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Bradleya 24/2006 39
Summary: The genus Micranthocereus includes
nine endemic Brazilian species distributed in the
states of Bahia, Minas Gerais, Goiás and
Tocantins. In the present study the floral biology
of M. flaviflorus, M. steckeri and M. purpureus
from “campo rupestre” vegetation of the Chapada
Diamantina, Bahia, was investigated. Data on
floral morphology and nectar production (concen-
tration and volume) were collected throughout
anthesis. Flowers of all species are tubular and
present coloured perianth-segments. Nectar is
accumulated within a nectar-chamber, located
inside the floral tube. Flowers of M. flaviflorus
and M. streckeri are predominantly nocturnal,
opening in the night (at about 7 p.m.). Each
flower lasts c.36 hours, with a concentration of
sugar in the nectar between approximately
18–24%. Both species present floral features typ-
ical for ornithophily, and were pollinated by the
hummingbird Clorostilbon aureoventris, whose
visits occurred in regular intervals and were
characterized by territorialist behaviour. Species
of bees and butterflies were also observed visiting
flowers of M. flaviflorus and M. streckeri. M.
streckeri was additionally visited by the hum-
mingbird Phaethornis squalidus, mainly in the
afternoon. Flowers of M. purpureus are noctur-
nal, and each flower lasts c.17 hours and present
longer corollas with wider diameter than those of
the other two species studied; sugar concentra-
tion in the nectar was about 21–22%. Three
sphingid and one bat species were observed visit-
ing flowers of M. purpureus, with a greater fre-
quency of visits of the sphingids. Pollen viability
was high (80–90%) and similar between the three
species of Micranthocereus studied.
Zusammenfassung: Die Gattung Micran-
thocereus umfasst neun in Brasilien endemische
Arten, und ist in den Bundesstaaten Bahia,
Minas Gerais, Goiás und Tocantins verbreitet. In
der vorliegenden Arbeit wurde die Blütenbiologie
der Arten M. flaviflorus, M. purpureus und
M. streckeri aus den “campos rupestres”
(Felssavannen) der Chapada Diamantina (Bahia)
untersucht. Während der gesamten Blühphase
wurden Daten über Blütenmorphologie und
Nektarproduktion (Konzentration und Volumen)
gesammelt. Die Blüten aller Arten sind
röhrenförmig and haben ein farbiges Perianth.
Der Nektar sammelt sich in der Nektarkammer,
die sich im Inneren der Blütenröhre befindet. Die
Blüten von M. flaviflorus and M. streckeri sind
hauptsächlich nachts geöffnet. Die Anthese
beginnt abends gegen ungefähr 19.00. Eine Blüte
dauert etwa 36 Stunden und hat eine
Zuckerkonzentration im Nektar zwischen
18–24%. Beide Arten weisen Blütenmerkmale
auf, die typisch für Vogelblumen sind. Sie
wurden von der Kolibriart Clorostilbon
aureoventris bestäubt, dessen Besuche in
regelmässigen Intervallen erfolgten und durch
BBrraaddlleeyyaa 2244//22000066pages 39 – 52
PPoolllliinnaattiioonn bbiioollooggyy ooff tthhrreeee BBrraazziilliiaann ssppeecciieess ooff MMiiccrraanntthhoocceerreeuussBBaacckkeebb.. ((CCeerreeeeaaee,, CCaaccttooiiddeeaaee)) eennddeemmiicc ttoo tthhee ““ccaammppoossrruuppeessttrreess””
Lidyanne Yuriko Saleme Aona1, Marlon Machado2, Emerson Ricardo Pansarin1,Cibele Cardoso de Castro3, Daniela Zappi4 and Maria do Carmo E. do Amaral11Dept. de Botânica, IB, Universidade Estadual de Campinas, Caixa Postal 6109, Cidade Universitária s.n.,13084-970, Campinas-SP, Brazil (email: [email protected]).2University of Zurich, Institute for Systematic Botany, Zollikerstrasse 107, CH-8008, Zurich, Switzerland.3Departamento de Biologia, Universidade Federal Rural de Pernambuco R. Dom Manoel de Medeiros, s/n- Dois Irmãos, 52171-900, Recife-Pernambuco, Brazil. 4Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK.
Bradleya 24/200640
territoriales Verhalten gekennzeichnet waren.
Ausserdem wurden verschiedene Arten von
Bienen und Schmetterlingen bei Blütenbesuchen
von M. flaviflorus und M. streckeri beobachtet.
Besonders am Nachmittag wurde M. streckeri
zusätzlich von der Kolibriart Phaethornis
squalidus besucht. M. purpureus ist
nachtblühend, und jede Blüte bleibt etwa 17
Stunden geöffnet. Ihre Blütenröhren sind länger
und weisen auch einen grösseren Durchmesser
auf als diejenigen der beiden anderen Arten. Die
Zuckerkonzentration des Nektars betrug
21–22%. Drei Arten von Schwärmern und eine
Fledermausart wurden bei Blütenbesuchen
beobachtet, wobei die Schwärmer häufigere
Besuche zeigten als die Fledermäuse. Die
Lebensfähigkeit des Pollens aller drei
untersuchten Arten war hoch und betrug ca.
