Evaluation of Pollination Syndromes in Antillean Gesneriaceae: Evidence for Bat,

Hummingbird and Generalized Flowers

Author(s): Silvana Martén-Rodríguez, Abel Almarales-Castro and Charles B. Fenster
Source: Journal of Ecology, Vol. 97, No. 2 (Mar., 2009), pp. 348-359
Published by: British Ecological Society
Stable URL: https://www.jstor.org/stable/20528861
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Journal of Ecology 2009, 97, 348-359 doi: 10.1111/j.1365-2745.2008.01465.x

Evaluation of pollination syndromes in Antillean

Gesneriaceae: evidence for bat, hummingbird and
generalized flowers
Silvana Marten-Rodriguezl 2*, Abel Almarales-Castro3 and Charles B. Fenster1"4
1Behavior, Ecology, Evolution and Systematics Program, University of Maryland, College Park, MD 20742, USA;
2Herbario de la Universidad de Costa Rica, Escuela de Biologia, Ciudad Universitaria Rodrigo Facio Brenes, San Jos
Costa Rica; 3Centro Oriental de Ecosistemas y Biodiversidad (BIOECO), Museo de Historia Natural Tomas Romay,
Enramadas No. 601, Esquina Barnada, Santiago, Cuba; and4Biology Department, University of Maryland, College P
MD 20742, USA

Summary
1. Current views about the predominance of generalization of pollination systems have stimulated
controversy concerning the validity of pollination syndromes. In order to assess the extent to which
floral characters reflect selection by the most important pollinators we evaluated pollination
syndromes in a florally diverse plant group, the tribe Gesnerieae, a monophyletic plant radiation
from the Antillean islands.
2. The study species include representatives of three groups of floral phenotypes, two of which
chiefly correspond to ornithophilous and chiropterophilous syndromes. The third group includes
subcampanulate flowers (characterized by a corolla constriction above the nectar chamber) with
combinations of traits not fitting classic pollination syndromes.
3. Pollination systems were characterized for 19 Gesnerieae species in five Antillean islands
between 2003 and 2007 and supplemented with observations of four Gesneriaceae species from
Costa Rica. Pollinator visitation and frequency of contact with anthers or stigmas were used to
calculate an index of pollinator importance. Eleven floral traits including morphology, phenology
and rewards were used to assess clustering patterns in phenotype space.
4. Multidimensional scaling analysis of floral traits resulted in two clusters comprising: (i) tubular,
red to yellow-flowered species with diurnal anthesis, (ii) bell-shaped-flowered species; two groups of
floral phenotypes were evident within the latter cluster, campanulate nocturnal and subcampanulate
flowers. Correlations between pollinator importance values and floral axes revealed strong associations
with the expected pollinators, hummingbirds for tubular flowers, and bats for campanulate flowers;
subcampanulate-flowered species had generalized pollination systems including bats, hummingbirds
and insects. Discriminant analysis of the multivariate set of floral traits correctly classified 19 out of
23 species into the predicted pollination categories.
5. Synthesis. This study provides support for classic hummingbird and bat pollination syndromes,
demonstrating the importance of pollinator-mediated selection in the floral diversification of
Antillean Gesnerieae. However, there was evidence for generalized pollination systems in species
characterized by a unique morphological trait (corolla constriction), but with variable combinations of
other floral traits. These findings suggests that floral phenotypes might also evolve under selection
by various functional groups of pollinators, and underscores the importance of considering the
presence and effectiveness of all floral visitors in pollination studies.

Key-words: Antilles, bat pollination, Costa Rica, generalization, Gesneriaceae, hummingbird

pollination, islands, pollination syndromes, specialization

*Correspondence author. E-mail: smartenr@gmail.com

?) 2009 The Authors. Journal compilation ?C 2009 British Ecological Society

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 Pollination syndromes in Antillean Gesneriaceae 349

