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ISSN 0103-4154
THREATENED PLANT-FRUGIVORE MUTUALISMS IN A BRAZILIAN ATLANTIC RAINFOREST ISLAND: REPORT ON FIELDWORK ON ILHA
DE SÃO SEBASTIÃO
Juan Carlos Guix, Marc Martín & Cristiane Leonel
GRUPO DE ESTUDOS ECOLÓGICOS SÉRIE DOCUMENTOS Nº 8(2)
JULHO 2005
Grupo Estud. Ecol., Sér. Doc. 8(2): 1-25 ISSN 0103-4154 São Paulo, julho 2005
THREATENED PLANT-FRUGIVORE MUTUALISMS IN A BRAZILIAN ATLANTIC RAINFOREST ISLAND: REPORT ON FIELDWORK ON ILHA DE
SÃO SEBASTIÃO
Juan Carlos Guix 1, Marc Martín 1 & Cristiane Leonel 2
1 Departament de Biologia Animal (Vertebrats), Facultat de Biologia, Universitat de Barcelona. Av. Diagonal 645, 08028 Barcelona, Spain.
e-mail: [email protected]
2 Parque Estadual de Ilhabela, Instituto Florestal, Rua do Horto 931, Horto Florestal, 02377-000 São Paulo, SP, Brazil.
ABSTRACT. Interactions between angiosperm fleshy fruiting species and frugivores are spread worldwide. Nevertheless, seed size and particularly seed diameter can limit the number of seed dispersers in a given area. Thus, large-seeded plant species tend to have few potential dispersers when compared to plants producing small seeds. Between February 1997 and April 1998, we studied plant-frugivore relationships between large-seeded species and their potential dispersers on São Sebastião Island, a 335 km2 area mostly covered by Brazilian Atlantic rainforest. Factors such as the geological history of the island or human interventions that have affected the island during the last four centuries - particularly the ongoing illegal hunting -, suggest that recruitment of fleshy-fruiting plants producing large seeds has been diminished as a consequence of the drastic reduction and/or local extinction of their potential dispersers. Under these conditions, mutualisms involving large-seeded species and large frugivores are threatened. Medium-term and long-term changes in plant communities are expected if plant-frugivore mutualisms are not managed. Those changes would include local extinction of several species of woody plants and palms. Key-words: plant-animal interactions, seed dispersal, local extinction, frugivores, fleshy fruiting plants, islands, animal-dispersed seeds, forest fragmentation.
1
INTRODUCTION
Mutualisms between plants and animals, which usually disperse their seeds, are not
species-specific but generalistic. In fact, interactions between a plant and its dispersers
often involve animal species belonging to different zoological groups, such as birds and
mammals. At the same time, animals obtain a wide source of nutrients and avoid high
concentrations of chemical components that could act as toxins by eating fruits and seeds
belonging to more than one plant species (Herrera, 1982, 1985; Rosenthal & Janzen, 1979;
Stiles, 1989; Tsahar et al., 2002). This way, a certain seed disperser does not depend only
on one or a few kinds of trophic resources, and, consequently, a certain plant does not
depend only on one or a few species of dispersers to spread its seeds (Herrera, 1982;
Jordano, 1995; Corlett, 1996).
In Angiosperms, though, fruit size and mainly seed size can be highly associated with
some characteristics of the seed-dispersers (Jordano, 1995). This may restrict the number
of species that can carry complete seeds far away from the mother-plant. Several works
world-wide have shown that as seed size increases, less animal species are able to act as
their dispersers (see Leighton & Leighton, 1983; Corlett, 1998; Kitamura et al., 2002, and
references therein). Thus, species that produce large seeds (covered or not by fleshy pulp)
are more likely to loose their potential dispersers by local or regional extinction than those
producing small seeds (Meehan et al., 2002).
Local extinction of seed dispersers are more likely to occur in small and isolated
habitats such as little islands or woods, than they are to occur in large continuous ones
(Guix, 1995, 1996; Bennett & Robinson 2000; Meehan et al., 2002). Therefore, studies on
seed dispersal patterns of large-seeded forest plant species could be of special interest to
the conservation of biodiversity in this type of environments.
São Sebastião Island, in southeastern Brazil, has been the frame of several zoological
and bigeographical studies since the end of the 19th century (see Ihering, 1897;
Luederwaldt, 1929; Müller, 1966, 1968; Vanzolini, 1973, Rebouças-Spieker, 1974;
Vanzolini & Rebouças-Spiker, 1976). Part of the specimens collected by those researchers
and several others were housed in the Museu de Zoologia of the Universidade de São
Paulo - MZUSP. In 1993-1994, Fábio Olmos compiled museum records and information
that had been published on the subject. He updated the species lists of birds and mammals
on São Sebastião Island with data based on his own observations (Olmos, 1996).
