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 CONFERENCE CORNER
SCIENCE
Notes on the floral biology, seed morphology and post-semi-
nal development of Vriesea minarum L.B.Sm., an endangered
Bromeliaceae of Southeastern Brazil

Pâmela Lavor1,2, Claudia M. Jacobi3, Flávio

F. Carmo3, Leonardo M. Versieux1,2,4
Abstract
Vriesea minarum is a bromeliad endemic to the Iron Quadrangle region in Minas
Gerais state, Brazil and is currently listed as an endangered species. The aim of our
study was to investigate the species floral biology, breeding system, and post-seminal
development. Observations and experiments were conducted in the Rola-Moça
State Park. Flowers have morphological characteristics typical for the genus but we
discuss the position of the ovary, oversimplified in some papers as superior. Seed
set indicates that V. minarum is predominantly outcrossing, but self-compatible as
well. The floral biology indicates flower protandry, and suggests a mixed pollination
syndrome, as was observed recently in other bromeliads. Due to the survival risk fac-
ing this species, we suggest that more studies investigating the potential to preserve
germplasm should be conducted, since its seeds appear to have a limited viability.
Key words - endemic species, Iron Quadrangle, Rola-Moça State Park, Tillandsioideae
Introduction
Vriesea minarum L.B. Sm. is an endemic species from the Iron Quadrangle (IQ), a
region in the southern portion of the Espinhaço mountain range in Minas Gerais state,
Brazil (Versieux 2005, 2011, Versieux & Wendt 2006, Jacobi et al. 2007, Versieux et al.
2008). This rupicolous bromeliad has at least 12 populations within the Iron Quadrangle
(Lavor et al. 2014). Due to severe habitat loss by mining, it is currently included as an
endangered species in the Red List of Brazilian Endangered Plant Species (CNCFlora
2013) and it is officially protected only in three full protection conservation units: Serra
de Gandarela National Park, Monumento Natural da Serra da Moeda and Rola-Moça
State Park (Versieux 2011, Lavor et al. 2014).
Considering this threatening scenario, it is desirable to inquire about its floral
biology, since the behavior of flowers and their pollinators will affect plant breeding
systems and fertility, which will be fundamental factors when assessing endangered

1
Programa de Pós-Graduação em Sistemática e Evolução, Universidade Federal do Rio Grande do
Norte, Natal, RN, Brazil.
2
Laboratório de Botânica Sistemática, Departamento de Botânica e Zoologia, Universidade
Federal do Rio Grande do Norte, Natal, RN, Brazil.
3
Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG,
Brazil.
4
Corresponding author: Leonardo Versieux (lversieux@yahoo.com.br)

J. Bromeliad Soc. 66(2). 2017.

87
 SCIENCE Floral biology of Vriesea minarum

species population viability and choosing appropriate conservation measures (Paggi

et al. 2007, 2013). The relationships between plant, pollinator and disperser are also
important for understanding the population structure, as they may influence the spatial
distribution of the genetic diversity through gene flow (Yamamoto et al. 2007).
Several studies are available in the literature about the reproductive biology of
bromeliad species (e.g. Martinelli 1994, 1997, Varassin & Sazima 2000, Wendt et
al. 2001, 2002, Matallana et al. 2010) or on the strategies used by the species of the
subfamily Tillandsioideae to disperse propagules (e.g. Paggi et al. 2010). Although the
Espinhaço range may be considered a “Bromeliaceae hotspot” few reproductive data
are available for its unique bromeliads. Thus, the aim of this study was to provide some
detailed information on V. minarum reproductive patterns, including floral biology,
reproductive systems, seed morphology and post-germination development which may
help conserve this threatened taxon.
Material and methods
Study area - The study was conducted between February and March 2012 in
Rola-Moça State Park (RMSP) (20°02’40”S 43°59’48”W), Minas Gerais, Brazil. The
species occurs in an area of open rocky field, more specifically ironstone outcrops (lo-
cally known as “canga”) (Jacobi et al. 2007, Lavor et al. 2014).
Floral biology – We studied the morphology of V. minarum flowers through
observation and photographic documentation in situ and ex situ, followed by dissec-
tion under stereomicroscope of the components of the floral whorls (calyx, corolla,
androecium and gynoecium and septal nectaries), completing the description made by
Versieux (2011). We conducted daily visits to observe the floral biology of eight genets
separated by a minimum distance of 5 meters from March 6 to March 27, 2012. We
observed the time of anthesis and floral senescence, flower duration (in days), period
of pollen availability, and number of open flowers per day per genet. We tested the
stigmatic receptivity three times a day (8:00 am, 12:00 and 5:00 pm) with hydrogen
peroxide, using a 10x magnification hand lens to observe the formation of bubbles
(Dafni et al. 2005). We measured and monitored nectar volume production in flowers
(N = 3) at three different periods (morning, noon and late afternoon) by removing all
nectar accumulated at the base of the ovary with a graded microsyringe (Hamilton) and
analyzed sugar concentration with the aid of a hand-held refractometer 0-50% Brix
(Kearns & Inouye 1993). To qualitatively investigate the floral odor we conducted a
“nose bioassay” (Kearns & Inouye 1993). Flowers (N=4) and flower buds (N=4) were
enclosed in a clean vial for 24 hours. After that, we questioned four volunteers if the
flowers or buds had odor, and if so, how they would describe it. We conducted visual
observations during the day, for one week, totaling 12 hours of direct observation,
noting the time and number of floral visitors (and collection of possible visitors) in
eight flowering individuals.

