Revista Brasil. Bot., V.33, n.2, p.207-213, abr.-jun. 2010
Floral attributes, ornithophily and reproductive success of Palicourea
longepedunculata (Rubiaceae), a distylous shrub in southeastern Brazil
CELICE ALEXANDRE SILVA1, MILENE FARIA VIEIRA2,3 and CIBELE HUMMEL DO AMARAL2
(received: September 04, 2008; accepted: March 11, 2010)
ABSTRACT – (Floral attributes, ornithophily and reproductive success of Palicourea longepedunculata (Rubiaceae), a
distylous shrub in southeastern Brazil). Floral attributes, ornithophily and reproductive success of Palicourea longepedunculata
Gardner were studied in a fragment of the Atlantic Forest in southeastern Brazil. This species is a distylous shrub that occurs in
wet forest understory. In an area of seven hectares, the frequency of the morphs was found at a ratio very close to the expected
1:1. The flowering period extended from March (end of the rainy season) to September, with a flowering peak in May/June
(dry season). The floral attributes of the morphs were similar, i.e., the flowering of the floral morphs was synchronous, and the
numbers of inflorescences per plant, flowers per inflorescence, open flowers per inflorescence and per plant of the floral morphs
were similar. The pollen grains of the morphs presented similar sizes, as well as their viability. Palicourea longepedunculata
is self-incompatible and mainly pollinated by Phaethornis rubber (Aves, Trochilidae), which accounted for 62.07% of the
foraging bouts. The reproductive success was similar between morphs: the numbers of fruits per inflorescence were, in average,
85.7 (L-morph) and 107.1 (S-morph) and there was no significant difference in the production of seeds (one or two) per fruit
between the morphs. Fruits were similar in height, width and weight.
Key words - Atlantic forest, flowering phenology, hummingbirds, Palicourea, Phaethornis
RESUMO – (Atributos florais, ornitofilia e sucesso reprodutivo de Palicourea longepedunculata (Rubiaceae), um arbusto
distílico no sudeste do Brasil). Os atributos florais, a ornitofilia e o sucesso reprodutivo de Palicourea longepedunculata Gardner
foram estudados em fragmento de Floresta Atlântica do sudeste do Brasil. Essa espécie é um arbusto distílico que ocorre em
sub-bosque úmido de florestas. Em uma área de sete hectares, os indivíduos dos morfos brevistilo e longistilo foram encontrados
em uma taxa muito próxima da esperada, 1:1. O período de floração estendeu-se de março (final da estação chuvosa) a setembro,
com um pico em maio/junho (estação seca). Os atributos florais dos morfos foram similares, isto é, a floração dos morfos florais
foi sincronizada e os números de inflorescências por planta, de flores por inflorescência, de flores abertas por inflorescência
e por planta dos morfos foram semelhantes. Os grãos de pólen dos morfos apresentaram tamanho e viabilidade similares.
Palicourea longepedunculata é autoincompatível e polinizada principalmente por Phaethornis ruber (Aves, Trochilidae), que
realizou 62,07% das ondas de forrageamento. Os morfos apresentaram sucessos reprodutivos similares: os números de frutos
por inflorescência foram, em média, 85,7 (longistilo) e 107,1 (brevistilo) e não houve diferença significativa na produção de
sementes (uma ou duas) por fruto entre os morfos. Os frutos foram similares em altura, largura e peso.
Palavras-chave - beija-flores, fenologia de floração, Floresta Atlântica, Palicourea, Phaethornis
Introduction
Palicourea Aublet comprises about 200 species
of shrubs and small trees found throughout the moist
and wet Neotropics (Taylor 1997). The flowers have
tubular corolla and are odorless, brightly colored and
hummingbird-pollinated (e.g. Feinsinger & Busby 1987,
Feinsinger et al. 1988, Ree 1997, Contreras & Ornelas
1999, Coelho & Barbosa 2003, Lau & Bosque 2003,
Ornelas et al. 2004a, b, Mendonça & Anjos 2006, Santos
1.
2.
3.
