Flora 208 (2013) 370–380

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Flora
journal homepage: www.elsevier.com/locate/flora

Melittophily and ornithochory in Tilesia baccata (L.f.) Pruski: An

Asteraceae of the Atlantic Forest understory with fleshy fruits
Rúbia Santos Fonseca a,∗ , Lúcio Antonio de Oliveira Campos b , Milene Faria Vieira a
a
Departamento de Biologia Vegetal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, Brazil
b
Departamento de Biologia Geral, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Many Asteraceae species inhabit open vegetation areas and, as a rule, members of this family have dry,
Received 27 July 2012 wind-dispersed fruits. Tilesia baccata, on the other hand, occurs in forested areas and, differently from all
Received in revised form 27 April 2013 neotropical Asteraceae, has fleshy fruits with ornithochorous characteristics. However, no studies have
Accepted 29 April 2013
confirmed the dispersion by birds or any other aspect of the reproductive biology of this unique Aster-
Available online 13 June 2013
aceae. The present study aims to investigate the reproductive phenology, floral biology and breeding
system and to identify the pollinators and seed dispersers of T. baccata. The study was carried out in a
Keywords:
natural population located in a semideciduous forest (Viçosa, Minas Gerais State), southeastern Brazil.
Endozoochory
Floral biology The reproductive cycle of T. baccata is annual and seasonal, related to precipitation, temperature and
Psycophily day length. The longevity of flowers and capitula depends on the performance of pollinators and dis-
Self-incompatibility persers. Hand pollination tests showed that the species is self-incompatible and therefore dependent on
Synchronous flowering synchronous flowering and pollinator availability. Pollination occurred in the morning, in the period of
pollen availability, and social bees were the major pollinator group. Seeds are dispersed by frugivorous
birds, that swallow the ripe fruits and defecate viable seeds later. Our study confirmed the bird dispersal
of Tilesia baccata seeds and also demonstrates that pollinator activity and fruit removal by birds influence
the magnitude of activity and the intensity of flowering and fruiting.
© 2013 Elsevier GmbH. All rights reserved.

Introduction species with wind-dispersed fruit must be related to species dis-

There are approximately 2024 Asteraceae species in Brazil
(Nakajima et al., 2012) and information on the reproductive
biology is available for only 1.5% of these species. Although
only few species were investigated, the results show different
reproductive mechanisms: flowering can be continuous or concen-
trated in a short period of the year (Espírito-Santo et al., 2003;
Karam et al., 2002; Romero and Vasconselos-Neto, 2005), and
self-compatibility, self-incompatibility, and apomixis or partheno-
genesis were observed (Grombone-Guaratini et al., 2004; Sazima
and Machado, 1983; Werpachowski et al., 2004), as well as differ-
ent pollinators, especially bees (Grombone-Guaratini et al., 2004;
Noronha and Gottsberger, 1980). Additionally, a recent study has
described a novel morphological trait related to reproduction in
the family, with regard to the location of the stigmatic areas of the
ornithophilous species Mutisia speciosa (Bessa et al., 2010).
Studies on fruit dispersal of the predominantly wind-dispersed
Brazilian Asteraceae are not yet available. The predominance of
∗ Corresponding author.
E-mail addresses: rubiafonseca@hotmail.com (R.S. Fonseca), lcampos@ufv.br
(L.A.d.O. Campos), mfvieira@ufv.br (M.F. Vieira).
tribution in open areas (Funk et al., 2005). Among the few species
found in forest environments, Adenostemma brasilianum (Pers.)
Cass. and Tilesia baccata (L.f.) Pruski are common in the under-
story of the secondary Atlantic Forest (Godinho et al., 2011; pers.
obs.) and both exhibit characteristics of fruit dispersal by animals
(Ferreira et al., 2009).
Tilesia baccata has radiate capitula (sensu Bremer, 1994) with
yellow florets, which are flower traits commonly observed in bee
or butterfly-pollinated species, the main pollinators of Asteraceae
(Lane, 1996; Mani and Saravanan, 1999). On the other hand, its
fleshy fruits are devoid of a pappus, odorless, with a dark green,
watery pulp with conspicuous orange paleas – characteristics of
ornithochory (Woodson et al., 1975), but unusual in the fam-
ily. Based on these features, Snow (1981) and Pruski and Sancho
(2004) inferred that T. baccata is the only Asteraceae whose seeds
are ingested and dispersed by birds in the Neotropics. However,
no studies have confirmed these previously published inferences
about endozoochory or addressed any aspect of the pollination of
this Asteraceae.
The present study aims to investigate the reproductive phen-
ology, floral biology and breeding system and to identify the
pollinators of T. baccata. Additional goals were to identify the
species’ fruit consumers and seed dispersers and describe their

