ECOTROPICA 17: 91–102, 2011
© Society for Tropical Ecology
DIVERSITY OF FLOWER VISITORS AND THEIR ROLE FOR
POLLINATION IN THE ORNITHOPHILOUS BROMELIAD
VRIESEA FRIBURGENSIS IN TWO DIFFERENT HABITATS IN
SOUTHERN BRAZIL
Simone Schmid1, *, Volker S. Schmid1, Anne Zillikens1,2 & Josefina Steiner2
1
Microbiological Institute, University of Tübingen,
Auf der Morgenstelle 1, 72076 Tübingen, Germany
2
Department of Cell Biology, Embryology and Genetics (BEG),
Centre of Biological Sciences (CCB), Federal University of Santa Catarina (UFSC),
Campus Universitário, 88.040-900 Florianópolis, SC, Brazil
Abstract. In order to analyze species richness of flower visitors to the bromeliad Vriesea. friburgensis, and to relate the visitor
spectrum to resource availability and differences in habitat, we studied its floral biology in two habitat types: dune vegetation and secondary Atlantic rain forest on Santa Catarina Island, southern Brazil. Flowering extends from October to
February, the anthesis is diurnal. We found the reproductive system to be partially autogamous without the possibility of
intra-floral selfing. Therefore the bromeliad is pollinator-dependent, but the flowers do not need to be cross-pollinated.
Mean nectar sugar concentration was 20.7% with a high sucrose proportion. Flowers secreted 73.9 μl nectar per day.
Although the flowers show ornithophilous features like tubular and scentless flowers and higher energetic nectar in the
morning hours, besides two hummingbird species we recorded 28 species of insects and spiders also associated with the
flowers of V. friburgensis. Species richness of flower visitors was higher in restinga than in secondary forest. In both habitat
types hummingbirds and bees were the most frequent visitor groups, but whereas hummingbirds were the most frequent
animals visiting flowers in secondary forest, followed by bees, the opposite was the case in the restinga habitats. Because
V. friburgensis is partially autogamous, small bees might also be pollinators, transferring self-pollen. Thus, there is redundancy in the pollination service provided by birds and bees, leading to a high probability of successful reproduction in this
bromeliad species. Accepted 31 January 2011.
Keywords: Bees, Bromeliaceae, flowering biology, hummingbird, nectar analysis, ornithophily, Santa Catarina Island, southern
Brazil, visitation frequency.
INTRODUCTION
The Neotropical plant family Bromeliaceae comprises about 2800 epiphytic, lithophytic, and terrestrial forms, many with large showy flowers (Benzing 2000). Flower morphology, floral rewards, and
flowering phenology constitute so-called floral syndromes, which have an influence on the flower visitor
community and have been regarded as signals for
specific flower visitor groups that can act as pollinators (Fenster et al. 2004). In bromeliads, the ornithophilous syndrome is commonest (Benzing 2000,
Kessler & Krömer 2000) and hummingbirds appear
to be effective pollinators (Benzing 2000). On the
other hand, there are several reports of insects, e.g.
bees and butterflies, visiting bromeliad flowers (Ber-
* e-mail: simigrohme@hotmail.com
nardello et al. 1991, Wendt et al. 2001, 2002;
Canela & Sazima 2003, 2005; Schmid et al. 2011b).
In particular, many short-corolla bromeliads with
otherwise typical ornithophilous syndrome are frequently visited by a high diversity of bees (Schmid
et al. 2011a).
Some floral visitors, like hummingbirds, are
specialized nectar feeders and depend on it as their
most important energy source (Krömer et al. 2008).
Nectar quality and quantity are important features
when it comes to floral choice. There are several
studies providing nectar volumes and concentrations
for Bromeliaceae (Bernardello et al. 1991, Buzato
et al. 2000, Canela & Sazima 2003, Krömer et al.
2008). Bromeliad nectar contains only the three
sugars sucrose, glucose, and fructose, and the proportion of sucrose to glucose and fructose is related to
pollinator types. Hummingbirds prefer dilute and
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Umbruch Ecotropica 17_1.indd 91
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SCHMID ET AL.
sucrose-rich nectars (Krömer et al. 2008). Therefore,
the attractiveness of bromeliad flowers to pollinators
is strongly influenced by nectar composition and
corresponding volume, both features not yet determined for Vriesea friburgensis.