2
In his paper, Olmos op. cit. emphasised the absence on the island of several bird and
mammal species that were common and relatively abundant in the mainland. He also
remarked the apparently low number of species of plants belonging to the family
Myrtaceae, as well as the absence of a conspicuous palmito palm species (Euterpe edulis;
Arecaceae).
The aim of the current work was detecting potential disruptions in plant-frugivore
mutualisms in this natural fragment of rainforest as a consequence of human intervention
that have been affecting the island during the last four centuries.
Study area
The study was conducted on the São Sebastião Island, which is located on the northern
coast of the State of São Paulo (23º 50' S, 45º 20' W; 33,593 ha), in southeastern Brazil
(figure 1). Most of the island's relief is formed by granites, gneisses and alkaline eruptive
rocks (França, 1951) ranging between sea level and 1,379 m of altitude. Rainfall in
clearings and open vegetation areas near sea level reaches 1,350 mm per year.
Nevertheless, hillsides and peaks of the island above 500 m are frequently covered by
dense fogs. The fog produces a water dripping effect that allows a relatively well preserved
Atlantic rainforest (composed by old secondary and mature successions) to grow in these
highest areas.
This island, as were several others along the coast of the States of São Paulo and Rio de
Janeiro, was land-connected to the mountain chain of the Serra do Mar during the last
glaciation, when the sea-level was lower than nowadays (Ângelo, 1989). About 8,000
years ago, when the climate became warmer and the sea-level rose, the São Sebastião
massif became separated from the continent by a channel that was 2 km wide at its
narrowest point (Vanzolini, 1973). Since then, the sea-level has varied between the current
level and 2-5 m above it (Olmos, 1996). Nowadays, a channel 1.7-3.5 km wide and 4.5-46
m deep separates the São Sebastião Island from the continent (Ângelo, 1989).
According to reports made by Jesuits during the middle 16th century, the São Sebastião
Island was not inhabited when the first Europeans arrived in 1563 (cf. Anchieta, 1565). At
the beginning of the 17th century, several slave settlements were established on the island:
the lowland forests started to be cut to be used as fuel and it was replaced by sugar cane. In
1788, there were at least 25 sugar factories on the island and the population was around
4,500 people, 1,000 of them being slaves. During the middle 19th century, sugar cane
3
plantations were replaced by coffee plantations and deforestation continued towards the
highlands. In 1854, there were 225 coffee farms on the island and the human population
was close to 13,000 people (Jornal da Vila, 1993a, 1993b). From the 1970's, part of the
island became a summer resort and nowadays human inhabitants range between 4,500
people during winter and 19,000 people during summer. Most of the island forests are
protected by the 260 km2 Parque Estadual de Ilhabela, which is managed by the
government of the State of São Paulo.
Figure 1. Situation of the Brazilian São Sebastião Island surveyed in 1997, for large-seeded woody plants and palms, and large frugivores (including line transects).
4
METHODS
Data and general information on hunting (mainly practices used and species hunted)
were collected on the island between February 1997 and April 1998. This information was
obtained through interviews to the guards of the park and completed with field
observations on the illegal traps found during our surveys.
During July and August 1997 we performed surveys in mature and old secondary
forests, including those located in highly isolated areas, in order to detect frugivore
vertebrates and plant species that produced large fleshy fruits.
At the same time, between the 10th of July and the 18th of August, a census of large
and medium size species of frugivores was conducted through walking line transects. In
each line transect we counted all individuals and groups of birds and mammal species
weighting more than 150 g, which usually consume fruit and transport large seeds.
Perpendicular distances of these animals in relation to the transect were estimated (see
Mateos et al., 2002 for a detailed description of the method). Also seed-hoarding animals
(squirrels and species of agoutis potentially occurring on the island) were searched during
our surveys.
Thirty-three transects (118.5 km overall) were performed along trails and unpaved
roads crossing areas of mature and old secondary forests in the Park (between 0-900 m of
altitude (see Guix et al., 1999; Martín, 2000). Counts were made by 1-3 researchers during
daily periods (7:00 a.m.-12:00 and 4:00 p.m.-6:00 p.m., local time).
Density estimates (individuals per square kilometre) and/or encounter rates (i.e.
individuals per linear kilometre) were estimated through the distance sampling method
(Buckland et al., 1993) and the DISTANCE 2.02 programme (Laake et al., 1993).
