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THERELATIVECONTRIBUTIONOFBIRDSANDANTSTOSEEDDISPERSALIN
DIPLOCHOROUSPLANTS:ATESTINTHEBRAZILIANCERRADO
Alexander V. Christianini
1
Paulo S. Oliveira
2
1 – Universidade Federal de S~ao Carlos, Campus Sorocaba, Rod. Jo~ao Lemes dos Santos km 110, Bairro Itinga, 18052 – 780,
Sorocaba, SP, Brazil. Phone number: 55 15 3229 – 5968-avchristianini@yahoo.com.br
2 – Universidade Estadual de Campinas, Instituto de Biologia, Departamento de Biologia Animal, Caixa Postal 6109, 13083 –
970, Campinas, SP, Brazil
INTRODUCTION
Since most plants are dependent on seeds for regeneration,
seed dispersal is one of the main processes in uencing plant
population ecology because the location where seeds land
produces a template for the process occurring latter in the
life cycle of a plant, including the spatial patterns of seedling
distribution and plant recruitment (Wang & Smith 2002).
Since most plants rely on animals for seed dispersal, an eval-
uation of how frugivores in uence this process may enhance
our understanding of plant recruitment and population dy-
namics.
The fruit crop size hypothesis states that plants producing
large fruit crops have a higher chance to attract frugivores
increasing their seed dispersal success compared to plants
with smaller fruit crops (Christianini & Oliveira
in press
,
and references therein). However, large fruit crops may
also increased the waste of fruits that are dropped under
the plant crown by bad seed dispersers, or that fall natu-
rally if not removed from plant canopy by frugivores. Plant
recruitment is unlikely in the vicinity of the parent plant
due to density – dependent mortality factors (see Harms
et al.,
2000). Thus, a non – standard vector of disper-
sal may markedly increase plant tness if it \rescues” such
wasted seeds away from beneath the parent plant. Never-
theless, such strategies of seed dispersal and their conse-
quences have been largely neglected. The remarkable abun-
dance of ants in soil makes them the most likely animals to
interact with those fallen seeds, and maybe provide to the
seeds another chance of successful dispersal and establish-
ment. In this study we compared the e ectiveness of seed
dispersal by vectors acting in the plant crown (birds) and
on the ground (ants) for the regeneration of the tree
Xylopia
aromatica
(Lam.) Mart. (Annonaceae) in the Brazilian sa-
vanna known as \cerrado”.
OBJECTIVES
We addressed the following questions: (i) Does the crop –
size hypothesis account for among – plant variation in the
quantity of fruit removed by birds away from plant crown?
(ii) What is the spatial scale of seed delivery by bird and
ant seed dispersal? (iii) What is the contribution of each
dispersal vector for plant regeneration?
MATERIALANDMETHODS
Seed production and seed fate
Field work was carried out from February 2004 to March
2006 in the reserve of the Estac~ao Experimental de Itirap-
ina (22
o
12’S, 47
o
51’W), a 200 ha fragment of cerrado in
Southeast Brazil. Trees of
Xylopia aromatica
(hereafter re-
ferred to by genus only) reach a density of 300 ind./ha in
the study site. Fruiting season is concentrated from March
to July, when multiple fruits (divided in follicles) open to
expose ca. 60 arillate seeds per fruit. Each seed is coated
by an aril that covers a quarter of the seed, forming the
diaspore (i.e. the unit of dispersal). Each diaspore is a
small, 0.6 cm arillate seed that weights 0.06 g fresh mass
(n = 30). Frugivorous birds are attracted by the contrast-
ing display of the bluish diaspores against the reddish inner
portion of the opened follicle. Plant reproduction is totally
dependent on seeds, which remain viable for up to 2 months
after dispersal.
To examine diaspore production and fate we placed 3 –
10 fruit traps under the crown of nine trees of
Xylopia
isolated from other reproductive conspeci cs. Traps con-
sisted of 0.14 m
2
plastic trays lined with 0.2 – mm ny-
lon mesh kept 20 cm above ground by four stakes, each
coated by a sticky resin (Tanglefoot
ยฎ
) to constrain ant
access to the fallen diaspores. Traps collected fallen folli-
cles, as well as diaspores dropped by birds. We checked
out the traps regularly throughout the fruiting season. Di-
Anais do III Congresso Latino Americano de Ecologia, 10 a 13 de Setembro de 2009, S~ao Lourenco – MG 1
aspores were then counted and classi ed as: (1) ripe, (2)
unripe or aborted seeds, (3) preyed on before dispersal, or
(4) diaspores dropped by primary dispersers (seeds regurgi-
tated/dropped by birds, or embedded in faeces). By the end
of the fruiting season (when all follicles fall to the ground),
we estimated crop size by counting the number of follicles
that reached fruit traps under trees. Unless diaspores are
removed by birds, they do not detach naturally from folli-
cles. Once removed, each diaspore leaves a scar in the inner
wall of the follicle. Thus the follicles on the ground allowed
us to estimate the number of diaspores produced and the
amount removed by birds. We estimated the number of di-
aspores removed by birds from the plant crown of each tree
by subtracting the sum of categories 1 to 4 sampled in traps
by the estimated crop size. To investigate the relationship
between crop size and diaspore removal or waste we applied
linear regressions.