Vriesea friburgensis var. paludosa (Bromeliaceae) is
endemic in Brazil and common in the coastal areas
of the southern states Santa Catarina, Paraná, and
Rio Grande do Sul (Reitz 1983). Plants reproduce
through clonal growth and via seeds, and each rosette
produces only one inflorescence. Floral traits like
tubular shape and the combination of red and yellow
colors suggest the flowers to be adapted to hummingbird visitation (Faegri & van der Pijl 1971, Sick
1993), and two hummingbird species, Thalurania
glaucopis and Amazilia fimbriata, have been previously reported as visitors to V. friburgensis flowers in
the Atlantic forest in Paraná (Piacentini & Varassin
2007, Cestari 2009). However, in Aechmea nudicaulis, a bromeliad species exhibiting an apparently ornithophilous syndrome with the same combination
of floral traits, bees can also be regarded as possible
pollen vectors (Schmid et al. 2011b). The much
longer corolla in V. friburgensis suggests a more pronounced ornithophily than in A. nudicaulis, so we
hypothesized that (i) the visitor spectrum of V. friburgensis is more restricted, especially in bee species,
due to flower morphology, and (ii) that bees do not
play a role in pollination.
Studying the species richness of bromeliad flower visitors and the diversity and nature of their animal-plant interactions, this study focused on recording the species spectrum and frequency of floral
visitors of V. friburgensis. To understand what attracts
visitors to the flowers, we (1) analyzed floral phenology and reproductive system, as well as the quality
and timing of floral rewards. We further hypothesized
that habitat has an influence on species richness and
visitation frequency of floral visitors (Tews et al.
2004, Schmid et al. 2011a), so we (2) compared the
species spectrum of flower visitors to V. friburgensis
between two habitat types, secondary forest and
restinga (sand dune habitat).
MATERIAL & METHODS
Study site. The study was conducted at Florianópolis
on Santa Catarina Island, southern Brazil, during
four flowering seasons of V. friburgensis, from
December to February 2005/2006, 2006/2007,
2007/2008, and 2008/2009. Fieldwork was carried
out at three sites, differing in habitat type: dune
vegetation at (1) Joaquina Beach (27°37’37”S,
48°26’59”W) and (2) Campeche Beach (27°40’38”S,
48°28’48”W) (‘restinga’; Sampaio et al. 2002), and
a hillside secondary forest area at (3) Santo Antônio de Lisboa (Zillikens et al. 2001; 27°30’26”S,
48°30’28”W, hereafter Sto. Antônio). The distance
between the forest and the restinga sites is 14 km.
Time specification is given in standard time instead
of daylight saving time, because the switch to and
from daylight saving time would interfere with our
time scales.
Flowering period and analysis of breeding system. Emergence and development of inflorescences were observed weekly from 24 August 2007 to 13 March
2008 at all study sites. Per site, all inflorescences visible along defined trails were counted. Three phenology categories were defined: (i) “new”, from first sight
of new inflorescences still covered by bracts till bud
stage; (ii) “open”, with open flowers; and (iii) “withered”, with only withered flowers and developing
fruits. The ramification pattern as well as the arrangement and orientation of the flowers are shown in
Grohme et al. (2007).
Total number of flowers per inflorescence was
counted for 17 inflorescences (ten from Sto. Antônio,
seven from Joaquina). The number of open flowers
per day and inflorescence was recorded for seven
inflorescences in Sto. Antônio throughout their
whole flowering phase. Additionally, the same flowering rate was assessed (without accounting for the
developmental state within the flowering phase) for
517 inflorescences in Joaquina on ten days while
always walking along the same trail. Because inflorescences flower over a long period, several inflorescences were scored not only once but were always
counted as independent inflorescences. The number
of days with open flowers for an inflorescence was
analyzed for seven plants located in the miconietum
vegetation (a pre-forest succession stage; Queiroz
1994, Zillikens & Steiner 2004) in Sto. Antônio.