Excepting the case of the red-breasted toucan (Ramphastos dicolorus), the effective strip
width, which could provide density estimates of the studied species of seed dispersers,
could not be assessed statistically due to the low number of records. Therefore, encounter
rates were used as an estimator of variation in population size (see Hochachka et al., 2000).
Density estimates (see Martín, 2000) and encounter rates (current data) of large-
frugivore species found on the island were compared with those of a continental area
covered by continuous and pristine Atlantic rainforest (the Paranapicaba fragment; see
González-Solís et al., 2001; Hernandez et al., 2002; Sanchez-Alonso et al., 2002).
Data on frugivory and seed dispersal of large-sized fruit/seed species of the island
(current data) were collected by means of direct observations on fruit consumption
5
(feeding bouts) and seed transport. Results were completed with observations of seeds
found in faeces and seeds discarded under feeding and roosting sites of frugivorous bats.
These data were compared to those collected in Eastern continental areas of the State of
São Paulo (see Guix, 1995, 1996).
For the purpose of this study, we considered "large seeds" to be those larger than 19
mm in diameter or length, and "large-frugivores", any species of vertebrates able to
swallow or transport them complete. Seed-hoarding animals included all bird and rodent
species that are common seed predators but that may disperse seeds by scatter-hoarding
them in fallen trunks or via burial.
Surveys of large-seeded woody plants and palms were performed walking along 85 km
inside the forest, outside of trails, path ways and other human influenced areas. During
these surveys, seedlings and juvenile plants of large-seeded species (up to 50 cm high)
were counted beneath the adult parent plants and surroundings.
RESULTS
Surveys of large-seeded rainforest plants
At least 14 species of large-seeded (see definition in Methods) woody plants and palms
were found in the areas surveyed on the São Sebastião Island: Astrocaryum
aculeatissimum, Attalea dubia (Arecaceae), Licania spp. (Chrysobalanaceae), Calophyllum
brasiliensis, Rheedia cf. gardneriana (Clusiaceae), Aniba firmula, Cryptocarya cf.
aschersoniana (Lauraceae), Eugenia spp. (Myrtaceae), Chrysophyllum spp. (Sapotaceae)
and Sterculia sp. (Sterculiaceae).
Considering the characteristics of the Eugenia spp. fruits and seeds found in our surveys
in forests of the São Sebastião Island, they might belong to species such as: E. coccifera, E.
glomerata, E. mosenii, E. obovata, E. prasina, E. stictosepala, E. stipitata, E. sulcata,
some undescribed species and tens of varieties and morphs.
The characteristics of some Licania spp. fruits and seeds found on São Sebastião Island
match with those of Licania octandra, L. gardneri, L. hoehnei, L. indurata, L. kunthiana,
L. nitida and L. tomentosa (see also Discussion).
A few adult woody trees belonging to species that produce large-seeded fleshy fruits
were found exclusively in areas of difficult access such as the Poço Valley. In the case of
6
Strychnos cf. trinervis (Loganiaceae; a species that produces medium-sized seeds) only
two adult individuals were found on the island. All large-seeded species found had large
deposits of cogeneric seeds and fruits under the crown of each tree.
The Licania spp. seeds found could be divided into three groups according to their size
and proportions: A- short (21-25 mm) and thick (18-20 mm); B- relatively small in
diameter (16-19 mm) but really long (39-46 mm); C- very large (24-29 x 39-44 mm)
(figure 2).
Figure 2. Types of seeds of Licania (Chrysobalanaceae) species and/or morphs found on the São Sebastião Island, classified according to its dimensions and proportion of length and width. Group A: short (21-25 mm) and thick (18-20 mm) seeds; group B: elongated seeds (39-46 mm); group C: very large seeds (24-29 x 39-44 mm).
Up to 300-1000 seeds per individual and between 0 and 23 seedlings and juvenile
cogeneric plants were found beneath eight large-seeded Licania trees. Most of the fruits
and seeds found beneath these trees had been partially eaten by rodents or perforated by
beetles. Radial searches for seedlings and juvenile plants to up to 25 m from the trunk of
the trees showed only one juvenile cogeneric plant 4 m away from the border of the
projection of the crown on the floor.
Up to 120-250 seeds per individual and between 3 and 14 seedlings of Astrocaryum
aculeatissimum were found beneath 11 parent palms. Similarly, most of the seeds found
beneath these palms had been partially eaten by rodents or perforated by beetles.
