P L A N T - A N I M A L I N T E R A C T I O N S - O R I G I N A L P A P E R
Plant–pollinator interactions and floral convergence in two species of Heliconia from the Caribbean Islands
Silvana Marte´n-Rodrı´guez•W. John Kress• Ethan J. Temeles•Elvia Mele´ndez-Ackerman
Received: 4 April 2010 / Accepted: 26 May 2011 ÓSpringer-Verlag 2011
Abstract Variation in interspecific interactions across geographic space is a potential driver of diversification and local adaptation. This study quantitatively examined vari- ation in floral phenotypes and pollinator service of Heli- conia bihaiandH. caribaeaacross three Antillean islands.
The prediction was that floral characters would correspond to the major pollinators of these species on each island.
Analysis of floral phenotypes revealed convergence among species and populations of Heliconia from the Greater Antilles. All populations of H. caribaea were similar, characterized by long nectar chambers and short corolla tubes. In contrast, H. bihai populations were strongly divergent: on Dominica,H. bihai had flowers with short
nectar chambers and long corollas, whereas on Hispaniola, H. bihai flowers resembled those of H. caribaea with longer nectar chambers and shorter corolla tubes. Mor- phological variation in floral traits corresponded with geographic differences or similarities in the major pollin- ators on each island. The Hispaniolan mango, Anthraco- thorax dominicus, is the principal pollinator of both H. bihaiandH. caribaeaon Hispaniola; thus, the similarity of floral phenotypes between Heliconia species suggests parallel selective regimes imposed by the principal polli- nator. Likewise, divergence betweenH. bihaipopulations from Dominica and Hispaniola corresponded with differ- ences in the pollinators visiting this species on the two islands. The study highlights the putative importance of pollinator-mediated selection as driving floral convergence and the evolution of locally-adapted plant variants across a geographic mosaic of pollinator species.
Keywords Convergent evolutionHeliconia HummingbirdIslands Pollination
Introduction
Variation in selective regimes imposed by pollinators across plant populations is thought to be a key element driving floral diversification (Johnson 1997, 2006; Boyd 2002; Herrera et al.2006; Nattero and Cocucci2007). As with local adaptation to the abiotic environment (e.g., different soil ecotypes; Wright et al. 2006), selection on floral traits that enhance reproductive performance under particular pollination environments can drive the evolution of locally-adapted floral variants or pollination ecotypes (Johnson 2006; Harder and Johnson2009). If populations are geographically isolated, limited gene flow between Communicated by Steven Johnson.
Electronic supplementary material The online version of this article (doi:10.1007/s00442-011-2043-8) contains supplementary material, which is available to authorized users.
S. Marte´n-Rodrı´guezW. John Kress
Department of Botany, National Museum of Natural History, MRC-166, Smithsonian Institution,
Washington DC 20013-7012, USA Present Address:
S. Marte´n-Rodrı´guez (&)
Departamento de Biologı´a Evolutiva, Instituto de Ecologı´a, AC, Ap. postal 63, 91070 Xalapa, VER, Me´xico
e-mail: smartenr@gmail.com; silvana.marten@inecol.edu.mx E. J. Temeles
Department of Biology, Amherst College, Amherst, Massachusetts 01002-5000, USA
E. Mele´ndez-Ackerman
Institute for Tropical Ecosystem Studies, University of Puerto Rico at Rio Piedras, P.O. Box 70377, San Juan,
PR 00936-8377, USA
DOI 10.1007/s00442-011-2043-8
ecotypes could ultimately lead to species divergence associated with shifts in pollination systems (Grant and Grant1965; Grant1992; Johnson 2006). Local adaptation of species using the same pollinators could also drive convergence of floral traits in sympatric species, although this phenomenon has seldom been documented (but see Anderson and Johnson2009). Therefore, placing the study of plant–pollinator interactions within a geographic context is important to gain insights into the conditions that have promoted floral diversification and convergence.