Seed removal from plant canopy and ant attendance to
fallen fruits
Information about diaspore removal by birds, diaspore
waste (i.e. dropped under the parent plant) and bird behav-
ior were obtained by focal observations of 16 fruiting trees,
totaling 110 tree/observation hours. Distances of seed dis-
persal by birds were estimated by records of post feeding
ight distances of birds departing from focal trees until the
rst landing perch.
To determine which ants interact with fallen diaspores of
Xylopia
, we recorded all ant – diaspore interactions observed
on diaspores placed by us at 30 ground stations (10 m apart
from each other), 1 – 2 m o two transects that crossed
the study site. Diaspores were set at 08:00 and 18:00 h
and checked through regular intervals during the fruiting
seasons. We recorded the ant species attracted, and their
behavior toward diaspores. We followed ants carrying di-
aspores until they entered their nests. The distance of dis-
placement was then measured. Ant voucher specimens are
deposited in the collection of the Universidade Federal Ru-
ral do Rio de Janeiro (CECL).
To evaluate the fate of diaspores we measured diaspore re-
moval rates beneath the crown of 30 focal trees over two
fruiting seasons (2004 and 2005). The relative contribution
of ants and vertebrates to diaspore removal was assessed
by means of an exclosure experiment. Vertebrates were ex-
cluded from diaspores by a wire cage (17 x 17 x 8 cm), fenced
on the top and sides with mesh (1.5 cm) and staked to the
ground. Diaspores used in the exclosure experiments were
marked with a small dot of enamel paint (Testors, Rockford,
USA) to distinguish them from other fallen diaspores. Pairs
of diaspores (arillate seeds) of
Xylopia
were set out at about
08:00 h at ve stations placed beneath fruiting trees. Each
pair consisted of a diaspore placed on the oor under a wire
cage, and an exposed diaspore (control) placed outside the
cage, 15 cm away. After 24 h we recorded the number of
diaspores missing. To evaluate if removal rates on the oor
were driven by seed predators we performed removal trials
using cleaned seeds (i.e. aril manually removed from dias-
pores by us) a few weeks later. Data on seed removal (square
root transformed) were analyzed using factorial analysis of
variance.
Seedling distribution and performance
To evaluate if ants may a ect the fate and spatial distri-
bution of seedlings we compared the number of seedlings of
Xylopia
growing on plots (0.5 x 0.5 m) established in ant
nests and in paired controls established at 2 m in a random
direction. Seedlings of
Xylopia
inside nest and control plots
were individually marked with numbered ags and moni-
tored for survival during one year.
RESULTSANDDISCUSSION
We observed 8 species of birds feeding on diaspores of
Xy-
lopia
. Several birds acted as legitimate dispersers by in-
gesting the whole diaspore, and afterwards defecating or
regurgitating intact seeds (e.g.
Elaenia avogaster
). Nev-
ertheless many diaspores were dropped beneath the parent
plant by birds that act as aril consumers, and provide no
dispersal away from parent plants (e.g.
Nemosia pileata
).
We observed that birds dropped 28% of the diaspores they
manipulated in the canopy, and many of which fell with the
aril still attached.
The fruit crop size hypothesis was rejected for
Xylopia
.
We found no relationship between fruit crop size and di-
aspore removal by birds beyond the plant canopy border
(p=0.18), neither between seed production and the propor-
tion of crop removed away (p=0.90). However, absolute
dispersal failure (the number of diaspores that fall under
parent plants) increased linearly with crop size (slope=0.95,
R
2
=0.88, p=0.001). The relative dispersal failure (the pro-
portion of the diaspore crop that falls beneath parents) was
independent of crop size for Xylopia. Thus, a higher num-
ber of mature diaspores reached the ground beneath rather
than away from parent trees as crop size increased in
Xy-
lopia
. Indeed, a great proportion of plant crops usually
fall under parent plants, irrespective of dispersal mode (e.g.
Clark
et al.,
2005).
A high proportion of the seed crop of
Xylopia
was wasted
under parent trees as ripe diaspores or as diaspores dropped
by birds, comprising together 26% and 43% of the total seed
crop in 2004 and 2005 fruiting seasons, respectively. More
than a third of the seed crop was usually lost as immature
seeds. Pre – dispersal seed predation accounted for the loss
of 6% of plant crops. Birds removed up to 56% of seed
crop from the plants. Thus many viable seeds were avail-
able under parent trees at each fruiting season. Ants may
compensate such waste by removing away the majority of
Xylopia
diaspores found under parent plants within 24 hs.