7
Surveys of large-seeds disperser animals
"Large frugivores"
Two species of "large frugivores" (see definition in Methods) that usually swallow and
defecate or regurgitate entire seeds (endozoochory) were found on the São Sebastião
Island: Pipile jacutinga (Cracidae) and Ramphastos dicolorus (Ramphastidae). Cebus
nigritus (= Cebus apella nigritus; Cebidae), which can transport large fruits in its hands or
in its mouth but does not swallow entire large seeds, was also spotted (Appendix I). We
did not find the following species: Selenidera maculirostris (Ramphastidae), Pyroderus
scutatus and Carpornis cucullata (Cotingidae). Local people reported the presence of a
large primate species living in the highlands of the island that might correspond to
Brachyteles arachnoides. Nevertheless, we failed to find this or any other species of
primate other than Cebus nigritus, even in the most isolated places of the island, such as
the Poço Valley.
An unidentified species of a large fruit-eating bat (Artibeus sp.; Phyllostomidae) was
also seen. It usually carries large fruits in its mouth and discards small and large seeds
under its feeding roosts (exozoochory).
Seed-hoarding animals
Sciurus ingrami (Sciuridae) was the only potential seed-hoarding species detected. It is
generally considered as a seed predator, but it can also act as seed disperser of part of the
seeds collected (exozoochoory).
No agouti (Dasyprocta sp.; Dasyproctidae) or spiny rat (Proechimys sp.; Echimyidae)
species were found, and neither was the giant Atlantic tree rat (Nelomys thomasi;
Echimyidae), an endemic species of the island. One adult paca (Agouti paca; Agoutidae)
was spotted, but the role of this species as potential seed-hoarding is unknown.
Density estimates
Four species of vertebrates that transport large seeds were counted along the transects
conducted on São Sebastião Island (Encounter rates: ind./lineal km): two large-bodied bird
species (Pipile jacutinga: 0.024+0.013 and Ramphastos dicolorus: 0.371+0.148), one
8
large-bodied primate species (Cebus nigritus: 0.030+0.030) and one seed-hoarding rodent
(Sciurus ingrami: 0.165+0.065). Our sampling effort was not enough to obtain count data
of Selenidera maculirostris and Procnias nudicollis.
Information on illegal hunting and live captures of large frugivores
The information compiled during the study period suggests that hunting and live
captures are widespread on the island all year through.
The most common practices to capture large bodied seed-dispersers were shooting (e.g.
Cebus nigritus and possibly other species of primates, as well as Pipile jacutinga) and
birdlime (with a particular impact on species belonging to the families Muscicapidae,
Cotingidae, Trogonidae and Ramphastidae). Live traps were also used by local people to
capture bird species (e.g. Procnias nudicollis, Platycichla flavipes, Turdus spp.) that are
able to ingest and regurgitate medium-sized seeds. Slipknot devices to capture ground-
dwelling mammals were found as well, but this practice has low success in the capture of
species that potentially disperse large seeds on the island.
We did not detect any hunting or capture practice that affected squirrels nor any species
belonging to the family Echimyidae.
DISCUSSION
Ecological assessment
In tropical regions, large vertebrate species are usually targeted by humans as a source
of protein supply and subsistence. Species living in small forest fragments are more
vulnerable to hunting than species inhabiting large continuous forests (see Robinson, 1996;
Corlett, 1998; Cullen et al., 2000; Peres & Roosmalen, 2002). Thus, hunting is one of the
major threats of medium and large animals in forest fragments.
Although hunting is formally forbidden by the Brazilian laws, several species of fruit
and seed-eating animals, such as some species of monkeys (Atelidae, Cebidae) agoutis
(Dasyproctidae) and guans (Cracidae), have been illegally captured in public and private
areas covered by forest in southeastern Brazil.
9
Most woody plant species and palms of the Brazilian Atlantic rainforest are dispersed
by animals (zoochory), and very few ones are exclusively dispersed by other means (e.g.
anemochory, hydrochory, autochory)(Guix, 1995, 1996; Negrelle, 2002; Tabarelli & Peres,
2002). Therefore, drastic declines or local extinction of seed disperser frugivores might
lead to the reduction of seedling establishment and lower plant recruitment (Bleher &
Böhning-Gaese, 2001). Consequently, disruptions in seed dispersal patterns may result into
demographic changes affecting the genetic structure of some populations of trees and
bushes, especially in small and isolated forest fragments (Pacheco & Simonetti, 2000).
Forest fragmentation usually affects the structure of species composition and diversity
of woody plants (Ochoa-Gaona et al., 2004; Zhu et al., 2004). When comparing small
fragments of Brazilian Atlantic rainforest to large fragments (Guix, 1995; Tabarelli &
Peres, 2002), Tabarelli et al. (1999) detected a 9% average decline of species
representation in four plant families (including Myrtaceae and Lauraceae) that are mostly
dispersed by birds and mammals.
