pollinator visitation and importance
A list of the floral visitors observed in all Costa Rican and Antillean Gesneriaceae is provided in Appendix S3. Pollinators of tubular-flowered species were almost exclusively hummingbirds, usually one or two hummingbird species. Visitation rates by hummingbirds to Gesneriaceae from the Antillean islands ranged from one visit per flower every three days to two visits per flower per day; visitation rates to Costa Rican Gesneriaceae ranged between three and six visits per flower per day (Table 1). Hummingbird pollinator importance values between 0.96 and 1.00; other visitors included Halictid bees and butterflies, with low importance values (0.03–0.04). We found little temporal variation in visitation rates and pollinator importance values for species that were observed in multiple years (Table 1).
Table 1. Pollination system, visitation frequencies and pollinator importance values recorded for 23 species of Gesneriaceae from the Antillean islands (19 species) and Costa Rica (4 species). Pollinator visitation was calculated as the number of visits per flower per day. Mean values over the number of study years are presented followed by the range across years in brackets. Pollinator importance was calculated as the product of proportional visitation rates and a proxy for efficiency (proportion of contacts with anthers and stigmas). Importance values were scaled to proportions. Number of years and hours of observation are provided in the last column
|Species||Locality||Floral phenotype||Pollinator||Pollinator visitation mean [range]||Scaled Importance mean [range]||Number of years [Number of hours]|
|Besleria solanoides||Costa Rica||Tubular||Hummingbird||3.0||0.97||1 |
|Capanea grandiflora||Costa Rica||Campanulate||Bat||1.7||1.00||1 |
|Columnea consanguinea||Costa Rica||Tubular||Hummingbird||4.2||1.00||1 |
|Columnea quercetii||Costa Rica||Tubular||Hummingbird||6.4||1.00||1 |
|Gesneria acaulis||Jamaica||Tubular||Hummingbird||0.3||1.00||1 |
|Gesneria calycosa||Jamaica||Campanulate||Bat||0.9||1.00||1 |
|Gesneria citrina||Puerto Rico||Tubular||Hummingbird||0.4 [0.3–0.5]||1.00||3 |
|Gesneria cuneifolia||Puerto Rico||Tubular||Hummingbird||0.5 [0.4–0.6]||1.00||3 |
|Gesneria fruticosa||Hispaniola||Campanulate||Bat||1.2 [0.9–1.6]||1.00||2 |
|Gesneria pedicellaris||Hispaniola||Tubular||Hummingbird||0.4 [0.3–0.5]||1.00||2 |
|Gesneria pedunculosa||Puerto Rico||Campanulate||Bat||3.9 [3.7–4.2]||0.84 [0.80–0.91]||3 |
|Bananaquit||1.0 [0.7–1.6]||0.09 [0.08–0.09]|| |
|Diurnal insects||0.6 [0.0–0.9]||0.07 [0.00–0.14]|| |
|Gesneria pulverulenta||Hispaniola||Tubular||Hummingbird||2.2 [1.7–2.7]||1.00||2 |
|Gesneria quisqueyana||Hispaniola||Subcampanulate||Bat||1.5 [0.9–2.1]||0.95 [0.90–1.00]||2 |
|Hummingbird||0.05 [0.0–0.1]||0.05 [0.00–0.10]|| |
|Gesneria reticulata||Puerto Rico||Tubular||Hummingbird||0.1 [0.0–0.2]||1.00||3 |
|Gesneria ventricosa||St. Lucia||Tubular||Hummingbird||0.5||1.00||1 |
|Gesneria viridiflora subsp. sintenisii||Puerto Rico||Subcampanulate||Bat||2.5 [1.3–3.6]||0.52 [0.32–0.72]||2 |
|Hummingbird||3.0 [2.5–3.5]||0.42 [0.28–0.57]|| |
|Moth||3.3 [3.0–3.6]||0.06 [0.00–0.11]|| |
|Pheidonocarpa corymbosa||Jamaica||Tubular||Hummingbird||2.0||1.00||1 |
|Rhytidophyllum asperum||Hispaniola||Tubular||Hummingbird||1.9 [1.5–2.1]||0.96 [0.93–1.00]||3 |
|Diurnal insects||0.1 [0.0–0.2]||0.04 [0.00–0.07]|| |
|Rhytidophyllum auriculatum||Puerto Rico||Subcampanulate yellow/red||Bat||[0.0–1.2]||0.20 [0.00–0.44]||2 |
