Nous avons étudié le comportement alimentaire et l'effet de la digestion sur les graines d'un arbre néotropical (Miconia cinnamomifolia) par les primates (Alouatta fusca fusca et Callithrix penicillata) dans une forêt du sud-est

        du Brésil. Alouatta fusca consomme en partie des fruits immatures et les taux de germination des graines ingérées sont réduits. Callithrix penicillata est un meilleur disperseur des graines de M. cinnamomifolia. Ces résultats confortent l'hypothèse selon laquelle les petites graines sont

        disséminées par des petits animaux

DE FIGUEIREDO, Rodolfo Antônio

LONGATTI, Claudia Aparecida

I-Revues

ECOLOGICAL ASPECTS OF THE DISPERSAL 
OF A MELASTOMATACEAE 
B Y  MARMOSETS AND HOWLER MONKEYS 
(PRIMATES : PLATYRRHINI) 
IN A SEMIDECIDUOUS FOREST OF SOUTHEASTERN BRAZIL 
Rodolfo Antônio de FIGUEIREDO* & Claudia Aparecida LONGATII**
Forest fragments generally show lower biodiversity than preserved areas, but 
sorne primate species seem to be apt to live in such small remnants (Lovejoy et al. ,  
1 986; Schwarzkopf & Rylands, 1 9 89). Diet and feeding behavior of neotropical
primates have been studied (Guillotin et al. , 1 994; Julliot, 1 994), but their role in 
tropical ecosystems is not completely understood (Heymann, 1 993). In the Old 
World, monkeys consume fruits brightly colored, with succulent pulp and are 
potential dispersers of the seeds (Hladik & Hladik, 1967 ; Gautier-Hion et al.,
1 985). Neotropical primate species are also capable to disseminate severa] plant 
species in the rainforest since seeds pass undamaged through their digestive tracts 
(Hladik & Hladik, 1 969; Chapman, 1 989; Julliot, 1 994).
The faunae surviving in semideciduous forest fragments of southeastem 
Brazil, as well as the ecological relationships between primates and plant species 
in these areas, are poorly known (see Morellato & Leitao-Filho, 1 995). Figueiredo
( 1 993,  1 994) found Howlers as inadequate dispersers of Ficus spp. seeds, and 
sorne studies proposed that small seeded plants are dispersed mainly by small 
monkeys, like Marmosets, while large seeded plants by Howler monkeys (Galetti 
& Pedroni, 1 994; Galetti et al. ,  1 994).
This study verifies the dispersal quality of Howlers and Marmosets on the 
small seeds of a Melastomataceae. 
STUDY AREA 
Fieldwork was conducted in a forest fragment of 30 ha at the Estaçao 
Experimental de Jundiai (Instituto Agronômico de Campinas), southeastem Brazil 
(23 ° 06' S, 46° 55' W, 7 1 5  rn ait.). The area is characterized by a cold and dry 
winter (May to August) and a warm and rainy summer (Novembl(r to February). 
Figure 1 shows the mean temperature and the monthly precipitation during the 
study period in the area. 
* Departamento de Botânica, Instituto de Biologia, C.P. 6 109, Universidade Estadual de
Campinas, 1 3083 .970 Campinas, SP, Brasil. 
** Facu1dade de Ciências, Associaçào << Padre Anchieta » de Ensino, Jundiai, SP, Brasil. 
Rev. Ecol. (Terre Vie), vol. 52, 1 997. 
- 3 -
Temperature 
30 
Precipitation 
380 
300 28 
280 
20 
200 
18 
180 
10 
100 
o+---�--.---.---.--,.--..-��-.---.---.---T O 
J F M A M J J A 8 0 N D 
Mont ha 
-&- Temperature � Precipitation 
Figure 1 .  - Average temperature and precipitation in a semideciduous forest of SE Brazil. 
The vegetation consists of secondary growth semideciduous forest. This type 
of vegetation is typical of southeastem Brazil, and descriptions can be found in 
Morellato ( 1 992) and Morellato & Leitao-Filho ( 1995). The fauna and flora of the
study area are little known, but semideciduous forests generally show high flora 
diversity (Morellato, 1 992). Three monkey species were found living in the forest : 
Alouatta fusca fusca (lhering, 1 9 1 4) (the Northem brown howler monkey), 
Callithrix penicillata (É. Geoffroy, 1 8 1 2) (the Black-tufted-ear marmoset) and 
Callicebus personatus nigrifrons (Spix, 1 823) (the Black-fronted titi monkey) 
(primate names follow Rylands et al. , 1 995). Only the first two monkey species 
were found ingesting seeds of Miconia cinnamomifolia (DC.)  Naud. (Melasto­
