Bird frugivory and seed germination of Myrsine umbellata and Myrsine lancifolia (Myrsinaceae) seeds in a cerrado fragment in southeastern Brazil

Abstract

Birds are known to be important dispersers of plants, since the passage of seeds through the digestive tract often has a positive influence on germination percentage and speed. In this study, proportions of germination in different substrates were compared between Myrsine (Myrsinaceae) seeds collected manually and those ingested by birds. The guilds of birds that fed on M. umbellata and M. lancifolia were identified and comprise 24 and 12 species, respectively. A higher germination proportion was found among seeds defecated by birds and sowed in the study area. The study also found differences between the guilds of frugivores in both synchronopatric species. Therefore, we suggest that M. umbellata and M. lancifolia are important food sources by birds that play a positive influence for enhance germination of Myrsine.

Full text

http://www.biotaneotropica.org.br/v11n4/en/abstract?article+bn00911042011 http://www.biotaneotropica.org.br
Biota Neotrop., vol. 11, no. 4
Bird frugivory and seed germination of Myrsine umbellata and Myrsine lancifolia
(Myrsinaceae) seeds in a cerrado fragment in southeastern Brazil
Rafael Soave Guerta1,5, Lucas Gustavo Lucon1, José Carlos Motta-Junior2,
Luís Augusto da Silva Vasconcellos3 & Rodolfo Antônio de Figueiredo4
1Centro de Ciências Biológicas e Saúde, Universidade Federal de São Carlos – UFSCar,
Rod. Washington Luiz, Km 235, CEP 13565-905, São Carlos, SP, Brasil
2Departamento de Ecologia, Laboratório de Ecologia de Aves – LABECOAVES, Instituto de Biociências,
Universidade de São Paulo – USP, CEP 05508-090, São Paulo, SP, Brasil
3ENGEVIX Engenharia S. A, Rua da Assembléia, 66, CEP 20011-000, Rio de Janeiro, RJ, Brasil
4Centro de Ciências Agrárias, Universidade Federal de São Carlos – UFSCar,
Rod. Anhanguera, Km 174, CEP 13600-970, Araras, SP, Brasil
5Corresponding author: Rafael Soave Guerta, e-mail: rsguerta@yahoo.com.br
GUERTA, R.S., LUCON, L.G., MOTTA-JUNIOR, J.C., VASCONCELLOS, L.A.S. & FIGUEIREDO, R.A.
Bird frugivory and seed germination of Myrsine umbellata and Myrsine lancifolia (Myrsinaceae) seeds in
a cerrado fragment in southeastern Brazil. Biota Neotrop. 11(4): http://www.biotaneotropica.org.br/v11n4/
en/abstract?article+bn00911042011
Abstract: Birds are known to be important dispersers of plants, since the passage of seeds through the digestive
tract often has a positive influence on germination percentage and speed. In this study, proportions of germination
in different substrates were compared between Myrsine (Myrsinaceae) seeds collected manually and those ingested
by birds. The guilds of birds that fed on M. umbellata and M. lancifolia were identified and comprise 24 and
12 species, respectively. A higher germination proportion was found among seeds defecated by birds and sowed
in the study area. The study also found differences between the guilds of frugivores in both synchronopatric
species. Therefore, we suggest that M. umbellata and M. lancifolia are important food sources by birds that play
a positive influence for enhance germination of Myrsine.
Keywords: zoochory, seed dispersal, Myrsine, frugivorous birds, Cerrado.
GUERTA, R.S., LUCON, L.G., MOTTA-JUNIOR, J.C., VASCONCELLOS, L.A.S. & FIGUEIREDO, R.A.
Frugivoria e germinação de sementes de Myrsine umbellata e Myrsine lancifolia (Myrsinaceae) por aves
em um fragmento de Cerrado no sudeste do Brasil. Biota Neotrop. 11(4): http://www.biotaneotropica.org.br/
v11n4/pt/abstract?article+bn00911042011
Resumo: As aves são reconhecidamente importantes agentes dispersores de plantas, uma vez que a passagem da
semente pelo trato digestório muitas vezes interfere positivamente na porcentagem e velocidade de germinação
de sementes. No presente estudo, as porcentagens de germinação, em diferentes substratos, foram comparadas
entre sementes ingeridas por aves e sementes não-ingeridas (coletadas manualmente) de Myrsine (Myrsinaceae).