88 J. Bromeliad Soc. 66(2). 2017.

 SCIENCE Floral biology of Vriesea minarum

Reproductive biology, seed morphology and post-seminal development – To

obtain seeds, we performed a preliminary test of reproductive biology. We used four
treatments to check if fruit and seeds would be produced and, after that, used the seeds
obtained to analyze morphology and post-seminal characteristics. The treatments were
performed on 8 inflorescences from 8 different genets, separated by ca. 5 m from each
other, along the top of one mountain. With the aid of pollinator and pollen exclusion
nets, a total of 59 flowers were treated. Treatments were: (1) manual self-pollination:
to test for self-compatibility, unopened flowers were bagged and, on the next day, after
anthesis, were pollinated with their own pollen and bagged again (N=12); (2) manual
cross-pollination: to test for cross-fertilization, bagged flowers were pollinated with
pollen from other flowers (preferably from plants at least 5 m apart to avoid collecting
pollen from relatives) and re-bagged (N=12); (3) spontaneous self-pollination: to test the
need for pollinator vectors, buds were bagged and no artificial pollination was performed
(N=16); (4) to test the effective contribution of pollinators in the system, senescent
flowers were bagged, serving as a control treatment (N=19). All the seeds obtained in
all treatments were counted (total=4,400), put to germinate in Petri plates with filter
paper soaked in distilled water, and placed under natural light at room temperature
for 30 days. The start of germination was measured by the appearance of the radicle.
Daily observations were made to verify the emergence and growth of the radicle and
other vegetative organs of the seedling, which were documented by photos, using a
portable digital microscope (Celestron 10x - 150x digital Microscope). Due to results
obtained for germination indicating low values of viability (data not shown) we will
only briefly discuss fruit and seed set, and not germination rates.
Results
Observations and floral biology - The reproductive period (measured from the
beginning to the end of the inflorescence production) of V. minarum is from January to
March. During January (the first month) there was the emergence of the inflorescence
peduncle and, in the second month, flower buds were already visible in an immature
inflorescence. In March, the inflorescences were mature and had two overlapping phe-
nophases (flower buds and open flowers) (Fig. 1). Inflorescence maturation occurs from
base toward the apex, with the opening of a single flower per day (Fig. 1a). Flowers last
for two days and have diurnal anthesis (after 8:00 am), remaining open during the first
night. Although observations were not carried out overnight, we deduced that flowers
remain opened during the night since from our last observation at 6:00 pm until our
first observations the next morning at 6:00 am, the flowers were still open. The first
sign of anthesis is the spreading of the petal apexes (Fig. 1b). After that, the stigma
emerges, but at this point it is not receptive yet (Fig. 1c), followed by the appearance
of the stamens, which nearly 3 hours later will be more exposed and with the anthers
completely exserted (Fig. 1d).

J. Bromeliad Soc. 66(2). 2017. 89

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Figure 1. Specimen of Vriesea minarum growing on typical ironstone habitat.

(a) blooming individual (b) flower bud (c) stigma protruding (d) stamens with
closed anthers (e) fully open flower (f) senescent flower. Bars: (a) = 10 cm, (b –
f) = 1 cm. Photos by Pâmela Lavor.

The anthers appeared close to the petal apex a few hours after anthesis, starting to
release pollen after 9:00 am, and continuing throughout the day until the early hours of
the following morning. The stigma was receptive from the end of the first day (around
4:00 pm) (Fig. 1e) until the morning of the second day. Flower senescence starts on
the morning of the second day. Senescence in V. minarum flowers is characterized by
the loss of the yellow color of the sepals and darkening of the petals (Fig. 1f ).
Nectar accumulated at the base of the corolla, and its production started around
8:00 am on the first day (mean = 0.023 ml ± 0.02 SD). There was a general trend of
decrease (Fig. 2), with the end of the production around 2:00 pm on the second day.
Similarly, the mean sugar concentration in the nectar was higher on the first day (mean
= 13% ± 9.5 SD). On the second day the average sugar concentration was 9%. As with
production, there was a general trend of decreasing sugar concentration throughout the
day (Fig. 2). When nectar was removed, the flower restored the same average amount
of nectar throughout the day and its output coincides with thecal dehiscence and the
release of pollen. Flowers have no perceivable odor after being kept in sealed vials.
Unfortunately, no floral visitors or pollinators were observed, although many dif-
ferent species of visitors (hummingbirds, butterflies, bees and beetles) were noticed
90 J. Bromeliad Soc. 66(2). 2017.
 SCIENCE Floral biology of Vriesea minarum

