the upper part of the fiIaments, the connective

tissue, the upper section of the style, and the stigma (determined by neutral red staining;

Vogel, I 9 6 3 ) . The pollen has a more or less pale yellow color depending on the species

and possesses the same fragance. The perfume of Bellucia has been compared to that of

Convallaria majalis L. (lily of the valley; Conva11 ariaceae) , citronei la (Cymbopogon

nardus (L.) Rendle; P o a c e a e ) , or pomarrosa (Eugenia s p . , M y r t a c e a e ) . No odor is percep-

table to humans in Bellucia a c u t a t a , but visitor behavior described below suggests that

Reproductive biology of ... 9?

 some scent is produced by this species a l s o . It is noteworthy that odor intensity is

strongest in second day flowers which have changed color from white to brown. N o nectar

is produced by Bellucia flowers.

Fig. 2. A - Bellucia grossularioides, petals 22 mm long; Β - Bellucia dichotoma to the

left, petals 20 mm long, held next to a putative hybrid between B . grossulari­
oides and B. dichotoma.
 Breeding Systems

Con t ro) 1 ed pol ) / na t ion exper iments were car r i ed out with Bellucia grossularioides,
B . dichotoma, and B . acutata near M a n a u s , Brazil. Results are given in Table I.

Table I. Results from pollination experiments on Bellucia near Manaus(198O-82

and 1984) .

Be 11 uc i a no. of self-pol1i nated cross-pol 1 i nated control

species plants flowers f ru i t flowers f rui t flowers frui t
treated set t reated set t reated set

d ichotoma 4 70 00 76 17 80 00

grossularioides 3 12 00 75 5 75 23
acutata 3 19 00 25 12 25 8

The strong self-ίncompatibi1ity shown agrees with the general finding of Bawa ct

al . ( 1 9 8 5 ) of self-incompatibility in a majority of the hermaphrod ί t ic t rees examined in

neotropical forests. The tested species were Íncapable of agamospermy. The wet type of
stigmatic surface and the binucleate pollen {Tobe & R a v e n , 1983) suggest a gametophytic

determi nat ion of self-i ncompat i biIi ty (Net tancourt, 1 9 7 7 ) . Art í f i c ί al pol1i nat 1.on between
B. grossularioides and B. dichotoma yielded fruit with few but viable seeds. Putative

hybrid trees with intermediate morphologicai characters were found along roads ides in the
vicinity of M a n a u s . They were vigorous but seemed to have low seed set. Their pol len was
viable as judged by a few back-crossing experiments with one p a r e n t , whi ch yiel ded fruits

with seeds. Because of the long t i m e per iod between fert i 1 ί zat ion , fru i t maturi ty, and seed
germination, viability of the seeds was not tested in tbis last experiment, The hybrids

have flowers intermediate between the parents in number of floral parts (Fig. 2 B ) .

Pollination Mechanism and Pollination

Bellucia grossularioides, B. dichotoma, and B. acutata were observed for about 80

hours each at different times of the year from October 1980 to November 1982 and from
April to November 1984. For Bellucia acutata observations were made near Manaus and in
the natural savannas at Humaita (upper Madeira river, A m a z o n a s ) . Bellucia grossularioi

des was studied near Manaus and in the upper Rio Negro region of Brazil and Venezuela
(in March 1985). Bellucia dichotoma was observed at Manaus and near Santarém (lower
Amazon river, P a r a ) . Limited observations were made on Bellucia pentamera near Humaitá
and Rio Branco (Acre) and on Bellucia aequiloba near Rio Branco.

Bellucia flowers were vísί ted exclusίvely by female bees which collected pollen as
food for their larvae. 2 7 species belonging to 11 genera were col lected from flowers of

the five Bellucia species (Table 2 ) . Where two Bellucia species occurred at the same
locality they were visited by the same species of bees.
Nocturnal observations of Bellucia grossularioides and B , dichotoma showed that

wasps (Apoica pallida) were the only visitors. They gleaned pollen grains from petals
Reproductive biology of ... 201
Table 2 . Bees collected on flowers of Bellucia a c u t a t a , B. aequiloba, B.
dichotoma, B. grossularioides, and B . pentamera. For localities
see explanation in text.