A guilda de aves que se alimentou de M. umbellata e M. lancifolia foi identificada com 24 e 12 espécies,
respectivamente. Verificou-se maior porcentagem de germinação nas sementes defecadas por aves, que foram
semeadas em solo da área de estudo. Além disso, constataram-se diferenças nas guildas de frugívoros entre as
duas espécies sincronopátricas. Portanto, nós sugerimos que M. umbellata e M. lancifolia são importantes fontes
alimentares para aves que têm uma influência positiva para o aumento na germinação de Myrsine.
Palavras-chave: zoocoria, dispersão de sementes, Myrsine, aves frugívoras, Cerrado.

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winter occurring between April to September and wet summer from
October to March; the mean temperature is around 21 °C, and the
annual precipitation lies between 1,138 and 1,593 mm (Valenti et al.
2008).
Motta-Junior & Vasconcellos (1996) and Francisco & Galetti
(2001) found 223 bird species at the studied site, 33% of which feed
on fruits at least sporadically. Therefore, it is possible that a significant
quantity of the seeds in the area is dispersed by birds.
Field observations occurred from 6:00 AM and 6:00 PM in
six M. umbellata specimens (three in 1986, 1988 and three plants
between 2007-2008) and two M. lancifolia specimens in 2007 and
2008 (Figure 1a,b), located in a transition area between a secondary
cerrado forest and a riparian forest. The first species was observed
between November and December 1986 and January 1988 (24.5 hours
of observations), and in December 2007 and January 2008 (30 hours
of study), while the second species was observed for 25 hours between
December 2007 and January 2008. Observations were done when
specimens were at their fruiting peak. The usual length fruiting period
in the study area for Myrsine is September to March.
Observation was performed at a distance of 10 to 15 m from
the trees. The birds were identified by their morphology and/or
vocalization and, when necessary, with the aid of field guides. During
the observations there were recorded the frugivorous species, the
time of their visits, the number of fruits eaten, the pattern of fruit
manipulation and length of stay in the tree for each bird. Agonistic
encounters (direct lunges, there being no physical contact necessarily)
were also registered.
There were collected all bird excreta found in a 2 meter-wide track
between the cerrado and the riparian forest, falling perpendicularly
from the Myrsine specimens towards the same and up to 50 m from
them, in addition to those occasionally found in others tracks near the
specimens (Figure 1c). These feces were identified as having been
defecated by birds due to the presence of uric acid in them. In the
laboratory, seeds were sorted from the excreta.
Germination tests were performed as described by Figueiredo &
Perin (1995). In December 2007, 300 Myrsine seeds from roughly
60 bird feces were randomly collected as well as 300 seeds directly
from the branches of four trees, two of each species (control seeds),
which, after being mechanically removed from the pulp, were washed
for 1 hour in tap water so as to eliminate germination-inhibiting
substances, and sowed on filter paper in a gerbox. Three replicates
were done for 100 seeds, which were kept under natural temperature
and lighting conditions and at a constant humidity level in the gerbox.
Following the same procedure, 600 seeds (300 control seeds and
300 dispersed seeds) were collected in 2007, which were then sowed
in soil from the area under investigation, transported to the laboratory.
As it was not possible to identify the seeds at the species
level, dispersed as well as control seeds were grouped in the same
germination tests, which thus verified, indistinctively, the germination
rate for all Myrsine species (Figure 1d).
In 1986, germination tests were carried out with 450 Myrsine
seeds: 150 seeds excreted by birds, 150 control seeds (mechanically
removed pulp), and 150 seeds with intact pulp. Laboratory tests were
performed on filter paper under natural temperature and lighting
conditions and at constant humidity.
In both different experiments, the seeds were monitored for
5 months after sowing, with no additional treatment to prevent
contamination from fungi and other microorganisms so as to
reproduce the conditions found in the area in question. The statistical
analysis of the 2007 test results was done by means of variance
analysis (single factor ANOVA) and chi-square test (χ2) in order to
verify differences among replicates and treatments. The 1986 test
results were compared by means of chi-square test (χ2).
