REPRODUCTIVE B I O L O G Y O F Bellucia ( M E L A S T O M A T A C E A E ) . (*)
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 t i diipzAizd by biidi, bati, monkzyi, tapiu, t u i t l e i , andanti. Szzdling zitabtÀAh-mznt izqailZA ^atí mnZight, and oczau on a vahizty o£ i o i l typZi. Thz iz.ploduoXi.vz itiatzgy ii int.ZApiZtzd ai tliat o^ a pionzzi ipzcÁiò.
(*) F u n d e d b y g r a n t s f r o m D e u t s c h e r A k a d e m i s c h e r A u s t a u s c h d i e n s t , D e u t s c h e F o r s c h u n g s -g e m e i n s c h a f t , a n d S m i t h s o n i a n I n s t i t u t i o n . (**) B o t a n i s k I n s t i t u t ; A a r h u s U n i v e r s i t e t ; N o r d l a n d s v e j 8 8 ; D K - 8 2 4 0 R i s s k o v ; D E N M A R K , A C T A A M A Z Ô N I C A , 1 6/ 1 7 (n<? ú n i c o ) : 1 9 7 - 2 0 8 . 1 9 8 6 / 8 7 . 1 9 7 I1ÍTR0DUCTI0H A s p a r t o f a n e f f o r t t o u n d e r s t a n d e v o l u t i o n a r y r e I a t i o n s h i p s i n a sitia 1 1 g r o u p o f c l o s e l y r e l a t e d s p e c i e s , t h e r e p r o d u c t i v e b i o l o g y o f B e l l u c i a ( M e l a s t o m a t a c e a e ) w a s I n -v e s t i g a t e d , T h i s n e o t r o p i c a l g e n u s c o m p r l s e s s e -v e n s p e c i e s , f o u r o f w h i c h a r e m e d i u m - s i z e d t r e e s , a n d t h e o t h e r t h r e e s h r u b s . T h e s p e c i e s d i f f e r f r o m e a c h o t h e r i n i n f l o r e s c e n c e p o s i t i o n , p u b e s c e n c e , a n d m o r p h o l o g y o f t h e c a l y x . A l i b u t t w o a r e c o r r m o n , w i d e - r a n g i n g s p e c i e s . T h e o b j e c t o f t h i s s t u d y w a s t o e s t a b l i s h w h e t h e r t h e s e s p e c i e s h a v e d i v e r s i -f i e d i n c r i t i c a i a s p e c t s o -f p h e n o l o g y , p o l l i n a t i o n b i o l o g y , b r e e d i n g s y s t e m , a n d s e e d d i s p e r s a i s t r a t e g y , D l s t r i b u t i o n T h e 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 i n F i g u r e 1 . B e l l u c i a g r o s s u l a r i o i d c s
occurs from southern M e x i c o to Bolivia and M a t o G r o s s o , B r a z i l ; Β . p e n t a m e r a c o v e r s a similar latitudinal span but has a m o r e western distribution and does not reach the G u i a n a s . Bellucia aequiloba o c c u r s at the southwestern periphery of the Amazon b a s i n , in Brazil and northern B o l i v i a ; B . d i c h o t o m a is found in the central and eastern A m a z o n b a s i n , and one shrub s p e c i e s , B. a c u t a t a , is confined to the savannas of Brazilian A m a z o n i a , mainly along the M a d e i r a river. A further two shrub species occur in M a t o G r o s s o and adjacent B o l i v i a , and T e r r . Fed. A m a z o n a s in V e n e z u e l a , respectively ( R e n n e r , in p r e s s ) . Bellucia occurs on several islands in the Caribbean w h e r e it has been intro d u c e d ; it has also been introduced in Africa and A s i a (Stone, 1 9 7 2 ; van S t e e n i s , 1975)· T h r e e species occur at e l e v a t i o n s from sea-level to between 800 and 1600 m e t e r s ; the other four are lowland s p e c i e s .
Flora Neotropica base map no ι
Fig.1. D i s t r i b u t i o n of B e l l u c i a . T w o additional species o c c u r in M a t o G r o s s o and adjacent Bolivia and in T e r r . F e d . A m a z o n a s in V e n e z u e l a , r e s p e c t i v e l y .