0367-2530/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.flora.2013.04.008
 R.S. Fonseca et al. / Flora 208 (2013) 370–380
visiting behavior. Answers to the following questions were sought:
(1) Are the phenophases flowering and fruiting related to abiotic
factors? (2) Does fruit set depend on pollinators? (3) What are the
pollinators? (4) What are the fruit-consuming and seed-dispersing
birds?
Materials and methods
Study area and species
The studies were conducted from August 2007 to March 2009, at
the Estação de Pesquisa, Treinamento e Educação Ambiental Mata
do Paraíso (EPTEAMP, 20◦ 45 07 S, 42◦ 55 31 W, 690 m asl), the
largest forest fragment (195 ha) in Viçosa, State of Minas Gerais,
southeastern Brazil. Its vegetation is part of the Atlantic Forest
domain and, according to the classification of Veloso et al. (1991),
a seasonal semideciduous forest.
According to the Koeppen classification, the climate of Viçosa
is defined as Cwb, i.e., mesothermal with hot and humid summers
and cold and dry winters. The annual averages of rainfall, relative
humidity and temperature for the 1961–1990 period are, respec-
tively, 1221.4 mm, 81%, and 19.4 ◦ C, and the average maximum and
minimum temperature 26.4 ◦ C and 14.8 ◦ C, respectively (DNMET,
1992). The dry and cold season is from April to September, with less
than 60 mm monthly rainfall and temperatures between 11.1 ◦ C
and 26.6 ◦ C. The warm and rainy season begins in October and lasts
until March, with rainfall above 100 mm and monthly tempera-
tures between 15.8 ◦ C and 30 ◦ C. The meteorological data for the
study period were similar to those presented earlier (Fig. 1A). The
day length was longer in the rainy and shorter in the dry season
(Fig. 1A).
Tilesia baccata is widely distributed in Brazil; it occurs in the
Amazon Forest, Caatinga, Cerrado and Atlantic Forest (Magenta,
2012). It is a procumbent shrub, reaches a height of 2–3 m, with
opposite leaves (Ferreira et al., 2009). Its radiate capitula are
arranged in terminal clusters, the receptacle is flat, into which the
numerous florets are inserted (Ferreira et al., 2009). At the study
site, Tilesia baccata grows in partially shaded areas, e.g., along trails
and in the forest understory. Voucher specimens were deposited in
the VIC (No. 31930).
Reproductive phenology
Fifteen randomly marked plants along a trail of 2.5 km (D’eça-
Neves and Morellato, 2004; Fournier and Charpantier, 1975) were
monitored weekly during the reproductive phase and every fort-
night outside this period. The phenophases flower buds, flowering
(open flowers), immature fruits (light green fruits) and mature
fruits (dark green fruits with watery pulp) were evaluated.
The flowering and fruiting patterns were classified according
to Newstrom et al. (1994). The phenological events were quanti-
fied by calculating the activity (% of plants) and intensity (Bencke
and Morellato, 2002a). To calculate the intensity, each phenophase
was scored as absent = 0, little intense = 1, moderate = 2 or very
intense = 3 (modified from Opler et al., 1980). The synchrony of
phenophases was classified according to Bencke and Morellato
(2002b) as: asynchronous (<20% of the plants), little synchronous
(20–60%) and highly synchronous (>60%).
To calculate the relationship between phenological data and
meteorological variables (rainfall, and overall average, monthly
maximum and minimum of temperature, and day length) of the
month of occurrence of the event and the previous three months,
correlation analyses were conducted using Spearman correlation
coefficients (Zar, 1999).
371
To assess whether the distribution of activity and intensity of
the phenophases was seasonal in 2008, circular statistics were
used (Morellato et al., 2010; Zar, 1999). For this purpose, the
months were converted into angles at intervals of approximately
30◦ (0◦ = January, and December = 330◦ ) and the following parame-
ters were calculated: average angle, average date (for phenophases
with significant average angle), vector length and standard devia-
tion of the angle. The significance of the mean angle was evaluated
by the Rayleigh test (Zar, 1999).
Floral biology
Nineteen capitula of 10 individuals were observed from the
opening of the first florets to fruiting (mature fruits). Addition-
ally, the florets of other 20 capitula of five plants were counted
and monitored daily from opening to senescence.
The period of receptivity of the stigmatic lines (sensu Bremer,
1994) was deduced from the color after their exposure: white
lines – receptive and brown lines – non-receptive. The pollen grain
viability was tested with acetic carmine (Radford et al., 1974),
using 25 flower buds in pre-anthesis of five plants (five flower
buds per plant), with counts of 200 grains per bud. The presence
of floral scent was evaluated by the method of odor concentra-
tion, using 10 capitula with open florets (Dafni et al., 2005). The
osmophores were localized using neutral red in 10 previously iso-
lated florets (Dafni et al., 2005; Vogel, 1990). The activity of the
nectary was determined based on the affinity to neutral red at dif-
ferent floral stages. We verified the presence of simple sugars in
the floral secretion collected by visitors, using a glucose enzyme
test band (Tiras de Glicosa® , Alamar Tecno Científica Ltd.; Dafni
et al., 2005).
Breeding system
The usual breeding tests were performed (Dafni et al., 2005)
using the capitulum as pollination unit for: spontaneous self-
pollination, hand self-pollination, agamospermy (sensu Richards,
1997), cross-pollination, and open pollination (control). For
hand self-pollination and cross-pollination, the florets were not
emasculated and fertilized with additional geitonogamous and
xenogamous pollen, respectively.
Open pollination was carried out in two reproductive events:
the first from January to February 2008 and, the second,
November/December 2008–January/February 2009. In the first
event, capitula were exposed to pollinators for the periods prior to
the flowering peak (01/05–15/2008) and at the peak of flowering
(01/20–30/2008). In the second, capitula were exposed to pollina-
tors in the periods prior (11/15–30/2008), during (12/15–30/2008)
and after (01/15–30/2009) the flowering peak. To determine the
association between flowering synchrony and fruit set, Pearson cor-
relation analyses were conducted between the percentage of fruit
set in each period (prior, during and after the flowering peak) and
the average activity of the weekly assessments for each period, in
both reproductive events.
The fruit set was calculated for all breeding tests from the num-
ber of florets per capitulum and the number of fruits produced.
These data were subjected to ANOVA and means compared by the
Tukey test at 5% probability for each reproductive event. The self-
incompatibility index (ISI, Zapata and Arroyo, 1978) was estimated
as the ratio of fruit set after self- and cross-pollination.
Fruits were measured (length and diameter, n = 132) and the
seed quality assessed by the presence (viable seeds) or absence
(non-viable seeds) of the embryo. Germination was tested by pla-
cing the seeds (after removing the fleshy mesocarp) in boxes with
moist filter paper. These seeds were assessed daily for 30 days.
372 R.S. Fonseca et al. / Flora 208 (2013) 370–380