underlie patterns of floral convergence. We studied the

Introduction Antillean tribe Gesnerieae to determine to what extent floral
Closely related plant species often display great variation in phenotypes defined by morphology, phenology and rewards
flower form and function. Darwin (1862) proposed that the are explained by the pollinators. This group of plants provides
evolution of this floral diversity reflected pollinator-mediated an excellent study system for various reasons. First, the tribe
selection. Patterns of convergence of floral phenotypes across Gesnerieae is a monophyletic radiation from the Antilles
the angiosperms provide strong support for Darwin's paradigm that consists of 73 species encompassing considerable floral
and suggest that suites of floral characteristics have evolved in diversity (Skog 1976; Smith 1996; Zimmer et al. 2002). Second,
association with particular groups of pollinators. These floral the tribe comprises floral phenotypes that have been tradi
phenotypes are known as 'pollination syndromes' (Faegri & tionally associated with hummingbird and bat pollination,
van der Pjil 1978), and they comprise morphological as well but previous to our studies, no field data were available to
as biochemical (e.g. composition of attractants and rewards, support these predictions. Furthermore, despite the great
Baker & Baker 1990) and phenological traits (e.g. patterns of floral diversity displayed by Neotropical Gesneriaceae, only a
anther dehiscence, Castellanos et al. 2006). For example, large limited number of studies have documented pollinators in the
bell-shaped flowers that produce large quantities of dilute field (e.g. Podolsky 1992; Sazima et al. 1996; Lara & Ornelas
nectar and shed pollen at night tend to be associated with 2002; Carlson 2008), and only for the tribe Sinningieae in
bat pollination, whereas tubular red flowers with diurnal Brazil has there been a systematic assessment of pollinators
schedules are commonly associated with pollination by birds. in a group of closely related species (Sanmartin-Gajardo &
Syndromes therefore imply that flowers have become specialized Sazima 2004, 2005a,b). Third, oceanic archipelagos provide
for pollination by specific groups of floral visitors, that is, floral unique conditions of natural selection and opportunities for
traits have evolved to increase pollen transfer by the most evolutionary change that may differ from mainland regions.
effective visitors and to deter antagonistic visitors (Stebbins And last, our preliminary phylogenies indicate at least five
1970; Faegri & van der Pjil 1978; Fenster et al. 2004). independent origins of bell-shaped corollas that differ from
During the past decade, however, the notion that pollination the tubular corollas of the ancestral phenotype; this suggests
specialization underlies the observed patterns of floral pollinators played a significant role in the floral diversification
convergence has been debated (Waser et al. 1996; Fenster et al. of the clade. We included four species from three additional
2004). Community and taxon surveys predominantly from tribes of the family Gesneriaceae from Costa Rica to obtain
temperate regions reveal that many flowers have generalized phylogenetically independent evidence from mainland
visitation patterns (e.g. Robertson 1928; Lindsey 1984; Herrera taxa. The selected species fall into three general classes of
1996; Olesen et al. 2007), pollinator communities vary in time floral phenotypes corresponding to ornithophilous and
and space (e.g. Herrera 1995; Fenster & Dudash 2001; Horovitz chiropterophilous syndromes, and a class of more variable
& Schemske 2002), and animals often use floral resources from phenotypes that do not clearly match classic syndrome
different plant species (e.g. Herrera 1996). Furthermore, predictions (Fig. 1).
syndromes do not predict all floral visitors, and flowers that For this study, we specifically address the following questions:
conform to particular syndromes are sometimes pollinated by (i) what are the pollination systems of Gesneriaceae species
animals that do not fit the expectations (Ollerton et al. 2007). representative of the different floral phenotypes?; (ii) when
These observations have led some authors to question the floral traits are used to search for patterns in multivariate
validity of the pollination syndrome concept (Waser et al. 1996; space, is there evidence for discontinuous associations of
Ollerton et al. 2007). While syndromes were not originally meant species corresponding to traditional pollination syndromes?;
to be used as substitutes for field observations, there is a valid (iii) which floral traits contribute most to distinguishing
concern regarding the use of floral traits as predictors of the the floral associations defined in multivariate space?; and
pollinators, particularly when biased or no field data have been (iv) are pollination syndromes good predictors of the floral
collected (Feinsinger 1987; Waser et al. 1996). Obtaining impartial visitors for Antillean Gesneriaceae? We evaluate the pre
characterizations of pollinators at the level of communities or dictions that tubular flowers in the Gesnerieae are primarily
higher order plant taxa, particularly from understudied tropical pollinated by hummingbirds, and bell-shaped (campanulate
regions, is critical to solving the apparent disagreement between and subcampanulate) nocturnal flowers are primarily
observed evolutionary patterns of floral specialization and the pollinated by bats. We also provide the first descriptions of
patterns suggested by field ecology (Johnson & Steiner 2000). pollinators for Rhytidophyllum species with mixed floral
Furthermore, despite the clear difficulties involved in obtaining traits not fitting classic pollination syndrome categories.
direct measures of pollinator efficiency, an attempt should be
made at distinguishing between potential pollinators and non
pollinating floral visitors. This approach should lead us to a Methods
more comprehensive understanding of the different selective
agents that have influenced the great floral diversification ST UDY S ITE S
observed in some plant taxonomic groups. Pollinator observations and floral biology studies were conducted in
Pollination studies of closely related insular species could Costa Rica (February-March 2007), Cuba (September 2007-February
provide important insights into the selective pressures that 2008), the Dominican Republic (June-August 2004-2007), Jamaica

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350 S. Marten-Rodriguez, A. Almarales-Castro & C. B. Fenster

Fig. 1. Three predominant floral phenotypes

in Antillean Gesneriaceae. Photos A-C corres
pond to Gesneriafruticosa, G. viridiflora subsp.
sintenisii and G. pedunculosa, representing the
bat-pollination syndrome (green or white
bell-shaped flowers with nocturnal anthesis
and high nocturnal nectar production). Photos
D-G correspond to Colwnneaquercetii, Gesneria
citrina, G. decapleura and G. pulverulenta
representing the hummingbird-pollination
syndrome (tubular red or yellow corollas with
diurnal anthesis and nectar production).
Photos H-I correspond to Rhytidophyllum
leucomallon, R. vernicosum, with mixed traits
of diurnal and nocturnal-pollination syndromes
(yellow to spotted red bell-shaped flowers with
nocturnal and/ or diurnal anthesis and nectar
production). Corolla constriction indicated
by white arrow.