Universidade Estadual de Mato Grosso, Centro de Pesquisas,
Estudos e Desenvolvimento Agro-Ambientais (CPEDA) câmpus
de Tangará da Serra, 78300-000 Tangará da Serra, MT, Brazil.
Universidade Federal de Viçosa (UFV), Departamento de Biologia
Vegetal, 36570-000 Viçosa, MG, Brazil.
Corresponding author: mfvieira@ufv.br
et al. 2008). Palicourea longepedunculata Gardner is a
distylous shrub found in the forest understory in southern
Brazil (Taylor 1997, Pereira et al. 2006).
Distylous species are commonly self-incompatible
(further details in Barret et al. 2000), thus depending on
intermorph pollination through pollinators (legitimate
pollination) for fruit production. The reproductive
success of the long-styled (hereafter L-morph) and the
short-styled (hereafter S-morph) morphs are associated
to several factors: the incompatibility level of the morphs
in different populations (Sobrevila et al. 1983), the
distribution pattern of the morphs (Wesselingh et al.
1999) and their proportion in the population (Sobrevila
et al. 1983, Pailler & Thompson 1997) and the floral
attributes (e.g. the number of inflorescences and open
flowers) of each morph, which contribute to attract floral
visitors (Ornelas et al. 2004b). The floral dimorphism,
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C. A. Silva et al.: Floral attributes, ornithophily and reproductive success of Palicourea longepedunculata
i.e., differences in the length of the corolla, style, stigma
and stamen and in the pollen sizes between the morphs,
common in distylous species, is another factor that may
influence the reproductive success of the morphs (Lloyd
1979, Ornelas et al. 2004a, González et al. 2005).
Studies on the reproductive success of morphs
of distylous Palicourea species are rare. Sobrevila
et al. (1983) demonstrated that fruit and seed set of
P. fendleri Standl. and P. petiolaris Kunth are highly
variable among the different populations. Wesselingh
et al. (1999) stated significant differences in the natural
fruit set between the P. brenesii Standl. floral morphs:
the S-morph fruit set were higher than in L-morph.
Intermorph pollinations of P. padifolia (Willd. ex Roem.
& Schult.) C.M. Taylor & Lorence resulted in significant
difference in fruit production between floral morphs,
independent of the pollination treatment and pollinator
species (hummingbirds); S-morph flowers developed
proportionally almost twice as many fruits as L-morph
flowers (Ornelas et al. 2004a). On the other hand,
González et al. (2005) observed a similar fruit production
in P. padifolia morphs, in five years of evaluation at the
same study site as Ornelas et al. (2004a).
The purpose of this study was to investigate aspects
of reproductive biology of P. longepedunculata to answer
to the questions: 1) Are the floral attributes of the morphs
similar? 2) Which are the visiting hummingbirds? 3) Are
the fruit and seed sets of the morphs similar?
Material and methods
Study site and species – Fieldwork was carried out in 2004
and 2005, in the forest Mata do Paraíso (20°48’07” S and
42°51’31” W, 680 m asl), a preservation area located in
the municipality of Viçosa, Minas Gerais, Brazil. In the
19th century, after deforestation, the Mata do Paraíso was
replaced by coffee plantations and pastures. Nowadays, a
secondary succession forest (Castro 1980) covers an area of
194.36 ha, where P. longepedunculata grows in the shaded
areas. The natural vegetation of Mata do Paraíso is part of the
Atlantic Forest region (Rizzini 1992), in which the climate is
characterized by a dry and cool (April to September) followed
by a rainy and hot season (October to March). The annual
average rainfall in this area varies from 1.300 to 1.400 mm,
and the annual average temperature is 19 °C.