80–90%.
Resumo: O gênero Micranthocereus inclui nove
espécies endêmicas do Brasil e restritas aos
Estados da Bahia, Minas Gerais, Goiás e
Tocantins. Foi estudada a biologia floral de
M. flaviflorus, M. steckeri e M. purpureus em
campos rupestres na Chapada Diamantina, BA.
Análises da morfologia floral e medições do
volume e concentração do néctar desde a antese
até o pré-fenescimento das flores foram
realizadas. As flores das três espécies estudadas
são tubulares, apresentando segmentos do
perianto diversamente coloridos. O néctar é
armazenado na câmara nectarífera, localizada no
interior do tubo floral. As flores de M. flaviflorus
e M. streckeri apresentam antese noturna,
abrindo no início da noite (aproximadamente 7
horas da noite). Cada flor dura cerca de 36 horas
e apresenta concentração de açúcares entre 18 e
24%. Ambas as espécies apresentam
características típicas de flores polinizadas por
aves e são visitadas e polinizadas pela mesma
espécie de beija-flor, Clorostilbon aureoventris. As
visitas ocorreram em intervalos regulares e o
beija-flor apresentou comportamento
territorialista, quando dois indivíduos visitavam
simultaneamente as flores. Visitas de abelhas e
borboletas também foram observadas nestas
espécies. M. streckeri também foi visitado por
outro beija-flor, Phaethornis squalidus, que
efetuou um maior número de visitas no período
vespertino. As flores de M. purpureus
apresentam antese noturna, e cada flor dura
aproximadamente 17 horas. O comprimento e
diâmetro floral são superiores aos das espécies
diurnas e a concentração de açúcares varia entre
21 e 22%. Foram observadas visitas de três
espécies de esfingídeos e de uma espécie de
morcego. Foi observada uma maior freqüência de
visitas dos esfingídeos em relação ao morcego. O
teste de viabilidade polínica foi semelhante entre
as espécies estudadas (80–90%).
IInnttrroodduuccttiioonn
The family Cactaceae forms a monophyletic
group (Wallace & Cota, 1996) with approximate-
ly 100 genera and 1300 species distributed near-
ly exclusively in the New World (Barthlott &
Hunt, 1993). Eastern Brazil presents the third
main geographical centre of diversity of the fam-
ily (Zappi, 1994; Taylor & Zappi, 2004). The core
geographical area defined within Eastern Brazil
has been recognized primarily for its remarkable
endemism of Cactaceae genera and species, espe-
cially those of the “caatingas” of the North-east-
ern states and associated highland known as
“campos rupestres” (Taylor & Zappi, 2004).
Cactaceae present a wide range of floral fea-
tures regarding shape, colour, size, odour, time of
anthesis and position of the reproductive parts,
which indicate pollination by several groups of
biotic agents (Porsch, 1939; Hunt & Taylor, 1990;
Vogel, 1990), like medium-sized (McFarland et
al., 1989) and large bees (Viana et al., 2001),
sphingids and other moths (Suzan et al., 1994;
Holland & Fleming, 1999), hummingbirds
(Scobell & Scott, 2002), bats (Ruiz et al., 1997;
Tschapka et al., 1999), or even nocturnal and
diurnal vectors in the same species, such as by
hummingbirds and bats (Fleming et al., 1996;
Sahley, 2001). According to Vogel (1990), around
9% of the species of Cactaceae are pollinated by
hummingbirds. Other studies on Cactaceae also
reported several reproductive strategies like self-
compatibility (Bianchi et al., 2000) and self-
incompatibility (Boyle, 1996; Metz et al., 2000),
as well as the presence of sexual and asexual
reproduction in the same species (Mandujano et
al., 1998; Negron-Ortiz, 1998).
The Brazilian genus Micranthocereus Backeb.
(Cactoideae, Cereeae) includes nine species dis-
tributed in the states of Minas Gerais, Bahia,
Goiás and Tocantins (Taylor & Zappi, 2004).
Studies concerning the reproductive biology of
Brazilian Cactaceae recorded melitophily in
Opuntia Mill. (Schlindwein & Wittmann, 1995,
1997), sphingophily in Cereus Mill. (Silva &
Sazima, 1995; Locatelli & Machado, 1999a) and
Selenicereus (Berg.) Britton & Rose (Barthlott et
Bradleya 24/2006 41
al., 1997), ornithophily in Melocactus Link &
Otto and Opuntia (Locatelli & Machado, 1999b;
Raw, 1996), and chiropterophily in Pilosocereus
Byles & Rowley (Locatelli et al., 1997). The repro-
ductive biology of Micranthocereus species is
unknown, but the genus presents great diversity
in flower morphology.
