Plusieurs auteurs ont reconnu le rôle des vertébrés comme disperseurs de graines de Cecropia. Nous avons comparé sous des traitements différents (lumière et absence de lumière) les taux de germination de graines de Cecropia hololeuca provenants des fèces de Didelphis aurita à ceux de graines issues de fruits prélevés sur des arbres. En outre, les graines des arbres ont été séparées en trois goupes pour des tests de germination : fruits frais, 15 jours après collecte et 30 jours après collecte. La germination sous lumière a eu plus de succès que sans lumière, pour tous les groupes (fruits frais, 15 jours après collecte et 30 jours après collecte, et fèces). Le taux de germination des graines provenant des fèces ont été plus proches de ceux de 30 jours après collecte que des autres groupes. Ces résultats suggèrent que D. aurita se nourrit au sol de fruits de C. hololeuca. La possibilité que D. aurita disperse les graines dans des zones au-delà des arbres parentaux, jointe au fait que les taux de germination similaires entre graines issues des fèces et graines provenant de fruits récoltés impliquent que D. aurita serait un disperseur potentiel de C. hololeuca

DE VIVEIROS GRELLE, Carlos Eduardo

GARCIA, Queila S.

I-Revues

POTENTIAL DISPERSAL OF CECROPIA HOLOLEUCA BY 
THE COMMON OPOSSUM (DIDELPHIS A URITA )  IN ATLANTIC 
FOREST, SOUTHEASTERN BRAZIL 
Carlos Eduardo de Viveiros GRELLE* and Queila S. GARCIA**
RÉSUMÉ 
Plusieurs auteurs ont reconnu le rôle des vertébrés comme disperseurs de graines de 
Cecropia. Nous avons comparé sous des traitements différents (lumière et absence de 
lumière) les taux de germination de graines de Cecropia hololeuca provenants des fèces de 
Didelphis aurita à ceux de graines issues de fruits prélevés sur des arbres. En outre, les 
graines des arbres ont été séparées en trois goupes pour des tests de germination : fruits frais, 
15 jours après collecte et 30 jours après collecte. La germination sous lumière a eu plus de 
succès que sans lumière, pour tous les groupes (fruits frais, 15  jours après collecte et 30 jours 
après collecte, et fèces). Le taux de germination des graines provenant des fèces ont été plus 
proches de ceux de 30 jours après collecte que des autres groupes. Ces résultats suggèrent que 
D. aurita se nourrit au sol de fruits de C. hololeuca. La possibilité que D. aurita disperse les
graines dans des zones au-delà des arbres parentaux, jointe au fait que les taux de germination 
similaires entre graines issues des fèces et graines provenant de fruits récoltés impliquent que 
D. aurita serait un disperseur potentiel de C. hololeuca.
SUMMARY 
Severa! authors have recognized the role of vertebrates as seed disperser of Cecropia. 
Germination rates of Cecropia hololeuca from scats of Didelphis aurita and from trees were 
tested in different treatments (light and dark). In addition, seeds from trees were separated in 
three groups for germination tests : fresh-fruit, 1 5  days after collection, 30 days after 
collection. Seed germination under light were more successful than in dark for ali groups 
(fresh-fruit, 1 5  days after, 30 da ys after, and from scats). Germination rate of seeds from scats 
were doser to germination rates of the 30 days after collection group than other groups. These 
results insinuate that D. aurita feeds on fruit of C. hololeuca on the ground. The possibility
that D. aurita disperses seeds to areas beyond parent trees, plus the similar germination rates 
of seeds from scats with seeds from fruiting trees imply that D. aurita is a potential disperser 
of C. hololeuca.
* Departamento de Zoologia and Programa de P6s-Graduaçào em Ecologia, Conservaçào e
Manejo de Vida Silvestre. ICB. Universidade Federal de Minas Gerais. CP 486, Belo Horizonte. 
3 1 .270-9 10.  Minas Gerais. Brazil. 
Present adress: Laborat6rio de Vertebrados, Departamento de Ecologia, Universidade Federal do Rio 
de Janeiro. CP 68020 - 2 194 1 -590 - Rio de Janeiro, RJ. Brazil.