Figure 2. Nectar production (ml) and nectar sugar concentration (%) along a period
of 2 days in Vriesea minarum flowers. Figure by Pâmela Lavor.

around other plant species that were flowering in the same area. In one of the observed
V. minarum plants, an unidentified ant circulated along the axis of the inflorescence,
and got into the flowers sporadically without touching stamen or stigma or causing
damage to the floral parts. The flowers of V. minarum have a trimerous perianth (three
sepals and three petals) (Fig. 3a), with two basal petal appendages per petal (Fig. 3c).
The ovary is nearly superior (Figs. 3a and 3g), and is 3-locular (Figs. 3b and 3d), with
a fraction of each locule base going below the point of petal attachment. Nectaries are
infralocular, with septal nectaries well developed (Fig. 3a). The anthers are dorsifixed
and have longitudinal dehiscence (Figs. 3e and 3f ). The stigma type (Fig. 3h) is classi-
fied as convolute blade in the Brown and Gilmartin (1984, 1989) system.
Reproductive biology – All treatments produced fruits and seeds, indicating that
the species can produce seed under either self- or cross-pollination (see Table 1). The
number of fruit was proportionally higher in the control, untouched and unbagged, in
which 18 out 19 (94.7%) flowers treated set fruit, followed by manual self-pollination
(75%), spontaneous self-pollination (68.8%), and by the manual cross-pollination
(41.7%). The proportion of seeds per fruit (seed set divided by the fruit set), however,
was higher in manual cross-pollination (263.6), followed by manual self-pollination
(199.6), spontaneous self-pollination (93.2) and by the control (14.4). In all the treat-
ments, we observed aborted seeds that were not counted.

J. Bromeliad Soc. 66(2). 2017. 91

 SCIENCE Floral biology of Vriesea minarum

Seed morphology and post-

seminal development - Vriesea
minarum has seeds nearly 6 mm
long (± 0.06 SD; N = 5), which
are filiform, brown, bearing whit-
ish feathery appendages along
the base (Fig. 4a). The germina-
tion was initiated at 12-13 days
after imbibition (Fig. 4b). The
radicle arises close to the coty-
ledonary sheath. A post-seminal
characteristic in V. minarum is
the presence of the undeveloped
hypocotyl. The first leaf (eophyll)
appears five days after radicle
(primary root) emergence (Fig.
4c), and it takes five more days
before the second leaf becomes
visible (Fig. 4d). After the ap-
pearance of the third leaf, leaves
(eophylls) develop so intertwined
that the shape of a miniature ro-
sette, typical of Bromeliaceae, is
already apparent (Fig. 4e).
Figure 3. Flower morphology of Vriesea minarum. (a) Discussion
longitudinal section of V. minarum showing the well-de-
Observations and floral
veloped infra-locular septal nectaries (*), the locules (§),
chamber delimited between the ovary and the petal ap-
biology - The reproductive phase
pendages (γ), and appendages (»); (b) transversal section
observed here for V. minarum in
of the ovary showing the locules and the terminal por-
RMSP coincides with the rainy
tions of the nectaries opening (arrow head); (c) dissected
season, corroborating Versieux’s
basal petal appendages; (d) ovary sectioned along the
data (2011). Nevertheless, the
mid portion, showing placentation and ovules; (e) anther
in front view; (f) anther in dorsal view; (g) conical shape
flowers only started to open in
of the mostly superior portion of the ovary; (h) convolute
March. In other areas of the IQ
blade stigma. Bars = 1 mm. Photos by Pâmela Lavor.
the blooming of V. minarum ap-
pears to be longer, from December to March based on herbarium records (Versieux
& Wendt 2006, Versieux 2011). The lack of floral visitors observed may be due to the
size of the population analyzed (8 blooming individuals, a small number if compared
to the massive bloom seen in other rocky outcrops, L.M. Versieux pers. obs.) and by
the low number of flowers on individual plants and in the whole population. A fire in
the RMSP preceeding the study was responsible for these low numbers. The opening

92 J. Bromeliad Soc. 66(2). 2017.

 SCIENCE Floral biology of Vriesea minarum

Table 1 – Results of the pollination treatments for Vriesea minarum in Rola-Moça

State Park, Minas Gerais.
Spontanous
Control (un-
Manual self- Manual Cross- self-pollination
touched and
pollinaion pollintion (untouched and
unbagged)
bagged)
Flowers
12 12 16 19
treated