(January 2004) and St. Lucia (June 2003). Rhytidophyllum minus

was observed at Castillo San Pedro de la Roca located on coastal
POLLINATOR VISITATION AND IMPORTANCE
limestone cliffs, south of the city of Santiago, in western Cuba. In To document pollinator visitation we conducted field observations on
the Dominican Republic, plants were observed at various sites of 23 species of Gesneriaceae for a total of 602 h. Detailed descriptions
Cordillera Central, Cordillera Septentrional, Parque Nacional of the methodology and floral biology of five Puerto Rican species
Sierra de Bahoruco and Sierra Neiba. All of these sites are located of Gesneria are reported elsewhere (Marten-Rodriguez & Fenster
in mountain regions between 300 and 2000 m. Most species occur 2008); thus, we only briefly describe the methods for pollinator
in limestone soils but they occupy a diversity of habitats including observations here. The total number of individuals observed per
pine forests, moist and cloud forests, and roadsides. In Jamaica, species ranged from 80 to 60, depending on the population size and
Gesneria calycosa plants were observed in the forest surrounding density of each species. The number of study years varied from one
Windsor Biological station in the NW side of the island (a.k.a. cockpit to three, but for each floral phenotype at least three species were
country) and Pheidonocarpa corymbosa at Cane River Falls in the observed for more than 1 year. For most species we made both direct
foothills of the Blue Mountains. In St. Lucia, observations of G. observations and observations with video cameras (SONY Handycam
ventricosa were conducted in Edmund Forest along the road to En DCR-HC42 and DCR-TRV350); the observer or the camera stood
Vasseux Waterfall, 500 m. Specific localities and geographic 2-5 m from the focal plant and recorded the time of visitation, type
coordinates for the study sites for each species are listed in of visitor (e.g. bird species, bat, moth, and diurnal insect order or
Appendix S1 (Supporting Information). family), contact with the flower's reproductive organs, and the number
To obtain phylogenetically independent samples, we also observed of flowers visited. Both diurnal and nocturnal observations were
four species of Gesneriaceae from three different tribes (Beslerieae, conducted for most species. For species with nocturnal and diurnal
Gloxinieae and Episcieae, according to Zimmer et al. 2002) that visitors, approximately half to three quarters of the time reported
occur in Costa Rica. Observations for these species were conducted was dedicated to nocturnal observation. The larger time effort put
in the forest of the Biological Station in Monteverde (for Besleria into night observations was necessary to compensate for the limited
solanoides) and in the rainforest of San Gerardo Biological Station number of flowers that video cameras could be focused on at night
(for Capanea grandiflora, Columnea consanguinea and C. quercetii); (one to four), as opposed to the ability to conduct direct observation
these sites are located on the western and eastern slopes of the Tilaran on patches of flowers during the day.
Mountain range, respectively. We also used data from a detailed study We classified pollinators into 'functional groups', defined on the
of the pollination biology of five Puerto Rican Gesneria performed basis of taxonomic affinity and similarity in feeding behaviour.
in January and March 2003-2007 in two regions of the island (Marten Functional groups are expected to represent sets of animal taxa that
Rodriguez & Fenster 2008). exert similar selective pressures on floral traits, because they share

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 Pollination syndromes in Antillean Gesneriaceae 351

similar feeding behaviours, physiology and morphology (Fenster (06.00-18.00), or (1) both; (ix) timing of nectar production, same
et al. 2004). For this study, the taxonomic classes of floral visitors coding as trait eight; (x) colour, coded as (1) green, (2) yellow, (3)
differed primarily in feeding schedule (active at flowers during day or orange or (4) red; (xi) spots: coded for (0) presence or (1) absence of
night), reward sought (pollen or nectar) and behaviour while feeding dark red or brown markings on the inside of the corolla. Measurements
(e.g. hovering vs. perching). Thus, the functional groups of pollinators of length, width and pistil exertion were taken with calipers and
that visited Gesnerieae species include hummingbirds, bats, moths and rounded to the nearest 0.1 mm. Floral measurements for most species
diurnal insects (small bees and flies that visited flowers primarily were taken by one person (S. Marten-Rodriguez), except for meas
for pollen). For each year, pollinator visitation rates by each functional urements for R. minus, which were taken by A. Almarales-Castro; all
group were calculated as the number of visits per flower per hour; this measurements are listed in Appendix S2.
rate was multiplied by 12 to obtain visitation frequencies per day or To document the timing of anthesis and nectar production, two
night, according to the schedule of the pollinator. At the latitudes where species of each floral phenotype were selected (nocturnal campanulate
the study was conducted, daylight hours range between 12 and 13; thus, and subcampanulate: G fruticosa, G quisqueyana; tubular: G pedicellaris,
for the sake of consistency, we calculated visitation for 12-h days. R. asperum; subcampanulate mixed traits: R leucomallon, R vemico
To distinguish non-pollinating floral visitors from animals that sum). We also used data for five Puerto Rican Gesneria previously
have the ability to transfer pollen we carefully observed visitor studied (Marten-Rodriguez & Fenster 2008). Flower buds of one to
behaviour and frequency of contact with the reproductive organs. two flowers per plant, in five to 14 plants per species were bagged
Whenever possible we observed virgin flowers and checked them after a and checked every 3 h for a continuous 24-h period starting at 15.00;
visit to determine whether pollen had been removed from anthers or the earliest time at which anther slits were noticed open was
deposited onto stigmas. However, since these data were collected recorded. Nectar was extracted from bagged first-day flowers using
only for a subset of the flowers, we quantified efficiency as the capillary tubes or with a 50-gL Hamilton Syringe (Hamilton, NV,
number of times the visitor contacted stigmas or anthers divided by USA), and sugar concentration was measured with a hand-held
the total number of visits (Armbruster & Herzig 1984). We recognize refractometer (Sugar/Brix Refractometer, 0-32% w/ATC, Sper Scien
that contact is an approximate measure of efficiency but due to the tific, Scottsdale, AZ). For the remaining species, plants were checked
logistical difficulties of obtaining pollen removal and deposition at least four times over the course of 24 h, such that we could tell
data for a large group of species, we consider this approach provides whether pollen shedding occurred at night (18.00-06.00) or day
a better characterization of the pollination system than a simple list (06.00-18.00). Nectar concentration on these plants was measured
of floral visitors. Pollinator importance values for each group of in flowers that were not previously bagged. Nectar production coded
visitors were calculated as the product of visitation and efficiency. as nocturnal started as early as 15.00 and generally stopped by
To obtain a comparable index of pollinator importance we stand 07.00; nectar production coded as diurnal started as early as 04.00
ardized each value, dividing it by the sum of importance values and stopped at different times of the day, depending on the species.
across all functional groups of pollinators. Therefore, pollinator For anther dehiscence, nocturnal schedules were generally from
importance indices range from 0 to 1.We report mean pollinator 18.00 to 20.00 while diurnal anther dehiscence started as early as
visitation and range across years for species observed for more 05.00. Nectar volume was not included because this measure
than 1 year. Importance values obtained from 1 year of sampling, ment required bagging flowers and sample sizes were insufficient to
particularly those of bats and infrequent insect visitors, may not be obtain reliable measurements for almost half of the species. In order
accurate estimators. However, we have a representative sample of to identify scent production, first-day flowers of at least two spe
species (including the principal floral phenotypes) that were observed cies of each floral phenotype (nine species total) were left in glass
for many hours in multiple years. Since these results are mostly containers for 2-3 h and then checked by smelling them. No perceiv
consistent across the data set, we considered it appropriate to able scent was detected for any of these species; thus, this trait was
include the understudied species. We excluded visitors that were not included in the analysis.
never observed contacting the reproductive organs or carrying pollen
(e.g. grasshoppers, beetles) and the introduced honeybee Apis mellifera,
STATISTICAL ANALYSES
since it is unlikely this species has been long enough in the New
World (a few hundred years) to be responsible for evolutionary changes All analyses were performed in SAS version 9.1.3 (SAS Institute 2004).
underlying the floral diversification of the tribe Gesnerieae. We used multidimensional scaling to examine patterns of association
among species with floral characters traditionally linked with
pollination syndromes. Eleven floral characters described above
MEASUREMENTS OF FLORAL TRAITS
were used to calculate dissimilarity matrices using the DISTANCE
To characterize floral phenotypes we measured 11 floral charactersprocedure with method = dgower specified to calculate distances
from two to three flowers of 7-23 individuals per species. Flowersbased on Gower's coefficient; this coefficient allows the use of nominal
were collected from all plants available when population densitiesand different kinds of quantitative variables (Gower 1971). The MDS
were low (< 20 individuals); otherwise, flowers were collected from aprocedure using the ordinal level option was used to indicate non
sample of the population. Flower measurements of fresh flowersmetric ordinations. Two ordinations using floral characters were
included: (i) corolla length, the shortest length of the corolla tube; performed: one that included all species and one that excluded
(ii) pistil exertion, measured in pistillate-phased flowers as the differencespecies with tubular flowers. The latter analysis was conducted to
between pistil length and corolla length; (iii) diameter of the corollaevaluate floral characters that might help discriminate between
bat-pollinated and generalist species. Multidimensional scaling by
opening; (iv) corolla constriction, coded as present or absent; (v) corolla
curvature, taken with a protractor for curvature of the dorsal side ofpollinator visitation and importance values was also performed to
the corolla tube; (vi) nectar concentration (see below); (vii) symmetry,compare the grouping patterns produced by floral characters with
coded as (0) subactinomorphic (reproductive organs not symmetricallythe groupings suggested by the pollinators. The patterns using
positioned, otherwise actinomorphic) or (1) zygomorphic; (viii) timingvisitation data were the same as those using importance values;
of anther dehiscence, coded as (0) nocturnal (18.00-06.00), (2) diurnal therefore, we report only the latter below.