Oceanic archipelagos offer ideal settings to assess the role of geographic variation and local adaptation on plant and animal diversification. For instance, adaptive radia- tions in archipelagoes reflect repeated opportunities for speciation in response to environmental selective mosaics, resulting in wide phenotypic diversification and conver- gence (e.g., Grant1986; Losos1992; Givnish et al.2009).
However, knowledge of spatial variation in plant–pollina- tor interactions across islands of oceanic archipelagoes is limited. This paucity of information is particularly true for the Caribbean Islands where strict characterization of plant–pollinator interactions over a range of island popu- lations has only been attempted for the genus Heliconia (e.g., Temeles and Kress2003; Gowda2009).Accordingly, we examined floral and pollination system variation in Heliconia populations from three Antillean islands.
CaribbeanHeliconiaoffer an ideal study system for vari- ous reasons. First, only two species ofHeliconiaare native to the Antilles, but these species display great variation in floral traits across islands (Berry and Kress1991). Second, the Caribbean Islands are moderately isolated from each other; therefore, limited gene flow among islands might favor the evolution of stable, locally-adapted variants.
Third, comprehensive studies of plant–pollinator interac- tions, floral ecology, and hummingbird behavior are available for various islands of the Lesser Antilles, pro- viding baseline information for comparative studies (Temeles et al.2000,2005,2009; Temeles and Kress2003;
Gowda2009.
Earlier studies on the islands of St Lucia and Dominica showed a strong association between Heliconia floral phenotypes and the bills and energy requirements of their sexually-dimorphic hummingbird pollinator, the purple- throated carib (Eulampis jugularis) (Temeles et al. 2000;
Temeles and Kress2003).Heliconia bihaihas long, curved flowers that are pollinated by female purple-throats, whereasH. caribaeahas shorter and straighter flowers that are pollinated primarily by male purple-throats (Temeles and Kress 2003; Fig. 1). The geographic range of the purple-throated carib is restricted to the Lesser Antilles (Raffaele et al.1998), but the native ranges ofH. bihaiand H. caribaeaextend to the Greater Antilles (Berry and Kress 1991). Here, we assess floral variation in relation to
pollinator assemblages on three islands that have different pollinator communities: Dominica (Lesser Antilles), His- paniola and Puerto Rico (Greater Antilles).
Extending the study of Heliconiafloral variation to the Greater Antilles, where the purple-throated carib is absent, allows us to start assessing the hypothesis that floral traits in Caribbean Heliconia have diversified under selective regimes imposed by local pollinator faunas. Accordingly, we expect to find an association between Heliconia floral trait variation and variation in bill characteristics of the major pollinators of Heliconia on each island. This cor- relative approach is the first step to investigate whether local adaptation to pollinator assemblages is potentially driving floral diversification of heliconias on the Caribbean Islands. To evaluate our predictions we: (1) quantified patterns of pollinator visitation for H. bihai and H. cari- baea on Hispaniola and Puerto Rico, (2) characterized variation of floral traits important for pollination in Heli- conia populations from Hispaniola, Puerto Rico (Greater Antilles) and Dominica (Lesser Antilles), and (3) examined the association between pollinator assemblages and floral variation across the three islands.
Materials and methods
Study system The plants
Heliconia bihai (L.) Griggs andH. caribaeaLamarck are two closely related species that comprise the only native representatives of the genus Heliconia in the Antilles.
Heliconia caribaeais distributed across the Antilles, from Eastern Cuba to Saint Vincent, with populations present on all mountainous islands (Anderson1981).Heliconia bihai is distributed from northern South America through the Lesser Antilles, and is also present on Hispaniola (Greater Antilles). Heliconia bihai has also been reported from Puerto Rico (Acevedo and Strong 2010); however, it is known only from one collection (Acevedo, personal com- munication), and we were not able to find it in our survey across the island. For this reason, we report data for both Heliconiaspecies from Hispaniola and Dominica, but only for H. caribaeafrom Puerto Rico.