|Bananaquit||[0.0–0.5]||0.10 [0.00–0.20]|| |
|Hummingbird||2.5 [1.7–3.4]||0.70 [0.56–0.80]|| |
|Rhytidophyllum grandiflorum||Hispaniola||Subcampanulate yellow/red||Hummingbird||3.0||0.27||1 |
|Diurnal insects||9.7||0.50|| |
|Rhytidophyllum leucomallon||Hispaniola||Subcampanulate yellow||Bat||2.4 [0.0–4.7]||0.24 [0.00–0.48]||2 |
|Hummingbird||8.1 [6.0–11.9]||0.65 [0.44–0.86]|| |
|Moth||4.1 [1.3–6.9]||0.07 [0.03–0.12]|| |
|Diurnal insects||0.3 [0.3–0.4]||0.04 [0.03–0.04]|| |
|Rhytidophyllum minus||Eastern Cuba||Subcampanulate yellow||Hummingbird||4.7||1.00||1 |
|Rhytidophyllum vernicosum||Hispaniola||Subcampanulate yellow/red||Hummingbird||8.7 [7.0–10.4]||0.76 [0.75–0.77]||2 |
|Moth||3.3 [1.5–5.0]||0.14 [0.09–0.19]|| |
|Diurnal insects||1.1 [0.5–1.7]||0.10 [0.04–0.16]|| |
Gesneriaceae species with campanulate green or white flowers were primarily pollinated by bats; bird and insect visitors, when present, had low importance values (Table 1). Visitation rates by bats ranged between one and four visits per flower per night and importance values between 0.80 and 1.00 (Table 1). As reported in a previous study, subcampanulate G. viridiflora subsp. sintenisii from Puerto Rico was pollinated both by bats and hummingbirds. Pollen is available for pollen transfer by hummingbirds in late afternoon (second-day flowers), and at dawn (unvisited third-day flowers); therefore we consider this species an ecological generalist despite its mostly nocturnal pollination syndrome (Martén-Rodríguez & Fenster 2008). In contrast, G. quisqueyana from the Dominican Republic and sister to G. viridiflora subsp. sintenisii, restricts access to diurnal visitors by an active exclusion mechanism. The flowers of G. quisqueyana are protogynous; however, unlike its bat-pollinated relative, which has mid-afternoon anthesis, flowers of G. quisqueyana open between 19.00 and 20.00 and the pistillate phase lasts only one night. Corollas close up completely the next morning between 06.00 and 07.00 h and open the second and last night in male phase; receptive stigmas are not exposed during the day.
Generalized pollination systems were characteristic of Rhytidophyllum species with subcampanulate corollas and mixed combinations of other floral traits. The two-day protogynous flowers were visited by different sets of animal taxa, including bats, hummingbirds, moths and small diurnal insects (Halictid bees and flies). All these animals contacted stigmas and anthers at least occasionally, but differences in efficiency among visitors may be considerable. Bat and hummingbird visits often result in pollen removal and deposition (checked on virgin flowers after one visit), and large pollen loads deposited on foreheads or bills. In contrast, most insect visitors carry little pollen. Overall visitation to generalist flowers ranged from 3 to 26 visits per flower per day (Table 1).
ordinations by floral traits and pollinator importance
Two distinct clusters separate along dimension 1 of the floral ordination, corresponding to tubular and bell-shaped flowers (both campanulate and subcampanulate) (Fig. 2). The cluster of tubular flowers includes species from various clades (Zimmer et al. 2002, Martén-Rodríguez et al. unpublished data), and are all strictly hummingbird-pollinated. Within the cluster of species with bell-shaped flowers, two subgroups can be distinguished, one associated with bat pollination (above the zero value of dimension 2), and the other associated with generalized pollination (mostly below the zero value).