Introduction
Mechanisms of seed dispersal by animals have been the object
of study for a long time (e.g. Corner 1949, van der Pijl 1969,
Levey et al. 2002, Dennis et al. 2007). Among dispersers, birds and
mammals play a key role in this process (Howe & Smallwood 1982).
Barnea et al. (1992) indicate that birds can increase the temporal
and spatial distribution of ingested seeds thereby promoting their
germination and the establishment of seedlings. The effects of seed
ingestion are variable; it affects germination proportion, rate, and
speed in different ways depending on the disperser species, even when
researchers have studied closely related plant species and the same
habitat (Barnea et al. 1990, Izhaki & Safriel 1990, Traveset 1998,
Traveset et al. 2001, Paulsen & Högstedt 2002). In addition, the fruit
pulp is known to contain chemicals that inhibit germination and its
removal usually fosters the success of the embryo (Figueroa & Castro
2002, Robertson et al. 2006). However, this effect is not uniform, nor
is it applicable to all seeds dispersed by birds (Barnea et al. 1991).
Myrsinaceae comprises 40 genera, eight of which occur in Brazil,
with roughly 70 species (Souza & Lorenzi 2008). Among them, the
genus Myrsine, which has Rapanea Aubl as principal synonymous
(Freitas & Carrijo 2010), popularly known as capororoca (Lorenzi
1992), has 26 species, distributed from the northeast to the south of
Brazil (Freitas & Carrijo 2010). The species Myrsine umbellata and
M. lancifolia are synchronopatric in the region under investigation,
fruiting between October and February. They are medium-sized trees
that produce a large quantity of small globose purple drupes, odorless
and tasteless to humans, with a thin pericarp and a hard testa seed
(Lorenzi 1992, Ramos et al. 2008).
Eight Myrsine species have been studied with respect to the
dispersal of their diaspores. Pineschi (1990) studied seven of them
(M. acuminta, M. ferruginea, M. gardneriana, M. guyanensis,
M. lineata, M. schwackeana, and M. villosissima) in the Atlantic
Forest and Francisco & Galetti (2001) studied M. lancifolia in the
cerrado (Brazilian savanna) in São Carlos (São Paulo State). Both
studies found birds as the main consumers and, thus, are potential
disperses. Also in São Paulo State, Pascotto (2007) found most
disperser (80.6%) feeding on fruits of M. ferruginea in the edge of
a riparian forest. The study conducted by Pineschi (1990) included
germination tests with seeds ingested by birds. The author employed
filter paper as substrate and found a low germination percentage
(8.4%), in agreement with other authors’ findings (Joly & Felippe
1979, Lorenzi 1992).
Taking into consideration the importance of Myrsine ssp. fruits
to bird feeding reported in previous studies and the paucity of
information on the quality of fruit dispersion in the literature, which
mainly focuses on frugivory research, the purpose of this study was:
1) to survey the birds that feed on M. umbellata and M. lancifolia
fruits in a cerrado fragment; and 2) assess the effects of passage
through the digestive tract of disperser birds on the germination of
seeds of two Myrsine species.
Material and Methods
The study was conducted in non-urban area located on the campus
of Universidade Federal de São Carlos, in the central part of São
Paulo State, Brazil (21° 58’ S and 47° 52’ W). This area encompasses
124.68 ha of cerrado vegetation, 3.60 ha of riparian forest, 93.84 ha
of Eucalyptus plantation with cerrado undergrowth, 222.73 ha of
Eucalyptus spp. plantation, and 83.67 ha consisting of dams, tracks,
and altered fields (Paese 1997), a total of 528.52 ha. The site has
been relatively disturbed, with tracks and the presence of cyclists
principally at weekends, and affected by occasional fires. At 850 m
above sea level, the regional climate is warm temperature with dry

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Bird frugivory and germination of Myrsine spp. seeds
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Figure 1. Studied plant species. a) Myrsine umbellata. © J. C. Motta-Junior; b) Myrsine lancifolia; c) Seeds defecated by birds; d) Germination tests with
filter paper and soil from the study area. © R. A. Figueiredo.