** Departamento de Botânica. ICB. Universidade Federal de Minas Gerais .  CP 486, Belo 
Horizonte. 30. 1 6 1 -970. Minas Gerais. Brazil. 
Rev. Ecol. (Terre Vie), vol. 54, 1 999. 
327 
INTRODUCTION 
Seed dispersal by animais can increase reproductive success of plants either 
by removing seeds from high-mortality habitat, by dispersing seeds to adequate 
sites for germination (Fleming & Sosa, 1 994; Howe, 1 993 ;  Julliot, 1 994) and by 
enhancing seed germination. In the Neotropics, studies on lizards and frogs 
(Fialho, 1 990), marsupials (Medellin, 1 994), bats (Fleming & Heithaus,  1 98 1 )  and 
primates (e.g. Julliot, 1994; Passos, 1 997) suggest that dispersal by zoochory 
enhances seed survival and germination. 
The pioneer Cecropia species have a wide distribution in South America 
(Berg, 1 978) and their seeds are animal-dispersed: C. obtusa and C. sciadophylla
are dispersed by birds, marsupials, bats and primates (Charles-Dominique, 1 986); 
C. obtusifolia by marsupials, primates and carnivores (Estrada et al. ,  1 984; 
Medellin, 1 994); C. peltata by marsupials ,  bats, primates and rodents (Fleming & 
Williams, 1 990); and C. concolor by birds (Silva, 1 980). Otherwise, Cecropia
fruits are frequent items in the diet of frugivorous vertebrates (Estrada et al. ,  1 984; 
Fleming & Williams, 1990), and can be considered keystone species (Medellin, 
1994).  However, seed consumption does not necessarily imply seed germination. 
Studies of seed dispersal rarely determine seed viability after dispersal . 
C. hololeuca Miq. (Urticales - Cecropiaceae) occurs in States of Bahia, 
Espîrito Santo, Rio de Janeiro, Minas Gerais and Sao Paulo (Brazil) .  This species 
is an evergreen and light-demanding tree, with height of 6- 1 2  rn and logs with 
20-30 cm of diameter. Each kilogram of seeds counts 900 000 units approximately, 
and the phenology data indicate that C. hololeuca ftourishes in more than a time 
a year, but with larger intensity in the months of October and November (Lorenzi, 
1992). We don't  know any study about frugivory of this species, neither have 
observed any animal species consuming the fruits of C. hololeuca in the nature. 
Moreover, we have observed fruits of C. hololeuca on the ground, being sorne 
whole and other partially eaten. 
The common opossum, Didelphis aurita Wied-Neuwied, 1 826 (Didelphimor­
phia - Didelphidae), is an endemie widely distributed species in the Atlantic forest 
(Cerqueira, 1985). This species occurs in primary and secondary forests (Fonseca 
& Robinson, 1 990), feeding on a large range of food types,  including many fruits 
(Grelle 1 996; Santori et al. ,  1 995), which makes D. aurita a potential disperser. 
Here we report the results of seed germination of C. hololeuca Miq. 
(Urticales - Cecropiaceae) collected from scats of D. aurita, and from fruiting trees 
at the same site. Our objective in this study was to determine potential of D. aurita
as a disperser of C. hololeuca seeds. We compared the viability of seeds of 
C. hololeuca collected from scats of D. aurita with the viability of seeds collected 
from trees.  
STUDY AREA 
Field research was performed in the Parque Estadual do Rio Doce, State of 
Minas Gerais, Brazil ( 1 9° 48'- 19°  29' S, and 42° 3 8'-28' W). The climate of the 
park is tropical humid with mean annual temperature of 22 °C. The vegetation of 
the site is tropical semi-deciduous forest (Stallings, 1 989). Additional details about 
the study site are given in Stallings ( 1989). 
- 328 -
METHODS 
Scats of D. aurita were collected between March and October, 1994. Seeds 
found in faecal samples were washed in tap water, dried, counted and the 
percentage of damaged seeds determined. Seeds were put to germinate in Petri 
dishes with paper filter moistened with distilled water (25° ± 2 °C), and separated 
in two treatments : light or darkness.  Four replicates with 25 seeds each were done 
for the treatments (light and dark) . We collected seeds from 20 fruits of two trees 
as control and put them to germinate in three groups: one group immediately 
(hereafter fresh-fruit), other group fifteen days after (hereafter 1 5d), and another 
group 30 days after (hereafter 30d) . In ail treatments four replicates with 25 seeds 
were used, and the observations were carried out for 30 days. 