The breeding system was assessed with handpollination treatments on plants taken to the laboratory: autonomous self-pollination, manual self-pollination, and manual cross-pollination (n = 8 flowers
each treatment) (Dafni 1992). Additionally, flowers
in the field (n = 13 flowers of 12 plants) were marked
as control for natural pollination. The “Index of
self-incompatibility” (ISI) and “Index of automatic
self-pollination” (IAS) were calculated according to
Zapata & Arroyo (1978).
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DIVERSITY OF FLOWER VISITORS OF VRIESEA FRIBURGENSIS
Analysis of nectar composition. Nectar samples were
collected with 2-μl end-to-end micropipettes from
05:00 h to 15:00 h at 2-hour intervals (12 flowers of
four plants) and sugar composition and concentration were analyzed by HPLC (Piechowski 2007). The
total volume was then determined by measuring the
remaining nectar with 5- to 20-μl micropipettes (Assistent, Germany) and adding this volume to the
previously collected 2 μl. Correlations of the concentrations of the three sugar types, as well as differences between concentrations, were tested with the
statistical software package JMP 8.0.1 (SAS Institute
Inc. 2009). The total nectar energetic value was
calculated by multiplying total sugar weight (μg) for
the three sugars glucose, fructose, and sucrose with
the energy-per-mass factors (0.0156 J μg-1, 0.0157 J
μg-1, and 0.0165 J μg-1, respectively, Wieser 1986).
The products were added together. For the nectar
measurements at 05:00 h, the time period of its secretion may exceed or fall below two hours because we
did not exactly know the onset of nectar secretion.
Sugar concentration was not measured after 15:00 h
because almost no nectar was present at that time.
RESULTS
Flowering biology and breeding system of V. friburgensis. Inflorescences started to appear in October. The
SCHMID to
ETFebruAL.
flowering period extended from November
ary. Bud stage as well as flowering period and presence of infructescences were synchronous at the three
sites (Fig. 1). The zygomorph flowers were tubular
Bud
100
Open
Withered
Campeche
Joaquina
Sto Antônio
75
50
01/03/08
01/02/08
01/01/08
01/12/07
01/11/07
0
01/10/07
25
01/09/07
Proportion of flowering plants (%)
Flower visitor spectrum, visitation frequency, and foraging
behavior. In total, 80 inflorescences were observed in
situ at Joaquina Beach and Sto. Antônio either directly
or with binoculars (314 observation hours) to record
taxa and frequency of flower visitors. As flowers open
only for a single day, one inflorescence observed on
different days was counted as two independent observation events because the flowers were different in position and number. We recorded floral visitors in the
widest sense, so all animals touching a flower were
counted as visitors. For every approaching visitor we
recorded species, time of arrival and leaving, and the
kind of reward collected. Voucher specimens were deposited in the collection of Josefina Steiner, LANUFSC, Federal University of Santa Catarina, Brazil.
Date
FIG. 1. Period of Vriesea friburgensis inflorescences with buds, open, and withered flowers at the three sites
Fig 1
Campeche Beach (triangle), Joaquina Beach (diamond), and Sto. Antônio (circle) on Santa Catarina Island,
Brazil. Since sample size differed between sites the number of inflorescances with at least one open flower is
given in % of the maximum weekly number of flowering plants.
93
Umbruch Ecotropica 17_1.indd 93
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SCHMID ET AL.
Frequency of occurrence
SCHMID ET AL.
25
20
15
10
5
0
0
1
2
3
4
5
6
No. of open flowers / day
FIG. 2. Frequency distribution of the number of open flowers per inflorescence and day of Vriesea friburgensis (n = 7 plants) in Sto. Antônio, Santa Catarina Island, Southern Brazil. Each data point represents the
Fig. 2 of days with the corresponding number of open flowers (0 – 6 flowers open per day) during the
number
flowering period of one inflorescence.
and without scent. Anthers and stigma protruded
from the corolla. Flowers began to open between
01:00 h and 02:00 h. The stigma came out first,
followed by the anthers. Around 05:00 h the flower
was fully open, but the anthers did not dehisce until
06:00 h with sunrise. Effective depth of flowers (the
depth of the corolla which a visitor has to overcome
to reach the nectar) was 29 mm (median; Q1 = 28,
Q3 = 32; range 24.8 – 37.5 mm; n = 33 flowers, 10
plants). Flower entrance width measured 5 mm
(median; Q1 = 4.5, Q3 = 5, range 3.9 – 6.1 mm; n =
33 flowers, 10 plants).