ab
cd
Figure 2. Some birds recorded in this study. a) Female Blue Dacnis (Dacnis cayana), the most frequent visitor among the visitors of Myrsine lancifolia, during
2007/08 observations; b) Pale-breasted Thrush (Turdus leucomelas), fed of Myrsine umbellata during the two periods of this study and consumed the highest of
number of fruits during the 86/88 period; c) Sayaca Tanager (Thraupis sayaca) visited the two species of Myrsine spp.; d) Lesser Elaenia (Elaenia chiriquensis),
migrant living in the study area during spring and summer. © J. C. Motta-Junior.
ab
cd

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Table 1. Bird species that fed on Myrsine umbellata in November-December 1986 and January 1988 (a), from December 2007 to January 2008 (b) and
Myrsine lancifolia from December 2007 to January 2008 (c), in São Carlos, SP, with total number of visits, total number of consumed fruits, diet and migratory
status (M.S.). Nomenclature according to CBRO (Comitê… 2011). Diet and migration according to Motta-Junior (1990) and Motta-Junior & Vasconcellos (1996).
Family/species Total number of
visits Total of consumed
fruits Consumed fruits per
visit Diet * M.S.**
Myrsine umbellata (a)
Picidae
Colaptes melanochloros 15 256 17 INS R
Pipridae
Antilophia galeata 1 2 2FRU R
Chiroxiphia caudata 2 4 2FRU R
Tityridae
Pachyramphus validus 1 30 30 INS M
Tyrannidae
Elaenia chiriquensis (Figure 2d) 13 102 7,8 ONI M
Elaenia flavogaster 14 58 4,1 ONI R
Elaenia mesoleuca 10 24 2,4 ONI M
Elaenia obscura 13 82 6,3 ONI R
Elaenia spp. 23 72 3,1 ONI R
Empidonomus varius 2 8 4INS M
Myiarchus ferox 1 2 2INS R
Myiozetetes similis 2 6 3ONI R
Pitangus sulphuratus 4 20 5ONI R
Tyrannus melancholichus 4 14 3,5 INS M
Tyrannus savanna 1 4 4INS M
Vireonidae
Vireo olivaceus 33 130 3,9 ONI M
Turdidae
Turdus rufiventris 30 366 12,2 ONI R
Turdus amaurochalinus 58 490 8,4 ONI R
Turdus leucomelas 47 580 12,3 ONI R
Thraupidae
Dacnis cayana 14 30 2,1 ONI R
Tangara cayana 3 3 1ONI R
Thraupis sayaca 2 4 2ONI R
Myrsine umbellata (b)
Tyrannidae
Elaenia flavogaster 5 18 3,6 ONI R
Empidonomus varius 1 3 3INS M
Vireonidae
Vireo olivaceus 19 135 7,1 ONI M
Turdidae
Turdus leucomelas 3 29 9,7 ONI R
Thraupidae
Tangara cayana 1 6 6ONI R
Dacnis cayana 6 45 7,5 ONI R
Thraupis sayaca (Figure 2c) 4 16 4ONI R
Tersina viridis 1 4 4ONI R
Ramphocelus carbo 1 30 30 ONI R
*FRU = frugivore, INS = insectivore, ONI = omnivore; **R = resident, M = migratory.

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Discussion
Species feeding on M. umbellata recorded in 2007/2008 (Table 1)
belong to four families and are classified as omnivores, whereas the
guild recorded for the same species in 1986/1988 was composed of
22 species belonging to seven families, including Picidae, Pipridae,
and Tytiridae (Table 1). The landscape alteration, due to new buildings
and Eucalyptus spp. plantations, that occurred in between the two
observation periods may have affected frugivores, especially the
families that were absent in 2007/2008. However, this reduction
should not be seen as absolute, since other variables could have had
an effect on this difference, e.g., more abundant fruits in this area
during the observation period of two decades ago and/or observed
plants more favorably positioned for the birds in question. Moreover,
sampling efforts and observers were different in 1986/1988 and
2007/2008.