T h e four arborescent species grow i η u n d i s t u r b e d and disturbed v e g e t a t i o n , and are tolerant of a range from s a n d y , well drained to waterlogged (at least for part of the year) s o i l s . The shrubs g r o w in savannas which are submitted to regular burning and flooding. L o g g i n g , road-bui1 d i n g , and pasturing h a v e provided excellent habitats for the light-demanding species of B e l l u c i a . B . dichotoma and B . g r o s s u l a r i o i d e s are amongst the most important pioneer species in terms of n u m b e r s of individuals per area in c e n tral A m a z o n i a , (n extra A m a z o n i a n r e g i o n s , B . pentamera is often found invading newly deforested land.
The species' ranges o f t e n o v e r i a p but no m o r e than two species occupy the same S u s a n n e S. R e n n e r
habitat at any o n e locality.
P h e n o l o g y
T h e flowering p e r i o d s 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 w e r e determined by per iodic o b s e r v a t i o n s from October 1980 to November I 9 8 2 and April 1982 to November 1 9 8 4 . In addi t ion , col laborators of the "Minimal c r i 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 . d i c h o t o m a and B. g r o s s u l a r i o i d e s in the same area from 1981 to 1 9 8 4 .
T h e s e three species flowered for lengthy periods o r c o n t i n u o u s l y throughout the y e a r . During the b e g i n n i n g o f the rainy season from about October to January there w a s a high a b undance of new flower buds but some flowering occur red i η a 11 months of the y e a r . Some individual trees of B . d i c h o t o m a flowered c o n t i n u o u s l y for at least five y e a r s ; others paused for several m o n t h s at irregular intervals. F l o w e r i n g w i t h i n the species w a s thus partly a s y n c h r o n o u s . In o t h e r p a r t s o f the range o f B . g r o s s u l a r i o i d e s this spec ies ei ther prefers the ra i ny season (Croat, 1 9 7 8 ; C a v a l c a n t e , 1979) o r shows no clearcut flowering period ( R o o s m a l e n , p e r s . c o m m . ) . A c c o r d i n g to local residents B . pentamera, and B . a e q u i l o b a flower all year round near R i o B r a n c o and C r u z e i r o d o Sul (Acre, B r a z i l ) . T h e fruiting phenology is the same as the flowering p h e n o l o g y .
Near Manaus an a v e r a g e tree or shrub o f B e l l u c i a 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 , o r B. a c u t a t a p u t s out ten to twenty-five fresh flowers p e r d a y .
F l o r a l M o r p h o l o g y a n d Floral C y c l e
All six species have very similar flowers (comp. F i g . 2 A , B ) . T h e flowers have five to eight pure w h i t e (in B e l l u c i a dichotoma) or external 1y ρ ink-flushed petals w h i c h vary slightly in length between the s p e c i e s . T h e tree species h a v e flowers six to eight c e n t i m e t e r s a c r o s s , w h i 1 e the shrub spec i es 1 flowers a r e three to four cent irneters indiame-ter. The buds begin to spl it o p e n in the e v e n i n g a n d by s u n r i s e the petals spread horizontal ly. Upon opening o f the f l o w e r s , the ten to sixteen stamens form a compact ring around the style w h i c h then bends to the lower ( i . e . , closest to the g r o u n d ) side o f the flower and c o m e s to lie between two stamens w i t h the st igma protrud ing from the r ing o f stamens (Fig. 2 A , B ) . T h e stigma is large (about 3~5 m m d i a m . ) and sticky. T h e stamens a r e thick and have the a n t h e r s turned inward w i t h the two m i n u t e apical a n t h e r pores pointed slightly inward, t o o . The stamens a r e w h i t e except for a y e l l o w area externally at the base o f the c o n n e c t i v e . In all s p e c i e s , the petals c h a n g e color from w h i t e to brown on the s e c ond day o f a n t h e s i s . T h e flowers d o not c l o s e during the night and the flower parts are shed on the third d a y .