Palicourea longepedunculata has elongate and
pendulous inflorescences; the central axis and branches are
red with yellow-reddish flowers (figure 1). The anthesis lasts
24 hours (Pereira et al. 2006). The carnose and purple fruits
are dispersed by birds (Tachyphonus coronatus Vieillot, 1822)
and have one or two seeds. In the Mata do Paraíso, the style
and stamen length of P. longepedunculata differ in S-morph
and L-morph flowers and are reciprocally positioned; there
Figure 1. Phaethornis ruber visiting an inflorescence of
Palicourea longepedunculata, in a forest fragment in Viçosa,
Minas Gerais State, southeastern Brazil. Note pollen (white
spot) in the distal region of the bill.
are significant differences in the length of the corolla and
stigma between the floral morphs (longer in the S-morph); and
incompatibility reaction after illegitimate in vitro pollinations
(Pereira et al. 2006). Voucher specimen is deposited in the
VIC herbarium (Pereira & Basílio 61)
Frequency of morphs and floral attributes – All individuals
present in an area of seven hectares were sampled and
classified as S-morph or L-morph. The floral attributes: the
number of inflorescences per plant, number of open flowers
per inflorescence and number of open flowers per plant in
22 S-morph and 17 L-morph plants were weekly monitored
during the flowering season in 2004, and 10 plants per
morph in 2005. Besides, the number of flowers produced in
24 inflorescences was counted; three inflorescences of four
plants per morph were used. To verify differences between
the inflorescence lengths, one inflorescence of 10 plants per
morph was measured (from the first to the last flowers).
To verify pollen grain viability, five buds per plant in
pre-anthesis were collected from five plants in each morph.
The anthers of each bud were macerated in a drop of acetic
carmine on a slide (Radford et al. 1974). Up to 200 grains per
slide were counted. The diameter of pollen grains of the floral
morphs was measured. Five buds per plant in pre-anthesis
Revista Brasil. Bot., V.33, n.2, p.207-213, abr.-jun. 2010
of five plants of each morph were used for this purpose.
The anthers of each bud were macerated in a drop of acetic
carmine on a slide (Radford et al. 1974). Images of eight
grains per slides (200 grains per morph) were captured using
a Olympus AX70 microscope with a 40X lens, zoom 1.0.
Measures were obtained using Image-Pro Plus software.
Breeding system – Controlled pollinations were performed
in vivo (details in Bawa & Beach 1983), with a total of 80
flowers: 11 flowers for S×S (self-pollination), 20 for S×S
(intramorph), 14 for L×L (self), 14 for L×L (intramorph), 07
for S×L (intermorph) and 14 for L×S (intermorph). To evaluate
the fruit set under natural conditions, 12 inflorescences per
morph were used as control. In this case, the fruits produced
per inflorescence were counted and the percentage of fruit
set calculated considering the mean number of flowers per
inflorescence per morph.
To test the possibility that seedless fruits (see results)
are a result of interspecific pollination, 13 L-morph and
nine S-morph flowers in pre-anthesis were protected with
bags. In the anthesis, they were pollinated with pollen of the
ornithophilous Geissomeria schottiana Nees (Acanthaceae).
Five flowers per morph were collected 24 hours after
pollination and analyzed by fluorescence microscopy to verify
pollen tube growth. For this purpose, the pistils were stained
with aniline blue (Martin 1959). The other flowers were
observed until abortion or fruit set. Geissomeria schottiana
was chosen because the flowering period is synchronous with
P. longepedunculata, it also inhabits the forest understory
of the study area and both are visited by four common
hummingbird species (Abreu & Vieira 2004, this study).
Pollinators – In 2004, hummingbirds were identified in
binocular observation and photographic documentation. Sites
of pollen deposition on the bird were noted. In 2005, at the
flowering peak (see results), on June 8, 9 and 11, from 7h00
to 12h00 or from 14h00 to 18h00 (a total of 11 hours), the
number of foraging bouts, the number of flowers visited per
foraging bout and the interval between the foraging bouts
of each flower visitor were recorded. All these counts were
made in a place with four P. longepedunculata plants. The
choice of the place was based on the ease of observation of
the flowers and hummingbirds.
209
Results
Frequency of morphs and floral attributes – In this study
32 S-morph and 27 L-morph plants were counted, which
is very close to the expected 1:1 ratio, and the variation in
morph frequency was not significant (χ2 = 0.51, P = 0.91).