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352 S. Maruen-Rodriguez, A. Almarales-Castro & C. B. Fenster

The sample of species used in the floral ordination was not phylo both by bats and hummingbirds. Pollen is available for pollen
genetically corrected; therefore, some similarities among species may transfer by hummingbirds in late afternoon (second-day
reflect common ancestry. Being aware of this problem, we attempted flowers), and at dawn (unvisited third-day flowers); therefore
to ensure a higher level of independence by including, for both we consider this species an ecological generalist despite its
chiropterophilous and ornithophilous flowers, species from at least
mostly nocturnal pollination syndrome (Marten-Rodriguez &
two clades within the Antillean tribe Gesnerieae (Marten-Rodriguez
Fenster 2008). In contrast, G quisqueyana from the Dominican
et al. unpublished data) and four Costa Rican species from three
Republic and sister to G viridiflora subsp. sintenisii, restricts
additional tribes (Zimmer et al. 2002). Therefore, we can be confident
access to diurnal visitors by an active exclusion mechanism.
that the results reported below reflect more than taxonomic affinities.
To evaluate the association between floral characters or pollinator
The flowers of G quisqueyana are protogynous; however,
importance with the first two dimensions of the ordination, we conducted unlike its bat-pollinated relative, which has mid-afternoon
Spearman rank correlations. Correlation coefficients are reported anthesis, flowers of G quisqueyana open between 19.00 and
significant at the P = 0.05 level after sequential Bonferroni correction to 20.00 and the pistillate phase lasts only one night. Corollas
adjust for multiple comparisons. Likewise, Spearman rank correlations close up completely the next morning between 06.00 and
were used to assess the degree of association among floral characters. 07.00 h and open the second and last night in male phase;
To evaluate the predictability of pollination syndromes in Antillean receptive stigmas are not exposed during the day.
Gesneriaceae, we conducted non-parametric discriminant analysis
Generalized pollination systems were characteristic of
using the first two dimensions of the floral ordination (all species
Rhytidophyllum species with subcampanulate corollas and
included) to represent the suite of floral traits. We used the DISCRIM
mixed combinations of other floral traits. The two-day
procedure in SAS, specifying the 'kernel normal' option to allow for
protogynous flowers were visited by different sets of animal
a nonlinear discriminant search. We made no assumptions about
the underlying multivariate distribution and used a non-pooled taxa, including bats, hummingbirds, moths and small diurnal
covariance matrix. A priori groupings were based on the observed insects (Halictid bees and flies). All these animals contacted
pollination systems (i.e. hummingbird specialists, bat specialists and stigmas and anthers at least occasionally, but differences in
generalists). To classify species as generalist or specialist we used our efficiency among visitors may be considerable. Bat and humming
pollinator importance index, which combines visitation frequency bird visits often result in pollen removal and deposition (checked
and frequency of contact with the reproductive organs. Fenster et al. on virgin flowers after one visit), and large pollen loads deposited
(2004) used a cut-off of a 75% visitation frequency for the most on foreheads or bills. In contrast, most insect visitors carry little
abundant pollinator to determine their categories of specialization
pollen. Overall visitation to generalist flowers ranged from 3
and generalization. Here, we utilized a natural break in the data near
to 26 visits per flower per day (Table 1).
that cut-off point and classified species as generalists if the importance
index of the most important pollinator was 76% or below, and as
specialists if the index was 77% or higher. The lowest most important ORDINATIONS BY FLORAL TRAITS AND POLLINATOR
pollinator index for species classified as specialists was 84% (for G. IMPORTANCE
pedunculosa).
Two distinct clusters separate along dimension 1 of the floral
ordination, corresponding to tubular and bell-shaped flowers
Results (both campanulate and subcampanulate) (Fig. 2). The cluster
of tubular flowers includes species from various clades
POLLINATOR VISITATION AND IMPORTANCE
(Zimmer et al. 2002, Marten-Rodriguez et al. unpublished
A list of the floral visitors observed in all Costa Rican and data), and are all strictly hummingbird-pollinated. Within the
Antillean Gesneriaceae is provided in Appendix S3. Pollinators cluster of species with bell-shaped flowers, two subgroups can
of tubular-flowered species were almost exclusively humming be distinguished, one associated with bat pollination (above
birds, usually one or two hummingbird species. Visitation rates the zero value of dimension 2), and the other associated with
by hummingbirds to Gesneriaceae from the Antillean islands generalized pollination (mostly below the zero value).
ranged from one visit per flower every three days to two visits Most floral characters were highly correlated with the first
per flower per day; visitation rates to Costa Rican Gesneriaceae dimension of the ordination plot. The correlations indicate
ranged between three and six visits per flower per day (Table 1). that, moving towards the left side of the plot along dimension
Hummingbird pollinator importance values between 0.96 and 1, flowers have wider corollas, some constriction above the
1.00; other visitors included Halictid bees and butterflies, with nectar chamber, lower nectar concentration, noctumal schedules
low importance values (0.03-0.04). We found little temporal of nectar production and anther dehiscence, colours towards
variation in visitation rates and pollinator importance values the yellow/green part of the spectrum, and the presence of
for species that were observed in multiple years (Table 1). dark red spots (Fig. 2). In contrast, moving to the right side
Gesneriaceae species with campanulate green or white along dimension 1, the trend is for tubular corollas with solid
flowers were primarily pollinated by bats; bird and insect bright colours, greater nectar concentration, and diurnal
visitors, when present, had low importance values (Table 1). nectar production and anther dehiscence (i.e. hummingbird
Visitation rates by bats ranged between one and four visits pollination syndrome). For the colour trait, which was coded
per flower per night and importance values between 0.80 and as a multi-state character, the coding was set to reflect the
1.00 (Table 1). As reported in a previous study, subcampanulate colour spectrum; therefore, moving to the right along the
G. viridiflora subsp. sintenisii from Puerto Rico was pollinated dimension 1 indicates more orange and red corollas.