Fragance is produced by the p e t a l s , the upper part o f the f i I a m e n t s , the c o n n e c t i v e t i s s u e , the upper section o f the s t y l e , and the stigma (determined by neutral red s t a i n i n g ; V o g e l , I 9 6 3 ) . T h e pollen has a m o r e o r less pale y e l l o w color depending o n the species and p o s s e s s e s the same f r a g a n c e . T h e p e r f u m e of Bellucia has been compared to that o f C o n v a l l a r i a m a j a l i s L. (lily of the v a l l e y ; Conva11 a r i a c e a e ) , citronei la (Cymbopogon nardus (L.) R e n d l e ; P o a c e a e ) , or pomarrosa (Eugenia s p . , M y r t a c e a e ) . N o odor is p e r c e p
-table to humans in Bellucia a c u t a t a , but visitor behavior described below suggests that
some scent is produced by this species a l s o . It is noteworthy that o d o r intensity is strongest in second day flowers w h i c h have changed color from w h i t e to b r o w n . N o nectar is produced by Bellucia f l o w e r s .
F i g . 2 . A - Bellucia g r o s s u l a r i o i d e s , p e t a l s 22 mm long; Β - B e l l u c i a d i c h o t o m a to the l e f t , petals 20 mm long, h e l d next to a putative hybrid b e t w e e n B . g r o s s u l a r i oides and B . d i c h o t o m a .
Breeding Systems
Con t ro) 1 ed pol ) / na t ion exper iments w e r e car r i ed out with Bellucia g r o s s u l a r i o i d e s , B . d i c h o t o m a , and B . acutata near M a n a u s , B r a z i l . R e s u l t s are given in T a b l e I.
T a b l e I. Results from p o l l i n a t i o n e x p e r i m e n t s on Bellucia near M a n a u s (1 9 8 O - 8 2 and 1984) .
Be
11
uc i a no. of s e l f - p o l1i nated cross-pol 1 i nated controlspecies p l a n t s 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
g r o s s u l a r i o i d e s 3 12 00 75 5 7 5 23
a c u t a t a 3 19 00 2 5 12 2 5 8
The strong s e l f - ί n c o m p a t i b i1i t y shown agrees with the general finding of Bawa ct al . ( 1 9 8 5 ) o f self-incompatibility in a majority of the hermaphrod ί t ic t rees examined in
neotropical f o r e s t s . The tested species w e r e Íncapable of a g a m o s p e r m y . The wet type o f 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 t a n c o u r t , 1 9 7 7 ) . Art í f i c ί al pol1i nat 1.on between B. g r o s s u l a r i o i d e s and B . dichotoma yielded fruit with few but viable s e e d s . Putative hybrid trees w i t h intermediate morphologicai c h a r a c t e r s w e r e found along roads ides in the vicinity of M a n a u s . They w e r e vigorous but seemed to have low seed set. Their pol len was v i a b l e as judged by a few back-crossing e x p e r i m e n t s with one p a r e n t , whi ch yiel ded fruits with s e e d s . Because of the long t i m e per iod between fert i 1 ί zat ion , fru i t maturi ty, and seed g e r m i n a t i o n , viability of the seeds was not tested in tbis last e x p e r i m e n t , The h y b r i d s
have flowers intermediate between the parents in number of floral parts (Fig. 2 B ) .
Pollination M e c h a n i s m and Pollination
Bellucia g r o s s u l a r i o i d e s , B. d i c h o t o m a , and B . acutata w e r e observed for about 80 hours each at different times of the y e a r from O c t o b e r 1980 to November 1982 and from April to November 1 9 8 4 . For Bellucia a c u t a t a o b s e r v a t i o n s w e r e m a d e near M a n a u s and in the natural savannas at Humaita (upper Madeira r i v e r , A m a z o n a s ) . Bellucia grossularioi des w a s studied near Manaus and in the upper Rio Negro region of Brazil and Venezuela
(in March 1 9 8 5 ) . Bellucia dichotoma was o b s e r v e d at M a n a u s and near Santarém (lower Amazon r i v e r , P a r a ) . Limited o b s e r v a t i o n s w e r e m a d e on Bellucia pentamera near Humaitá and Rio Branco (Acre) and on Bellucia aequiloba near R i o B r a n c o .