Fig. 1. Meteorological data of Viçosa, Minas Gerais State, southeastern Brazil (A) and activity (continuous line) and intensity (dotted line) of flower buds (B), flowers (C) and
immature (activity, represented by a continuous line with circles) and mature fruits (D) of Tilesia baccata, from August 2007 to March 2009.

Seeds with protrusion of the primary root were considered ger- The flower visitors were captured and specimens were
minated (Labouriau, 1983). deposited in the Regional Museum of Entomology (UFVB), Federal
University of Viçosa.

Flower visitors
The visitation frequency (number of visits per insect species per
total number of visits) was registered on four non-consecutive days,
during the peak of flowering intensity in January 2008. For this pur-
pose, visitors were continuously monitored between 7:00 am and
5:00 pm, totaling 40 h of observation. The insects that touched the
reproductive organs of florets during visitations were considered
effective pollinators and the ones that barely touched these organs
occasional pollinators.
Fruit consumers and seed dispersers
The fruit consumption of birds was monitored between 6:00 am
and 5:00 pm on non-consecutive days during the peak of ripe
fruits, March 10–28, 2008. The observations consisted of ten 5-h
blocks, three between 12:00 pm and 05:00 pm and seven between
6:00 am and 11:00 am, totaling 50 h. Based on the mode of fruit
consumption, the birds were classified as: dispersers – swallow the
fruit; pulp-consuming – peck at the pericarp, removing pieces; and
 R.S. Fonseca et al. / Flora 208 (2013) 370–380 373