Differences between treatments were tested using Kruskal-Wallis test (Sokal 
& Rohlf, 1 9 8 1 ) . This methodology implies sorne assumptions relative to the 
collection of seeds from two trees :  ( 1 )  no phylogenetic effects, (2) no spatial 
effects due to disease, and (3) no temporal effects due the season. 
We used x2 test, with Yates '  correction for continuity (Sokal & Rohlf, 1981 )  
to  compare percentages of  germinated seeds among fresh-fruit, 1 5d, 30d and seeds 
found in scats . This last test was done to examine which experimental group fits 
better with germination of seeds from scats . 
RESULTS AND DISCUSSION 
From March to October 1 994, 968 seeds of C. hololeuca were collected from 
the scats of six individuals of common opossum. Seeds of C. hololeuca made up 
to 53  % of scat weight (Table I) . Indices of damaged seeds were generally low 
(Table I). 
TABLE I 
Number of seeds, percentage of damaged seeds, and percentage of seeds weight for 
sample (pooled by month) of Cecropia hololeuca collected in scats of Didelphis aurita 
from Parque Estadual do Rio Doce, Minas Gerais, Brazil in 1994. 
Mon th Nu rn ber Number of Mean (SD) of % of damaged % of seeds in of scats seeds seeds/scat seeds total scat weight 
March 1 17  17 0 5.0 
July 2 143 7 1 .5 (9 1 .3) 2.6 19. 1  
September 3 501 1 67.0 ( 174.3) 14.0 24.5 
October 2 307 153 .5 (71 .4) 2.3 53.0 
Seed germination under light was more successful than in dark for the 
fresh-fruit group (U = 1 6.0, DF = 3 ,  p = 0.02, Table II), 15d group (U = 1 6.0, 
DF = 3, p = 0.02, Table II), 30d group (U = 16.0, DF = 3,  p = 0.02, Table II) and 
- 329 -
for seeds from scats (U = 1 6.0, DF = 3 ,  p = 0.02, Table II) . However, a subtle 
difference exists among the germination rates submitted to the two treatments 
(light and dark), if we consider the groups of origin of the seeds (fresh-fruit, 1 5d, 
30d and from scats) .  Ali seeds of these groups germinated more under the light, 
however, the tests with seeds 1 5  days and 30 days after crop, and those with seeds 
coming from scats of D. aurita, indicated that these seeds germinated practically 
only under the light (Table Il) . 
TABLE Il 
Number of seeds germinated (mean ± SD) of Cecropia hololeuca collected in scats of 
Didelphis aurita and from fruiting trees in the Parque Estadual do Rio Doce, Minas 
Gerais, Brazil in 1994. 
Fresh-fruit 1 5  days 30 days Scats of D. aurita 
Rep1icates Light Dark Light Dark Light Dark Light Dark 
1 20 06 20 03 10  0 1 2  0 
2 1 8  07 17  02 14  03 Il 1 
3 23 07 1 8  0 1  1 2  02 1 3  1 
4 16 03 22 0 1  08  0 1  1 5  0 
mean ± SD 1 9.3 ± 2.9 5.7 ± 1 .9 19.3 ± 2.2 1 .7 ± 0.9 1 1 .0 ± 2.6 1 .5 ± 1 .3 1 2.7 ± 1 .7 0.5 ± 0.6 
Although there was no difference in germination rate under light treatments 
between seeds from scats and seeds from fruiting trees (X2 with Yates correction, 
p > 0.05 for all groups), germination rates of seeds from scats were closer to 
germination rates of the 30d group than to those of other groups (Table III) . 
TABLE III 
Percentage of seeds germinated of Cecropia hololeuca collected in scats of Didelphis 
aurita and from fruiting trees in the Parque Estadual do Rio Doce, Minas Gerais,
Brazil in 1994. 