The main goal of this study was to investigate
and compare the pollination biology of three
Brazilian Micranthocereus species: M. flaviflorus
Buining & Brederoo, M. streckeri van Heek & van
Criekinge and M. purpureus (Gürke) Ritter
endemic to northeast Brazil.
MMaatteerriiaall aanndd MMeetthhooddss
The floral biology of the species studied was
investigated in the Chapada Diamantina (Bahia
State), a mountain complex that presents a large
diversity of Cactaceae species (Machado, 1999;
Taylor & Zappi, 2004) and which is located in the
Cadeia do Espinhaço, a mountain range which
extends over c.1000 km from NE to SE Brazil.
The study was conducted in August 2001 for M.
flaviflorus and M. streckeri and in October 2003
for M. purpureus.
The studied population of M. flaviflorus con-
sisted of c. 20 individuals located in the munici-
pal district of Morro do Chapéu (10°50’S–12°00’S
and 40°40’W–41°30’W)1
. The plants grow in
quartzitic sand in an area occupied by transition-
al vegetation including ‘cerrado’ (savanna),
‘campo rupestre’ (upland or highland savanna)
and ‘caatinga’ (deciduous low thorn forest). The
population of M. streckeri consisted of 40 individ-
uals and was located upon rocks in an area of
‘campo rupestre’ vegetation surrounded by forest
areas, being endemic to the study area, in the
Municipality of Seabra (12º25’52S and
41º59’36W). M. purpureus presents a much larg-
er distribution range, occurring from Rio de
Contas to Jacobina (Aona, 2003). The population
studied consisted of 40 individuals and is located
in the Municipality of Morro do Chapéu
(11º36’03S and 41º09’52W), occurring in an area
of ‘campo rupestre’ vegetation.
The growth habit, phenology and floral fea-
tures, such as morphology, colour and scent, were
recorded through field observation. Floral lifes-
pan and anthesis events were recorded for a pop-
ulation of each species through the observation of
tagged flowers from pre-anthesis until flower
senescence. Fresh flowers of each species were
randomly collected in a minimum of 15–30 indi-
viduals/species, fixed in FAA 50, stored in alcohol
70% and used for illustrations and for floral mea-
surements (flower-tube length and diameter,
17–32 flowers/species). Floral measurements
were obtained with a digital calliper (error 0.01
mm) and compared between species with an
ANOVA analysis coupled with a t-Test LSD
(Sokal & Rohlf, 1969).
Nectar concentration and volume were esti-
mated in flowers bagged from the pre-anthesis
stage, using a pocket refractometer and micro-
liter syringes, respectively. Data were collected c.
24 hours after the beginning of the anthesis for
M. flaviflorus (n=12 flowers) and M. streckeri
(n=10 flowers, five individuals for both), and 3
hours (n=10, eight individuals) and 9 hours (n=8,
six individuals) after anthesis for M. purpureus.
Pollen viability was estimated using the acetate-
carmine technique (Radford et al., 1974, 5-7 flow-
ers/species, 200 pollen grains/flower).
Floral visitors were recorded through direct
observations in the field, in a total of 10h for
M. flaviflorus, 40h for M. streckeri and 40h for
M. purpureus. Time and duration of visiting
bouts were recorded, as well as the visitor’s
behaviour on the flowers, such as contact with
the anthers and the stigma, type of floral
resource collected and interactions with other
visitors. Buds/mature flowers were tagged in the
afternoon and examined early in the morning for
detecting possible nocturnal pollination in
M. flaviflorus and M. streckeri. The humming-
birds were identified in the field and using pho-
tographs taken during their visits, then com-
pared with ilustrations in Ruschi (1986) and
Grantsau (1989).
Others floral visitors of M. purpureus were
identified using photos taken during their visits
to the flowers; these photos were also used to
check the sites of pollen deposition on their bod-
ies. Insect visitors of all species were collected
and identified as far as possible through compar-
ison with specimens deposited in the Museum of
the Universidade Estadual of Campinas (ZUEC).
Pollinators were characterized based on their fre-
quency of visits and visiting behaviour.
Frequency of visits of the main floral visitors of
1
This population belongs to the taxon recently recognized as M. polyanthus (Werderm.) Backeb. subsp. alvinii M. Machado &
Hofacker. These plants are to some degree intermediate between M. flaviflorus and M. polyanthus (Werderm.) Backeb. which are
similar species (Taylor & Zappi, 2004: 355).
Bradleya 24/200642
each species was compared using a Student’s t
test (Sokal & Rohlf, 1969).
Voucher specimens were deposited in the
Herbarium of the Universidade Estadual de
Campinas (M. flaviflorus: UEC 120736,
M. streckeri: UEC 139459 and M. purpureus UEC
132282).