Due to the fact that the numbers of flowers per
inflorescence in the two habitats Joaquina and Sto.
Antônio were not normally distributed and also
significantly different (Mann-Whitney U-test, JMP
8.01, SAS Institute Inc, 2009; χ2 = 11.6667, d.f. = 1,
p = 0.0006), medians for Joaquina and Sto. Antônio
were computed separately. Number of flowers per
inflorescence was 54 in Sto. Antônio (median; Q1 =
46.5, Q3 = 72.5; range 26 – 53) and 113 in Joaquina (median; Q1 = 85.75, Q3 = 152.75; range 80
– 172). Number of open flowers per day was 1 (median; Q1 = 1; Q3 = 2; range 0 – 7; n = 517 infl.).
Between zero and two open flowers per day were
most frequently observed (see Fig. 3). Median number of days with open flowers was 44 ± 10.3 (Q1 =
36.5; Q3 = 49; range 26 – 53; n = 7 infl.).
There was seed set in the two treatments manual self- and manual cross-pollination as well as in
naturally pollinated flowers (Table 1). The ISI resulted in 0.61 (n = 16) and the IAS was 0 (n = 16).
Induction of seed set, tested with manually crosspollinated flowers, was possible during the whole
phase of anthesis (from flower opening till closure,
see Fig. 3).
TABLE 1. Seed numbers resulting from pollination experiments to analyze the breeding system of Vriesea
friburgensis on Santa Catarina Island, southern Brazil.
Pollination treatment
manual cross-pollination
manual self-pollination
autonomous selfing
natural pollination
N
08
08
08
13
Mean no. of seeds per fruit
188.1
115.4
000
361.62
Range
000-316
000-242
000
237-442
SD
094.5
106.0
000
071.79
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SCHMID ET AL.
No. of seeds per fruit
DIVERSITY OF FLOWER VISITORS OF VRIESEA FRIBURGENSIS
y = -197.69x + 285.78
r2 = 0.0792
400
350
300
250
200
150
100
50
0
3
5
7
9
11
13
15
17
19
21
Time of day
FIG.
3. Temporal
pattern of the possibility of ovule fertilization in flowers of Vriesea friburgensis, Santa Catarina
Fig.
3
SCHMID ET AL.
Island, southern Brazil.
18.68%
± 2.0
25.02%
± 8.8
16.34%
± 0.7
17.43%
± 1.3
14.50%
± 0.7
300
25
Mean nectar volume [µl]
350
250
20
200
15
150
10
100
5
50
0
0
5
7
9
11
Hour of day
13
Mean sugar content [µg/µl]
30
32.44%
± 7.5
15
Volume
Sugar content
FIG. 4. Diel pattern of mean nectar volume (columns), nectar sugar content (diamonds), and sugar concenFig. 4(gray boxes) every two hours of anthesis in flower of Vriesea friburgensis, Santa Catarina Island,
tration
southern Brazil. Standard error bars or values are given for each mean.
Mean number of seeds per successfully developed
fruit after natural pollination was 361.6 ± 71.8 and the
percentage of undeveloped fruits under natural field
conditions was 62.2% ± 16.7, of which 26.1% ± 15.6
were found to be parasitized by eurytomid wasps.
Nectar analyses. Nectar volume per flower and hour
was 6.4 ± 5.3 μl (mean ± SD). Nectar production
was not evenly distributed over anthesis but peaked
at 11:00 h (Fig. 4). Sugar concentration over the day
was 19.5 ± 6.8% (w/w, mean ± SD); highest concen95
Umbruch Ecotropica 17_1.indd 95
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SCHMID ET AL.
SUPPLEMENTARY TABLE 1. Spearman correlations between pairs of sugars contained in floral nectar of V.
friburgensis on Santa Catarina Island, southern Brazil. Bonferroni correction yields a significance level of alpha
= 0.05/18 = 0.0028. Significant p values are designated by an asterisk (*). G: glucose, F: fructose, S: sucrose.
