Journal of
Ecology 2002
90 , 517 – 528
© 2002 British
Ecological Society
Blackwell Science, Ltd
Ants affect the distribution and performance of seedlings of
Clusia criuva, a primarily bird-dispersed rain forest tree
LUCIANA PASSOS and PAULO S. OLIVEIRA*
Departamento de Botânica, C. P. 6109, Universidade Estadual de Campinas, 13083–970 Campinas SP, Brazil, and
*Departamento de Zoologia, C. P. 6109, Universidade Estadual de Campinas, 13083–970 Campinas SP, Brazil
Summary
1 We studied the dispersal system of the tree Clusia criuva (Clusiaceae) in a tropical rain
forest in south-east Brazil. An observational/experimental approach was adopted to
estimate the probability of transitions between consecutive stages in the recruitment
process (i.e. fruit production and removal by birds, ant–seed interactions on the forest
floor, seed germination, and establishment and early survival of seedlings).
2 Clusia trees produce hundreds of capsules with small lipid-rich arillate seeds. Crop size
ranges from 393 to 3709 capsules per tree. Birds (14 species) eat 83% of the diaspores on
the tree, while the remaining 17% fall to the ground and are removed by ants (16 species).
3 Ants remove 89% of the fallen diaspores and 98% of the seeds found in bird faeces.
Ponerine ants (Odontomachus, Pachycondyla) carry the diaspores to their nests, while
small myrmicines (Pheidole, Crematogaster) remove the aril where found. Aril removal
by ants and removal of seeds from bird defecations increase germination success in
C. criuva.
4 Seedlings are more frequent close to ponerine nests than in control areas without
such nests. Early seedling survival (1 year) in nests of Pachycondyla striata is greater than
in control areas. Soil samples from nests of P. striata also had higher concentrations of
total nitrogen and phosphorus than random soil samples.
5 This is the first study to demonstrate the combined effects of ants on the distribution
and survival of seedlings of a primarily vertebrate-dispersed plant in a tropical forest.
Key-words: ants, birds, Brazil, Clusia, Clusiaceae, seed dispersal, seedling survival,
tropical rain forest
Journal of Ecology (2002) 90, 517– 528
Introduction
Seeds that are dispersed primarily by frugivorous
vertebrates may also be secondarily distributed by
ants (reviewed by Böhning-Gaese et al . 1999). The
ecological consequences of ant activity in such two-
phase dispersal systems are still poorly understood
(but see Kaufmann et al . 1991; Pizo & Oliveira 1998;
Böhning-Gaese et al . 1999), unlike those of myrmeco-
chorous (i.e. ant-dispersed) species with elaiosome-
bearing seeds (e.g. Hanzawa et al . 1988; Hughes &
Westoby 1992a,b; Garrido et al . 2002).
Typical myrmecochorous species occur worldwide
but are especially common in arid Australia and
South Africa, and temperate forests (Beattie & Culver
1981; Milewski & Bond 1982; Beattie 1985). Although
myrmecochory can be an important dispersal strategy
for some plant taxa in neotropical forests (Horvitz &
Beattie 1980; Passos & Ferreira 1996), nearly 90% of
dicots there have fleshy fruits and rely on vertebrate
frugivores for seed dispersal (Frankie et al . 1974). Many
diaspores are found on the forest floor (Jordano 1993),
where they have fallen, been dropped by frugivores
(Howe 1980; Laman 1996) or deposited in vertebrate
faeces (Kaspari 1993; Pizo & Oliveira 1999), and the
abundance of litter-foraging ants (Hölldobler & Wilson
1990) suggests that ant–diaspore interactions may be
common. Indeed, a 2-year survey carried out in the
Atlantic forest of south-east Brazil recorded 886 ant–
diaspore interactions involving 36 ant species and 56
plant species (Pizo & Oliveira 2000). Recent studies in
neotropical areas have shown that ants can rearrange
the seed shadow generated by vertebrate dispersers
(Roberts & Heithaus 1986; Kaspari 1993), affect seed
bank dynamics (Levey & Byrne 1993), facilitate seed
germination (Oliveira et al . 1995; Leal & Oliveira 1998;
Pizo & Oliveira 1998) and promote seedling establishment
Correspondence: Paulo S. Oliveira, Departamento de
Zoologia, Universidade Estadual de Campinas, C. P. 6109,
13083–970 Campinas SP, Brazil (fax 55 19 32893124; e-mail
pso@unicamp.br).