The number of frugivorous species recorded for M. lancifolia
in 2007/2008 was similar to that observed by Francisco & Galetti
(2001). However, the rate of visits per hour in our study (1.0) was
lower than that reported by the aforementioned authors, i.e., 3.31
visits per hour (202 birds, altogether). These authors reported
three species, Turdus leucomelas (Figure 2b), Elaenia sp., and
Colaptes melanochloros as the main frugivores, responsible for the
removal of 80% of all fruits. Whereas the observations conducted in
our study (2007/2008) pointed to Dacnis cayana as the most frequent
visitor, accounting for 30.2% of all fruits removed, followed by
T. amaurochalinus (28.6%). The other species together accounted
for 41.2% of fruit removal (Table 1).
The predominance of omnivorous birds was verified in all
observations carried out at the study site. Francisco & Galetti (2001)
reported that omnivorous birds were responsible for 68% of all
M. lancifolia fruits eaten, followed by insectivorous species (29%).
Observations of our study indicated that omnivorous birds ate
91.36% (275) and insectivorous species removed 8.64% (26) of the
Results
The 1986 and 1988 observations of M. umbellata (Table 1)
indicated 22 bird species feeding on its fruit, a total of 293 visits
and 2,287 eaten fruits at 11.95 visits per hour. During this period,
Turdus spp., Elaenia spp. and Vireo olivaceus were the most recurrent
bird species, which made up 46, 24.9 and 11.2% of the visits,
respectively. The 2007/2008 observations of M. umbellata indicated
nine bird species, a total of 41 visits (Table 1) with 1.36 visits per
hour. The most frequent bird was Vireo olivaceus: 46.3% of the visits.
Myrsine lancifolia specimens observed in 2007/2008 were visited
by 12 bird species, totaling 25 feeding bouts (Table 1), at a rate of
1.0 visit/h. Dacnis cayana was the most frequent, with 24% of visits
(Table 1) (Figure 2a).
Two agonistic encounters were recorded during observations of
M. lancifolia. One visitor, Dacnis cayana, was sent off by another
visitor, Turdus amaurochalinus, while feeding on the fruits. The latter
bird ate about 15 fruits and remained on the tree fruit for 1.5 minutes.
During this time, one individual of Vireo olivaceus landed on the
tree and, upon being attacked by T. amaurochalinus, both flew away.
The tests conducted with Myrsine in 1986 indicated the
germination of 73 seeds defecated by birds (48.7%) and 70 control
seeds (46.7%). The seeds with intact pulp did not germinate. There
was no significant difference in germination between control
seeds and those ingested by birds (χ2 = 0.04, P = 0.83, df = 1). In
tests conducted with filter paper as substrate in 2007, there was
no significant difference in germination between control seeds
(4.67 ± 0.57) and those ingested by birds (3.67 ± 1.53) (F = 1.13,
P = 0.35, df = 1). In the test with soil from the study site as substrate
there was a significant difference in germination between control
seeds (9.33 ± 0.58) and those ingested by birds (51.67 ± 3.79)
(F = 366.57, P < 0.001, df = 1). Overall, the number of germinated
seeds in soil was significantly larger than that of germinated seeds
sown on filter paper (χ2 = 27.43, P < 0.001, df = 1).
Family/species Total number of
visits Total of consumed
fruits Consumed fruits per
visit Diet * M.S.**
Myrsine lancifolia (c)
Tyrannidae
Elaenia spp. 4 31 7,7 ONI R
Elaenia flavogaster 1 5 5ONI R
Myiarchus ferox 1 21 21 INS R
Hemitriccus margaritaceiventer 1 5 5INS R
Vireonidae
Vireo olivaceus 3 12 4ONI M
Corvidae
Cyanocorax cristatellus 1 15 15 ONI R
Turdidae
Turdus amaurochalinus 4 86 21,5 ONI R
Thraupidae
Dacnis cayana 6 91 15,2 ONI R
Thraupis sayaca 1 9 9ONI R
Tersina viridis 1 13 13 ONI R
Tachyphonus coronatus 1 3 3ONI R
Ramphocelus carbo 1 10 10 ONI R
*FRU = frugivore, INS = insectivore, ONI = omnivore; **R = resident, M = migratory.
Table 1. Continued...

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M. lancifolia fruits. With respect to M. umbellata, omnivorous birds
ate 86% of the fruits (1,967) in 1986/1988, followed by insectivorous
species: 13.73% (314). The two exclusively frugivorous species,
i.e., Antilophia galeata and Chiroxiphia caudata, contributed just
0.08% (2) and 0.17% (4), respectively. In 2007/2008, the proportion
of M. umbellata fruits eaten by omnivores rose to 98.9% (283).