FRUIT SET 9 5 11 18

% Fruit set
per 75.0 41.7 68.8 94.7
treatment

SEED SET 1797 1318 1025 260

of a single flower a day per inflorescence in V. minarum, could be less attractive if com-
pared to several options of flowers in other shrubs and herbs nearby. Moreover, as the
observations were made only during the day and there are indications that its flowers
remain open during the night, perhaps the floral visitors were more active in this time.
A similar fact is reported by Van Sluys & Stotz (1995) with other species of Vriesea that,
by presenting a limited offer of flowers per inflorescence during the flowering season,
received fewer floral visitors, while groups of flowering plants with a larger number of
open flowers received more visits by hummingbirds.
The basic characteristics of the flowers of V. minarum suggest a mixed pol-
lination syndrome. Mixed pollination systems are found in several Mesoamerican
Bromeliaceae species, with some species of Tillandsia presenting flowers that last for
almost 48 hours, a strategy to allow access of pollinators that are active during the night
(Benzing 2000b). The flower of V. minarum has typical ornithophily features, such as
exposed flowers and inflorescence, tubular and odorless flowers, diurnal anthesis, con-
spicuous or contrasting colors among floral parts, lower concentration of nectar sugar,
stigma and anthers away from the nectaries and positioned to optimize the contact
with birds, and absence of a landing platform (Machado & Semir 2006). Marques &
Lemos-Filho (2008) observed birds visiting V. minarum (at that time identified as V.
citrina) in Serra da Piedade, 41 km northeast of RMSP. These authors also noted that
above 1,500 m.a.s.l. in the area of Serra da Piedade ornithophily was most common
among the Vriesea species. Other morphologically similar species were also indicated
as ornithophilous, as is the case of V. marceloi Versieux & Machado, from Serra do

J. Bromeliad Soc. 66(2). 2017. 93

 SCIENCE Floral biology of Vriesea minarum

Figure 4. (a) Mature seed of V. minarum. (b-e) Post seminal development of Vriesea minarum. ;
(b) onset of germination with the emergence of the radicle (primary root); (c) the first leaf (eo-
phyll) appearance; (d) formation of the second leaf; (e) appearance of the third leaf. Bars = 2 mm
(Legends: Co = Coma; Cs = Cotyledonary sheath; Eo = Eophyll; Pr = Primary root; Se = Seed). Line
drawings by Rhudson Cruz.
Caraça (Versieux & Machado 2012). Versieux (2011) also made personal observations
of hummingbird visits to V. minarum.
On the other hand, flowers of V. minarum have a duration of two days, do not
close during the night, and the stigma becomes receptive in the late afternoon, sug-
gesting visits by nocturnal pollinators, maybe bats. Currently, 36 species of bats have
been inventoried in the caves in the ironstone outcrops, four nectarivorous species and
12 frugivorous (Gomes et al. 2015). Bats are the main pollinators in several bromeliad
genera, including Vriesea Section Xiphion (e.g. Vogel 1969, Sazima et al. 1989, 1995,
Martinelli 1997, Kessler & Kromer 2000, Benzing 2000c), although most bat-pollinated
Vriesea species have wide-mouthed flowers and stamens positioned on one side of the
flower (Sazima et al. 1995). Bats can be opportunistic and sometimes visit flowers that
do not conform to the classic ‘bat pollination syndrome’; the color of bat flowers ranges
from white, brown and green to pink, fuchsia and yellow. Bat flowers/inflorescences
can be roughly divided into three categories based on their shape: (1) ‘shaving-brush’ or

94 J. Bromeliad Soc. 66(2). 2017.

 SCIENCE Floral biology of Vriesea minarum

‘stamen ball’ with many projecting stamens; (2) ‘bell-shaped’ with the corolla forming
a tube; and (3) ‘cupshaped’ with an open corolla (Fleming et al. 2009). Recent works
indicate interesting results for bromeliads that have flowers remaining open during
day and night, and this strategy may be similar in V. minarum (Marques et al. 2015,
Aguilar-Rodrıguez et al. 2014, 2015, Queiroz et al. 2016).
Pollination by bats may explain recent results of population genetics for the species.
Lavor et al. (2014) found a low genetic population structure attributed either to efficient
seed or pollen dispersal among separated mountains. Bats can travel great distances to
feeding sites (up to 38 km), whereas many species of hummingbirds are territorial, thus
restricting cross-pollination distances (Proctor et al. 1996). Nevertheless, the low levels
of gene flow obtained with the similarly rupicolous and closely related genus Alcantarea
lead Barbará et al. (2007) to suggest that bats do not contribute so much to cross-
pollination between inselberg (isolated granitic rock outcrops) bromeliad populations.
Considering the floral morphology, our dissections indicate that the ovary in this
species has a positioning similar to what is seen in Alcantarea (Versieux & Wanderley
2015). The basal 1/8 of locules is below the point of attachment of the petals (Fig. 3a).
This would classify the ovary as cryptically half-inferior or nearly superior (as described
by Mez 1934, Smith & Till 1998). In contrast, some descriptions of Vriesea, suggest
that a fully superior ovary is the only type found in the entire genus.
Reproductive biology - There are many characteristics that may influence the
proportions of selfing and outcrossing breeding systems in Bromeliaceae. Protandry is
the main means of promoting outcrossing in self-compatible species (Benzing 2000b)
and this is an attribute observed in V. minarum. This strategy was recorded by Martinelli
(1994) in 17 Vriesea species pollinated by hummingbirds and bats in southeastern
Brazil Atlantic rainforest. The mean number of seeds produced by both manual and
spontaneous self-pollination (Table 1) indicates that the species is self-compatible and
capable of reproducing in case of pollinator shortage, despite the higher value of seed
set seen for manual cross-pollination. For V. minarum the reproductive pattern is like
those observed in the bromeliad species studied by Martinelli (1994) and Matallana et
al. (2010) that presented characteristics of an outcrossing breeding system (an advan-
tage when pollinator availability is high). However, inferences about the reproductive
system of this species can not be fully understood now, and are still speculative in the
present work and will demand additional experiments, including overnight observa-
tions (to make sure bats are visiting the inflorescences) and seed viability tests. Because
the flowering season was atypical that year and only 8 rosettes were blooming for this
experiment, only a limited number of inflorescences and flowers were available for
treatments. This limited the number of flowers in each treatment category. We hope
to expand the study in the future with a larger numbers of flowers and to avoid any
loss of seed viability due to delays in transportating and counting. Germination rates