A rich ant fauna (30 species in 15 genera) was attracted
to fallen diaspores. Small myrmicine ants like
Pheidole
spp. and
Wasmannia auropunctata
accounted for most
records at diaspores (70%), whereas large ponerines (
Pachy-
condyla
,
Odontomachus
and
Dinoponera
) comprised 10%
of the interactions seen. Most fallen diaspores of
Xylopia
were removed within 24 hs (82%). The exclusion treat-
ment had no e ect on removal over two fruiting seasons
(ant removal=4.1
1.3 diaspores; vertebrate removal=4.4
1.1 diaspores; p=0.23), indicating that ants are the main
source of diaspore removal on the ground. Aril covered seeds
were much more removed than cleaned seeds (p
<
0.001).
Plant location (block e ect) in uenced diaspore removal (p
<
0.001), but there was no e ect of fruiting season (2004 –
Anais do III Congresso Latino Americano de Ecologia, 10 a 13 de Setembro de 2009, S~ao Lourenco – MG 2
2005) (p=0.86). Based on these data we suggest that ants
can be quantitatively as important as birds for seed disper-
sal in
Xylopia
. For instance, take the 2004 fruiting season.
If removal rates by ants of diaspores fallen under parents
(mean of 4.1 diaspores/exclusion treatment, or 83%) are
balanced against the amount of mature diaspores that fall
under parents (mean of 26% of total plant crop size), it is
possible to realize that ants may a ect the fate of 22% of
total plant crop. For comparison, birds a ected the fate of
32% of total plant crop of
Xylopia
in the same year. Using
the same approach for the 2005 fruiting season, we nd that
ants switched the main role of seed dispersal with birds, in-
uencing the fate of 34% of total crop size against 15% of
birds. Thus, the trend found for
Xylopia
suggests that, at
least for some years and/or trees, ants can have a relevant
contribution to the quantitative component of disperser ef-
fectiveness as birds. Ants may have a relevant role as seed
rescuers in other plant – frugivore systems as well, especially
for plants producing small – and lipid – rich eshy diaspores
that are frequently harvested by ants (Passos & Oliveira
2002, Christianini
et al.,
2007).
The rst landing perch of birds after consumption of
Xy-
lopia
diaspores was 16
12 m (N=16). Ants, on the other
hand, displaced fallen diaspores to much shorter distances
(0.8
0.9 m, N=40, mean
SD). The dispersal kernel
of
Xylopia
suggests that the action of two vectors of dis-
persal may increase the chance of seed transport farther
away from the parent plant, and also produce a larger vari-
ance in seed rain across distances compared to plants that
rely only on birds as seed dispersers. Because birds fre-
quently carry seeds to distances over 40 m they are more
e ective in removing seeds from the predation – prone zone
near the parent tree and in delivering seeds to new sites
for plant colonization and recruitment, with possible con-
sequences for plant metapopulation dynamics (Jordano
et
al.,
2007). On the other hand, seed rescuing by ants de-
crease seed density beneath parent plants and bring seeds
close to ant nests. This would produce a distribution of re-
cruits likely to match the spatial distribution of adult plants
due to relatively short distances of seed dispersal by ants.
Thus birds and ants switch roles as a function of spatial
scale and provide complementary seed dispersal to
Xylopia
and possibly to other eshy – fruited trees in the cerrado.
Seedlings of
Xylopia
were found in small numbers, but only
close to the refuse piles of ant nests. Sampled ant nests (N =
81) had a mean of 0.1
0.3 (range 0 – 2) seedlings against
zero seedlings recorded in paired control plots (Wilcoxon
paired – sample sign rank tests: Z=2.2; p=0.028). Seedling
survival after one year was nearly 60%. The fact that
Xy-
lopia
seedlings were only found in refuse piles of ant nests
suggests that seed – rescuing ants may act as ne – tuned di-
rected dispersers following long distance dispersal by birds
(see Passos & Oliveira 2002). Although a fraction of the
seed crop is probably lost to granivorous ants such as
Phei-
dole
, our data show that ants do have a relevant contribution
to plant regeneration. Ant nests in poor soils are usually
nutrient enriched sites that increase seedling growth and
survival (reviewed by Rico – Gray & Oliveira 2007). Thus,
the action of two vectors of dispersal should increase the
chance of a seed hitting a safe site in patchy environments
such as savannas.
CONCLUSION
We rejected the fruit crop size hypothesis for
Xylopia
. On
the contrary, we found a positive relationship between crop
size and seed waste under parent plants. Such large amount
of fallen seeds under parent plants is quickly harvested by
ants that rearrange the seed shadow to short distances.
Birds, on the other hand, removed seeds from plant canopy
and deliver them to much longer distances. Thus, birds and
ants provide spatially complementary seed dispersal in the
cerrado. Furthermore, we found that ants may be as impor-
tant as birds for seed dispersal in
Xylopia
, at least for some
individual plants and/or years. (Acknowledgements: This
study was supported by FAPESP [no. 02/12895 – 8], and is
part of the PhD dissertation of A.V.C. at the Programa de
Pos – Graduac~ao em Ecologia da Unicamp. P.S.O. was sup-
ported by research grants from the CNPq [no. 304521/2006
– 0] and FAPESP [no. 08/54058 – 1]).
3