These effects may be worse in islands covered by rainforest, considering their time of
geological isolation (see Maunder et al., 2002). For example, it is predicted that lots of late-
successional plant species on several Pacific islands will lose their dispersal agents as a
consequence of the high human hunting pressure on large avian frugivores (Hamann &
Curio, 1999; Meehan et al., 2002).
Another problem related to the conservation of large-seeded plant species is linked to
the fact that large seeds tend to be dispersed within shorter distances than small seeds (see
Howe et al., 1985; Hedge et al., 1991; Brewer, 2001; Clausen et al., 2002; Charalambidou
& Santamaría, 2002, Silvius & Fragoso, 2003, and references therein). Thus, genetic
interchange between populations of large-seeded plants and their chances of successfully
colonising new areas could be lower than those of small-seeded plants.
It is possible that part of the nowadays extinct megafauna of the Late Pleistocene was
able to disperse (mainly by endozoochory) the large-seeded plant species across longer
distances than the animals that exploit their fruits today (see below). Also, the lack of large
terrestrial herbivores on the island, such as the tapir (Tapirus terrestris) or deers (Mazama
americana, M. gouazoubira, M. bororo), which usually consume plants in the early stages
of development, could be enhancing seedling establishment of the small-seeded species of
plants (which, hypothetically, are the most easily dispersed). This would be disrupting the
recruitment of large-seeded plant species due to competitive exclusion.
10
Encounter rates of Cebus nigritus and Pipile jacutinga on the São Sebastião Island were
two and three times lower, respectively, than those found in the large pristine forests of the
Paranapiacaba continental area (Table I). Nevertheless, data on C. nigritus (= C. apella
nigritus) on the island are based only on one encounter of three individuals, being the
standard error considerably large.
Data from surveys performed during July and August 1997 strongly suggest that the
São Sebastião Island suffers from both local extinction and very low population densities
of large-frugivores. One exception is the population density of R. dicolorus on the island
(16.96±13.37 ind./km2; Martín, 2000), which is five times larger than that found in the
Paranapiacaba continental area (3.23±1.25 ind./km2; Hernández et al., 2002). This
difference in population densities could be the result of the absence of potential
competitive species of toucans, guans and other frugivores on the island (Martín, 2000;
Guix et al., 2001).
Table I. Encounter rates (individuals per lineal km) of "large-frugivores" and the seed-hoarding Sciurus ingrami on the São Sebastião Island, compared to those found in the Paranapiacaba fragment (1,400 km2), a continental area of pristine forests in southeastern Brazil (see Methods). (--) = data not collected.
Group/Species São Sebastião Paranapiacaba
MAMMALS
Cebidae: Cebus nigritus 0.030±0.030 0.057±0.012
Sciuridae:
Sciurus ingrami 0.165±0.065 (--)
BIRDS
Cracidae: Pipile jacutinga 0.024±0.013 0.079±0.019
Ramphastidae:
Ramphastos dicolorus 0.371±0.148 0.11±0.039
Medium and large frugivore species have been hunted for meet supply (made by local
people) or game hunting (by people coming from other regions) on the São Sebastião
Island (authors' personal observations). Several potential large seed disperser species, such
11
as Tapirus terrestris, Dasyprocta leporina, Alouatta guariba (=A. fusca), Penelope
obscura, Pyroderus scutatus, are missing from the island (Olmos, 1996; cf. Pereira et al.,
2001).
Tree species that produce fruit covered by hard walls such as Eriotheca pentaphylla
(Bombacaceae), Hymenaea courbaril (Caesalpinaceae), Carpotroche brasiliensis
(Flacourtiaceae), Strychnos spp. (Loganiaceae), Inga cf. sessilis (Mimosaceae),
Posoqueria cf. acutifolia, Posoqueria latifolia (Rubiaceae) also occur on the São Sebastião
Island. These plants usually produce medium-sized seeds (between 5 and 19 mm in
diameter or length) that are locked up inside hard coverings (including capsules and
legumes). In other areas of the Brazilian Atlantic rainforest, hard seed coverings are
usually opened by primates (Atelidae, Cebidae) and rodents, and in some cases
successfully dispersed by these animals (Guix, 1995, 1996).
Nevertheless, it is possible that during the Quaternary Period some of these fruits (such
as Posoqueria spp. and Strychnos spp.) were swallowed whole and the seeds were
successfully dispersed by the megafauna which are now extinct (see below). Also, some of
the small seeds, such as those of Passiflora spp. (Passifloraceae), are enfolded in
coriaceous coverings hardly accessible for birds but easily opened by Atelid and Cebid
monkeys, tayras (Eira barbara; Mustelidae) and coatis (Nasua nasua; Procyonidae).