F–S
Spearman ρ
-0.2909
-0.1727
-0.3636
-0.2168
-0.1469
-0.0061
Hour of day
05:00
07:00
09:00
11:00
13:00
15:00
G–S
Spearman ρ
-0.1727
-0.1636
-0.0559
-0.3007
-0.1329
-0.1394
p
0.3855
0.6115
0.2453
0.4986
0.6488
0.9867
tration was measured at 05:00 h (Fig. 4). Sucrose
secretion was higher than that of the hexoses and
most of the time the nectar was sucrose-dominant.
Overall sucrose/hexose ratio [S/(F+G)] was 1.65 ±
0.62 (mean ± SD). Mean sucrose proportion per
hour was high in the first hour of secretion and decreased steadily during anthesis from 71.4% (05:00
h) to 43.1% (15:00 h), while those of fructose and
glucose remained more or less unchanged. Total
sugar secreted per flower and day was 14 565.7 μg =
14.5 ± 0.9 mg (mean ± SD). Fructose values were
significantly higher than those of glucose (Wilcoxon
Signed-Rank Test Statistic 1173.000, p < 0.0001)
and both hexoses were significantly correlated with
each other (Spearman correlation) whereas sucrose
concentration was not significantly correlated with
concentration of both hexoses (Suppl. Table 1).
Energy value per flower was 218.3 ± 104.3 J.
Multiplication by the median number of flowers per
p
0.6115
0.6307
0.8629
0.3423
0.6806
0.7009
G–F
Spearman ρ
0.9455
0.9636
0.8531
0.9091
0.9021
0.9515
p
<0.0001*
<0.0001*
<0.0004*
<0.0001*
<0.0001*
<0.0001*
inflorescence (Sto. Antônio: 54; Joaquina: 113) resulted in an average caloric nectar value per inflorescence of 9.6 kJ for Sto. Antônio and 24.7 kJ for
Joaquina.
Flower visitor species spectrum, frequency, and foraging
behavior. We recorded a total of 30 species as visitors,
in the widest sense, to flowers of V. friburgensis (Table
2). The restinga habitat had a higher species richness
(21 species, n = 1073 visitors) than the secondary
forest (14 species, n = 304 visitors). Secondary forest
and restinga sites
sharedET6 AL.
species. One species, the
SCHMID
hummingbird Eupetomena macroura, was only observed attending flowers in an urban area. In both
habitats the most frequent visitors were hummingbirds and bees. Whereas hummingbirds were the
commonest animals visiting flowers of V. friburgensis
in secondary forest followed by bees, it was the opposite on flowers in the restinga habitats (Fig. 5).
Mean number of visits / hour
4
3
Restinga
Forest
2
1
0
Trochilidae
Apoidea
Others
FIG. 5. Visitation frequency (mean number
of visits per hour) of
flower-visitor groups
on Vriesea friburgensis
in restinga and secondary forest habitat
on Santa Catarina
Island, southern Brazil.
96
Fig. 5
Umbruch Ecotropica 17_1.indd 96
07.06.11 14:20
DIVERSITY OF FLOWER VISITORS OF VRIESEA FRIBURGENSIS
TABLE 2. Species spectrum and frequency with resource collected by flower visitors to Vriesea friburgensis
on Santa Catarina Island, southern Brazil. N = number of visits observed in field experiments are given in
parentheses. Visitation aims: n = nectar, p = pollen, o = oviposition, h = herbivory, pr = predator. Because
bees of the taxon Augochlorini could not be identified to species during flower visits, frequency and number
of visits are given as sum and x in the table show the species occurrence in the habitats.
Taxon
Trochilidae
Amazilia fimbriata
Thalurania glaucopis
Eupetomena macroura*
Apoidea
Apidae
Apis mellifera
Ceratina (Crewella) sp.1
Plebeia droryana
Trigona spinipes
Xylocopa brasilianorum
Halictidae
Augochlora (A.) amphitrite
Augochlora (A.) sp.2
Augochlora (A.) sp.3
Augochlorella ephyra
Augochloropsis cfr. cleopatra
Augochloropsis cfr. patens
Dialictus cfr. opacus
Thectochlora hamata
Apoidea n.i.
