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: jcguix@pangea.org

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.

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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).

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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

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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.

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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.

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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

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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)).

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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).

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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).

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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