In 2004, the flowering period lasted from March to
August and in 2005, from April to September (figure
2), both in the dry season. Flowering was synchronous
in the floral morphs (figure 2). There was no difference
between the number of flowers per inflorescence in
S-morph (in average, 407.5 ± 232.24) and L-morph (in
average, 381.9 ± 142.32) (F = 0.10, P = 0.75) plants, as
well as between the number of inflorescences per plant
and open flowers per inflorescence (table 1). Only in
2004, the number of open flowers per plant was higher in
L-morph (table 1). It is worth highlighting that S-morph
flowers were significantly longer (mm) than L-morph
(respectively, 11.75 ± 1.23 and 8.27 ± 0.79, P < 0.01;
Pereira et al. 2006), but the L-morph inflorescences
were significantly longer (cm) than S-morph (in average,
respectively, 15.8 ± 4.73 and 9.6 ± 9.68, P = 0.017). All
data indicate that the flower attributes of the morphs are
largely similar.
The pollen grains of the morphs are similar in
morphology as well as viability (table 2). In 11 S-morph
and five L-morph flowers it was not possible to count
the 200 grains per slide. The anthers were partially
dehydrated and the number of pollen grains reduced
(range from 0 to 110).
Reproductive success – The reproductive success, as
suggested by Dafni et al. (2005), was measured by the count
of the numbers of fruits and of seed per fruit produced in 10
inflorescences per morph. The height and width of mature
and fresh fruits (n = 30 per morph) was measured by a
digital caliper (approximate precision of 0.01 mm). The fresh
fruits (n = 24 per morph) were weighed on analytical scales
(precision of 0.01 g).
Data analysis – To meet parametric analysis assumptions,
pollen grains viability and diameter data were square root
or arcsine transformed as required (Zar 1999). All statistical
analyses for floral attributes were run using general linear
modeling with software Statistica (StatSoft 2002).
Figure 2. Flowering period of the floral morphs of Palicourea
longepedunculata, in a forest fragment in Viçosa, Minas
Gerais State, southeastern Brazil, in 2004 and 2005.
( = S-morph; * = L-morph).
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C. A. Silva et al.: Floral attributes, ornithophily and reproductive success of Palicourea longepedunculata
Table 1. Mean numbers of inflorescences per plant, of open flowers per inflorescence and of open flowers per plant of the floral
morphs of Palicourea longepedunculata, in a forest fragment in Viçosa, Minas Gerais State, southeastern Brazil.
Year/ Morph
(number of plants)
Inflorescences per plant
X ±S
2004/
S-morph (22)
L-morph (17)
09.93 ± 08.04
09.18 ± 06.44
2005/
S-morph (10)
L-morph (10)
12.90 ± 12.60
07.90 ± 04.74
Open flowers per inflorescence
P
X ±S
0.33
19.85 ± 28.96
25.97 ± 15.22
0.26
11.70 ± 03.08
15.80 ± 04.15
Open flowers per plant
P
X ±S
P
0.38
33.31 ± 30.80
58.05 ± 23.55
0.009*
0.93
177.10 ± 230.12
255.20 ± 171.42
0.400
* significant at 1% probability.
Table 2. Mean diameter and viability of pollen grains and mean width, height and weight of fruits of floral morphs of Palicourea
longepedunculata, in a forest fragment in Viçosa, Minas Gerais State, southeastern Brazil.
Morph
Attribute
S-morph
L-morph
X ±S
X ±S
P
Pollen
Diameter (μm)
Viability (%)
9.27 ± 0.25
79.40 ± 30.65
8.83 ± 0.21
86.78 ± 30.65
0.16
1.81
Fruit
Width (mm)
Height (mm)
Weight (g)
0.77 ± 0.06
0.73 ± 0.04
0.117 ± 0.046
0.77 ± 0.01
0.72 ± 0.09
0.113 ± 0.031
0.66
0.62
0.58
Breeding system – No fruits were produced by selfing
and intramorph pollinations. Intermorph pollinations
accounted for 57.1% (S-morph × L-morph) and 78.6%
(L-morph × S-morph) of fruit set. These results showed
that P. longepedunculata is self-incompatible, confirming
the results of Pereira et al. (2006). In average, there
was no difference between the fruit sets of the control
(F = 0.52, P = 0.48), which was 26.3% in S-morph and
22.4% in L-morph flowers.