seed-predators – crunch the seed, separating it from the pericarp sequence, for up to 10 consecutive days (Fig. 2). The number of open
(Gondim, 2001; Moermond and Denslow, 1985). The bird nomen- florets per capitulum increased until the fourth day, when the peak
clature and systematics were based on the updated list of Brazilian was reached (42% florets). The disc florets remained open for two
birds CBRO (2011). to four days.
To capture some birds, mist nets (2.8 m × 12 m) were set from On the 15th day after the beginning of flowering of the disc flo-
6:00 am to 11:00 am, on three days in February 2009. Each cap- rets, the fruits became visible and flanked by yellow paleas (Fig. 2).
tured bird was kept in a cotton bag for 20 min and then released Throughout fruiting, the initially plane receptacle, became largely
(Blendinger et al., 2011). The stool was collected, observed under a convex. After 55 days, the fruits were mature, i.e., with fleshy,
stereomicroscope and the seeds in it tested for germination. turgid, translucent and dark green mesocarp, each one flanked by
orange palea with stiff apex. Sixty days after the first opening of
disc florets, the un-dispersed fruits adhered to the receptacle and
Results
the paleas had become dry and black (Fig. 2).
The disc florets are protandrous, opening in the morning. During
Reproductive phenology
anthesis, the floret has two sexual phases: staminate and pistillate
(Fig. 3). The staminate phase begins with the dehiscence of anthers
The reproductive phenophases occurred mainly during the rainy
and pollen release into the anther tube of the bud in pre-anthesis,
season, when temperature, day length and rainfall were highest
at around 4:00 am. At 5:00 am, the florets open up, characterized
(Fig. 1). Flower buds were observed during almost the entire study
by the separation of the corolla laciniae, exposure of the anther
period (Fig. 1B). However, the activity and intensity peaked in
apex and elongation of the ovary. At 8:00 am, filament elongation,
January (86.7% and 2.3, respectively) and December 2008 (73.3%
exposing the anther tube, and style elongation occur. At 10:00 am,
and 1.4, respectively).
the style extends further, which initiates the secondary presen-
Flowering was observed from January to February 2008, and
tation of pollen grains to visitors (pollen exposed at the apex of
from November 2008 to March 2009 the first and second repro-
the anther tube). At 12:00 pm, the filaments retract, so that the
ductive event, respectively (Fig. 1C). Activity peaks of 66.6% and
anther tubes return almost entirely into the corolla, and the style
60% were recorded in February and December 2008, respectively,
grows longer, continuing the secondary presentation of pollen. At
i.e., a highly synchronous event in the first flowering and low syn-
this time, most grains are accumulated on the fully exposed style
chrony in the second. Peaks of intensity were recorded in January
branches and the nectary is in intense activity; nectar is accumu-
and December 2008 (1.46 and 1.05, respectively). The mean dura-
lated within the corolla tube (positive test with the glucose enzyme
tion of flowering per plant was 34.3 ± 13.6 days (Min = 6, Max = 43,
test band). The mean pollen viability was 98%. After the presenta-
n = 15), characterizing a brief or intermediate annual phenologi-
tion of pollen grains, the filaments retract even further and anthers
cal pattern; the flowering pattern of the population was annual
return completely into the interior of the corolla tube. During the
intermediate.
staminate phase, the style branches remaine juxtaposed.
Immature fruits were recorded from January to July 2008
The pistillate phase begins at about 2:00 pm, characterized
(Fig. 1D) and from November 2008 onwards. The activity peaked in
by the partial separation of the style branches (Fig. 3); at about
March 2008 and January 2009 (86.7% in both events; Fig. 1D) and
4:00 pm, the style branches are separated horizontally, fully expos-
also showed high synchrony. Peak of intensity occurred in February
ing the stigmatic lines (four lines, two per branch; sensu Bremer,
2008 and 2009 (2.1 and 1.9, respectively). Fruiting of each plant
1994), located along the edges of the branches, white and recep-
lasted 94.2 ± 33 days, following an annual extended pattern at the
tive. At that time, no pollen is available to visitors and therefore the
individual and population level.
pollination of florets in the pistillate phase occurs in the morning
Mature fruits were recorded from March to May 2008 and from
of the second day, when the florets are receptive again and have
December 2008 onwards (Fig. 1D). The peaks of activity and inten-
nectar.
sity occurred in March 2008 (53.3% and 1.0, respectively) and in
The pistillate phase of the pollinated florets ends at 4:00 pm
January 2009 (13.3% and 0.2, respectively, Fig. 1D), both events in
of the second day, when the style branches are completely curled
low synchrony. Activity and intensity were lower than reported for
up (Fig. 3), stiff, with brownish, unreceptive stigmatic lines, the
immature fruits in the same period. Ripe fruits were found on each
nectary is inactive, and the ovary augmented, indicating the onset
plant for 34 ± 19.5 days, corresponding to a brief or intermediate
of fruiting. In unpollinated florets, the pistillate phase was extended
annual pattern at the individual level and an intermediate pattern
for up to four days.
at the population level.
In the flowers in both phases, no scent was perceptible, although
The activity and intensity of the phenophases were related to
the neutral red had stained the style branches, apices of the corolla
meteorological variables. All phenophases were significantly cor-
laciniae, apical appendage of the anthers and the nectary, indicating
related with abiotic variables in the month of occurrence and/or in
secretory activity in these structures.
previous months (Table 1).
The Rayleigh test (p < 0.01) and length of the average angle
Breeding system
(r ≥ 0.71) showed concentrated seasonal and synchronous distri-
bution of the flower buds, flowering, immature and mature fruit in
The results showed that T. baccata is self-incompatible
the population (Table 2). The length of the average angle (r) showed
(ISI = 0.02), non agamospermous and therefore dependent on pol-
higher temporal concentration of intensity than of activity. More-
lination for fruit set (Table 3). The low fruit set obtained by
over, for all phenophases except immature and mature fruit, the
hand-selfing (Table 3) was probably caused by accidental pol-
average date of activity preceded that of intensity.
lination (contamination) with pollen from other plants during
manipulation of the capitula.
Floral biology In the first reproductive event, fruit set resulting from open
pollination at the flowering peak was highest and differed signif-
The capitula had on average 8.9 (SD = 2.7) neuter ray florets, and icantly from fruit set resulting from open pollination in the period
on average 75 (SD = 21.3) perfect disc florets. Anthesis of the ray prior to the flowering peak and from cross-pollination (F = 4.628,
florets occurred two days before that of the disc florets and lasted p = 0.013; Table 3). In the second event, fruit set was higher during
up to nine days. The disc florets opened in groups, in a centripetal the flowering peak period than before and after the flowering peak,
374 R.S. Fonseca et al. / Flora 208 (2013) 370–380

Fig. 2. Dynamics of the disc floret opening and longevity of the capitulum Tilesia baccata from the 1st (anthesis of the first florets) to the 60th day (end of the fruiting period;
the fruits shrivel). Centripetal opening of florets within 10 days and capitula with developing fruits flanked by bracts (from the 15th day after beginning of floret anthesis)
until maturity of the seeds with fleshy pericarp (on the 55th day, when seeds were dispersed.). The drawings show longitudinal sections and the pictures capitula seen from
above.

Fig. 3. Anthesis of Tilesia baccata flowers: staminate phase of flower bud, from pre-anthesis (4:00 am) to pollen exposure on the branches of the juxtaposed style (12:00 pm),
on the first day of anthesis; pistillate phase: from the beginning of the style branch separation (2:00 pm of the first day of anthesis) to the total exposure of the stigmatic
lines (4:00 pm of the second day). an = anthers, co = corolla, fi = filament, ne = nectary, ov = ovary, sb = style branches.
 R.S. Fonseca et al. / Flora 208 (2013) 370–380 375

Table 1
Significant Spearman correlation coefficients (p ≤ 0.05) between the phenophases of Tilesia baccata and the meteorological data of the observation period, for the month of
occurrence of the phenophase (0) and the previous three months (1–3), in Viçosa, southeastern Brazil. FB = flower buds, Fl = flowers, I Fr = immature fruits; M Fr = mature
fruits.