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 Pollination syndromes in Antillean Gesneriaceae 353

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354 S. Marten-Rodriguez, A. Almarales-Castro & C B. Fenster

Floral trait Dim 1 Dim 2

2 Corolla length ventral 0.449 0.252
Pistil exertion -0.328 -0.079
CG& Corolla width at mouth -0.781 0.012
1 Corolla constriction -0.712 -0.456
1 | GF G&A Corolla curvature -0.478 -0.565
GPEAG CC Nectar concentration 0.549 -0.115
GQ *V CPU Symmetry -0.627 -0.537
a 0 GVI' GCI+ +BS Timing of anthesis 0.851 -0.149
E RAU* RL* +GAC Timing of nectar 0.851 -0.149
RGI RM RA Colour 0.503 -0.431
+ GVE Spots -0.812 0.117
-1 Pollinator Importance
Hummingbird 0.719 -0.297
Bananaquit -0.349 0.105
RV Bat -0.575 0.555
-2 Moth -0.500 -0.430
______________2__
-2-1 0 1 2
Dimension 1

Fig. 2. Multidimensional scaling analysis of 23 Gesneriaceae species based on 11 floral characters. Triangles represent species that specialize on bat
pollination, plus signs represent species that were exclusively hummingbird-pollinated and dots represent species with mixed hummningbird and
nocturnal pollination (bats and/or moths). Spearman correlation coefficients are listed for associations of dimensions 1 and 2, with floral traits and
with pollinator importance values. Coefficients in bold indicate significant correlations following sequential Bonferroni adjustment (P < 0.05).

The ordination conducted excluding tubular-flowered Other high correlations (significant before Bonferroni
species shows a stronger separation of the two subgroups of correction) included: pistil exertion, corolla curvature, and colour.
bell-shaped flowers; however, two oddities are evident: R. Thus, moving to the right along dimension 1 (associated with
minus (RM) appears clustered within the generalists but only specialized bat pollination), pistils tend to be more exerted,
hummingbirds were observed as native pollinators. Given its corollas less curved, light green or white, and not constricted
nocturnal schedule of nectar production and anther dehiscence, above the nectar chamber.
we cannot rule out the possibility of bat pollination until Pollinators also separated Gesneriaceae species into clusters
observations in multiple seasons are conducted. The second corresponding to ornithophilous and chiropterophilous
inconsistent case is G quisqueyana (GQ), a strict bat specialist flowers in the ordination using pollinator importance values
that was placed within the generalists cluster. This species (Fig. 4). However, in contrast with the clustering defined
restricts diurnal visitors by closing flowers during the day (see by floral traits (Fig. 1), species with subcampanulate flowers
above description). Thus, although the floral morphology appeared scattered throughout the plot, reflecting the
would allow a wider range of visitors, the floral phenology variability in pollinator importance values and pollinator
filters out diurnal visitors. assemblages (Fig. 4). The only trait that correlated with dimension
With tubular-flowered species excluded from the ordination, 1 was colour, indicating red colours present in most species
the corolla constriction became the single most important visited by hummingbirds, both specialists and generalists.
trait separating the two subgroups of bell-shaped flowers Correlations among floral traits revealed 11 significant
(associated with generalized and bat pollination) (Fig. 3). associations (Table 2). These indicate flowers with wide

Table 2. Spearman correlation coefficients among all floral traits of 23 Gesneriaceae species used for floral ordinations. Numbers in bold
indicate significant correlations after sequential Bonferroni adjustment