Lepidoptera
Lepidoptera n.i.*
Strymon serapio*
Coleoptera
Diptera
Diptera n.i.
Saltatoria
Saltatoria n.i.
Mantidae
Mantidae n.i.
Vespidae
Vespidae sp.1
Vespidae sp.2
Eurytoma sp.1
Blattaria
Blattaria sp.1
Blattaria sp.2
Araneae
Araneae n.i.
Thomisidae n.i.*
Salticidae n.i.
Total
Visitation frequency
Aims
Total
% (N)
Forest
% (N)
Restinga
% (N)
15.0 (207)
10.3 (142)
4.7 (65)
60.9 (185)
46.7 (142)
14.1 (43)
2.1 (22)
2.1 (22)
81.6 (1121)
11.1 (151)
3.3 (45)
0.4 (5)
0.1 (1)
6.9 (95)
0.4 (5)
70.4 (969)
37.1 (113)
1.9 (6)
1.6 (5)
0.3 (1)
35.2 (107)
x
x
x
-
93.9 (1008)
13.6 (145)
4.2 (45)
8.9 (95)
0.5 (5)
80.3 (862)
x
x
x
x
x
x
x
0.1 (1)
0.8 (9)
1.5 (16)
(16)
0.2 (2)
0.1 (1)
0.7 (9)
1.3 (18)
0.1 (2)
0.1 (1)
(1)
0.8 (11)
0.4 (6)
0.1 (1)
0.5 (7)
100 (1378)
0.1 (1)
0.1 (1)
x
0.7 (2)
(2)
0.3 (1)
0.3 (1)
0.3 (1)
x (1)
0.7 (2)
(1)
(1)
100 (305)
0.1 (1)
(1)
0.9 (10)
x
x
0.5 (5)
x
0.5 (5)
x
(5)
100 (1073)
n
n
n
n
p+n
p
p+n
p+n
p+n
p+n
n+o
n
n+o
h
pr
pr
pr
pr
pr + n
pr + n
pr + n
o
h
h
h
pr
pr
pr
pr
* Individuals were observed as visitors but not during regular observation sessions so there is no frequency
available.
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SCHMID ET AL.
Hummingbirds inserted their bills into open
flowers and touched the anthers and stigmata while
hovering in front of the flowers (Fig. 6A-B, Video
S1). One individual of the bee species Xylocopa
brasilianorum was observed piercing the corolla tube
to reach the nectar chamber (Fig. 6C). Trigona
spinipes, Ceratina sp., and halictid bees collected
pollen with their forelegs while hanging upside down
on the anthers (Fig. 6D-F, respectively). They then
stored the pollen in corbiculae (Fig. 6D) or the ventral abdominal and hind leg scopae (Fig. 6D-F).
Individuals of these bee species were also slender
enough to enter the flowers to collect nectar. Trigona
spinipes individuals also sometimes gnawed holes in
the corolla base when the tube was too narrow for
them. Halictids were the most frequent flower visitors in restinga sites (Table 2) and collected pollen
during 50% of their visits, mainly in the first hours
B
A
D
F
of anthesis. Occasionally the augochlorine bees
touched the stigma while foraging for pollen. One
individual was observed expanding a regurgitated
nectar droplet between hypostomal fossa (Engel
2000) and the proximal section of the proboscis
(cardines and hypopharynx) (Krenn et al. 2005) after
the visit (Fig. 6G). Beetles and cockroaches were
observed on the inflorescences feeding on open and
withered flowers. Flower mites gathered on the anthers to feed on pollen (Fig. 6H). Vespid wasps were
observed walking on the inflorescences, one individual tried to enter an open flower. Jumping spiders,
crab spiders (Fig. 6I), and praying mantises lurked at
the inflorescences for potential prey, for example ants
(Fig. 6I). Ants at the flowers were not recorded systematically but they were observed regularly on and
in flowers (Fig. 6J), preying on other animals, and
SCHMID ET AL.
collecting nectar inside the flowers.
C
E
H
G
I
J
FIG. 6. Visitors on flowers of Vriesea friburgensis on Santa Catarina Island, southern Brazil. (A) Thalurania
glaucopis and (B) Amazilia fimbriata hovering in front of flowers. (C) Xylocopa brasilianorum acting as nectar
robber. (D) Trigona spinipes collecting pollen. (E) Ceratina female collecting pollen at the anthers. (F) Pollencollecting augochlorine bee, (G) and an individual sitting on the stigma while “dehydrating” a nectar droplet.