Indices Meteorological data Month FB Fl I Fr M Fr

Activity Rainfall 0 0.50 0.49 0.49 –

1 0.49 0.61 0.67 0.57
2 0.63 0.46 0.77 0.68
3 – – 0.78 0.63
Minimum temperature 0 0.54 0.58 0.59 0.45
1 0.56 0.47 0.77 0.67
2 0.53 – 0.80 0.65
3 – – 0.75 0.64
Mean temperature 1 0.44 – 0.59 0.53
2 0.61 – 0.68 0.54
3 0.53 – 0.82 0.56
Maximum temperature 3 0.51 – 0.64 –
Day length 0 – 0.71 – –
1 0.69 0.60 0.69 0.49
2 0.54 0.53 0.86 0.64
3 0.46 – 0.81 0.72

Intensity Rainfall 0 – 0.52 0.49 –

1 – 0.61 0.69 0.60
2 – 0.45 0.81 0.69
3 – – 0.77 0.64
Minimum temperature 0 – 0.56 0.62 0.48
1 – 0.47 0.79 0.69
2 – – 0.83 0.65
Mean temperature 1 – – 0.61 0.53
2 – – 0.72 0.52
3 – – 0.79 0.55
Maximum temperature 3 – – 0.60 –
Day length 0 0.51 0.71 – –
1 0.53 0.60 0.71 0.51
2 – 0.52 0.87 0.65
3 – – 0.81 0.71

Table 2
Results of circular statistic analysis for the occurrence of seasonality on the activity and intensity of the reproductive phenology of Tilesia baccata in Viçosa, southeastern
Brazil.

Variable Buds Flowers Immature fruit Ripe fruit

Activity Intensity Activity Intensity Activity Intensity Activity Intensity

Mean angle (a) 2.075 15.899 12.899 22.239 55.783 54.871 82.781 82.597
Mean date 2nd January 16th January 13th January 23rd January 26th February 25th February 24th March 24th March
Length of mean vector (r) 0.84 0.96 0.89 0.97 0.71 0.95 0.86 0.97
Circular deviation 34.181 16.495 27.447 14.528 47.296 17.576 30.904 15.403
Rayleigh test (p) <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001

but only differed significantly from fruit set in the period prior
to the flowering peak (F = 6.816, p = 0.003; Table 3). Significant
correlations were observed between the percentage of fruit set
from open pollination in different periods and the average activity
(synchrony) of each period (r = 0.96, p = 0.0090).
Mean fruit length and diameter are 0.45 cm and 0.38 cm, respec-
tively. The embryos of most seeds from open pollination (92.2%,
n = 228) and cross-pollination (86.4%, n = 146) looked healthy and
shiny white, characterizing them as viable. The percentage of
germination of open-pollinated (n = 200) and cross-pollinated
seeds (n = 200) was low (4% and 6%, respectively).
Flower visitors
We recorded 379 visits of 29 insect species to the T. baccata
florets. The visitors were of the orders Hymenoptera (bees, ants

Table 3
Results of pollination tests in two flowering events (first: January–February 2008, and second: November 2008–February 2009) of Tilesia baccata, in Viçosa, southeastern
Brazil. OP = open pollination.

Flowering event Tests Capitula Florets number of structures Fruits Reproductive success %*

1st Spontaneous selfing 21 1851 0 00.0

Agamospermy 21 1673 0 00.0
Hand self-pollination 15 1202 8 00.6
Cross-pollination 16 1058 319 30.0a
OP (prior to the flowering peak) 14 1180 324 27.5a
OP (flowering peak) 25 1846 772 41.8b

2nd OP (prior to the flowering peak) 14 946 86 09.1a

OP (flowering peak) 14 1113 277 24.8b
OP (after the flowering peak) 07 444 60 13.5a,b
*
Means followed by the same letter in the last column in each flowering event did not differ statistically by the Tukey test at 5% probability.
376 R.S. Fonseca et al. / Flora 208 (2013) 370–380

Table 4
Flower visitors of Tilesia baccata, their frequency (n = 379 visits), food resource used and pollination category. N = nectarivorous; PF = polliniferous; Ph = phytophagous;
EP = effective pollinator, OP = occasional pollinator.

ORDER Frequency (%) Food resource used Pollination category

Family
Subfamily
Species

COLEOPTERA
Curculionidae
Morpho-species 1 0 Ph OP

DIPTERA
Morpho-species 1 1.32 N OP
Morpho-species 2 0 N OP

HYMENOPTERA
Apidae
Apinae
Apis mellifera (Linnaeus 1758) 50.92 N–PF EP
Melissoptila vulpecula (Bertoni & Schrottky 1910) 3.96 N EP
Melipona quadrifasciata (Lepeletier, 1836) 15.04 N–PF EP
Paratetrapedia (Paratetrapedia) fervida (Smith 1879) 0 N EP
Trigona spinipes (Fabricius 1793) 10.55 N–PF EP
Halictidae
Halictinae
Augochlora patens (Vachal 1909) 2.64 N–PF EP
Neocorynura oiospermi (Schrottky 1909) 0 N–PF EP
Megachilidae
Megachilinae
Megachile (Acentris) eburneipes (Vachal 1904) 2.90 N–PF EP
Megachile (Autromegachile) susurrans (Haliday 1836) N–PF EP
Megachile (Ptilosarus) cfr. bertonii (Schottky 1908)
Formicidae
Camponotussp. 0 ?
Acromyrmexsp. 0 ?
Vespidae
Eumenidae
Morpho-species 1 1.85 N EP