In the flowers pollinated with pollen grains of G.
schottiana the pollen tubes grew to the style base and
there was no fruit production.
Pollinators – Four hummingbird (Aves, Trochilidae)
species were recorded (table 3) visiting various open
flowers per plant, all day long. A fifth hummingbird,
Amazilia fimbriata (Gmelin, 1788), was observed only
towards the end of the flowering period 2004. The visits
were single, i.e., one hummingbird species per foraging
bout. Pollen was deposited in the distal region of the
hummingbird’s bill (figure 1).
Phaethornis ruber (Linnaeus, 1758) (figure 1) was
the main pollinator, observed in 18 of the 29 foraging
bouts recorded (table 3). These foraging bouts were
repeated every 15 to 50 minutes, when the hummingbirds
performed from one to 60 visits. In the afternoon of
June 8, 232 visits were counted in six foraging bouts;
in the morning of June 11, 273 visits were counted in
12 foraging bouts. Phaethornis ruber performed 79%
and 95% of these visits, respectively.
Reproductive success – Both fruit and seed set were
similar in the morphs (table 4). The fruits were also
similar in height, width and weight (table 2).
Seedless fruits were observed, which developed
until half the size of fruits with seeds; at this point,
they dropped. The percentage of seedless fruits was
significantly higher in L-morph flowers (table 4).
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Revista Brasil. Bot., V.33, n.2, p.207-213, abr.-jun. 2010
Table 3. Hummingbird species, bill length and visitation frequency (n = 29 foraging bouts) of flowers of Palicourea
longepedunculata, in a forest fragment in Viçosa, Minas Gerais State, southeastern Brazil.
Subfamily/Species
Bill length*
(cm)
Frequency
(%)
Reddish Hermit
Dusky-throated Hermit
2.2
2.4
62.07
17.24
Glittering-bellied Emerald
Violet-capped Woodnymph
1.4
1.7
06.89
13.79
Common name
Phaethornithinae/
Phaethornis ruber (Linnaeus, 1758)
P. squalidus (Temminck, 1822)
Trochilinae/
Chlorostilbon lucidus (Shaw, 1812)
Thalurania glaucopis (Gmelin, 1788)
* According to Ruschi (1982).
Table 4. Total number of fruits and seeds produced in 10 inflorescences of floral morphs of Palicourea longepedunculata,
mean number of fruits per inflorescence and percentage of fruits with 0, 1 or 2 seeds, in a forest fragment in Viçosa, Minas
Gerais State, southeastern Brazil.
Morph
Total fruits – seeds
S-morph
L-morph
1071 – 1809
0857 – 1210
Fruits per inflorescence
X ±S
Seeds per fruit (%)
0
107.1 ± 46.47
085.7 ± 47.34
05.06
16.90
1.040
40.32
0.320
00.007
F
P
*
1
2
21.00
25.00
73.94
58.10
02.40
00.43
0.200
0.880
* Significant at 1% probability.
Discussion
The similarity of floral attributes in the P.
longepedunculata morphs was favored by the
equilibrium morph ratio and flowering synchrony, and
suggests similar allocation to pollinator attraction and
pollen dispersal. González et al. (2005) verified that
L-morph plants of Palicourea padifolia initiated more
floral buds per inflorescence than S-morph, suggesting a
strong relation with pollinator attraction and, potentially,
an increase in male fitness through pollen donation;
although fruit set was similar between morphs. The floral
morphs of several distylous species specialize in their
reproductive effort through male and female function
(Lloyd 1979). The similar reproductive performance of
the P. longepedunculata morphs suggests the participation
of both as pollen donor and recipient in the population.
However, S-morph plants tended to produce more fruits
and seeds and therefore, more samplings over a longer
period is needed to detect gender specialization, as
proposed by González et al. (2005).
The flowering strategy of P. longepedunculata
seems to be efficient to attract hummingbirds, mainly
Phaethornis ruber, in view of its high frequency and
constancy of visitation. Vieira et al. (2007) observed
a similar strategy in the ornithophilous Corymborkis
flava (Sw.) Kuntze, a terrestrial orchid of the forest
understory in the same study area. This orchid produces
abundant bright yellow flowers per plant and day and this
abundance of flowers seems to maintain the constancy
of hummingbird visitation.