OXAEIDAE

Oxaea flavescens (Klug)

ANTHOPHORIDAE

Centris lilacina (Cockrell) Xylocopa frontalis (Olivier)

Centris sp. nov. Xylocopa tegulata Friese

Ptilotopus superbus (Ducke) Xylocopa símil is F. Smith

Epicharis cónica F. Smith

Epicharis rústica (Olivier)

Epicharis affinis F. Smith

HAL ICTI DAE

Augochloropsis hebescens (F. Smith)

AP I DAE

Eulaema c f . meriana (Olivier) Melipona fulva Lepeletier

Eulaema nigrita Lepeletier Melipona compress!pes

Eulaema mocsaryi (Friese) manaoensis Schwarz

Euglossa intersecta Latreille Melipona rufiventris

Euglossa cf. ignita Smith Lepeletier

Bombus spp.

Trigona dallatorreana Friese

Trigona recursa F. Smith

Trigona f u W i v e n t r í s fulviventris Guerin-Menevi 1 le

Trigona hyalinata branneri Cockerel 1

Trigona (Plebeia) sp.

and stamens. Except for bees, no other insects were reguiar visitors of Bel lucia flowers.

All bees alighted directly on the stamens and curved their bod i es o v e r a few or all

of the stamens depending on size. A! i bees except for those of the genus Trigona

employed a specific foraging technique to release pollen from the poricida 1 anthers. They

produced vibrations of their thorax with the indirect flight muscles (wings held closed

over the back) which were transmitted via the insects' legs onto the anthers and caused

a cloud of pollen to shoot out of the anther pores. For this to be effective, a firm

grip and close contact between the bee's body and the anthers was essential. Sees used

their m a n d i b l e s , in addition to the legs, to hold onto the external upper part of the

stamens, often injuring tissue in the process. Flowers that had been visited repeatedly

showed brown necrot i c s ta I ns on the connec t i ves that wou 1 d gradua 1 i y form a r ing a 1 1 around the

androecium; these stains are caused by the smaller bees' turning between each buzzing

period during a single visit,

Bellucia pollen grains are small (ca 10 ]_im) , smooth, and dry. They adhere to the

bees' abdomens and to a minor extent to the rest of their bodies. Thus there t s no spec i -

ficity of pollen placement. Due tij their morphology, the bees cannot completely clean

themselves, and persistent pollen residues are usually found in a longitudinal line in the

center of the abdomen, which is the region where the bee's body,when curved tÍght1y over

the androecium, contacts the large, sticky stiçroas. At the same t ime, the sfctgsna is com­

pletely covered by the bee's abdomen and thus is protected from the flower's own pollen.

Pollen leaves the anthers only when they art νibra ted a t higb frequencies, e.g., ^20 H z ,

which was the frequency of a tuning fork used to qu ι ck 1 y co 1 tec t I arge amount s of pollen

by simply striking it and holding it to the anthers. Wind dees not cause pol len to leave

the anthers. Morphological separation o f p o 1 1 en and stigma (herkogamy) conipl Ρ te) y precludes

automatic selfing in Bellucia flowers; bee νisitations of the fIowers sre obligatory fur

fertilization of the ovules.

Both large and small bees vibrated the stamens in the described manner; however,

only bees large enough to contact a particular B e l l u c i a species' stigma were legitimate

pollinators of that species. The very wide range in size of the bees visiting any one

Bellucia species is illustrated by Figure 3 A.

Traplinlng behavior was exhibited by X y l o c o p a , C e n t r i s , Ptilotopus, Epichari s, and

Eulaema bees. An easily spotted large (3 em long) individual with a bright red thorax

(Centris sp, nov. , the third bee from the left in Lhe topmost row in Fig. 3A) arrived at

the tree under observation at 8 : 2 5 , 9:30, 8:32, and 8 : 3 7 A.M. on consecutive days.

Analyses of the proportional composition of pollen loads of )3 bees of the five

trapjining genera mentioned above indicated h í gh fide 1ity to Bel 1ucia on indiνiduaI forag­

ing flights. These visitors carried almost pure loads of Bellucia pollen with a few

graTn-5 of Myrtaceae, Apocynaceae, Loranthaceae, and Verbenaceae which were probably

visited for nectar. Additionally, Cassia (Fabaceae) pollen, for which the bees forage

In the Same manner as for Bellucia pollen, i.e., vibrating the poricidal a n t h e r s , was

present In two cases,

Fig. 3. A - Bees captured on Bellucia grossularioides near Manaus (Βraxί1); Β - B e l l u c i a
grossularioides fruits placed on a leaf; average fruit is 2,5 cm long.