Bellucia flowers w e r e v í s ί ted exclusίvely by female bees w h i c h collected pollen as
food for their larvae. 2 7 species belonging to 11 genera w e r e col lected from flowers of
the five B e l l u c i a species (Table 2 ) . Where two Bellucia species occurred at the same locality they were visited by the same species of b e e s .
Nocturnal o b s e r v a t i o n s o f B e l l u c i a g r o s s u l a r i o i d e s and B , dichotoma showed that w a s p s (Apoica pallida) were the only v i s i t o r s . They gleaned pollen grains from petals
T a b l e 2 . Bees collected on flowers of Bellucia a c u t a t a , B . a e q u i l o b a , 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 . p e n t a m e r a . For localities see explanation in text.
OXAEIDAE
Oxaea flavescens (Klug)
ANTHOPHORIDAE C e n t r i s lilacina (Cockrell) C e n t r i s sp. nov. P t i l o t o p u s superbus (Ducke) E p i c h a r i s cónica F. Smith E p i c h a r i s rústica (Olivier) Epicharis a f f i n i s F. Smith
HAL ICTI DAE
A u g o c h l o r o p s i s h e b e s c e n s (F. Smith)
X y l o c o p a frontalis (Olivier) Xylocopa tegulata Friese X y l o c o p a símil is F. Smith
AP I DAE
Eulaema c f . meriana (Olivier) Eulaema nigrita Lepeletier Eulaema mocsaryi (Friese) Euglossa intersecta Latreille Euglossa c f . ignita Smith Bombus spp.
T r i g o n a dallatorreana Friese T r i g o n a recursa F. Smith
T r i g o n a f u W i v e n t r í s fulviventris Guerin-Menevi 1 le T r i g o n a hyalinata branneri Cockerel 1
T r i g o n a (Plebeia) s p .
Melipona fulva Lepeletier M e l i p o n a compress!pes
m a n a o e n s i s Schwarz Melipona rufiventris
and s t a m e n s . Except for b e e s , no other insects w e r e 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 s i z e . 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 m u s c l e s (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 p o r e s . For this to be e f f e c t i v e , a firm grip and close contact between the bee's body and the anthers was e s s e n t i a l . 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 s t a m e n s , often injuring tissue in the p r o c e s s . 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 b e e s ' turning between each buzzing period during a single v i s i t ,
Bellucia pollen g r a i n s are small (ca 10 ]_im) , s m o o t h , and dry. They adhere to the b e e s ' abdomens and to a minor extent to the rest of their b o d i e s . Thus there t s no spec i -ficity of pollen placement. Due tij their m o r p h o l o g y , the bees cannot completely clean t h e m s e l v e s , and persistent pollen residues are usually found in a longitudinal line in the center of the a b d o m e n , w h i c h is the region w h e r e the bee's body,when curved t Í g h t1y over
the a n d r o e c i u m , 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 f r e q u e n c i e s , e.g., ^20 H z , which w a s 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 a n t h e r s . Wind dees not cause pol len to leave the a n t h e r s . Morphological separation o f p o1 1 en and stigma (herkogamy) conipl Ρ te) y precludes automatic selfing in Bellucia flowers; bee νisitations of the fIowers sre o b l i g a t o r y fur fertilization o f the o v u l e s .
Both large and small bees vibrated the stamens in the described m a n n e r ; h o w e v e r , only bees large enough to contact a p a r t i c u l a r B e l l u c i a s p e c i e s ' stigma w e r e legitimate pollinators o f that s p e c i e s . 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 , P t i l o t o p u s , Epichari s, and Eulaema b e e s . A n easily spotted large (3 em long) individual w i t h 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 : 3 0 , 8 : 3 2 , and 8 : 3 7 A . M . on c o n s e c u t i v e d a y s .