LEPIDOPTERA
Hesperiidae
Hesperiinae
Morpho-species 1 0.53 N OP
Pyrginae
Autochthon sp. 0 N OP
Urbanus teleus (Hübner 1821) 0.79 N OP
Nymphalidae
Heliconinae
Heliconius erato (Linnaeus 1764) 0 N OP
Heliconius ethilla (Godart 1819) 0 N OP
Ithomiinae
Hypothyris euclea (Haensch 1905) 0 N OP
Ithomia agnosia (Hewitson 1852) 0.26 N OP
Mechanitis polymnia (Linnaeus 1758) 0 N OP
Nymphalinae
Anartia amathea (Eschscholtz 1821) 0 N OP
Tegosa claudina (Eschscholtz 1821) 0.53 N OP
Pieridae
Coliadinae
Eurema albula (Cramer 1775) 0.53 N OP
Riodinidae
Riodininae
Synargis phillone (Godart 1824) 0.26 N OP

ORTHOPTERA
Gryllidae
Morpho-species 1 7.92 PF ?

and wasps), Lepidoptera (butterflies), Diptera (flies), Coleoptera
(beetles) and Orthoptera (grasshoppers): Table 4. The visits
occurred mainly in the morning, between 10:00 am and 11:00 am,
when nectar and pollen is available (see floral biology); visits were
sporadic after 3:00 pm.
The number of bee and butterfly species was high (Table 4), but
the bee visitation frequency (87.0%) was higher than of butterflies
(2.9%), demonstrating the fundamental role bees play in the polli-
nation of T. baccata. Butterflies are therefore considered occasional
pollinators (Table 4).
The exotic bee Apis mellifera and the native Melipona quadrifas-
ciata and Trigona spinipes accounted for 76.5% of bee visits. Apis
mellifera visits were concentrated in two periods, one in the morn-
ing and another in the early afternoon; the visitation frequency of
 R.S. Fonseca et al. / Flora 208 (2013) 370–380
Table 5
Birds that feed on fruits and/or seeds of Tilesia baccata: modes of fruit intake and ecological activity. G = grinds the seed, P = pecks the pulp, S = swallows the fruit.
Famíly/species
Thraupidae/Tangara cayana (Linnaeus, 1766)
Tangara cyanoventris (Vieillot, 1819)
Tachyphonus coronatus (Vieillot, 1822)
Trochilidae/Thalurania glaucopis (Gmelin, 1788)
Parulidae/Basileuterus culicivorus (Deppe, 1830)
Pipridae/Manacus manacus (Linnaeus, 1766)
Psittacidae/Forpus xanthopterygius (Spix, 1824)
a
Alves and Vecchi (2009).
b
Parrini et al. (1999).
Melipona quadrifasciata peaked in the morning and Trigona spinipes
visited especially late in the morning, when other species were
uncommon.
The visitation behavior of these bees was similar: they are land-
ing directly on the disc florets, move about for 15 s, removing pollen
or nectar, and fly to another capitulum of the same plant. During
nectar collection, the bees touched the juxtaposed style branches
with their head, abdomen and legs, which contain pollen grains in
the staminate flower phase, and the open branches, including the
stigmatic lines in the pistillate phase, pollinating them. Pollination
is facilitated by the large amount of pollen deposited on the bodies
of these insects.
The foraging butterflies landed directly on the disc or ray flo-
rets; they accessed the disc florets in search of nectar. Pollen was
observed on their feet, which eventually came into contact with the
reproductive flower structures. Other infrequent visitors touched
the stigmatic lines occasionally.
Fruit consumers and seed dispersers
Seven bird species belonging to five families were observed
in 45 visits for fruit consumption (Table 5). Based on the mode
of fruit consumption, these birds could be differentiated in:
fruit-dispersing (passeriform: Thraupidae, Parulidae and Pipridae),
fruit-consuming (hummingbirds: Trochilidae), and seed-predator
birds (parrots: Psittacidae). Therefore, only the passerines behaved
as dispersers, since they swallow the whole fruits and defecate
seeds, which germinate at a rate of 20% (n = 15).
The most frequent bird was Basileuterus culicivorus (40% of all
visits), followed by Tangara cayana (20%) and Tachyphonus corona-
tus (15.5%). All Tilesia baccata plants were growing very close to
another ornithochorous plant, Schinus terebinthifolius Raddi (Anac-
ardiaceae), such that the branches of the first were supported by
the second. During foraging, the passerines perched first within
the canopy of S. terebinthifolius and collected its fruits. Then, they
landed on the branches of T. baccata and ate its fruits without dam-
aging the flanking paleas.
Basileuterus culicivorus was the first bird feeding on the fruits,
between 06:30 am and 08:00 am. Solitary T. cayana individuals,
male or female, were observed from about 8:30 am to 9:30 pm. T.
coronatus was seen visiting from 08:00 am to 09:00 am. Manacus
manacus was also observed at about 8:00 and Tangara cyanoven-
tris was the last species seen in the morning, between 09:00 am
and 11:00 am. On rainy days, in the short periods without rain,
different passerine species visited T. baccata at the same time. On
this occasion only, agonistic interactions were observed between
B. culicivorus and female M. manacus.
During foraging, birds would occasionally scatter mature fruits
on the ground under the plant and ants (Atta sp.) were observed car-
rying those fruits away, indicating a myrmecochorous secondary
dispersion. The mature fruits that were not removed from the capit-
ula dried and dropped on the ground by gravity. However no ants
were observed carrying them away.
377
Popular name Mode of ingestion Activity
Burnished-buff Tanagera S Disperser
Gilt-edged Tanagerb S Disperser
Ruby-crowned Tanagera S Disperser
Violet-capped Woodnympha P Pulp-consumer
Golden-crowned Warblera S Disperser
White-bearded Manakinb S Disperser
Blue-winged Parrotleta G Predator
The pulp-consuming and seed predator birds, respectively,
Thalurania glaucopis and Forpus xanthopterygius (Table 5), were
observed only once. The individual of T. glaucopis pierced the