On the average, a Bellucia dichotoma tree with seventy to twenty-three open flowers

was visit ed b y c i g h t l e g i t i m a t e p o l l i n a t o r s p e r hour during the pertod (8-10 A.M.) ofltiost

intensive bee activity {n = 8 hrs on four consecut i ve days i η Decembe r 1 900). These polli­

nators normally visited all fresh flowers on a tree before flying o n , often to another
individual of Bellucia (as indicated by the pollen load c o m p o s i t i o n ) . Along roadsides
and in savannas, individual large bees could be followed with binoculars. Visits to two
co-occurring species on the same foraging trip were observed for the pairs Bellucia gros_

sularioides - B. dichotoma and B. pentamera - B. grossularioides near Manaus andnearHu

ma it! respectively.

Trigona bees were frequently encountered on Bellucia flowers at al I localities, but

did not vibrate the stamens in order to obtain the pollen. Instead, they were pollen
scavengers and robbers (depending on the s p e c i e s ) , showing a complex behavior described
in detail previously (Renner, 1983). T r i g o n a bees were somet imes present in great numbers,
working on a single flower for several m i n u t e s . The large bees did not alight on flowers

that had individuals of Trigona on them, and thus these pollen scavengers may enhance
inter-plant movements of legitimate pollinators.

Flowers of the previous day, distinguishable by their brown c o l o r , were not visited
except by an occasional Melipona or Trigona bee. It is interesting to recall that second

day flowers had a stronger scent than fresh flowers. Bees probabl y used scent in addition
to visual clues fo find the fl owers . Th i s became obv i ous when flowers of Bellucia acutata,

that nad been bagged in the bud stage with insect-proof white gauze the evening before
anthesis, were approached by bees during the morning they opened even though the flowers
were not visible.

Fruit Dispersal
Bel lucia frui ts are pale green to yel low semi-globose berries about 2 - 3 χ 2 . 5 - 3 - 5 cm

in size (Fig. 3 B ) . Their slightly m u c i 1 a g i n o u s pu 1 ρ contains about 3000 small (0.5-1 mm

long) brown seeds. Hypanthia of fertilized and unfertl1ized flowers persist unchanged

for eight to 25 days before development or abscission o c c u r s . Fruit ripening is com­

pleted in about eight weeks and the seeds take five to twenty-five weeks to germinate.
Because of the almost continuous flowering of Bellucia plants fruits are available over

most or all of the year in any particular area of the g e n u s ' range.

The berries have a faint, fruity odor and sweet, slightly astringent taste. They

are taken by a wide range of animals: monkeys (M. Roosmalen, p e r s . c o m m . ) , birds (pers.

o b s . ) , and bats (S. M a r q u e z , pers. c o m m . ) , and — once they have fallen to the ground —
by tapirs (label d a t a ) , turtles (M. Roosmalen, D. Moskowitz, pers. comm.) and ants(pers.
obs.). The fruits have been fed to monkeys and hogs and are sometimes eaten by humans.
Birds are not the principal consumers and seed dispersers of Bel 1 u c i a ; the fruits'

position, size, color, scent, and taste indicate that they are most effective at a t ­
tracting mammals. The relative importance of the different d i sperser c1 asses will be an
object of future studies.

In repeated experiments germination rates of the seeds were low (ca. 1¾). Bellucia
saplings are light-demanding and attain reproductive maturity in four years.
DISCUSSION

Although extended flowering is not uncommon among tropical p l a n t s , continuous

flowering, such as here documented for B . dichotoma, is r a r e ( J a n z e n , 1 9 & 7 ; Hallê et a l . ,

I978). Other species of Bel lucia al so flower for extended per iods , and clear-cut flower ing

periods are absent in all of them. Bellucia individual s, having reached the reproductive

stage, invest a large part of their energy into almost continuous production of flowers

and fruits. Self-ίncompat1bi1ity, shown for the three species whose breedίng system w a s

tested, is generally regarded as disadvantageous for colonizing species such as the

members of Bellucia; this may be balanced by the very high number of seeds per fruit,

which makes simultaneous germination of several seedlings at a new site likely. Provided

flowers are visited repeatedly, the sticky, large st i gmat i c s u r f a c e may enhance reception

of the amount of pollen needed to fertilize the numerous ovules and increase chances for

pollen from different parents to be received. Obligate outcrossing in self-incompatible

tropical tree species often is correlated with a high proportion of big, traplining bees

among their flower visitors (Frankie et a l . , 1 9 8 3 ) .