Fleshy fruit plant species, such as the palmito palm (Euterpe edulis, Arecaceae; fruit
diameter: 11-15 mm; seed diameter: 9-13 mm), which produces medium-sized seeds that
can be dispersed by small and medium-bodied frugivorous bird species (Guix, 1995),
could also be suffering the effects of habitat simplification on the island. Although the
palmito palm grows spontaneously on the near continent and, apparently, on very small
islands near São Sebastião (i.e. the Búzios Island with 755 ha, the Ilha do Mar Virado with
119 ha, the Ilha do Prumirim with 30 ha, and also diminute islands such as the Ilha da
Ponta with 6.5 ha; Vieitas, 1995), no palmito palm individuals (neither adult, juvenile or
seedlings) were found in the forests of the island.
Since complete check lists of plants species on São Sebastião Island are not available,
several other medium-seeded and large-seeded plant species may not have been detected
but could still be declining (for example, species belonging to the genera Aniba,
Cryptocarya, Ocotea and Nectandra (Lauraceae), Andira spp. (Leguminosae-
Papilionoidea), Virola (Myristicaceae), Eugenia, Marlierea, Myrcia, Plinia (Myrtaceae),
Euplassa (Proteaceae) and Pouteria (Sapotaceae)).
12
The large-seeded Licania species
In the Brazilian Atlantic rainforest, Licania spp. seeds may be dispersed following three
major patterns: 1. Endozoochory: swallowing whole fruits and regurgitating whole seeds
(e.g. by toucans, the black-fronted piping guan, the red-ruffed fruitcrow) or defecating
them (e.g. by howler monkeys, the dusky-legged guan); 2. Exozoochory: transport in the
mouth and discard (Phyllostomid bats, Atelid and Cebid monkeys); 3. Exozoochory:
Scatter-hoarding them via burial by seed predators (agoutis, spiny rats).
Taking into account the frugivore assemblages of the São Sebastião Island nowadays
(Olmos, 1996 and our data), Licania seeds belonging to group "A" have probably scarce
potential dispersers (both considering number of species and number of individuals per
species). Probably, the only frugivore species on the island that are able to swallow seeds
of Licania spp. of group "A" are Pipile jacutinga and Ramphastos dicolorus (cf. Guix,
1995, 1996). Nevertheless, seeds belonging to the groups "B" and "C" can not be ingested
entire by any of the frugivore species remaining on the island: they are too large (in width
and/or length) in relation to the bill width and gape of the largest frugivores left (nule
endozoochory; see figures 3 and 4). Only one Licania seed-hoarding species (Proechimys
iheringi; Echimydae) is known to occur in the study area (Olmos, 1996). Another way out
for these types of seeds on the island could be one or more Phyllostomid bat species that
eat Licania fleshy fruits and transport seeds in their mouths to the feeding roosts
(exozoochory).
13
Figure 3. Relationship between seed width and the number of species (birds and mammals) that disperse each plant species in their digestive tract (endozoochory). Each dot represents one plant species living in the coastal Atlantic rainforest of the State of São Paulo, according to Guix (1995) and data from the São Sebastião Island. Types of seeds of Licania (Chrysobalanaceae) species and/or morphs found on the São Sebastião Island: Group A (short seeds); group B (elongated seeds); group C (very large seeds).
Figure 4. Relationship between seed length and the number of species (birds and mammals) that disperse each plant species in their digestive tract (endozoochory). Each dot represents one plant species living in the coastal Atlantic rainforest of the State of São Paulo, according to Guix (1995) and data from the São Sebastião Island. Types of seeds of Licania (Chrysobalanaceae) species and/or morphs found on the São Sebastião Island: Group A (short seeds); group B (elongated seeds); group C (very large seeds).
14
The large-seeded Eugenia species
The Eastern Brazilian Myrtaceae trees are the least known woody plants of the
Brazilian Atlantic rainforest (see Aguiar, 1991; Negrelle, 2002). It is a very complex group
that has been poorly studied in terms of taxonomy, systematics and natural history (Guix &
Ruiz, 1995; Pizo, 2002). There are several species of Eugenia living in the Brazilian
Atlantic forests still to be described and probably several species names to be reviewed and
sinonimized. In this situation some or several large-seeded Eugenia species may be
threatened by deforestation and loss of seed-dispersers.