The remainder (3) was eaten by only one insectivorous species:
Empidonomous varius.
Although almost all large and specialized frugivores are extinct
or very rare in the study area (Motta-Junior & Vasconcellos 1996,
Francisco et al. 2007), Myrsine spp. fruits are small and frequently
eaten by generalist birds, with nutritive importance for omnivorous
and insectivorous as previously detailed (Francisco & Galetti 2001,
this study), which present short-stay behavior. This fact, as observed
in other plants studied in the same area (Francisco & Galetti 2002a,b,
Francisco et al. 2007, Silva et al. 2008), increases the chances of
their being dispersed far away from parent plants, where predation
and competition, tend to be lower (Janzen 1970, Howe & Smallwood
1982, Howe et al. 1985).
Agonistic interactions may inhibit fruit consumption and seed
dispersion by birds (Francisco & Galetti 2001). However, only
two records of agonistic encounters occurred in M. lancifolia,
involving three main dispersers of this species, as recorded by
Francisco & Galetti (2001). This low number of agonistic interactions
may be explained by the abundance of fruits produced per specimen
(e.g. Willis 1966) as well as the availability of other resources in the
area (Pascotto 2007).
Pineschi (1990) conducted germination tests with Myrsine spp.
seeds using only filter paper as substrate and found a very low
germination rate (8.4%), which was confirmed in our study for tests
using control seeds and filter paper as substrate. That author found
that none of the 300 control seeds germinated and bird-defecated
seeds germinated for only three species (4 out of 10 M. lineata seeds;
2 out of 10 M. gardneriana seeds, and 2 out of 35 M. schwackeana
seeds). Similar to these species, the number of germinated
Myrsine spp. seeds in this study, whereas was not possible identify
the seeds at the species level, also indicates that passage through the
digestive tract of birds fosters seed germination. Additional tests are
importants to investigate the response of that passage through the
digestive tract of birds have on each Myrsine’ species of the study area.
Figueiredo & Perin (1995) found differences between germination
rates of Ficus spp. seeds sown on filter paper and soil and showed
that the closer to natural conditions, the more accurate germination
tests become, which was also verified in this work. Thus, although
germination of seeds of the genus Myrsine is low, the germination
response is better when they pass through the digestive tract of birds
and when sown in soil from the study area. Futhermore, the highest
proportion of germination in soil, as compared to filter paper, for
defecated seeds may be related to some of soil characteristics, such
as temperature variation and presence of chemical substances and/or
microorganisms, as suggested by Figueiredo & Perin (1995). These
different patterns show that germination can be affected by factors
associated with both disperser and substrate. Moreover, studies with
other plant species indicate that the germination rate is not affected,
or may even improve, when seeds are sown in soil (Barnea et al.
1990, 1991, Mangan et al. 2010). Future studies should concentrate
in detail the environmental factors that influence germination, in order
to clarify their action mechanisms.
Therefore, we suggest that M. umbellata and M. lancifolia are
important food sources by birds that play a positive effect enhancing
germination of Myrsine. Nevertheless, in order to better establish
the above mentioned conclusions, further experiments need to be
carried out. As suggested by Jordano & Schupp (2000), for similar
assemblages of frugivorous birds, which was also verified in this
work, the seed disperser effectiveness is related to feeding and fruit
handling behaviors and post-foraging patterns of habitat use. The
observations of these components, as well as, total fruit production by
plants and the percentage of that fall under parent trees are stimulated
(e.g. Schupp 1993, Pizo 1997, Christianini & Oliveira 2009).
Acknowledgements
Alice Moralez de Figueiredo for help in germination tests, Luis
Carlos Bernacci (IAC) and Maria Inês Salgueiro Lima (Botany
Department, UFSCar) for help in identifying plant species, and
two anonymous reviewers for providing valuable comments and
suggestions that improved an earlier version of the paper.
References
BARNEA, A., YOM-TOV, Y. & FRIEDMAN, J. 1990. Differential
germination of two closely related species of Solanum in response to
bird ingestion. Oikos 57: 222-228.