RReessuullttss
MMoorrpphhoollooggyy aanndd fflloorraall bbiioollooggyy
The plants of all studied species are columnar,
branching at the base, with decumbent or erect
stems and covered with flexible, golden to pale
golden spines. Flowers are born in a specialized
fertile zone (cephalium), more or less perpendicu-
lar and lateral to the stem axis. The flowers pre-
sent a nectariferous chamber with a nectary
inside the base of the flower-tube, where the nec-
tar is produced and accumulated (Figures 1–3).
All the species presented high pollen viability
(77–90%) which is similar between species
(F=3.35, P=0.06).
In M. flaviflorus and M. streckeri the fertile
zone consists of a lateral, superficial to sunken
cephalium with flower-bearing areoles, which
have white to yellowish hairs with long, pale to
brownish golden bristles in M. flaviflorus, and
compact, white to brownish hairs and long, pale
golden to reddish brown bristles in M. streckeri.
In M. purpureus, the fertile portion of the stem is
a lateral cephalium sunken into the stem and
composed of congested flower-bearing areoles
which bear pale brown, pinkish or grey, abun-
dant, loose or compact hair and few long golden
or brownish bristles.
M. flaviflorus flowered from May to
September and produced fruits from July to
November, whereas M. streckeri produced flowers
from May to September and fruits from August to
December. Both species present an annual
3mm
3mm
FFiigguurree 11. Longitudinal section of flower of M. flavi-florus. Note the nectar chamber (arrow). Illustrationby R. Lupo.
FFiigguurree 22. Longitudinal section of flower of M. streck-eri. Note the nectar chamber (arrow). Illustration byR. Lupo.
Bradleya 24/2006 43
flowering pattern (sensu Newstron et al., 1994).
Flowers of M. flaviflorus have outer perianth-
segments spreading to erect, reddish pink; the
inner perianth-segments opened very slightly
and are yellow to pale cream (Figures 4 & 5);
those of M. streckeri have outer perianth-seg-
ments spreading and deep pink, the inner peri-
anth-segments are erect and purplish pink
(Figures 6–9). The flowers of both species are
tubular, the stamens are positioned inside the
floral tube; the stigma is 4- to 6-lobed, and the
stigma-lobes are also inserted (Figures 1–3).
Flower length of M. flaviflorus (12.3 ± 0.1mm,
mean ± SE) was smaller than that of M. streckeri
(13.1 ± 1.2mm, mean ± SE, t=-2.618, P=0.01,
n=32 for both), whereas the diameter was similar
(1.8 ± 0.2mm for M. flaviflorus, 1.8 ± 0.9mm for
M. streckeri, mean ± SE, t=-1.593, P>0.01, n=32
for both, 1).
Flowers of M. flaviflorus and M. streckeri
started to open at about 7 p.m. (5–10 flowers each
individual daily), and lasted c.36 hours, wilting
in the morning of the third day. In recently
opened flowers the stigma-lobes were closed and
the pollen was released; between the end of the
first day and the beginning of the second day of
the anthesis, the stigma-lobes opened and
became perceptibly moist. The flowers of both
species were scentless and produced similar nec-
tar volumes, whereas the concentration of sugar
was higher in M. flaviflorus (Table 1).
The flowering period of M. purpureus
occurred from May to November, and the plants
developed fruits between July and December,
indicating an annual flowering pattern (sensu
Newstron et al., 1994). The floral tube of M. pur-
pureus is deep pink-magenta, the outer perianth-
segments are recurved and deep pink to reddish;
the inner perianth-segments are spreading or
recurved, white. The stamens are numerous
(c.400), being disposed as a dense ring inside the
tube. The style is long, tube-like and exceeds the
anthers by about 10mm; the exerted stigma is 10-
lobed. Flowers are larger than those of the other
two species (F=793.64 for corolla length and
F=239.81 for corolla diameter, P=0 for both,
Table 1).
Individuals of Micranthocereus purpureus
opened 2-3 flowers each in the afternoon (5 p.m.),
which reached full anthesis 2 hour later,
remained open during the night, and were com-
pletely closed by 10–11 a.m. the next morning.
When the flower was completely open, the stig-
mas were moist (indicating receptivity), laterally
or adaxially displaced; after c. 2 hours it began to
move slowly towards the center of the flower,
where it remained until the end of anthesis.
The flowers of M. purpureus presented a
slightly sweet and sour scent. Sugar concentra-
tion in the nectar decreased during the period
between 8 p.m. and 2 a.m. Nectar volume was
higher in M. purpureus than in the other two
species (F=142.16, P=0), which presented similar
volume values (P=0.21); on the other hand, the
highest nectar concentration was observed in M.
flaviflorus, being followed by M. purpureus and
M. streckeri (F=18.29, P<0.05 for all comparisons,
Table 1).