The pollination syndrome found in Bellucia and all lowland melastomes observed so

far (Renner, 1984 a, b) has been described in recent years from a number of other plant

species with poricidal anthers (see Bruchmann, 1 9 8 3 , for a review). The majorÍty of these

plants have stamens which release pollen only when vibrated by bees. Applied to Bellucia

flowers, vibrating stamens is an efficient method for the bees to quickly gather large

amounts of pollen, particularly because bees are abi e to start pol 1 en harvesting i mmed i atei y

upon landing. Bellucia is different from many bee-pollinated flowers of other plant

families, in that the stamens not only provide visual and olfactory cl ues but at the same

time a landing platform; thus no orientation or further walking are necessary once the

bee has landed. Pollen release and stigma receptivity are simultaneous in these flowers.

There is no indication of partitioning of pollinator resources by the sympatric

Bellucia species. One may specu 1 ate that the conservat i sm i η f lora 1 morphology in Bellucia

is the result of stabilizing selection, with thei r shared pol 1 inators being the selective

agent. T h e lack of divergence in floral morphology and the lack of temporal separation

of the sympatric species' flowering p e r i o d s , together with the observed indiscriminate

visitor behavior and lack of genetic interspecific barriers (at least in some sympatric

s p e c i e s ) , result in constant hybridization. However, as noted again recently (Carson,

I985), the genetic coherence of a (plant) species' gene pool will not be seriously

threatened by interspecific hybridization.

Species of Bellucia are characterized by super ior reproduct ive ability and means of

dispersal. They are specialized for occupation of transient habitats in physiological

features such as their seedling's light requirements and abi1ity to establish on a varie­

ty of soil types, and in vegetative traits such as the fast growth of the light w o o d .

It appears that species occupying early phases in sucession have a high reproductive

effort, in this case in the form of a very large number of seeds, and a correspondingly

high intrinsic rate of natural increase: r-selected species in the sense of MacArthur and
206 Susanne S. Renner
Wilson (1967). Most species of Bellucia cart be regarded a s tropical w e e d s ; their popu-

lations grow predominantly in sítuations disturbed by man and with man's help Bellucia

bas spread to the Caribbean and the Old World tropics.

ACKNOWLEDGMENTS

M y t h a n k s a r e due to the foi lowing apidoiogists : M . C . Almeida (Trígona) , R. Dressier

(Euglossini), Eickwort (Halictidae), V. Graaf (Oxaeidae) , J . Moure (Meliponini), D. Roubik
(Mel i pon i ni) , R. Snelling (Centr i d i n i) . Further I would 1 i ke to t h a n k D r . M . L . Absy for
use of laboratory fácilities at the Instituto Nacional de Pesquisas da Amazônia(INPA)in
Manaus (Brazil) and the curators and staff at INPA for their helpfulness and kindness
during my stay there.

RESUMO

Voham inveitigadaò, quanto ã biologia n,epn.oduti.va, cinco dai 02X0, eipêciei de Betíu-
cÃA {Melaitomataceae), um geneno de anbu.òtoi e ÕnvoneA de pequeno ponte na Amazônia.
Vaha. ai plantai de QeZlucJjx pn.oduzin.em fautoò, e neceaóJU.o havQA a visita de abethai
ai ^lonei. Ai filoieó òão pn.oduzi.dao o ano todo e ião viAitadaé pon. uma va/Uedade de abe
Úiai fiemininai, tendo 00 p.n.Ã.ncipaÁJ> poliyiÂ.zadon.ei a.6 abelha* dos ge.yien.oi Kytocopa, Cen-
tnXi, Vtilotopui, EpichanXi, Eutaema e Oxaea. Ai, ^tonet, atnxiem peta cone pelo odoh. p/10
duzido peto põlen, peíoi eitama e pelai pétala,},. Ai abethaò ido fiecompemadai com pÕ~
len. Tiêi eipéciei de B&llixcia. ido auto-incompatZveÁA. Vevido CLÒ VÍAÍXOÍ ind-ü>cnimina
dai petoi v-Uitantei, e ã~ ^atta de banAeiAai faenotegica-!,, monjologicai ou genética*, OCOK

ne com Seqüência a hibnidação entAe eipecieò iimpatAÁ.cai. Nunca ^on.am encontAada^i

mai* de duai eipéciei no meimo habitat em cada uma localidade. 0 fitiuto de. BetlucÃa. é
uma baga com pQ.quq.nai e viumeAoiai iejnentei di^pçAiada* pon. paiiÓAOi, moncegoi, macacoi,
aytta,&, jabotii e ^onmigai. Ai plântutai n.equen.em iol pte.no paxaie eit.abalecen.em e c-t&ó
ceAem iobne vaxioi tipa de iolo. Comidenamoi a eòtnategia n.epn.odutiva como iendo a de
ama planta pioneiKa.
References