BARNEA, A., YOM-TOV, Y. & FRIEDMAN, J. 1991. Does ingestion by
birds affect seed germination? Funct. Ecol. 5: 394-402.
BARNEA, A., YOM-TOV, Y. & FRIEDMAN, J. 1992. Effect of frugivorous
birds on seed dispersal and germination of multi-seeded fruits. Acta
Oecol. 13(2): 209-219.
CBRO 2011. http://www.cbro.org.br/CBRO/listabr.htm (accessed in
04/05/2011).
CHRISTIANINI A.V. & OLIVEIRA P.S., 2009. The relevance of ants as seed
rescuers of a primarily bird-dispersed tree in the Neotropical cerrado
savanna. Oecologia 160: 735-745.
CORNER, E. J. H. 1949. The durian theory of the origin of the modern tree.
Ann. Bot. 13(4): 367-414.
DENNIS A. J., GREEN, R., SCHUPP, E. W. & WESCOTT, D., (eds) 2007.
Frugivory and seed dispersal: theory and applications in a changing world.
Wallingford, UK: CAB International.
FIGUEIREDO, R. A. & PERIN, E. 1995. Germination ecology of Ficus
luschnathiana drupelets after bird and bat ingestion. Acta Oecol. 16(1):
71-75.
FIGUEROA, J. A. & CASTRO, S. A. 2002. Effects of bird ingestion on seed
germination of four woody species of the temperate rainforest of Chiloé
island, Chile. Plant Ecol. 160: 17-23.
FRANCISCO, M. R. & GALETTI, M. 2001. Frugivoria e dispersão de
sementes de Rapanea lancifolia (Myrsinaceae) por aves numa área de
cerrado do Estado de São Paulo, sudeste do Brasil. Ararajuba 9(1): 13-19.
FRANCISCO, M. R. & GALETTI, M. 2002a. Aves como potenciais
dispersoras de sementes de Ocotea pulchella Mart. (Lauraceae) numa
área de vegetação de cerrado do sudeste brasileiro. Revista Brasileira de
Botânica 25(1):11-17.
FRANCISCO, M. R. & GALETTI, M. 2002b. Consumo dos frutos de Davilla
rugosa (Dilleniaceae) por aves numa área de cerrado em São Carlos,
Estado de São Paulo. Ararajuba 10(2): 193-198.
FRANCISCO, M. R. LUNARDI, V.O. & GALETTI, M. 2007. Bird attributes,
plant characteristics, and seed dispersal of Pera glabrata (Schott, 1858),
(Euphorbiaceae) in a disturbed cerrado area. Brazilian Journal of Biology,
67(4): 627-634.
FREITAS, M. F. & CARRIJO, T. T. 2010. http://floradobrasil.jbrj.gov.br/2010/
(accessed in 04/05/2011).
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Ann.
Rev. Ecol. Syst. 13: 201-28.
HOWE, H.F., SCHUPP, E.W. & WESTLEY, L.C. 1985. Early consequences
of seed dispersal for a neotropical tree Virola surinamensis. Ecology
66(3): 781-791.
IZHAKI, I. & SAFRIEL, U. N. 1990. The effect of some Mediterranean
scrubland frugivores upon germination patterns. J. Ecol. 78(1): 56-65.

65
Bird frugivory and germination of Myrsine spp. seeds
http://www.biotaneotropica.org.br/v11n4/en/abstract?article+bn00911042011 http://www.biotaneotropica.org.br
Biota Neotrop., vol. 11, no. 4
JANZEN, D. H., 1970. Herbivores and the number of tree species in tropical
forests. Am. Nat., 104: 501-528.
JORDANO, P. & SCHUPP, E.W. 2000. Seed disperser effectiveness: the
quantity component and patterns of seed rain for Prunus mahaleb.
Ecological Monographs 70(4): 591-615.
JOLY, C. A. & FELIPPE, G. M. 1979. Dormência das sementes de Rapanea
guianensis Aubl.. Revista Brasileira de Botânica 2(1): 1-6.
LEVEY, D. J., SILVA, W. R., & GALETTI, M. (eds) 2002. Seed dispersal
and frugivory: ecology, evolution and conservation. Wallingford, UK:
CAB International.