mataceae), a common tree in gaps and borders of the area. This plant species 
reaches heights up to 22 rn, with trunks up to 50 cm dbh, and produced thousands 
of purple fruits between April and July 1 995. The fruits have a diameter of 
3.9 ± 0.4 mm, and 33 . 1 ± 8.7 seeds within (N = 1 0).
METHODS 
Primates were observed feeding on ten M. cinnamomifolia individuals. 
Faeces of monkeys species containing melastome seeds were searched along 
established traits in forest edge and towards the interior of the forest (n = 10; a 
total of 2 500 rn). The faeces of Howlers and Marmosets were easy to be 
- 4 -
distinguished from each other because the former monkey species consumes a 
great quantity of leaves in addition to fruits . These surveys, and the germination 
experiments, were done in the last week of July 1995. 
One thousand seeds of Miconia cinnamomifolia were chosen randomly from 
faecal droplets of each monkey species (total 2 000 ingested seeds). As a control, 
it was chosen 1 000 seeds from randomly collected mature fruits undemeath the 
fruiting trees ( 1  000 non-ingested seeds). Germination sets of 1 00 seeds in 10 
replicates were made for each of the three treatments . Half of the replicates of each 
treatment were sown on filter paper in covered Petri plates, kept moistened with 
distilled water and placed in an uncontrolled light and temperature regime inside 
the laboratory. The other half of the replicates was sown on Petri plates filled with 
soil, because differences in germination rates observed in laboratory may not be 
confirmed when seeds experience a more real situation (Figueiredo & Perin, 1995). 
The soil samples were collected near the site of natural occurrence of M. 
cinnamomifolia. These plates were covered to maintain moisture and exclude seed 
predators and placed in a forest gap.  
The number of germinated seeds in each replicate was verified after two 
months, and the differences observed were tested using analysis of variance 
(one-way ANOVA). 
RESULTS 
Howler monkeys were observed feeding on M. cinnamomifolia in two 
occasions. Their feeding bouts lasted ca. 20 minutes. They eat whole mature and 
immature fruits. Eighteen Howlers ' faeces were found in gaps and forest edges. 
Their contents revealed hundreds of M. cinnamomifolia seeds, as weil as pieces of 
mature and immature Miconia fruits, and sorne seeds of Syagrus oleraceae 
(Arecaceae), Myrcianthes pungens (Myrtaceae), and Copaifera langsdoif.fii (Cae­
salpiniaceae ) .  
Marmosets were observed on M. cinnamomifolia on nine occasions. They fed 
only on mature fruits, mashing and swallowing the whole fruit. Twenty-five faecal 
droplets, with M. cinnamomifolia and Ficus sp. seeds, were also found in forest 
edges and gaps. 
The number of Miconia seeds germinated in each treatment are shown in 
Table I (for laboratory trials) and in Table II (for field ones). Laboratory experi­
ments indicated that the germination rates of Marmoset-ingested seeds were 
similar to control ones (F = 2.96, p = 0. 1 3 ). Howler-ingested seeds, however, 
showed a smaller germination rate when compared both with control (F = 1 84.07, 
p < 0.0 1 )  and Marmoset lots (F = 149.33,  p < 0.0 1 ). In the field experiments, 
germination rates were lower than those observed in the laboratory. The results, 
however, were similar : Howler-ingested seeds gerrninated less than control 
(F = 95.34, p < 0.0 1 )  and than Marmoset-ingested seeds (F = 1 38 .03, p < 0.0 1 ), 
and Marmoset-ingested and control seeds did not differ significantly (F = 1 .35, 
p = 0.29). 
DISCUSSION 
Primate ingestion did not inhibit germination of Miconia cinnamomifolia 
seeds. The reduction of germination rates observed for Howler-ingested seeds is 
- 5 
TABLE 1 
Number of vertebrate-ingested and non-ingested Miconia cinnamomifolia 
seeds germinated in laboratory trials. 
Replicates 
Treatment i ± SD 
2 3 4 5 
Control 69 73 74 68 7 1  7 1 .0 ± 2.6 
Howler-ingested 39 43 36 47 42 4 1 .4 ±4.2 
Marmoset-ingested 69 73 80 79 74 75.0±4.5 