Bawa, Κ, S.; Perry, D. R.; B e a c h , J. H. - 1985. Reproductive biology of tropical lowland

rain forest trees. I. Sexual systems and incompatibility mechanism. Am. J. Bot,
72: 331-345.

Buchmann, 3. L. - 1983. Buzz pollination in angiosperms. In: J o n e s , C.E. & L i t t l e , R.

J. Handbook of Experimental Pollination Biology. Scientific & Academic P r e s s , New
York. 558 p .

Carson, H. L. - 1985. Unification of speciation theory in plants and animals . Syst. Bot.
1 0 ( 4 ) : 380-390.

Cavalcante, P. Β. - 1979. Frutas Comestíveis da Amazonia. III. Museu G o e l d i , Belem-

PA. (Publ. A v u l s a s , 3 3 ) . 61 p .

Croat, Τ. B. - 1978. Flora of Barro Colorado Island. Stanford University Press,

California. 943 p.

Frankie, G. W.; H a b e r , W. Α.; O p l e r , P. Α.; B a w a , K. S. - 1983. Characteristics and

organization of the large bee pollination system in the Costa Rican dry forest. I n :
J o n e s , C. E. & L i t t l e , R. J. Handbook of Experimental Pollination Biology. Scien­
tific & Academic P r e s s , New Y o r k . 558 p .

H a l l é , F.; Oldeman, R. Α. Α.; Tomlinson, P. B. - 1978. Tropical Trees and Forests - an

Architectural A n a l y s i s . Springer, New Y o r k . 441 p.

Janzen, D. H. - 1967. Synchronization of sexual reproduction of trees within the dry

season in Central America. Evolution, 2 1 : 6 2 0 - 6 3 7 .

Lovejoy, Τ. E . ; Rankin, J.M.; Bierregaard, R.O.; Brown, K.S.Jr.; E m m o n s , L. H.; van der
Voort, Μ. E . - 1984. Ecosystem decay of Amazon forest remnants. I n : Μ. H. Nitecki:
Extinction. Univ. Chicago P r e s s , Chicago & L o n d o n . 354 p.

MacArthur, R. H. & Wilson, E . 0. - 1 9 6 7 . The Theory of Island Βiogeography. Princeton

Univ. P r e s s , Princeton. 203 p.

Nettancourt, D. de - 1977. Incompatibility in A n g i o s p e r m s . Springer. 230 p .

Renner, S. S. - 1983. The widespread occurrence of anther destruction by Trigona bees

in Melastomataceae. Biotropica, 1 5 ( 4 ) : 257-267.

1984. Pollination and breeding systems in some Central Amazonian Melastomataceae.

P r o c . 5th Int'l Symp. Pollination, INRA p u b l . : 175-280.

- 1984. Phaenologie, Bluetenbiologie und Rekombinationssysteme einiger Zentralama

zonischer Melastomataceen. Doctoral d i s s . [Printed c o p y ] , University of Hamburg.

- 1984. Bellucia (Melastomataceae). Mem. N e w York Bot. Garden.

Steenis, C. G. G. J. van - 1975. The introduction in West Malesia of Bellucia axinanthera

(Melastomataceae), an American ornamental and fruit tree. Blumea, 2 2 ( 2 ) : 169.

Stone, B. C. - 1972. Discovery in West Malaysia of Bellucia, a cultivated tree from

South America. Planter, Kuala Lumpur, 4 8 : 276-278.

Tobe, H. & Raven, P. H. - 1983. An embryological analysis of M y r t a l e s : Its definition

and characteristics. A n n . Missouri B o t . Gard., 7 0 : 71-94.

Vogel, S. - 1963. Duftdruesen im Dienste der Bestaeubung. Ueber Bau und Funktion der
Osmophoren. Akad. W i s s . L i t . M a i n z , M a t h . -Nat. K l . , 10: 6 0 1 - 7 6 3 .

(Aceito para publicação em 19.11.1986)

208 Susanne S. Renner