LORENZI, H. 1992. Árvores Brasileiras: manual de identificação e cultivo
de plantas arbóreas nativas do Brasil. Nova Odessa: Editora Plantarum.
MANGAN, S. A., SCHNITZER, S. A., HERRE, E. A., MACK, K. M. L.,
VALENCIA, M. C., SANCHEZ, E. I. & BEVER, J. D. 2010. Negative
plant-soil feedback predicts tree-species relative abundance in a tropical
forest. Nature 466: 752-755.
MOTTA-JUNIOR, J.C. 1990. Estrutura trófica e composição das avifaunas
de três hábitats terrestres na região central do estado de São Paulo.
Ararajuba1:65-71.
MOTTA-JUNIOR, J. C. & VASCONCELLOS, L. A. S. 1996. Levantamento
de aves do campus da Universidade Federal de São Carlos, estado de
São Paulo, Brasil. Anais do Seminário Regional de Ecologia 7: 159-171.
PAESE, A. 1997. Caracterização e análise ambiental do campus da
Universidade Federal de São Carlos (UFSCar), São Carlos, SP.
Dissertação de Mestrado, Universidade Federal de São Carlos, São Carlos.
PASCOTTO, M. C. 2007. Rapanea ferruginea (Ruiz & Pav.) Mez.
(Myrcinaceae) como uma importante fonte alimentar para as aves em uma
mata de galeria no interior do Estado de São Paulo. Revista Brasileira de
Zoologia 24(3): 735-741.
PAULSEN, T. R. & HÖGSTEDT, G. 2002. Passage through bird guts increases
germination rates and seeding growth in Sorbus aucuparia. Funct. Ecol.
16: 608-616.
PINESCHI, R. B. 1990. Aves como dispersores de sete espécies de Rapanea
(Myrsinaceae) no maciço do Itatiaia, estados do Rio de Janeiro e Minas
Gerais. Ararajuba 1: 73-78.
PIZO, M.A. 1997. Seed dispersal and predation in two populations of Cabralea
canjerana (Meliaceae) in the Atlantic Forest of southeast Brazil. Journal
of Tropical Ecology 13: 559-578.
RAMOS, V. S., DURIGAN, G., FRANCO, G. A. D. C., SIQUEIRA, M. F. &
RODRIGUES, R. R. 2008. Árvores da floresta estacional semidecidual:
guia de identificação de espécies. São Paulo: Edusp/Biota-Fapesp.
ROBERTSON, A. W., TRASS, A., LADLEY, J. J. & KELLY, D. 2006.
Assessing the benefits of frugivory for seed germination: the importance
of the deinhibition effect. Funct. Ecol. 20: 58-66.
SCHUPP, E.W., 1993. Quantity, quality and the effectiveness of seed dispersal
by animals. Vegetatio. 107-108: 15-29.
SILVA, I. A., FIGUEIREDO, R. A. & MATOS, D. M. S. 2008. Feeding visit
time of fruit-eating birds in Cerrado plants: revisiting the predation risk
model. Revista Brasileira de Zoologia 25(4): 682-688.
SOUZA, V. C. & LORENZI, H. 2008. Botânica Sistemática: guia ilustrado
para identificação das famílias de fanerógamas nativas e exóticas no
Brasil, baseado em APGII. Nova Odessa: Plantarum.
VALENTI, M.W., CIANCIARUSO, M.V. & BATALHA, M.A. 2008.
Seasonality of litterfall and leaf decomposition in a cerrado site. Brazilian
journal of Biology 68(3): 459-465.
TRAVESET, A. 1998. Effect of seed passage through vertebrate frugivores’
guts on germination: a review. Perspectives in Plant Ecology, Evolution
and Systematics 1/2: 151-190.
TRAVESET, A., RIERA, N. & MAS, E. 2001. Passage through bird guts
causes interspecific differences in seed germination characteristics.
Funct. Ecol. 15: 669-675.
van der PIJL, L. 1969. Principles of dispersal in higher plants. New York:
Springer-Verlag.
WILLIS, E. O. 1966. Competitive exclusion and birds at fruiting trees in
Western Colombia. The Auk 83:479-480.
Received 18/01/2011
Revised 25/09/2011
Accepted 21/10/2011