TABLE Il 
Number of vertebrate-ingested and non-ingested Miconia cinnamomifolia 
seeds germinated in field germination trials. 
Replicates 
Treatment i ± SD 
2 3 4 5 
Control 46 49 47 36 41 43.8 ± 5.3 
Howler-ingested 10 06 18 15 15 1 2.8  ±4.8 
Marmoset-ingested 39 44 38 4 1  42 40.8 ± 2.4 
probably due to the behaviour of feeding on immature fruits showed by this 
monkey. Howlers, therefore, can be considered a non-specialized disperser of M. 
cinnamomifolia. Almost half of the Howler-ingested seeds germinated, hence 
Howlers can contribute to increase the recruitment of the plant species in gaps and 
forest edges.  Marmosets, contrariwise, are better seed dispersers . Marmoset 
activity, mainly in successional, disturbed and edge habitats (Stevenson & 
Rylands, 1 988), may increase seedling recruitment of M. cinnamomifolia in the 
forest fragment. 
Fragmentation of native forests and hunting can provoke extinction or 
extreme population declines of several primate species (Lovej oy et al., 1 986), and 
this can lead to long-term effects on the recruitment of several plant species 
(Howe, 1984). Sorne studies showed the importance of monkeys on seed dispersal 
and germination of several plant species (lzawa, 1 975  ; Garber, 1 986; Galetti et 
al. ,  1 994; Zang & Wang, 1 995) .  In this study, both primate species may contribute
to regeneration of forest edges and gaps by dispersing the seeds of a pioneer tree. 
The maintenance and regeneration of forest remnants are very important in 
southeastem Brazil, because the Northem howler monkey and the Black-fronted 
titi monkey are on the verge of extinction (Mittermeier, 1 986 ; Fonseca et al., 
1994), and the Black-tufted-ear marmoset is threatened by deforestation of its 
small geographie range (Emmons, 1 990) .  
- 6 
The present study strengthened the hypothesis that smaller monkey species 
are better dispersers of small seeds than larger monkey species like Howlers. 
ACKNOWLEDGEMENTS 
The au thors are indebted to Fernando P. Martins for permission to work in the 
Estaçao Experimental de Jundiaf, and José Luiz Hernandes for discussions. 
Rodolfo A. de Figueiredo acknowledges a doctoral fellowship from CNPq 
(Conselho Nacional de Desenvolvimento Cientifico e Tecnol6gico, process num­
ber 1 40055/94-0). Two anonymous reviewers greatly improved an early version of 
the manuscript. 
SUMMARY 
Feeding behavior and digestion effect on fruits and seeds of a pioneer tree 
(Miconia cinnamomifolia) by primates (Alouatta fusca fusca and Callithrix 
penicillata) were investigated in a forest fragment of southeastem Brazil. Howler 
monkeys consumed mature as weil as immature fruits, and the germination rates 
of ingested seeds were reduced when compared with non-ingested ones. Marmo­
sets defecated unharmed seeds and were considered better seed dispersers than 
Howlers. These results strengthened the hypothesis that plant species with small 
seeds are dispersed mainly by small monkey species . 
RÉSUMÉ 
Nous avons étudié le comportement alimentaire et l'effet de la digestion sur 
les graines d 'un arbre néotropical (Miconia cinnamomifolia) par les primates 
(Alouattafuscafusca et Callithrix penicillata) dans une forêt du sud-est du Brésil. 
Alouattafusca consomme en partie des fruits immatures et les taux de germination 
des graines ingérées sont réduits . Callithrix penicillata est un meilleur disperseur 
des graines de M. cinnamomifolia. Ces résultats confortent l 'hypothèse selon 
laquelle les petites graines sont disséminées par des petits animaux. 
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8 


Ecological aspects of the dispersal of a melastomataceae by marmosets and howler monkeys (Primates : Platyrrhini) in a semideciduous forest of southeastern Brazil

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Ecological aspects of the dispersal of a melastomataceae by marmosets and howler monkeys (Primates : Platyrrhini) in a semideciduous forest of southeastern Brazil

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