J. Bromeliad Soc. 66(2). 2017. 95

 SCIENCE Floral biology of Vriesea minarum

could then be used to determine which of the treatments would, in fact, guarantee
more efficient reproduction.
Morphology of seeds and post-seminal development - The seeds of V. minarum
are morphologically similar to those from other Tillandsioideae species. This subfamily
is characterized mainly by the coma, the flight apparatus allowing anemochory. The
appendages increase the surface/volume ratio, reducing speed of the fall during disper-
sal by air streams or winds in the dry season (Paula & Silva 2004). Seed germination
time is considered intermediate according to the Pereira et al. (2008) classification and
similar to what have been described for other Tillandsioideae, as well as their post-
seminal characteristics, such as the presence of the undeveloped hypocotyl, and straight
cotyledonary sheath and reduced primary root (Tillich 2007).
Conservation - In terms of ecological importance, the family Bromeliaceae is
remarkable, but the amount of scientific literature available about the floral biology,
phenology and reproductive systems is still limited compared to the richness and domi-
nance of Bromeliaceae taxa in many habitats, although an increase in the last decade
is noticed (e.g. Martinelli 1997, Siqueira-Filho & Machado 2001, Nara & Webber
2002, Machado & Semir 2006, Pereira & Quirino 2008, Rios et al. 2010, Marques et
al. 2015, Aguilar-Rodríguez et al. 2014, 2015, Queiroz et al. 2016). This knowledge
is fundamental, since the bromeliads are biodiversity promoters and help in the estab-
lishment and maintenance of other organisms, such as other plants, invertebrates, and
vertebrates (Benzing 2000b).
Although no floral visitors were seen in the present study, data presented here on
nectar production in V. minarum show the plant may be considered an important
source of nectar for diurnal and nocturnal fauna in the ferruginous fields. As proposed
by Lavor et al. (2014) we suggest that more conservation units be created within the
entire IQ to protect micro-endemic taxa such as V. minarum, and that more studies
investigating the potential to preserve germplasm of this taxon (including techniques
to prolong seed viability) should be conducted.
Acknowledgements
We thank CAPES for the first author’s M.Sc. CMJ and LMV thank the Brazil-
ian National Council for Scientific and Technological Development (CNPq) for
their Research Productivity Scholarships and research grants (304778/2013-3 and
455510/2014-8). The Rola-Moça State Park and the State Forest Institute (IEF-MG)
are gratefully acknowledged for providing personnel to assist with collection and ob-
servation of specimens in the field. We also thank Profs. Fabio de Almeida Vieira and
Vânia Cristina Rennó Azevedo for their constructive suggestions to an earlier version of
this manuscript, as well as the anonymous reviewers and editors. Interns A.S. Medeiros
and E.C. Tomaz are acknowledged for their patience and help while counting seeds.