Figure 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 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).
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Most floral characters were highly correlated with the first dimension of the ordination plot. The correlations indicate that, moving towards the left side of the plot along dimension 1, flowers have wider corollas, some constriction above the nectar chamber, lower nectar concentration, nocturnal schedules of nectar production and anther dehiscence, colours towards the yellow/green part of the spectrum, and the presence of dark red spots (Fig. 2). In contrast, moving to the right side along dimension 1, the trend is for tubular corollas with solid bright colours, greater nectar concentration, and diurnal nectar production and anther dehiscence (i.e. hummingbird pollination syndrome). For the colour trait, which was coded as a multi-state character, the coding was set to reflect the colour spectrum; therefore, moving to the right along the dimension 1 indicates more orange and red corollas.
The ordination conducted excluding tubular-flowered species shows a stronger separation of the two subgroups of bell-shaped flowers; however, two oddities are evident: R. minus (RM) appears clustered within the generalists but only hummingbirds were observed as native pollinators. Given its nocturnal schedule of nectar production and anther dehiscence, we cannot rule out the possibility of bat pollination until observations in multiple seasons are conducted. The second inconsistent case is G. quisqueyana (GQ), a strict bat specialist that was placed within the generalists cluster. This species restricts diurnal visitors by closing flowers during the day (see above description). Thus, although the floral morphology would allow a wider range of visitors, the floral phenology filters out diurnal visitors.
With tubular-flowered species excluded from the ordination, the corolla constriction became the single most important trait separating the two subgroups of bell-shaped flowers (associated with generalized and bat pollination) (Fig. 3). Other high correlations (significant before Bonferroni correction) included: pistil exertion, corolla curvature, and colour. Thus, moving to the right along dimension 1 (associated with specialized bat pollination), pistils tend to be more exerted, corollas less curved, light green or white, and not constricted above the nectar chamber.
Figure 3. Multidimensional scaling analysis of 11 Gesneriaceae species based on 11 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).
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Pollinators also separated Gesneriaceae species into clusters corresponding to ornithophilous and chiropterophilous flowers in the ordination using pollinator importance values (Fig. 4). However, in contrast with the clustering defined by floral traits (Fig. 1), species with subcampanulate flowers appeared scattered throughout the plot, reflecting the variability in pollinator importance values and pollinator assemblages (Fig. 4). The only trait that correlated with dimension 1 was colour, indicating red colours present in most species visited by hummingbirds, both specialists and generalists.
Figure 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).
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Correlations among floral traits revealed 11 significant associations (Table 2). These indicate flowers with wide corollas tend to have nocturnal schedules, green to white colours and dark red or brown spots, while flowers with narrow corollas tend to have diurnal schedules and solid bright red or orange colours. These associations reflect the suites of floral characters associated with classic bat and hummingbird pollination syndromes, respectively. The presence of a corolla constriction that makes subcampanulate corollas, was associated with nocturnal schedules of nectar production and anther dehiscence. As a general rule, this subcampanulate floral phenotype indicates generalized pollination systems in the tribe Gesnerieae.
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
|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|
evaluation of pollination syndromes
Discriminant analysis was used to evaluate the ability of suites of floral traits to predict the pollination system; the three a priori designated pollination system categories were based on our field observations: hummingbird, bat and generalist. When cross-validation was used to evaluate the ability of the model to classify species into expected pollination systems, floral traits were able to predict hummingbird pollination 12 out of 13 times; R. minus was classified as a generalist (Table 3). For the bat pollination category, one species out of five was misclassified (G. quisqueyana was classified as a generalist), and for the generalist, two out of five species were misclassified, one into the hummingbird (R. leucomallon) and one into the bat (G. viridiflora subsp. Sintenisii) pollination categories (Table 3).
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
|A priori||Classified as||Total||Posterior probability 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)|| || |