pericarp of mature fruits with its beak, and five F. xanthoptery-
gius individuals crunched the seeds of immature and mature
fruits.
Discussion
The annual and seasonal patterns of reproductive phenophases
of T. baccata during the rainy season are similar to those of most
species of the semideciduous forests (Morellato, 1992). The signifi-
cant correlations between the activity and intensity of reproductive
phenophases and meteorological data showed that the time and
abundance of flowering and fruiting were related to rainfall, tem-
perature and day length. Our results also suggest that the dry season
prevents the sexual reproduction, because in a coastal environment
in Brazil, with a weakly seasonal climate, T. baccata flowering was
observed to be continuous (Albuquerque et al., 2007).
Day length was the main modulating factor of phenological
expression, since it influenced all phenophases. Other studies
also demonstrated that day length is an important factor regu-
lating phenology in tropical communities (Morellato et al., 2000;
Zimmerman et al., 2007). According to Rubim et al. (2010), this vari-
able, unlike temperature and rainfall, is not stochastic and therefore
the best predictor of phenophases.
The correlations between the activity and intensity of flower
buds, flowering and fruiting with the abiotic variables of up to
three months earlier, as observed in this study, suggest that this is
the period required from the stimulus to the phenophase expres-
sion, characterizing delay in its manifestation. Similar results were
found by Paise and Vieira (2005), who observed a lag of up to
two months between variations in temperature and precipita-
tion and detectable responses in the fruiting of animal-dispersed
species.
In T. baccata, no simultaneity between the activity and inten-
sity peak of flowering was recorded in the first reproductive event.
This result, along with the higher concentration of the intensity
peak than of the activity peak shown in the circular analysis, indi-
cates variation in the distribution of flowering peaks during the
reproduction period. This non-simultaneity may be due to differ-
ent responses to modulating factors, since some authors interpret
the activity peak as related to endogenous characteristics and abi-
otic factors (Bencke and Morellato, 2002a; Schaik et al., 1993),
but the intensity peak to biotic factors, because it determines the
abundance of resources (Bencke and Morellato, 2002a). In fact,
in T. baccata, flower abundance seems to be stimulated by abi-
otic factors (significant correlation) and regulated by biotic factors,
since flower longevity is greater in the absence of pollinators. This
absence makes the capitula longer-living and consequently extends
flowering. Similarly, the presence of mature fruits was clearly influ-
enced by fruit removal by dispersers, resulting in low activity and
intensity of this phenophase.
378 R.S. Fonseca et al. / Flora 208 (2013) 370–380
These considerations highlight the importance of combining
qualitative (activity) and semi-quantitative methods (intensity) in
phenological investigations. By this combination, the population
synchrony, determined by the activity of phenophases, can be asso-
ciated to the availability of resources, as stated by Bencke and
Morellato (2002a).
The high synchrony of flowering and fruiting observed in T.
baccata is of utmost importance for its reproduction, since the
species is self-incompatible and with zoochorous dispersion. The
ecological consequence of the synchrony of these phenophases
can be explained by different hypotheses: higher chances of cross
pollination, which is the compulsory reproductive system in self-
incompatible species (Opler et al., 1976); reduction of time and
energy spent by pollinators to visit different plants (Heinrich and
Raven, 1972); greater attraction of pollinators (Augspurger, 1981;
Gentry, 1974) and dispersers (Poulin et al., 1999), besides a reduced
proportion of predated seeds (Augspurger, 1981).
In addition, the long-lived capitula of T. baccata also seem to
favor their reproduction. They lasted about 55 days from anthe-
sis of the first floret to fruit maturation, unlike shorter life-times
observed in other Asteraceae (up to 20 days, Eiterer, 2005; Godinho,
2007). This longevity must be related to the dynamics of open-
ing of various florets of the capitulum, the longevity of each floret
(2–4 days) and mainly to the endozoochorous dispersal mecha-
nism, which involves, besides the formation of a fleshy mesocarp,
the growth of paleas, adjacent to the fruit.
In radiate capitula such as T. baccata, neuter ray florets (about
9 florets) are brightly colored and have the function of attracting
pollinators, as suggested by Stuessy et al. (1986). The disc florets, on
the other hand, have all the other reproductive functions, including
nectar production. The morning anthesis, the protandry, the sec-
ondary pollen presentation and the staminate and pistillate flower
phases of these flowers are common characteristics of Asteraceae
(e.g., Cerana, 2004; Jones, 1976; Mani and Saravanan, 1999; Proctor
and Yeo, 1973; Pruski and Sancho, 2004).
The resources nectar and pollen in T. baccata flowers are typ-
ical of the Asteraceae family (Mani and Saravanan, 1999). Nectar
was the main source removed by pollinators, while pollen adhe-
sion to their bodies was a result of visiting in search of nectar.
The gradual exposure of the pollen, aside from preventing wastage,
promotes pollen transfer between flowers of different plants (Yeo,
1993), which in T. baccata is performed mainly by social bees.