96 J. Bromeliad Soc. 66(2). 2017.

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Literature cited
Aguilar-Rodríguez, P.A., Krömer, T., García-Franco, J.G., Mac Swiney, G.M.C.
2015. From dusk till dawn: nocturnal and diurnal pollination in the epiphyte
Tillandsia heterophylla (Bromeliaceae). Plant Biology 18: 37-45.
Aguilar-Rodríguez, P.A., MacSwiney, G.M.C., Krömer, T., García-Franco, J.G.,
Knauer, A., Kessler, M. 2014. First record of bat-pollination in the species-rich
genus Tillandsia (Bromeliaceae). Annals of Botany 113: 1047-1055.
Barbará, T., Martinelli, G., Fay, M.F., Mayo, S.J., Lexer, C. 2007. Population
differentiation and species cohesion in two closely related plants adapted to neo-
tropical high-altitude ‘inselbergs’, Alcantarea imperialis and Alcantarea geniculata
(Bromeliaceae). Molecular Ecology 16: 1981-1992.
Benzing, D.H. 2000a. Pollination. In: D.H. Benzing (ed.). Bromeliaceae: profile of
an adaptive radiation. Cambridge University Press, Cambridge.
Benzing, D.H. 2000b. Relationship with the fauna. In: D.H. Benzing (ed.). Bro-
meliaceae: profile of an adaptive radiation. Cambridge University Press, Cam-
bridge.
Benzing, D.H. 2000c. Reproductive structure. In: D.H. Benzing (ed.). Bromelia-
ceae: profile of an adaptive radiation. Cambridge University Press, Cambridge.
Brown, G.K & Gilmartin, A.J. 1984. Stigma structure and variation in Bromelia-
ceae – neglected taxonomic characters. Brittonia 36: 364-374.
Brown, G.K. & Gilmartin, A.J. 1989. Stigma types in Bromeliaceae – a systematic
survey. Systematic Botany 14: 110-132.
CNCFlora - Centro Nacional de Conservação da Flora. 2013. Lista Vermelha de
Espécies. Available from http://www.cncflora.jbrj.gov.br/?q=pt-br/lista_vermel-
ha/redlisting (accessed in 20 Feb 2016).
Dafni, A., Kevan, P.G., Husband, B.C. 2005. Practical Pollination Biology. Enviro-
quest, Ltd. Cambridge, Ontario, Canada.
Dutra, V.F., Vieira, M.F., Garcia, F.C.P., Lima, H.C. 2009. Fenologia reprodutiva,
síndromes de polinização e dispersão em espécies de Leguminosae dos campos
rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguésia
60: 371-387.
Fleming, T.H., Geiselman, C., Kress, W.J. 2009. The evolution of bat pollination:
a phylogenetic perspective. Annals of Botany 104: 1017–1043.
Gomes, A.M., Silva, L.H.D., Tavares, V.C. 2015. Morcegos associados a Ecos-
sistemas Ferruginosos de Minas Gerais. In: F.F. Carmo, Kamino, L.H.Y. (Org.).
Geossistemas Ferruginosos do Brasil: áreas prioritárias para a conservação da
diversidade geológica e biológica, patrimônio cultural e serviços ambientais. 3i
Editora Ltda. Belo Horizonte.
Jacobi, C.M., Carmo, F.F., Vincent, R.C., Stehmann, J.R. 2007. Plant commu-
nities on ironstone outcrops: a diverse and endangered Brazilian ecosystem.

J. Bromeliad Soc. 66(2). 2017. 97

 SCIENCE Floral biology of Vriesea minarum

Biodiversity and Conservation 16: 2185-2200.

Kearns, C.A. & Inouye, D.W.1993.Techniques for pollination biologists. Univer-
sity Press of Colorado, Niwot, Colorado.
Kessler, M. & Krömer, T. 2000.Patterns and ecological correlates of pollination
modes among bromeliad communities of Andean Forests in Bolivia. Plant Biol-
ogy 2: 659-669.
Lavor, P., Van den Berg, C., Jacobi, C.M., Carmo, F.F., Versieux, L.M. 2014.
Population genetics of the endemic and endangered Vriesea minarum (Brome-
liaceae) in the Iron Quadrangle, Espinhaco Range, Brazil. American Journal of
Botany 101: 1167-1175.
Machado, C.G. & Semir, J. 2006. Fenologia da floração e biologia floral de brome-
liáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Revista
Brasileira de Botânica 29: 163-174.
Marques, A.R. 2002. Ecofisiologia e contribuições para a conservação das bromélias
da Serra da Piedade. Dissertation. Universidadede Federal de Minas Gerais. Belo
Horizonte, Brazil.
Marques, A.R. & Lemos Filho, J.P. 2008. Fenologia reprodutiva de espécies de
bromélias na Serra da Piedade, MG, Brasil. Acta Botanica Brasilica 22: 417-424.
Marques, J.S., Tagliati, M.C., Faria, A.P.G. 2015. Diurnal versus nocturnal pol-
lination success in Billbergia horrida Regel (Bromeliaceae) and the first record of
chiropterophily for the genus. Anais da Academia Brasileira de Ciências. [online]
87: 835-842.
Martinelli, G. 1994. Reproductive biology of Bromeliaceae in the Atlantic rainfor-
est of Southeastern Brazil. PhD thesis, University of St. Andrews, St. Andrews,
Scotland.
Martinelli, G. 1997. Biologia reprodutiva de Bromeliaceae na Reserva Ecológica
de Macaé de Cima. In: H.C. Lima, Guedes-Bruni, R.R. (eds.). Serra de Macaé
de Cima: diversidade florística e conservação em mata atlântica. Instituto de
Pesquisas do Jardim Botânico do Rio de Janeiro, Rio de Janeiro.
Matallana, G., Godinho, M., Guilherme, F., Belisario, M., Coser, T., Wendt, T.
2010. Breeding systems of Bromeliaceae species: evolution of selfing in the con-
text of sympatric occurrence. Plant Systematics and Evolution 289: 57-65.
Mez, C. 1934. Bromeliaceae. In: A. Engler (ed.). Das Pflanzenreich, regnivegetabi-
lisconspectus. ImAuftrage der Preuss. Akademie der Wissenschaften. Wilhelm
Engelmann, Berlin, pp 1-667.
Nara, A.K. & Webber, A.C. 2002. Biologia floral e polinização de Aechmea beeriana
(Bromeliaceae) em vegetação de baixio na Amazônia Central. Acta Amazônica
32: 571-588.
Paggi, G.M., Palma-Silva, C., Silveira, L.C.T., Kaltchuk-Santos, E., Bodanese-
-Zanettini, M.H., Bered, F. 2007. Fertility of Vriesea gigantea Gaud. (Bromelia-
ceae) in southern Brazil. American Journal of Botany 94: 683–689.