Analyses o f the proportional composition of pollen loads of )3 bees of the five
trapjining genera mentioned a b o v e indicated h í gh fide 1ity to Bel 1u c i a on indiνiduaI forag ing f l i g h t s . These visitors carried almost pure loads of B e l l u c i a pollen with a few graTn-5 o f M y r t a c e a e , A p o c y n a c e a e , L o r a n t h a c e a e , and V e r b e n a c e a e w h i c h w e r e probably visited for n e c t a r . A d d i t i o n a l l y , C a s s i a (Fabaceae) p o l l e n , for which the bees forage
In the Same m a n n e r as for Bellucia p o l l e n , i.e., vibrating the poricidal a n t h e r s , was present In two c a s e s ,
Fig. 3. A - Bees captured on B e l l u c i a g r o s s u l a r i o i d e s near M a n a u s ( Β r a x ί 1 ) ; Β - B e l l u c i a grossularioides fruits placed on a leaf; average fruit is 2,5 cm long.
On the a v e r a g e , a Bellucia dichotoma tree w i t h 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 p o l l i 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 s a v a n n a s , individual large bees could be followed with b i n o c u l a r s . V i s i t s to two co-occurring species on the same foraging trip w e r e observed for the pairs Bellucia gros_ sularioides - B. dichotoma and B . pentamera - B. g r o s s u l a r i o i d e s near Manaus a n d n e a r H u ma it! respectively.
T r i g o n a bees w e r e frequently encountered on B e l l u c i a flowers at al I localities, but did not vibrate the stamens in order to obtain the p o l l e n . Instead, they w e r e 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 w e r e somet imes present in great n u m b e r s , 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 T r i g o n a on them, and thus these pollen scavengers may enhance inter-plant m o v e m e n t s of legitimate p o l l i n a t o r s .
Flowers of the previous d a y , distinguishable by their brown c o l o r , w e r e not visited except by an occasional M e l i p o n a or T r i g o n a b e e . It is interesting to recall that second day flowers had a s t r o n g e r scent than fresh f l o w e r s . Bees probabl y used scent in a d d i t i o n to visual clues fo find the fl owers . Th i s became obv i o u s w h e n flowers of Bellucia a c u t a t a , that nad been bagged in the bud stage w i t h insect-proof w h i t e gauze the evening before a n t h e s i s , w e r e approached by bees during the morning they opened even though the flowers were not v i s i b l e .
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 ) . T h e i r slightly m u c i1a g i n o u s pu 1 ρ contains about 3000 small ( 0 . 5 - 1 mm
long) brown s e e d s . 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 w e e k s and the seeds take five to twenty-five w e e k s to g e r m i n a t e . Because of the almost continuous flowering of B e l l u c i a plants fruits are a v a i l a b l e over most or all of the year in any particular area of the g e n u s ' r a n g e .
The berries have a f a i n t , fruity o d o r and s w e e t , slightly astringent t a s t e . They are taken by a w i d e range of a n i m a l s : monkeys (M. R o o s m a l e n , p e r s . c o m m . ) , birds (pers. o b s . ) , and bats (S. M a r q u e z , p e r s . c o m m . ) , and — once they have fallen to the ground — by tapirs (label d a t a ) , turtles (M. R o o s m a l e n , D. M o s k o w i t z , p e r s . c o m m . ) and a n t s ( p e r s . o b s . ) . T h e fruits have been fed to monkeys and hogs and are sometimes eaten by h u m a n s . Birds are not the principal consumers and seed dispersers of Bel 1u c i a ; the f r u i t s ' p o s i t i o n , s i z e , c o l o r , s c e n t , and taste indicate that they a r e most e f f e c t i v e at a t tracting m a m m a l s . The relative importance of the d i f f e r e n t d i sperser c1 asses will be an object of future s t u d i e s .
In repeated e x p e r i m e n t s germination rates o f the seeds w e r e low (ca. 1¾). Bellucia saplings are light-demanding and attain reproductive m a t u r i t y in four y e a r s .