PPoolllliinnaattiioonn pprroocceessss
The main floral visitors of Micranthocereus flavi-
florus were males of the hummingbird
Chlorostilbon aureoventris Boucier & Mulsant
(Figure 4), which were observed from early morn-
ing until 2 p.m. This hummingbird visited the
flowers at regular intervals of approximately
10–30 minutes. The females visited the flowers
only sporadically, being frequently chased away
by the males during the visits. Chlorostilbon
aureoventris has a straight bill (19.09 ± 2.1mm
length, mean ± SE, n = 5), that contacted the
5mm
FFiigguurree 33. Longitudinal section of flower of M. pur-pureus. Note the nectar chamber (arrow). Illustrationby R. Lupo.
Bradleya 24/200644
FFiigguurree 44. Female of Chlorostilbon aureoventris visiting flower of M. flaviflorus. FFiigguurree 55. The butterfly Phoebisphilea on flowers of Micranthocereus flaviflorus. FFiigguurree 66. Males of Chlorostilbon aureoventris visiting flower ofM. streckeri. FFiigguurree 77. Males of Chlorostilbon aureoventris on flower of M. streckeri. Note the presence of pollengrains on the bill of the hummingbird. Photos by E.R. Pansarin.
4 5
6 7
Bradleya 24/2006 45
FFiigguurree 88. The hummingbird Phaethornis squalidus visiting flower of M. steckeri. FFiigguurree 99. The hesperid Vettius sp.(arrow) on flowers of M. streckeri. FFiigguurree 1100. The hawkmoth Agrius cingulatus visiting a flower of M. purpureus.Note the extend proboscis being introduced in the perianth. FFiigguurree 1111. The hawkmoth Erynnyis alope visiting aflower of M. purpureus. Note the extend proboscis being introduced in the perianth. Photos 8 & 9: E.R. Pansarin;10 & 11: L.Y.S. Aona.
8 9
10 11
Bradleya 24/200646
anthers and the stigma when collecting floral
nectar. The visitor prevented access by other
individuals of the same species to the population
of plants which it defended.
The butterfly Phoebis philea Johansson
(Figure 5) was occasionally observed visiting M.
flaviflorus flowers during the hottest hours of the
day (12 to 3 p.m.), when it collected nectar and
contacted the sexual parts of the flower. The bee
Trigona spinipes Fabricius was observed visiting
flowers of M. flaviflorus mainly from 10.30 to 11
a.m. and from 2 to 5 p.m., when it collected pollen
directly from the anthers, often damaging both
anthers, perianth-segments and floral tube, but
without contacting the stigma.
Flowers of M. streckeri were also pollinated by
Chlorostilbon aureoventris (Figures 6 & 7). In
this species the females were more frequent as
pollinators than males. The visits occurred
between 6 a.m. and 4 p.m., being more frequent
in the morning and occuring in intervals of
approximately 30 minutes, rarely up to 60 min-
utes. In the afternoon the visits were rare and
took place at intervals of 1hour 10 minutes,
approximately. Females of C. aureoventris pre-
sented the same territorialist behaviour observed
in males in M. flaviflorus, mostly during the
morning, when they defended the population
from males.
The hummingbird Phaethornis squalidus
Temminck was sporadically observed pollinating
M. streckeri flowers in late afternoon (Figure 8),
in a similar frequency to that of Chlorostilbon
aureoventris (t=0.896, P=0.394, Figure 12); birds
of this species were also chased away by females
of C. aureoventris. All hummingbird species had
the pollen grains deposited on the bill. In M. flav-
iflorus and M. streckeri, the visits by both species
of hummingbird to each flower were brief (c. 2
seconds). In most visits both hummingbirds visit-
ed more than one flower of each plant.
Some insects, like the skipper Vettius sp.
(Lepidoptera: Hesperiidae: Hesperiinae) species
(Figure 5), occasionally visited M. streckeri flow-
ers along the day, collected nectar and sometimes
touched the sexual parts of the flower with their
proboscis, being considered occasional pollina-
tors. Honey bees, Apis melifera, were observed on
flowers of M. streckeri mainly in the morning,
when they visited more than one flower of each
individual, or even flowers of the same cephali-
um. They landed at the apex of the floral-tube
and collected large amounts of pollen directly
from the anthers, sometimes causing anther
damage, and rarely contacted the stigma, thus
acting mainly as pollen robbers. Trigona spinipes
was also observed visiting flowers of M. streckeri
at the same period of the day and presenting sim-
ilar behaviour to that observed with M. flavi-
florus. Other occasional visitors were some non-
identified ants, beetles and caterpillar species,
which were observed cutting (ants) and eating
(beetles and caterpillars) floral parts.