Dispersal patterns of large-seeded Eugenia species may be closely related to those of
Licania spp. In fact due to the similar characteristics of large-seeded species of both genera
(e.g. fruit and seed sizes and shapes), the same seed-dispersing species may be included in
both patterns.
Under captivity conditions, Eugenia spp. seeds (diameter: 16-18 mm) were regurgitated
completely whole by Ramphastos vitellinus ariel (Ramphastidae) after 2-23 minutes of
the ingestion, after 20-23 minutes in the case of Ramphastos dicolorus, and after 4-9
minutes in Pyroderus scutatus (Cotingidae) (Guix, 1995).
Seed dispersal patterns are strongly influenced by fruit and seed size. For example, the
number of potential dispersers (animals) of each plant species living in the coastal Atlantic
rainforest of the São Paulo State is inversely proportional to seed width and seed length
(see figures 3 and 4).
In general Licania and Eugenia species have high variation (interespecific and
intraespecific) in fruit and seed morphology and size. If fruit and seed size determine in
part the type and the number of its dispersers, the seed morphotypes of each Licania and
Eugenia species could be subjected to different selective pressures induced by different
species of seed-dispersers.
On the other hand, the decline or local extinction of Astrocaryum, Attalea and Eugenia
seed dispersers could also disrupt several plant-disperser-pest evolutionary triads, and
affect negatively the larvae dispersal of beetle species (Curculionidae) that feed on their
endosperm (see Guix & Ruiz 1995, 1997, 2000).
15
Survivorship during establishment
Surveys of large-seeded rainforest woody species and palms in São Sebastião Island
may suggest that these species are very sensitive to forest fragmentation and frugivore
community simplification (see table II). In fact almost all individuals of large-seeded
species that were found during the present study were seeds, seedlings and large adult. Few
individuals were detected in the forest during walking surveys in intermediate stages of
development.
Table II. Comparison of “r” and “k” strategies of reproduction in plant species that produce fleshy fruits (i.e. seeds covered by pulp and arils) in the Atlantic rainforest of the State of São Paulo.
Species producing:
small size seeds large size seeds
Number of seeds produced high low
Number of seed dispersers (animal species) high low
Vulnerability of the seed dispersers to local extinction low high
Distance of seed dispersal high low
Survivorship during establishment low ?
Ability to colonise new environments (including those altered by man) high low
During the last 40 years most researchers have assumed that large-seeded species show
higher rates of survivorship during establishment than small-seeded species do (cf. Green
& Juniper, 2004). Nevertheless, new evidences based both on natural and experimental
conditions claim a revision for this assumption (see Moles & Westoby, 2004, and
references therein).
Traditionally, experimental ecologists have evaluated early seedling establishment to
assess survivorship success. However, other development stages in the establishment
process of small and large-seeded plant species must be surveyed and reassessed (Westoby
et al., 2002; Moles & Westoby, 2004; Moles et al., 2004).
16
Historical assessment
The Amazonian rainforests have many more large-seeded plant species than the
Brazilian Atlantic rainforest (e.g. comparing the number of species of Sapotaceae that
produce large fruits). In general, large-seeded plant species of the Brazilian Atlantic
rainforest have few potential dispersers, particularly concernig large-bodied species of
monkeys (see Guix, 1995, 1996; Roosmalen & Garcia, 2000).
During the Quaternary Period, several of the large mammalian herbivore and omnivore
species occurring ("megafauna"; i.e.: Litopterna, gomphotheres, giant forms of xenarthran
edentates, wild horses, camel-like herbivores) probably included large fruits in their diets,
being potential dispersers of large seeds (Janzen & Martin, 1982). With the massive
extinction of the South American megafauna at the end of the Pleistocene (Vivo &
Carmignotto, 2004), only few species groups were able to disperse large seeds in dense
forests: agoutis (Dasyproctidae), Spiny and tree rats (Echimyidae), some monkey species
(Atelidae, Cebidae) and, in some cases, guans (Cracidae), toucans (Ramphastidae) and
fruit-eating bats (Phyllostomidae: mainly Stenodermatinae).
Thus, two non-exclusive theories could explain the larger number of large-seeded
species in the Amazonian rainforests: 1. The megafauna in Amazonian forests was more
diversified in the late Quaternary and it got extinct later than the megafauna of the Atlantic
forests. 2. Humans still play an important role in seed dispersal patterns of large-seeded
plant species in the Amazon basin (Guix, 2005).
Nevertheless, the extensive anthropogenic interferences on the Atlantic rainforest bioma
over the last 400 years have led to a new crisis of extinction of large vertebrate species that
can leave several tree and bush species without their effective dispersers.