Fig.
6
(H) Flower
mites on the anthers. (I). Crab spider (Thomisidae) feeding on a Pseudomyrmex gracilis worker
ant. (J) Camponotus worker ant guarding the flower entrance.
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DIVERSITY OF FLOWER VISITORS OF VRIESEA FRIBURGENSIS
DISCUSSION
Flowering phenology and nectar production favor
hummingbird visits. The bromeliad species Vriesea
friburgensis has an annual flowering pattern (Newstrom et al. 1994). Rosettes flower over a longer
period, having a more synchronous and extended
flowering period and less open flowers per day than
sympatrically growing bromeliads of the genus
Aechmea (Schmid et al. 2011b, Dorneles et al. in
press, Kamke et al. 2011). A long flowering period
and few open flowers per day lead to a low standing
crop per plant, which in turn stimulates hummingbirds to forage by trap-lining along the V. friburgensis individuals. To collect enough nectar the hummingbirds have to visit many inflorescences, thereby
enhancing cross-pollination.
The temporal pattern of nectar production and
concentration throughout anthesis of V. friburgensis
is adapted to attract hummingbirds, because features
like high volume and sucrose content in the early
morning, as well as sucrose-dominant nectar, seem
to be common in hummingbird-pollinated flowers
(Baker 1975, Heinrich 1975, Freeman et al. 1984,
Bernardello et al. 1991, Stiles & Freeman 1993,
Krömer et al. 2008). Also, floral traits (long tubular
flowers, anthers and stigma exposed, stigma slightly
in front to touch the bird’s forehead first) match with
the morphology of hummingbirds with straight and
rather short bills. Therefore, based on nectar and
morphological properties, we assume the visiting
hummingbirds to be the main pollinators of V. friburgensis, but pollination experiments are needed to
confirm this assumption.
Large bees of genera like Bombus and Xylocopa,
or long-tongued bees of the genus Euglossa, are able
to drink high quantities of floral nectar and they can
reach the nectar even in flowers with moderately
ornithophilous features. These bees were reported as
visitors of A. nudicaulis (Schmid et al. 2011a) and
A. lindenii (Dorneles et al. in press) but they cannot
exploit, at least not in a legitimate way, V. friburgensis flowers and can only be considered nectar thieves.
Therefore more nectar is available for the hummingbirds. This might make visits to Vriesea flowers more
profitable for the birds than visits to Aechmea flowers.
The flower visitors of Vriesea friburgensis. From a
Natural Heritage Site in Paraná state, Piacentini &
Varassin (2007) reported solely T. glaucopis and Am.
fimbriata as visitors to V. friburgensis, the same hummingbird species observed by us. In contrast to their
findings, and to our own expectations considering
the ornithophilous floral syndrome, we recorded a
highly diverse arthropod assemblage, especially insects, on Santa Catarina Island. This assemblage was
similar to the visitor spectrum of A. nudicaulis in the
same habitats (Schmid et al. 2011a). Comparing the
bee spectrum of V. friburgensis with that of the sympatrically growing A. nudicaulis, A. lindenii, and A.
caudata, there is also some overlap, namely in the
Apidae and Halictidae (Schmid et al. 2011a, Dorneles et al. in press, Kamke et al. 2011). Clearly, these
bromeliad species partly share the same visitor species, and, flowering sequentially (A. lindenii: August
to October, A. nudicaulis: September to December,
V. friburgensis: November to February, and A. caudata: March to June) support the local hummingbird
and bee fauna over an extended period.
Contrary to the findings on flower-visiting ant
species on inflorescences of A. nudicaulis and A.
lindenii (Schmid et al. 2010), the species richness of
floral visitors to V. friburgensis was higher in the
restinga than in the secondary forest. In restinga,
flowers were almost exclusively visited by bees, most
of them augochlorine sweat bees, whereas visitation
frequency of hummingbirds was much lower than in
secondary forest. This may be due to the fact that
Joaquina and Campeche are low-vegetation restingas
which provide poorer environmental conditions (for
example nesting sites or nectar supply) for hummingbirds than for bees. In the early morning hours,
the pollen-loaded anthers were especially attractive
for bees. Additionally the low frequency of hummingbirds on V. friburgensis flowers resulted in a high
nectar standing crop which was then available to bees
small enough to crawl into the flowers. The exploitation of both of these rich resources explains the high
bee visitation frequency.