Flowers of M. purpureus were visited by
the bat Lonchophylla mordax Thomas
(Phyllostomidae, Glossophaginae), which was
observed after dusk until 5 a.m., in intervals of
30–60 minutes, often approaching the plant from
the same direction of the cephalium, hovering in
front of the flowers and visiting different individ-
uals at each bout. During its visits, this bat intro-
duced its head inside the floral-tube, touching
the stigma and receiving the pollen grains on the
head, neck and shoulders. Lonchophylla mordax
also visited flowers of Encholirium brachypodum
L. B. Sm. & Read (Bromeliaceae) in a higher fre-
quency (intervals of 5–30 minutes) than that
observed for M. purpureus, but displaying a sim-
ilar behaviour.
The sphingids Agrius cingulata Fabricius
Corolla NectarSpecies
Length (mm) Diameter (mm) Vol (µl) Conc (%)
M. flaviflorus 12.35 ± 0.99b 1.76 ± 0.25b 5.17 ± 2.25b 23.33 ± 1.28b
M. streckeri 13.09 ± 1.23c 1.85 ± 0.18b 7.3 ± 3.8b 19.3 ± 1.83c
M. purpureus 31.88 ± 1.87a 16.35 ± 1.49a 143.81 ± 49.32a 21.18 ± 1.54a
TTaabbllee 11. Floral morphometrics and nectar features (mean ± sd for both) of three species ofMicranthocereus in northeast Brazil. Different letters in the same column indicate statistically different data.Vol.: volume, Conc.: concentration.
Bradleya 24/2006 47
(Figure10), Erynnyis alope Drury (Figure11),
Erynnyis ello L. (Sphingidae) were observed vis-
iting the flowers of M. purpureus, between 9 p.m.
and 4.30 a.m., with a peak between 9 p.m. and 12
a.m. (Figure 13). The hawkmoths approached the
flower and introduced the proboscis into the nec-
tar chamber, hovering at variable distances in
front of the flower. Photographs of moths forag-
ing at flowers reveal thick deposits of pollen
along their proboscis. The hawkmoths sometimes
touched the flowers with their forelegs, mainly E.
ello, with visits lasting up to three seconds. All
hawkmoths displayed a similar visitation pat-
tern, visiting the flowers more or less in the same
sequence and at intervals varying from 5–30
minutes, rarely up to 60 minutes. Agrius cingu-
lata was the most commonly observed visitor,
with visits lasting up to 15–20 seconds while
making circular movements with the proboscis.
Frequency of visits of sphingids was greater than
that of the bats (t = -2.24, P=0.02, Figure 13).
During anthesis a large number of small bee-
tles were found inside the flowers of M. pur-
pureus, remaining there even after flower senes-
cence. They were never seen flying from flower to
flower or touching the stigma. It was not possible
to observe what kind of floral resource these
insects explored. The flowers of M. purpureus
were also visited by the hummingbirds
Chlorostilbon aureoventris in the late afternoon
of the first day and Augastes lumachellus Lesson
in the early morning of the following day.
However, the hummingbird visits were rare and
it was not possible to observe whether contact of
anthers or stigmas occurred. Apis melifera and
Trigona spinipes were observed between 5–8 a.m.
and 4 and 5 p.m. (Figure 13), respectively, dis-
playing the same behaviour as was observed with
M. flaviflorus and M. streckeri (Figure 12).
DDiissccuussssiioonn
Most floral features of M. streckeri and M. flavi-
florus are similar to those displayed by species
pollinated by hummingbirds in tropical commu-
nities, such as the easily accessible and unscent-
ed flowers, with tubular and conspicuously
coloured perianth, clear separation between flo-
ral resource (nectar) and sexual parts and nectar
with a relatively low concentration of sugars
(Faegri & van der Pijl, 1980; Arzimendi &
Ornelas, 1990; Araujo, 1996, Sazima et al., 1996;
Locatelli & Machado, 1999b; Buzatto et al., 2000;
Castro & Oliveira, 2001, 2002; Castro & Araujo,
2004), including Cactaceae species (Scogin, 1985).
The short-tubed flowers of M. flaviflorus and
M. streckeri allow the visits of both short- and
long-billed visitors, like Chlorostilbon aureoven-
tris and Phaethornis squalidus, respectively
(Grantsau, 1989) however only M. streckeri was
visited by both species. The absence of P.
squalidus on M. flaviflorus flowers may be relat-
ed to the lack of forest habitats near the studied
population, since this species is a typical pollina-
tor in Atlantic forests in Brazil (Buzato et al.,
2000). This hummingbird seemed to prefer indi-
viduals of M. streckeri located in areas at lower
elevations, which are close to a wooded area. The
period in which P. squalidus and Trigona spinipes
visited M. streckeri flowers (after 2 p.m.), and
that in which T. spinipes visited M. flaviflorus
flowers coincided with the decrease in the num-
ber of C. aureoventris visits, a strategy that prob-
ably minimizes the chances of being attacked by
this hummingbird.