98 J. Bromeliad Soc. 66(2). 2017.

 SCIENCE Floral biology of Vriesea minarum

Paggi, G.M., Sampaio, J.A.T., Bruxel, M., Zanella, C.M., Goetze, M., Buttow,
M.V., Palma-Silva, C., Bered, F. 2010. Seed dispersal and population structure
in Vriesea gigantea, a bromeliad from the Brazilian Atlantic Rainforest. Botanical
Journal of the Linnean Society 164: 317-325.
Paggi, G.M., Silveira, L.C.T., Zanella, C.M., Bruxel, M., Bered, F., Kaltchuk-
Santos, E., Palma-Silva, C. 2013. Reproductive system and fitness of Vriesea
friburgensis: a self-sterile bromeliad species. Plant Species Biology 28: 169–176.
Paula, C.C. & Silva, H.M.P. 2004.Cultivo prático de bromélias. Viçosa, Universi-
dade Federal de Viçosa.
Pereira, F.R.L. & Quirino, Z.G.M. 2008. Fenologia e biologia floral de Neoglazio-
via variegata (Bromeliaceae) na caatinga paraibana. Rodriguésia 59: 835-844.
Pereira, A.R., Pereira, T.S., Rodrigues, A.S., Andrade, A.C.S. 2008. Morfologia de
sementes e do desenvolvimento pós-seminal de espécies de Bromeliaceae. Acta
Botanica Brasilica 22: 1150-1162.
Proctor, M., Yeo, P., Lack, A. 1996. The Natural History of Pollination. Timber
Press, Portland, Oregon.
Queiroz, J.A., Quirino, Z.G.M., Lopes, A.V., Machado, I.C. 2016. Vertebrate
mixed pollination system in Encholirium spectabile: A bromeliad pollinated by
bats, opossum and hummingbirds in a tropical dry forest. Journal of Arid Envi-
ronments 125: 21-30.
Rios, P.A.F., Silva, J.B., Moura, F.B.P. 2010. Visitantes florais de Aechmea constan-
tinii (Mez) L. B. Sm. (Bromeliaceae) em um remanescente da Mata Atlântica do
Nordeste Oriental. Biotemas 23: 29-36.
Sazima, I., Vogel, S., Sazima, M. 1989. Bat pollination of Encholirium glaziovii, a
terrestrial bromeliad. Plant Systematics and Evolution 168: 167-179.
Sazima, M., Buzato, S., Sazima, I., 1995. Polinização de Vriesea por morcegos no
sudeste brasileiro. Bromélia 2: 29-37.
Siqueira Filho, J.A., Machado, I.C.S. 2001. Biologia reprodutiva de Canistrum
aurantiacum E. Morren (Bromeliaceae) em remanescente da Floresta Atlântica,
Nordeste do Brasil. Acta Botanica Brasilica 15: 427-443.
Smith, L.B. & Till, W. 1998. Bromeliaceae. In: K. Kubitzki (ed.). The families and
genera of vascular plants, IV flowering plants, Monocotyledons Alismatanae and
Commelinanae (except Gramineaee). Springer Verlag, Berlin, pp 74-99.
Tillich, H.J. Seedling diversity and the homologies of seedling organs in the order
Poales (Monocotyledons). Annals of Botany 100: 1413-1429.
Van Sluys, M. & Stotz, D.F. 1995. Patterns of hummingbird visitation to Vriesea
neoglutinosa in Espírito Santo, Southeastern Brazil. Bromélia 2:27-35.
Varassin, I.G. & Sazima, M. 2000. Recursos de Bromeliaceae utilizados por beija-
-flores e borboletas em mata atlântica no sudeste do Brasil. Boletim do Museu
de Biologia Mello Leitão 11/12: 57-70.
Versieux, L.M. 2005. Bromeliáceas de Minas Gerais: catálogo, distribuição geográ-