D I S C U S S I O N
Although extended flowering is not uncommon among tropical p l a n t s , c o n t i n u o u s flowering, such as here documented for B . d i c h o t o m a , is r a r e ( J a n z e n , 1 9 & 7 ; Hallê et a l . , I 9 7 8 ) . Other species of Bel lucia al s o flower for extended per iods , and clear-cut flower ing periods are absent in all of them. Bellucia individual s, having reached the reproductive s t a g e , invest a large part of their energy into almost c o n t i n u o u s production of flowers and f r u i t s . S e l f - ί n c o m p a t 1 b i 1 i t y , shown for the three species w h o s e breedίng system w a s tested, is generally regarded as disadvantageous for colonizing species such a s the members of B e l l u c i a ; 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 s t i c k y , large st i gmat i c s u r f a c e may e n h a n c e reception of the amount of pollen needed t o fertilize the numerous ovules and increase chances for pollen from different parents to be received. O b l i g a t e outcrossing in s e l f - i n c o m p a t i b l e tropical tree species often is correlated with a high proportion of b i g , traplining bees among their flower visitors (Frankie e t a l . , 1 9 8 3 ) .
The pollination syndrome found in B e l l u c i a and all lowland m e l a s t o m e s observed so far (Renner, 1984 a , b ) has been described in recent years from a number of other plant species with poricidal anthers (see B r u c h m a n n , 1 9 8 3 , for a r e v i e w ) . The m a j o r Í t y of these plants have stamens w h i c h release pollen only when vibrated by bees. A p p l i e d to Bellucia f l o w e r s , vibrating stamens is an efficient method for the bees to quickly gather large amounts of p o l l e n , 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 o t h e r plant f a m i l i e s , in that the stamens not only p r o v i d e visual and olfactory cl ues but at the same time a landing platform; thus no o r i e n t a t i o n or further walking are necessary o n c e the bee has landed. Pollen release and stigma receptivity a r e simultaneous in these flowers. T h e r e is no indication of partitioning of p o l l i n a t o r resources by the sympatric Bellucia s p e c i e s . One may specu 1 a t e that the conservat i sm i η f lora 1 morphology in Bellucia
is the result of stabilizing s e l e c t i o n , w i t h thei r shared pol 1 inators being the selective a g e n t . T h e lack of divergence in floral morphology and the lack of temporal s e p a r a t i o n of the sympatric s p e c i e s ' flowering p e r i o d s , together with the observed indiscriminate visitor behavior and lack of g e n e t i c interspecific barriers (at least in some sympatric s p e c i e s ) , result in constant h y b r i d i z a t i o n . H o w e v e r , as noted again recently (Carson, I 9 8 5 ) , the g e n e t i c coherence of a (plant) s p e c i e s ' g e n e pool will not be seriously threatened by interspecific h y b r i d i z a t i o n .
Species of Bellucia are characterized by super ior reproduct ive ability and m e a n s of d i s p e r s a l . They are specialized for o c c u p a t i o n of transient habitats in physiological features such as their seedling's light requirements and a b i1i t y to e s t a b l i s h on a v a r i e ty of soil t y p e s , 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 r e p r o d u c t i v e e f f o r t , in this c a s e in the form of a very large number of s e e d s , and a c o r r e s p o n d i n g l y high intrinsic rate of natural increase: r-selected species in the sense of M a c A r t h u r and 206 S u s a n n e S. R e n n e r
W i l s o n ( 1 9 6 7 ) . M o s t species of Bellucia cart be regarded a s tropical w e e d s ; their p o p u -lations g r o w predominantly in sítuations disturbed by m a n a n d with man's help Bellucia bas spread to the Caribbean and the Old World t r o p i c s .
ACKNOWLEDGMENTS
M y t h a n k s a r e d u e to the foi lowing a p i d o i o g i s t s : M . C . A l m e i d a ( T r í g o n a ) , R. Dressier ( E u g l o s s i n i ) , Eickwort ( H a l i c t i d a e ) , 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 . A b s y for use of laboratory fácilities at the Instituto Nacional de Pesquisas da A m a z ô n i a ( I N P A ) i n Manaus (Brazil) and the curators and staff at INPA for their h e l p f u l n e s s a n d kindness during my stay t h e r e .
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 VÍAÍXOÍind-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.
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