It was observed in the populations of
Micranthocereus streckeri that Phaethornis
squalidus invades the territory of Chlorostilbon
aureoventris after 11 a.m. (Figure 12). According
to Buzato et al. (2000), hermit hummingbirds
such as P. squalidus are the major pollinators of
hummingbird-pollinated of floras in Brazilian
forests. Phaethornis squalidus visited the plants
that occur near to the valley, nearby the forested
area. This behaviour might be related with the
visits decrease of C. aureoventris after 3 p.m. and
the visits increase of P. squalidus.
The decrease in the frequency of visits of
Chlorostilbon aureoventris to the flowers of M.
flaviflorus after 2 p.m. could be explained by the
presence of a sympatric Cactaceae species,
Melocactus paucispinus Heimen. & R. J. Paul,
whose flowers opened approximately at 2 p.m.
and were also visited by C. aureoventris.
However, it is necessary to test if this humming-
bird really prefers M. paucispinus flowers in com-
parison to those of M. flaviflorus.
The visiting behaviour of Chlorostilbon aure-
oventris to the flowers of M. flaviflorus and M.
streckeri revealed two types of feeding strategies:
territoriality (sensu Feinsinger, 1978; Stiles,
1981) and traplining. The traplining strategy
favours cross-pollination because it maximizes
pollen dispersion among different individuals
(Janzen, 1971), whereas the territorialist behav-
iour may reduce pollen flow in a population
(Linhart, 1973). The occurrence of these two
types of foraging behaviour (territorialist and
traplining) was also recorded for C. aureoventris
Bradleya 24/200648
in the flowers of Melocactus zehntneri (Britton &
Rose) Luetzelb. and Opuntia palmadora Britton
& Rose by Locatelli & Machado (1999b).
The protandry observed in M. flaviflorus and
M. streckeri is considered a reproductive strategy
that minimizes the interference between male
and female functions as well as the chances of
self-pollination (Webb & Lloyd, 1986). Protandry
was not found in M. purpureus, where the posi-
tion of the stigma (adaxial or lateral) in relation
to the stamens changed from adaxial or lateral to
central in the flower’s lifespan.
Flowers of M. purpureus present some typical
chiropterophilous features such as pale colour, a
short floral tube with wide aperture, nocturnal
anthesis and large amounts of nectar (Vogel,
1969; Faegri & van der Pijl, 1980). There is evi-
dence that the presence of a lateral sunken
cephalium, composed by congested, hairy flower-
bearing areoles, forming a cushion-like structure
is related with the protection of bat’s wings dur-
ing pollination (Zappi, 1994). The exerted posi-
tion of the stigma of M. purpureus seems to
favour cross-pollination because it is the first
reproductive part to be touched by the floral vis-
itors (Sazima & Sazima, 1975). However, a
6
3
0
8-9 9-10 10-11 11-12 12-13 13-14 14-15 15-16 16-17
Time Interval
Nu
mb
er
of
Vis
its
FFiigguurree 1122. Frequency of visiting bouts of M. flaviflorus and M. streckeri pollinators in NE Brazil. Males ofChlorostilbon aureoventris on flowers of M. flaviflorus (hatched bars); Phaethornis squalidus (grey bars) and maleof C. aureoventris (black bars) on M. streckeri flowers.
12
12
8
6
4
2
0
17-18 18-19 19-20 20-21 21-22 22-23 23-24 24-01 01-01 02-03 03-04 04-05 05-06
Time Interval
Nu
mb
er
of
Vis
its
FFiigguurree 1133. Frequency of visiting bouts of M. purpureus pollinators in NE Brazil. Sphingids (hatched bars),Loncophylla mordax (white bars), Chlorostilbon aureoventris (black bars) and Augastes lumachellus (grey bars).
Bradleya 24/2006 49
relatively low frequency of visits by bats was
recorded. The horizontally disposed position of
the flowers, as well as its presence at only on one
side of the plants of M. purpureus plants are fea-
tures expected in chiropterophilous species
(Vogel, 1969, Sazima et al., 1995; Machado et al.,
1998), because it seems that the one-side presen-
tation of the flowers facilitates their access by
bats, which are less able to maneuver in flight
than bees or hummingbirds. The low number of
flowers and sweet scent presented during the
anthesis by M. purpureus was found in bat-polli-
nated species in general (Sazima & Sazima,
1978; Machado et al., 1998; Sazima et al., 1999)
as well as in other bat-pollinated Cactaceae
species (Locatelli et al., 1997).
The regular paths coupled with the intervals
between visiting bouts observed for Lonchophylla
mordax visits to M. purpureus indicate a trapline
behaviour, as has been recorded for
Glossophagine species when feeding on flowers
(Baker, 1973; Fleming, 1982; Sazima et al., 1999).
This foraging pattern was already recorded in
several studies on bat-pollinated flowers in the
Brazilian Atlantic rainforest (Sazima et al., 1994,
Machado et al., 1998; Sazima et al., 1999),
“restinga” (Locatelli et al., 1997) and for L. boker-
manii in “campo rupestre” (Sazima et al., 1989).