J. Bromeliad Soc. 66(2). 2017. 99

 SCIENCE Floral biology of Vriesea minarum

fica e conservação das espécies. Universidade Federal do Rio de Janeiro, Rio de

Janeiro.
Versieux, L.M. 2011. Brazilian plants urgently needing conservation: the case of
Vriesea minarum (Bromeliaceae). Phytotaxa 28: 35-49.
Versieux, L.M. 2012. Bromeliaceae. In: M.C. Jacobi & Carmo, F.F. (Orgs.). Diversi-
dade florística nas cangas do Quadrilátero Ferrífero. IDM Editora, Belo Hori-
zonte, Minas Gerais.
Versieux, L.M. & Machado, T.M. 2012. A new ornithophilous yellow-flowered
Vriesea (Bromeliaceae) from Serra do Caraça, Minas Gerais, Brazil. Phtotaxa 71:
36-41.
Versieux, L. M. & Wanderley, M.G.L. 2015. Bromélias-gigantes do Brasil. Capim
Macio & Offset, Natal, pp 200.
Versieux, L.M. & Wendt, T. 2006. Checklist of Bromeliaceae of Minas Gerais, Bra-
zil, with notes on taxonomy and endemism. Selbyana 27: 107-146.
Versieux, L.M. & Wendt, T. 2007. Bromeliaceae diversity and conservation in
Minas Gerais, Brazil. Biodiversity and Conservation 16: 2989-3009.
Versieux, L.M., Wendt, T., Louzada, R.B., Wanderley, M.G.L. 2008. Bromeliaceae
da Cadeia do Espinhaço. Megadiversidade 4: 98–110.
Vogel, S. 1969. Chripoterophilie in der neotropischen Flora. Neue Mitteilugen III.
Flora 148: 289-323.
Wendt, T., Canela, M.B.F., de Faria, A.P.G., Rios, R.I., 2001. Reproductive
biology and natural hybridization between two endemic species of Pitcairnia
(Bromeliaceae). American Journal of Botany 88: 1760-1767.
Wendt, T., Canela, M.B.F., Klein, D.E., Rios, R.I. 2002. Selfing facilitates repro-
ductive isolation among three sympatric species of Pitcairnia (Bromeliaceae).
Plant Systematics and Evolution 232: 201-212.
Yamamoto, L.F., Kinoshita, L.S., Martins, F.R. 2007. Síndromes de polinização
e de dispersão em fragmentos da Floresta Estacional Semidecídua Montana, SP,
Brasil. Acta Botanica Brasilica 21: 553-573.

[Editor’s notes: In a floral biology study, the aim is to determine in detail the way a
plant is able to produce seeds. Do the flowers need cross-pollination, or can they
self-fertilize? If pollinated, how do they interact with pollinators? We are interested
in these characteristics for endangered species because the details may provide clues
to the forces limiting the population growth of the species. For instance, pollinators
having a long history with the species - and presumably quite efficient in carrying out
pollination - may suddenly become unavailable due to changes in rainfall patterns,
temperature or the arrival of new competitors and/or predators. If pollination is now
carried out by a less efficient pollinator, the potential seed set could well be limited.
Of course, such details may be intriguing for non-endangered as well as endan-

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gered species. The plants in your own collection provide you with an opportunity
to make similar observations. You can start by determining when the flowers open
and when they close. Most of the cultivated bromeliads have seasonal blooming
cycles. In southern Florida, there are plants, such as Billbergia species and the mem-
bers of several different species groups in Aechmea that bloom during the Northern
Hemisphere Fall and Winter. Larger Neoregelia species tend to flower primarily in
Spring. A large variety of species bloom preferentially during the Summer.
It is also possible, and interesting, to keep track of when the flowers open and
close during the day. Most bromeliad flowers last only a single day or part of a day,
but - as indicated in this article - there are exceptions. Usually, a fully open flower
can be recognized by outward bending of the petal tips. In Neoregelia, and several
other genera, these tips are easily seen due to their large size and the way they bend
sharply away from the tube formed by the lower portion of the petals, often ending
up at right angles to the tube. In the case of Billbergia, it is common for the petal
tips to arch away from each other gradually with the two lower petals ultimately
recurving. In contrast, many species of Vriesea have only a small proportion of the
petal (less than 1/8 of an inch or 2-3 mm) bending out. Also, there are some species
where the petals expand, but the tips remain curved inward, and the only opening
is a hole where the tips of the petals pull slightly away from each other.
In either case, once you can recognize an open flower, you start observing your
blooming plant at progressively earlier times. With some plants, you may have to be
out watching the flowers before the sun comes up. With a night-blooming plant, you
might have to start your observations in the evening to catch the hour of opening.
It is also of interest to know how long the flower stays open, so you want to
record what hour the flower closes. Flower ‘closing’ is usually marked by a change in
the appearance of the petals. Sometimes the petals will darken, sometimes they will
start to turn a light brown. Often, this color change will be visible before the petals
show any sign of changing physically, but Neoregelia provides a major exception. In
Neoregelia species, the spreading lobes of the petals typically retain color while the
lobes unbend over a rather long period of time until they are erect and touching
each other. It is probable the biological closure of the flower occurs sometime within
this period of petal straightening, but we can define the hour of flower closure as
the time the petal lobes touch again. Another note regarding Neoregelia: the time
of flower closing is strongly influenced by the cultural conditions of the plant. In
general, the flower opens (the petal lobes spread outward) early in the morning.
For plants grown under high light conditions, the petal lobes can start to unbend
before noon. When plants are grown in more shade - or are observed on a cloudy
day - the fully spread petals persist for a longer time.]

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