It is probable that, between the megafauna extinction crisis (at the end of the
Pleistocene) and the beginning of the European colonisation of the Brazilian coast (in the
16th century), the Tupi peoples played an important role in the dispersal of large-seeded
plant species in the Atlantic forests (see Guix, 1996, 2005).
Large seeds are usually covered by large amounts of fleshy pulp and other types of
nutritious coverings that were very appreciated by the pre-Columbian natives as an
important source of food (see Cristóvão de Lisboa, 1967; Cardin, 1980; Anchieta, 1565,
1988; Staden, 1988; Rosa, 1997). As it still occurs in some Indian and Caboclo
communities of the Amazonia (Guix, 2005), fruit was probably collected in the forest and
then transported to the settlements to be processed, which would have played an important
17
role in the seed dispersal patterns of the Atlantic forest. Despite of the transport, the
elimination of seed coverings (as well as pulp inhibitors of seed germination) could
enhance germination and seedling establishment. Although there is no information on
settlements of Tupi Indians long-term on the São Sebastião Island, it is known that some
Tupi populations inhabited several islands of the São Paulo State coast during irregular
periods in order to hunt and collect plant products (Staden, 1988). Since most of these
Indian communities were nomadic, the abandonment of the settlements could also enhance
a new forest succession around these sites with a large proportion of megafruits (Guix,
2005). In fact, it is possible that several clusters of palms (Guix, 1995, 1996) that
nowadays exist in the continuous rainforest throughout the Neotropical region were
originated this way (cf. Silvius & Fragoso, 2003 for other nonmutually exclusive
hypotheses).
Final considerations and suggestions
Several large-seeded plant species have survived until now in the Brazilian Atlantic
rainforest, probably in part due to their ability to recover from periods of low recruitment
by being stored in long-live adults with a long-term reproductive capacity (see Kelly &
Browler, 2002). Nevertheless, historical and ecological changes over the last 10,000 years,
and especially anthropogenic interferences over the last 400 years, have dramatically
reduced their options of dispersal and survival. Therefore, specific management practices
are needed for the long-term maintenance of these species in natural areas.
In the case of the São Sebastião Island, we suggest that the management plan of the
Ilhabela State Park considers the replantation of large-seeded species (e.g. Astrocaryum
aculeatissimum, Attalea dubia, Arecaceae; Eugenia spp., Myrtaceae; Licania spp.,
Chrysobalanaceae) and also species that produce hard-covered fruits (e.g. Hymenaea
courbaril, Caesalpiniaceae; Strychnos spp., Loganiaceae; Posoqueria spp., Rubiaceae),
from the remnant population stock of the island. Alternatively, the (re)introduction of a
burial scatter-hording species of large seeds (exozoochory), such as Dasyprocta leporina,
and a large species of monkey able to swallow and disperse large seeds (endozoochory),
such as Alouatta guariba from the nearest areas on the coast, could be considered.
Nevertheless, stopping illegal hunting is crucial for the maintenance of the diversity of the
forests on these and other Brazilian islands.
18
We strongly recommend studying and monitoring the genetic structure of the
populations of large-seeded plant species on the island in other to assess whether importing
seeds from the nearest continent forests should be considered.
Acknowledgements
Mizué Kirizawa and Maria Lucia Kawasaki provided helpful advice for the
identification of plant species. Permission to conduct research in the Ilhabela Park was
granted by the Instituto Florestal de São Paulo. The guard staff of the Park provided
logistic support and information. K.C. Burns and an anonymous referee made valuables
comments and suggestions on the manuscript. Núria López Mercader and Robin Rycroft
improved the English text.
19
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Appendix I. Species of large-seed dispersers living on the São Sebastião Island and in mainland areas covered by pristine Brazilian Atlantic rainforest (Serra do Mar mountain system), more than 7 km away from the São Sebastião Island. * = species reported by Olmos (1996), but not found during our surveys
Families/species Mainland areas S. Sebastião Island
MAMMALS
Tapiridae: Tapirus terrestris X
Cebidae: Alouatta guariba X Brachyteles arachnoides X Cebus nigritus X X
Dasyproctidae: Dasyprocta leporina X
Echimyidae: Nelomys nigrispinis X Nelomys thomasi * Proechimys iheringi X *
Sciuridae: Sciurus ingrami X X
Phyllostomidae: several species X X
BIRDS
Cracidae: Penelope obscura X Pipile jacutinga X X
Ramphastidae: Baillonius bailloni X Ramphastos dicolorus X X Ramphastos vitellinus X Selenidera maculirostris X *
Cotingidae: Carpornis cucullata X * Pyroderus scutatus X Procnias nudicollis X X
25