The short corolla tubes of the P. longepedunculata
permit the visitation of hummingbird species with
different bill dimensions (cf. Johnson & Edwards
2000, Consolaro et al. 2005). In fact, in a Neotropical
community, species with long corolla are associated with
a lower diversity of hummingbird pollinators, compared
to species with shorter corolla (Wolf et al. 1976).
Despite the diversity of hummingbirds observed
in Palicourea longepedunculata, Phaethornis ruber
stood out as the main pollinator. Abreu & Vieira (2004)
also observed the predominance of the visits of one
hummingbird species over the four other observed in
the ornithophilous Geissomeria schottiana, in the same
study area. These authors demonstrated that Thalurania
glaucopis (Gmelin, 1788) accounted for 64.8% of the
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C. A. Silva et al.: Floral attributes, ornithophily and reproductive success of Palicourea longepedunculata
visitation in about 15 hours of observation. Geissomeria
schottiana, as well as P. longepedunculata, flowers
abundantly during the dry season (Abreu & Vieira 2004).
These results indicate the existence of an organization
of the hummingbird community for an efficient use of
the nectar produced by the plant community (cf. Wolf
et al. 1976). However, studies on different aspects of
the birds and plants in the community are needed, for a
more in-depth analysis.
The other hummingbirds, due to the low frequency
of visitation, may be considered sporadic pollinators
of Palicourea longepedunculata. Among these,
Phaethornis squalidus and P. ruber are trapliners (Janzen
1971, Stiles 1975), favoring cross pollination (cf. Stiles
1975). However, these hummingbirds visited several
flowers per plant in the same foraging bout, a behavior
that favors geitonogamous pollinations and may result
in stigma clogging by the deposition of incompatible
pollen grains, resulting in low fruit set. For example, in
the distylous Turnera ulmifolia L. (Turneraceae), due
to the occlusion of stigmas, the fruit set of L-morph
tended to be lower than that of S-morph flowers
(Shore & Barret 1984). Although stigma clogging was
out of the scope of this paper, the results indicate that
P. longepedunculata morphs may be equally affected
by the deposition of incompatible pollen, considering
their similar natural fruit set. Higher natural fruit set
were observed in other distylous Palicourea species
(see Sobrevila et al. 1983, Ree 1997, Wesselingh
et al. 1999), aside from P. salicifolia (15% for both
flower morphs together; Wesselingh et al. 1999). The
percentages of natural fruit set of P. longepedunculata
were apparently low due to the high number of flowers
(> 381) per inflorescence. However, do not result in a
low fruit (> 85 per inflorescence) and seed production,
as shown in the results.
The likeness of both fruit morphology and set
between the P. longepedunculata morphs suggests
similar allocation to dispersor attraction. Thus, the
morphs have the same chances of establishing new
plants in the population, resulting in a balanced ratio
of the morphs, as verified here. Higher natural fruit set
with two seeds corroborated the effectiveness of the
hummingbirds, in particular of Phaethornis ruber, as
pollinator. Feinsinger et al. (1988) stated the necessity
of at least two pollen tubes for full seed set (also two
seeds) in Palicourea lasiorrachis.
The seedless fruits production, as verified in P.
longepedunculata, was not a result of the stimulus
triggered by the intramorph or interspecific pollinations.
Feinsinger et al. (1988) also verified seedless fruit
production in P. lasiorrachis. Future studies may address
this issue in these species.
Summing up, this study showed similarities in the
floral attributes and reproductive success between the
floral morphs of the ornithophilous P. longepedunculata,
which are poorly investigated aspects in research
on the reproductive biology of distylous species of
Rubiaceae.
Acknowledgements – The authors wish to thank the
CNPq (National Council of Scientific and Technological
Development) for a scholarship of Undergraduate Students’
Research Program of the third author and for the award
for Excellence in Research of the second author; they also
gratefully acknowledge the help of Geraldo T. de Mattos with
the identification of the hummingbirds and the administration
of the Mata do Paraíso for allowing the field work.
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