Fresh-fruit 15  days 30 days Scats of D. aurita 
Light Dark Light Dark Light Dark Light Dark 
77 23 77 07 44 06 5 1  02 
Although this is a short-tenu study, the presence of seeds of C. hololeuca in 
scats from March to October suggests a constant availability of Cecropia fruits at 
the study site. As in other studies (Estrada et al. , 1 984; Fleming & Williams, 1990; 
Medellin, 1994), seeds of Cecropia represent an abundant food item. Their high 
330 -
rate of consumption by D. auri ta plus the low rate of seed damage suggest that the 
common opossum may be an important disperser of this plant species. 
According to the Janzen-Connel model (revised in Clark & Clark, 1984) 
seeds deposited around parent trees have less opportunity for germination than 
seeds dropped away of the seed-shadow because of density-dependent predation 
and parasitism. Furthermore, Cecropia are known to germinate only under light 
(Alvarez-Buylla & Garcia-Barrios, 1 991 ) .  Therefore, seeds of Cecropia need to 
germinate in gaps, away from parent trees. However, fruits of C. hololeuca are 
heavy, with seeds strongly arrested in the pulp, what hinders the split of the seeds 
soon after the fruit bas dropped (Q. Garcia pers . obs.) .  Our results point out that the 
seeds of C. hololeuca placed to germinate 1 5d after its crop, practically only 
germinate under the light. Thus,  dispersal appears important to seed survival in this 
species .  
Because the quality of the site to be dispersed appears to be important to 
Cecropia seeds, sorne features of disperser can increase the success of seed 
germination. Opossums are habitat genera1ists, scansorial with high mobility 
which make them superior relative to other dispersers of Cecropia (see Medellin, 
1 994 for a recent review) . In fact, D. aurita is nomadic and occurs in a variety of 
habitats (Cerqueira, 1985 ;  Fonseca & Robinson, 1990; Gentile & Cerqueira, 1995 ; 
Grelle, 1 996). These characteristics and its potentiality to remove the seeds for 
sites more suitable for germination, suggest the importance of the didelphids as 
seed-dispersers (e.g. Medellin, 1 994). 
As already noticed (e.g. Figueiredo & Longatti, 1997 ; Lombardi & Motta 
Junior, 1 993), germination rates of seeds from scats are lower than germination 
rates of seeds collected from fruits . However, seeds of the 30d group germinated 
as well as those from scats (Table III) . Then, it is possible that the time between 
the collection of the seeds and the germination experiments can influence the 
germination rates, masking the results of the comparisons among the different 
germination rates .  
Recently, Medellin ( 1 994) discussed the role of D. marsupialis as disperser of 
C. obtusifolia, suggesting that the common opossum search for fruits, even 
climbing fruiting trees. However, the similarity between germination rates of seeds 
from scats and seeds from 30d group insinuates that D. aurita can feed on seeds 
of C. hololeuca on the ground. Two additional informations confirm this interpre­
tation. First, from 52 captures of D. aurita only 2 % were in traps above 5 rn, 
confirming the cursorial habit of common opossum in Parque Estadual do Rio 
Doce (Grelle, 1 996). In addition, experiments with digestibility of fruit, meat and 
shrimp show the high digestive effi.ciency of D. aurita (Santori et al. , 1995), 
indicating that the bulk of food items passed through the gut in 24 hours 
(R. Santori, pers . comm.) .  
In conclusion, the similar germination rates of seeds from scats and 30d seeds 
from fruiting trees, and the possibility of the common opossum disperse seeds to 
favorable habitats away from parent trees, imply that D. aurita is a potential 
disperser of C. hololeuca.
ACKNOWLEDGEMENTS 
G. Fonseca gave support for ali phases of this study. M. Vieira, R. Santori and D. Astua de 
Moraes for comments and criticisms on an earlier version of this paper. D. Astua de Moraes translated 
33 1 
the résumé. ECMVS-UFMG, U.S. Fish & Wildlife Service and IEF-MG gave logistic support. 
J.A. Lombardi helped with identification of Cecropia hololeuca. PADCT-CIAMB, PRPq-UFMG, 
CAPES and CNPq provided funds. 
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Potential dispersal of Cecropia hololeuca by the common opossum (Didelphis aurita) in Atlantic forest, southeastern Brazil

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Potential dispersal of Cecropia hololeuca by the common opossum (Didelphis aurita) in Atlantic forest, southeastern Brazil

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