The inter-plant pollen flow is essential in view of the obligatory
xenogamy of the studied species, the common reproductive sys-
tem of Asteraceae (Hiscock and Tabah, 2003; Hong et al., 2007;
Roitman, 1995).
The highest fruiting obtained by open pollination at the peak
of two flowering events of T. baccata showed the effective per-
formance of the pollinators and the influence of synchronous
flowering in the population. Augspurger (1981), who studied the
effects of flowering synchrony on fruit set in Hybanthus prunifolius
(Schult). Schulze (Violaceae), also found higher reproductive suc-
cess at the peak of flowering, which is mainly due to the attraction
of pollinators, since this species is self-compatible, but not autog-
amous. Importantly, the pollen flow between florets of different T.
baccata plants is a consequence of the morning activity of pollina-
tors (mainly from 10:00 am to 11:00 am), which coincides with the
opening, nectar availability and staminate phase of flowers, when
pollen is exhibited.
The lower percentage of fruiting obtained in cross-pollination
(30%) compared to that obtained at the peak of flowering (41.8%)
may be due to the manipulation of flowers on at least eight consec-
utive days to pollinate all flowers. For Roitman (1995), the lower
fruit set after hand-pollination is due to the difficulty of pollinating
all flowers of a capitulum. Moreover, chances of pollen deposition
on the stigma are greater in open pollination, due to the numerous
visitations by pollinators throughout the flower life (according to
Zapata and Arroyo, 1978).
That bees are the main pollinators, as observed, was an expected
result, according to Free (1993) and Lane (1996). These authors
commented that solitary bees are the most important pollinators
of the Asteraceae family, different from the findings in this study.
Our results showed that social bees, including the introduced A.
mellifera, were frequent visitors and have a higher potential to act
as pollinators in view of their visitation behavior. Solitary bees
(e.g., the three species of Megachile) were also observed on T. bac-
cata flowers, but with a very low frequency. These observations,
together with the comments of Free (1993) and Lane (1996), raise
the question of a possible competition, which may have caused a
displacement of the native pollinator group of T. baccata. Thus, in
areas with anthropogenic vegetation changes, as it is the study area,
social bees that live in perennial hives with large numbers of indi-
viduals may have dominated the resources previously exploited by
solitary bees. Studies in areas with well-preserved vegetation could
clarify this issue.
The melittophilous morphological characteristics of the T. bac-
cata flowers did not prevent visitations from other insect groups,
especially of butterflies. When these Lepidoptera feed on the
nectar, pollen adheres to their bodies, which makes them poten-
tial pollinators as well (cf. Roitman, 1995). Mani and Saravanan
(1999) considered psychophily to be the main flower feature
of Asteraceae, contrary to Free (1993) and Lane (1996). These
differences may be a result of the flower characteristics the
melittophilous and psychophilous species have in common: nec-
tariferous tubular, colorful flowers, organized in capitula, forming
a landing platform. In this case, further research similar to this
work is recommended, involving the identification, behavior and
frequency of visits for each insect group in order to define the main
pollinators.
The ornithochory of T. baccata, inferred by Snow
(1981) and Pruski and Sancho (2004), was confirmed. The
ornithochory–endozoochory characteristics of the fruits, i.e., no
pappus, brightly colored (orange) paleas that attract birds and a
fleshy mesocarp, which is ingested by seed dispersers, are rare
in the family (van der Pijl, 1982). The black and hard endocarp,
according to Woodson et al. (1975), together with the fleshy
mesocarp, are attributes of the drupe fruits, in contrast with the
cypsela, dried fruit, of other species of anemochoric or epizoo-
choric Asteraceae. The importance of a secondary myrmecochoric
dispersal of T. baccata seeds, first observed in this study, should be
evaluated because of its sporadic nature.
The passerine dispersers of T. baccata constitute a group of fru-
givorous birds typical of secondary tropical forests, according to
Fadini and Marco-Júnior (2004). In the process of seed dispersal of
T. baccata, the seeds seem to be defecated by these birds at a certain
distance from the mother plant, because no seedlings grew close to
the adult plants.
The interaction between T. baccata and S. terebinthifolius, sharing
the same habitat and seed dispersers, seems to be advantageous,
since the synchronous fruiting of these plants increases the chances
of attracting common dispersers, as similarly reported by Poulin
et al. (1999) for Psychotria (Rubiaceae) species of the understory.
This partnership is particularly interesting for T. baccata, since
according to Stapanian (1982) and Sargent (1990), the aggregated
fruiting benefits understory shrubs (e.g., the species studied) that
tend to produce less fruit than tree species (e.g., S. terebinthifolius).
Acknowledgements
The authors are indebted to the National Council for Scientific
and Technological Development – CNPq, for a Master’s scholarship
 R.S. Fonseca et al. / Flora 208 (2013) 370–380
and a competitive grant of the first and third author, respectively.
This work is part of the master’s thesis of the first author at the
Federal University of Viçosa, Department of Plant Biology.
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