PE CWM CC CUR NC SYM TAD TNP Colour Spots

Corolla length (CL) -0.02 -0.21 -0.53 -0.23 0.15 -0.36 0.38 0.38 0.26 -0.32
Pistil exertion (PE) 0.30 -0.07 0.26 -0.16 0.69 -0.25 -0.25 -0.37 -0.01
Corolla width at mouth (CWM) 0.50 0.28 -0.36 0.44 -0.84 -0.85 -0.54 0.70
Corolla constriction (CC) 0.28 -0.35 0.39 -0.65 -0.65 -0.15 0.51
Corolla curvature (CUR) -0.27 0.56 -0.11 -0.11 0.08 0.42
Nectar concentration (NC) -0.24 0.48 0.48 0.00 -0.55
Symmetry (SYM) -0.36 -0.36 -0.22 0.23
Timing anther dehiscence (TAD) 1.00 0.66 -0.73
Timing nectar production (TNP) 0.66 -0.78
Colour -0.42

?D 2009 The A

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 Pollination syndromes in Antillean Gesneriaceae 355

Floral trait Dim 1 Dim 2

2
Corolla length ventral 0.345 0.228
ACG Pistil exertion 0.596 -0.182
Corolla width at mouth 0.068 0.687
1 Corolla constriction -0.837 -0.418
A GF Corolla curvature -0.670 0.373
Nectar concentration 0.176 -0.200
.o RG @ GVI z A GPE Symmetry 0.200 -0.500
C, O GQ Timing of anthesis -0.500 0.300
E Timing of nectar -0.500 0.300
0 RAU A GCA Colour -0.724 -0.261
Spots 0.387 0.710
-1 Pollinator importance
RM Hummingbird -0.719 -0.330
RL Bananaquit 0.027 -0.242
Bat 0.796 0.278
-2
Moth -0.642 0.084
Diurnal insects -0.357 0.094
-3 -2 -1 0 1 2
Dimension 1

Fig. 3. Multidimensional scaling analysis of 1 1 Gesneriaceae species based on 1 1 floral characters (excluding 12 species with tubular flowers).
Rhytidophyllum minus (RM, plus sign next to RL) was included because with only one year of observation, the occurrence of bat pollination
cannot be discarded. As above, triangles represent bat-pollinated species and dots represent species with mixed hummingbird and nocturnal
pollination (bats and/or moths). Spearman correlation coefficients are listed for associations of dimensions 1 and 2, with floral traits and with
pollinator importance values. Coefficients in bold indicate significant correlations following sequential Bonferroni adjustment (P < 0.05).

2 Floral trait Dim 1 Dim 2

RAU Corolla length ventral -0.026 0.128
Pistil exertion 0.350 0.073
1 GPE, Corolla width at mouth 0.360 -0.595
GVE GR PC
BS GCI CQ GAC Corolla constriction -0.059 -0.476
RAS# CC Corolla curvature 0.160 -0.045
c GPI GCU GPU G G Nectar concentration 0.195 0.197
_n Symmetry 0.093 -0.156
E -1
_ RV
RL*Timing
RL Timing
ofof anthesis
nectar -0.5490.514
-0.608 0.504
Colour -0.724 0.192
-2 Spots 0.381 -0.331
Pollinator Importance
Hummingbird -0.555 0.573
Bananaquit 0.357 0.511
3 RG Bat 0.875 -0.333
Moth -0.177 -0.689
Diurnal insects -0.397 -0.414
-2 -1 0 1 2 3
Dimension 1

Fig. 4. Multidimensional scaling of 23 species of Gesneriaceae based on pollinator importance values. Importance was calculated as the product
of visitation rates and effectiveness (contact with reproductive organs) and standardized as a proportional value. Note the hummingbird-pollinated
species (plus sign) are mostly clustered in one point. Triangles indicate species primarily bat-pollinated and circles indicate generalist species.
Spearman correlation coefficients are listed for associations of dimensions 1 and 2, with floral traits and with pollinator importance values.
Coefficients in bold indicate significant correlations following sequential Bonferroni adjustment (P < 0.05).

corollas tend to have nocturnal schedules, green to white production and anther dehiscence. As a general rule, this
colours and dark red or brown spots, while flowers with subcampanulate floral phenotype indicates generalized
narrow corollas tend to have diurnal schedules and solid pollination systems in the tribe Gesnerieae.
bright red or orange colours. These associations reflect the
suites of floral characters associated with classic bat and
EVALUATION OF POLLINATION SYNDROMES
hummingbird pollination syndromes, respectively. The
presence of a corolla constriction that makes subcampanulate Discriminant analysis was used to evaluate the ability of
corollas, was associated with nocturnal schedules of nectar suites of floral traits to predict the pollination system; the

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356 S. Marhen-Rodrigue-, A. Almarales-Castro & C B. Fenster

Table 3. Number of observations classified into expected pollination system and posterior probabilities (in parentheses) under cross-validation
of discriminant analysis of multivariate set of floral traits of 23 Gesneriaceae species

Classified as
Posterior probability
A priori Bat Generalist Hummingbird Total Error rate