The flowers of bromeliad Encholirium brachypo-
dum are in the great number (c.30 flowers/inflo-
rescence daily) than M. purpureus and have dis-
agreeable odour, more typical of bat-pollinated
species. These characters observed in E. brachy-
podium at the study site may partially explain
the preference of the L. mordax for the bromeliad
and the irregular intervals in feeding bouts on M.
purpureus.
Despite the hawkmoths being generally con-
sidered less efficient and less important pollina-
tors than bats in chiropterophilous species (sensu
Baker et al., 1971; Sazima & Sazima, 1978;
Sazima et al., 1994), these insects were more fre-
quently observed visiting M. purpureus flowers
than bats. These results indicate that M. pur-
pureus may have, at the sudy site, a mixed bat-
hawkmoth pollination system, similarly to the
one described for Lafoensia densiflora Pohl
(Silberbauer-Gottsberger & Gottsberger, 1975)
and for Cereus peruvianus auctt. [=C. hildmanni-
anus K. Schum.] (Silva & Sazima, 1995). In fact,
M. purpureus seems to present floral features
such as the flower odour, which is weak and
sweet, rather than strong and disagreeable that
are somewhat ambiguous between bat and hawk-
moth syndromes, suggesting an adaptation to
attract both pollinator types. Moreover, the
traplining strategy presented by many hawk-
moth species (Janzen, 1971), that was also
observed in this study, coupled with their quick
movements and long flight distances (Linhart &
Mendenhall, 1977), favour cross-pollination.
Despite the frequent presence of beetles with-
in the flowers of Micranthocereus purpureus,
similarly observed in other species of Cactaceae
(Silva & Sazima, 1995; Locatelli et al., 1997),
some studies suggested that these insects are not
important pollen vectors for most cacti species
(Grant & Hurt, 1979), but seem to act only as
robbers (Locatelli et al., 1997). The humming-
birds and bees that were observed contacting
anthers and stigma during their visits to M. pur-
pureus flowers should not be considered pollina-
tors because no stigma receptivity was observed
in these periods of anthesis (Figure 13).
Moreover, the flowers had nearly empty anthers
when visited by Augastes lumachellus Lesson,
which was observed only once; this Trochilidae
species was observed using M. purpureus hairs
for building its nest (Machado et al., 2003). The
potential for using both nocturnal and diurnal
pollinators is known in Cactaceae (McGregor et
al., 1962) and in other chiropterophilous
angiosperms (Buzato et al., 1994; Sazima et al.,
1994).
The range of nectar concentration of M. pur-
pureus was slightly higher than the values
recorded for some Neotropical bat-pollinated
species (5%–29%, often 15%–17%, von Helversen,
1993; Sazima et al., 1999). Scogin (1985) com-
pared nectar analyses in some Cactaceae species
as 22–30%, 15–34% and 17–26%, for those
respectively pollinated by hummingbirds, moths
and bats. The value found for M. purpureus was
similar to that found in other Brazilian bat-polli-
nated Cactaceae (Locatelli et al., 1997) and in
species of other families in Brazil (Sazima et al.,
2003). The present study found overlapping val-
ues of sugar concentration between
Micranthocereus, with the two hummingbird pol-
linated species (M. flaviflorus and M. streckeri) at
each range of the spectrum, while the bat polli-
nated M. purpureus had intermediate values
between the two (Table 1).
It was also found that the range of variation
in sugar concentrations in Micranthocereus may
favour relationships with less specific pollinators
than was initially expected. Tribe Cereeae
(Taylor & Zappi, 2004) comprises several closely
Bradleya 24/200650
related genera, each one with more than one pol-
linator and sometimes displaying gradients
between pollination syndromes. For example,
Stephanocereus and Coleocephalocereus are like-
ly to be pollinated by bats and hummingbirds,
and species of Pilosocereus are pollinated by bats
and hawkmoths was studied by Locatelli et al.
(1997), Locatelli & Machado (1999a) and E. A.
Rocha, pers. com.). Our results show a remark-
able variability in the flower biology within the
genus Micranthocereus.
AAcckknnoowwlleeddggeemmeennttss
We thank Dr. Nigel Taylor and Dr. Volker
Bittrich for kindly read the manuscript, Dr. Keith
J. Brown for identification of the species sphin-
gids, Dr. Ivan Sazima and Dr. Marlies Sazima for
identification of the bat species, Ludmila
Mickeliunas and Renato P. Oliveira for their
assistance in the field studies and Rogério Lupo
for the illustrations. This study is part of a
Master thesis by the first author for the post-
graduation course in Plant Biology at the
‘Universidade Estadual de Campinas’ (São Paulo,
Brazil). This work was supported by the
Research Support Foundation of São Paulo State
- FAPESP (process no. 00/00369-7).
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