Pollination biology of V. friburgensis. In the selfcompatible flowers of V. friburgensis there is a spatial
separation of stamina and stigma. Due to this “approach herkogamy” (Barrett 2003) pollen is not automatically transferred to the stigma and intra-floral
selfing without an animal pollen vector is not possible. Consequently, pollination can take place when
hummingbirds, forced to insert their bills deep into
the corolla, touch the stigma with their foreheads
dusted with pollen (see Video S1 and S2). Pollination
by bees would have to occur in a different way. Pollen
gathered by sweat bees (Halictidae) and small carpenter bees (Ceratinini) is stored in the scopae of the
hind legs and the abdomen, and is not, as in the
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corbiculate bees (Apinae), mixed with nectar to stick
together as compact pellets. In fact, the rather
loosely packed pollen may be transferred to the
stigma while the bee is climbing over it. Therefore
even small bees with short tongues (Halictidae and
Ceratina), only engaged in pollen collection, may be
capable pollinators. Individuals of these species-rich
taxa are among the most abundant bees on Santa
Catarina Island (Steiner et al. 2010). They occur all
over the Neotropics, are abundant in forest as well as
restinga, in natural as well as modified habitats, and
are active almost all year round (multivoltine) (Michener 2000). Both taxa are similar in their ecotype
and therefore belong to the same functional group
(Fenster et al. 2004).
It appears that V. friburgensis uses both strategies
– xenogamy and autogamy – to ensure successful
pollination. Xenogamy is favored by forcing hummingbirds to perform trap-lining by offering, on
average, only one open flower per plant so that pollen from unrelated plants is transferred with almost
every flower visit. On the other hand, autogamy
could be performed by a species-rich group of generalist bees characterized by a distinct mode of
pollen collection and storing. Our results suggest
that in places where hummingbirds are rare visitors
or even absent, bees can fill the gap and pollinate
the flowers. Even if, from the plant’s point of view,
xenogamy is more desirable than autogamy, the
second strategy eliminates the risk of a total failure
of pollination in the absence of the legitimate pollinators. The high seed set per flower observed indicates that, at present, natural pollination is sufficient to ensure the persistence of this bromeliad
in the two habitats studied, even though there is
loss of seeds due to parasitism by Eurytoma wasps
(Grohme et al. 2007).
Although we did not measure individual pollinator effectiveness, the short-billed hummingbirds
occurring on Santa Catarina Island are supposedly
the most effective pollen vectors of V. friburgensis.
Somewhat unexpectedly for this bromeliad species
with such a pronounced ornithophilous syndrome,
bees may also be a crucial part of the visitor assemblage, and not just pollen and nectar thieves.
Araujo et al. (1994) also reported halictid bees to
be visitors of three Vriesea species with similar
flower morphology as V. friburgensis, but they do
not give information about the bees’ role in pollination. To what extent these bees provide pollination
service for bromeliads with long and tubular flowers
like V. friburgensis has to be further investigated in
carefully executed pollination experiments. In any
case, our study points to the high importance of V.
friburgensis flowers as food resource for the local bee
fauna.
ACKNOWLEDGMENTS
We thank Maike Hering de Queiroz (in memoriam)
and Diomário de Queiroz for granting access to the
study site. We are grateful to Gabriel Melo for identifying the augochlorine bee morphospecies and to
Wolf Engels and two anonymous reviewers for valuable comments on the manuscript. This study is part
of the projects “Internal dynamics of rain forests:
specificity of animal-plant interactions” and “Importância das bromélias para a manutenção da diversidade da fauna associada na Mata Atlântica”, a
Brazilian-German scientific cooperation within the
program “Science and technology for the Atlantic
Rainforest”, funded by BMBF (01LB0205A1); and
CNPq (690143/01-1; 590040/2006-5).
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