Bat 4 1 0 5 0.210
(0.820) (0.530)
Generalist 1 3 1 5 0.274
(0.670) (0.714) (0.731)
Hummingbird 0 1 12 13 0.021
(0.958) (1.000)

subtropical
three a priori designated pollination system plants (Tschapka & Dressler
categories were 2002), including
based on our field observations: other
hummingbird,
members of the familybat and
Gesneriaceae (e.g. floral
generalist. When cross-validation morphologies
was used to
that evaluate
facilitate access to the
nectar, open corollas to
ability of the model to classify species intodetection
facilitate expected pollination
by echolocation, exposed floral displays to
systems, floral traits were able to predict
enhance hummingbird
accessibility; Sanmartin-Gajardo & Sazima 2005b).
pollination 12 out of 13 times; R. Our
minus was
results also classified
support the existence as
of a distinct humming
a generalist (Table 3). For the bat pollination category,
bird pollination syndrome one
in the Gesneriaceae (tubular, red
species out of five was misclassified (G diurnal
or yellow quisqueyana was
flowers with dilute nectar), one of the most
widespread
classified as a generalist), and for the and accepted
generalist, patterns
two out ofof
floral convergence
five species were misclassified, one(e.g.
into
Sakai the hummingbird
et al. 1999; Kay & Schemske 2003; Hargreaves
(R. leucomallon) and one into the batet al.(G.
2004;viridiflora
Sanmartin-Gajardo & Sazima 2005a; Wilson
subsp.
Sintenisii) pollination categories (Table 3).Whittall & Hodges 2007). However, an intriguing
et al. 2006;
finding was the occurrence of high hummingbird visitation to
flowers that obviously do not correspond to the ornithophilous
Discussion syndrome (i.e. visitation to bell-shaped, green/light yellow
The validity of the pollination syndrome concept has been flowers).
recently called into question based on an argument derived Although hummingbird visitation to 'non-omithophilous'
primarily from the observed widespread generalization offlowers had been previously observed (e.g. Feinsinger 1976;
pollination systems in temperate regions (Waser et al. 1996; Stiles 1976), the significantly greater visitation to the green
Ollerton et al. 2007), although some recent community-level flowers of Gesneria was unexpected. In a sample of Gesnerieae
studies suggest generalized pollination systems may be equallyfrom Puerto Rico and the Dominican Republic we found
common in the tropics (Ollerton & Cranmer 2002). Thisthat the average nectar volume was greater for bell-shaped
study evaluated the correspondence between pollination flowered species (range 60-82 tL, n = 4 species), than in
ecology and patterns of floral diversity in the Antillean tubular-flowered ones (range 5-16 ,uL, n = 5 species; Marten
monophyletic tribe Gesnerieae. To obtain a better idea of theRodriguez & Fenster 2008 and unpublished data). Nectar
animals that could act as agents of selection on floral characters, volume, a trait that clearly separates bat-pollinated from
we made an effort to distinguish floral visitors that have the hummingbird-pollinated species was not included in this
ability to transfer pollen, from non-pollinating visitors. Westudy due to the small number of species for which accurate
also attempted to reduce underestimating the number of estimates were obtained. However, it appears that humming
potential pollinators by surveying a subset of species for birds are attracted to green bell-shaped-flowered Gesneria
various years and at various sites. Our study provides species due to their higher nectar content. Other floral traits
evidence for both extreme ecological specialization andassociated with the ornithophilous syndrome may serve to
generalization within a group of Neotropical Gesneriaceae, enhance efficiency of pollen transfer (tubular corollas; e.g.
and demonstrates that the occurrence of ecological generalCastellanos et al. 2004), or signal the presence of a common
ization (visits by many species) has not precluded the food source (corolla colour), but are not the primary attractants
evolution or maintenance of suites of floral traits thatfor the birds (Stiles 1976).
coincide with established pollination syndromes (Faegri & The lack of fidelity by hummingbirds to species with tubular
van der Pjil 1978). corollas explains the existence of generalized pollination
The patterns for bat and hummingbird pollination systems. Gesnerieae species with subcampanulate corollas
syndromes were the same for Antillean and more distantly and mixed floral traits had nocturnal (bats and moths)
related mainland Gesneriaceae; no generalists from theand diurnal (hummingbirds and flies) visitors potentially
mainland were identified in this study. Gesnerieae flowers contributing to fruit set. Floral traits that coincide with bat
show adaptations to bat pollination that correspond to traitspollination are: nocturnal schedules of nectar production
described in over 700 bat-pollinated species of tropical and and anther dehiscence, abundant dilute nectar, and light

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 Pollination syndromes in Antillean Gesneriaceae 357

yellow-green corollas in most species. Although some of these chances of pollination to unvisited flowers, by making nectar
traits also correspond with known adaptations to moth pollina more accessible or attractive to bats. Future work should
tion, moths do not always contact stigmas or anthers. In address the functional significance of corolla constriction in
contrast, some traits appear to be driven by selection to enhance relation to all observed functional groups of pollinators.
hummingbird pollination. These traits vary among generalist
Gesnerieae, but they include narrower bell-shaped corollas,
PREDICTABILITY OF POLLINATION SYNDROMES
yellow colours with variable amounts of bright red markings,
and diurnal as well as nocturnal nectar production and The current debate on pollination syndromes has focused on
anther dehiscence (in R. vernicosum). No floral adaptations two major issues: the role of pollination specialization and the
for the rare and inconsistent diurnal insect visitors were predictive power of syndromes (Fenster et al. 2004; Ollerton
detected, as indicated by the lack of correlation between these et al. 2007). The notion that syndromes reflect natural selection
visitors and floral traits (Figs 2-4). Species with intermediate to enhance pollen transfer by principal pollinators assumes
phenotypes between ornithophily and chiropterophily have that specialization into functional groups of pollinators (sensu
been described in at least two other plant families: the Armbruster et aL 2000) has been important in shaping floral
Lobeliaceae (e.g. Syphocampylus sulfureus, Sazima et al. 1994) evolution. We have demonstrated that floral characteristics in
and the Malvaceae (e.g. Abutilon, Buzato et al. 1994). In both Antillean Gesneriaceae assemble species into hummingbird
cases, floral traits have been interpreted as transitional and bat pollination syndromes as well as into an intermediate
phenotypes along an evolutionary pathway to bat pollination. floral phenotype that is closer to chiropterophily. Phylogenetic
There are other instances where bat-pollinated and hummingbird relatedness cannot account for all of the similarity among
pollinated species occur within the same genus but no species that fell into particular syndrome categories (Zimmer
intermediate phenotypes are found in nature, reflecting trade et al. 2002, Marten-Rodriguezet al. unpublished data phylogeny).
offs in corolla shape imposed by bats and hummingbirds For instance, the cluster that contains bat-pollinated specialists
(Muchhala 2007). in the ordination includes at least three independent origins of
In Gesnerieae, some traits display character states that appear this pollination system, while the cluster comprised by species
to reflect selection by two different functional groups of with generalized pollination systems includes two independent
pollinators, such as nocturnal and diurnal schedules of nectar origins. Hummingbird-pollinated species are distributed across
production and anther dehiscence, and colour variation in some at least four different clades, although in the tribe Gesnerieae
species. Whether these characters represent a transitional stage hummingbird pollination is most likely ancestral (Marten
or an equilibrium point maintained by divergent selective Rodriguez et al. unpublished phylogeny). Significant corre
pressures exerted by nocturnal and diurnal pollinators is not lations among traits and pollinators (e.g. timing of anthesis,
clear. However, these traits do not consistently explain the timing of nectar production, corolla shape and colour) suggest
phenotypic clustering of species with generalized pollination that sets of floral characters have responded to selection to
systems. The single trait that distinguished generalists from enhance pollination by the observed visitor guilds. Support
their bat-pollinated relatives was the presence of a corolla for syndromes has been found in various other plant taxa
constriction located right above the nectar chamber (see Fig. 1). using multivariate approaches (Sakai et al. 1999; Wilson et al
Wolfe & Stiles (1989) proposed that corolla constrictions in 2004; Wolfe & Sowell 2006). For example, in Bornean gingers,
hummingbird-pollinated flowers were part of an adaptive three clusters of floral phenotypes defined in multivariate
'fail-safe' mechanism that enticed visitation by secondary space corresponded with pollination by spiderhunters
pollinators, when the primary hummingbird specialists were (Nectarinidae) and two different groups of bees (Anthophoridae
absent. We hypothesize the corolla constriction in Gesneria and Halictidae; Sakai et al. 1999). Likewise, in Penstemon
and Rhytidophyllum facilitates nectar access to bats, while clustering of omithophilous and melittophilous species strongly
increasing the effectiveness of hummingbird pollination, thus corresponded with the predicted pollinators (Wilson et al.
promoting a dual pollination strategy in flowers predominantly 2004).
adapted for bat pollination. Predictability is the second major issue concerning the
In the generalist species of Gesneria and Rhytidophyllum, debate on pollination syndromes (Ollerton et al. 2007). Our
hummingbird visits occur mostly in the late afternoon and statistical evaluation indicates that floral traits are good
early morning, which could be interpreted as thieving of early predictors of specialized hummingbird and bat pollination in
or leftover nectar. However, the stigmas of Gesnerieae species Antillean Gesneriaceae. However, the classificatory scheme
remain receptive for nearly 30 straight hours, and pollen was not perfect: R. minus (hummingbird-pollinated) and G.
deposition was observed during hummingbird visits occurring quisqueyana (bat-pollinated) were both misclassified as
at dawn and dusk. The corolla constriction appears to direct generalists. The first species has been observed for only 1 year
the hummingbird's bill to contact stamens and pistils in and although nocturnal observation time (18 h) was within
flowers that would otherwise be too wide for effective the range of other bat-pollinated species in our sample, it is
pollination to occur (video 1, Supporting Information). The possible that further observations will reveal the expected
constriction also makes nectar overflow accumulate as a nocturnal pollinators. It is also possible that given the
nectar drop in the lower limb of the corolla, which is visible restricted present distribution of R. minus (one population in
during the late night hours. This nectar drop may enhance the eastemn Cuba isolated from undisturbed habitats), bat visits are

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358 S. Marten-Rodriguez, A. Almarales-Castro & C B. Fenster

rare and thus, the species relies largely on hummingbirds for existence of floral phenotypes that appear intermediate or
reproduction. The second misclassified species, G quisqueyana, that do not fit classic syndromes. The study of ecological
prevents hummingbird visitation by an active exclusion interactions between plants and different kinds of floral
mechanism: the two-night flowers of G. quisqueyana close up visitors, including mutualists and parasites, remains a major
during daytime. Therefore bat specialization is achieved by task to complete in order to elucidate the evolutionary
a unique phenological trait not included in the statistical processes responsible for the floral diversification of Antillean
analysis. This finding is evidence that, even within groups of Gesnerieae and other groups of tropical plants.
related species, the pathways to specialization vary, resulting
in different phenotypes associated with the same pollination
syndrome.
Acknowledgements
In contrast to specialized Gesnerieae species, suites of floral Authors are grateful to T. Clase, J. Cridland, X.S. Chen, A. Chuquin, M. Faife,
D. Fernandez, D. Growald, J. Hereford, C. Moreno, D. Stanton, for help
traits did not consistently predict generalized pollination
conducting field work and the Arecibo Observatory, the Institute of Jamaica,
systems (Table 3). However, the presence of a constricted and Jardin Botanico de Santo Domingo for logistical support. Authors thank
bell-shaped corolla was, in most cases, a good indicator of J. Agren, A. Baier, M. Dudash, D. Inouye, J. Ollerton, L. Zimmer and one
anonymous referee for insightful revisions to earlier versions of this article.
generalization. The variability of other floral traits in the
Authors thank R. Reynolds for statistical advice and L. Skog for information
generalists may reflect the more variable selective regimes to and support provided during various stages of the project. Funding for field
which species with noctumal and diumal pollinators are exposed. work was provided by American Gloxinia and Gesneria Society, The Explorers
Club-Washington Group, Graduate Woman in Science, Sigma Xi, University
Alternatively, certain associations may reflect phylogenetic
of Maryland (Bamford Fund and BEES Program) to SMR, and NSF DDIG
affinities rather than pollinator-mediated selection. For example, 0710196 to SMR and CBF.
in a multivariate analysis of South African asclepiads, Ollerton
et al. (2003) found distinct separation of wasp and beetle
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C 2009 The Authors. Journal compilation ?D 2009 British Ecological Society, Journal of Ecology, 97, 348-359

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