Heliconia plants are large perennial herbs mostly occurring in disturbed habitats, along roads, trails, rivers, and in forest gaps. They have rhizomatous growth, a mu- soid growth habit, and produce multiple inflorescences each of which can last from 1 to 3 months. Flowering seasons for both species ofHeliconiaon Hispaniola and for H. caribaeaon Puerto Rico ranged from February through July, with peak flowering in April–May. Inflorescences are
composed of large showy bracts that, on Puerto Rico and Hispaniola, are bright yellow in H. caribaea, and red- orange with yellow edges inH. bihai. Each bract holds an average of 10–24 flowers over the season, but no more than one flower is produced daily within a bract; anthesis lasts 1 day and there is no temporal separation of sexual phases (Temeles et al. 2005; Gowda 2009). The flowers are bisexual, zygomorphic, tubular, and greenish-white in color. BothHeliconia species have one ovule per carpel, and they usually produce from one to three seeds per fruit.
Breeding systems of Caribbean Heliconia vary across islands; populations of both species on Dominica are par- tially self-incompatible (Gowda2009), whereas hand-pol- lination crosses conducted in Puerto Rico revealed H.
caribaeaon Puerto Rico is fully self-compatible (Marte´n- Rodrı´guez, unpublished data). We lack data for breeding systems ofHeliconia from Hispaniola.
The birds
Previous work has demonstrated that the purple-throated carib is the primary pollinator of both H. bihai and H.
caribaeaon Dominica, accounting for 90% of the visits to H. caribaeaand 99.9% of visits toH. bihaiin our 9 years of studies on that island (Temeles and Kress2003, 2010;
Gowda2009). This hummingbird species exhibits extreme sexual dimorphism in bill length and curvature associated with sexual partitioning of these heliconias: males with short, straight bills visit H. caribaea, which has short, straight flowers, whereas females with long, curved bills occasionally visitH. caribaeabut are the primary visitor of
H. bihai, which has long, curved flowers (Temeles and Kress2003,2010; Gowda2009). Although three additional species of hummingbirds are present on Dominica, they visit the native heliconias at much lower frequencies than the purple-throated carib. Three hummingbird species are native to Hispaniola (Raffaele et al.1998), two of which, the long-billed Hispaniolan mango (Anthracothorax dom- inicus) and the short-billed Hispaniolan emerald (Chloro- stilbon swainsonii), we observed at heliconias. Six hummingbird species are native to Puerto Rico (Raffaele et al. 1998), three of which, the long-billed green mango (A. viridis) and green-throated carib (E. holosericeus) and the short-billed Puerto Rican emerald (C. maugeus), we recorded at heliconias. On both islands, we also observed bananaquits (Coereba flaveola) at heliconias. None of the hummingbirds on Hispaniola or Puerto Rico exhibit the extreme sexual dimorphism in bill length or shape of the purple-throated carib (Schuchmann 1999; Temeles, unpublished data). For analyses, we classified floral visitors into pollinator functional groups, sensu Fenster et al.
(2004), according to their size, bill length and feeding behavior (whether they were legitimate visitors or nectar robbers; see Results: ‘‘Pollinator visitation’’). Thus, we grouped bird visitors into three categories: long-billed hummingbirds, short-billed hummingbirds, and banana- quits (see Table1for bill dimensions).
Study sites
On Puerto Rico, H. caribaea was studied in El Yunque National Forest (various sites along roads 191 and 966, and Table 1 Floral visitors ofHeliconia caribaeaandH. bihaiin Hispaniola and Puerto Rico
Species Sex Bill length
(mm)
Body mass (g)
Island Common name Behavior Category
Anthracothorax dominicus
F 24.5±0.3 5.4±0.5 Hispaniola Hispaniolan mango
Pollinator LB
M 22.6±0.2 6.2±0.5 Anthracothorax
viridis
F 25.1±0.2 6.2±0.3 Puerto Rico Green mango Pollinator LB
M 23.1±0.2 6.6±0.3 Eulampis
holocericeus
F 23.3±0.3 – Puerto Rico Green-throated
carib
Pollinator LB
M 20.1±0.3 5.6±0.4 Chlorostilbon
swainsonii
F 17.6±0.4 3.7 Hispaniola Hispaniolan
emerald
Nectar robber/occasional pollinator
SB
M 16.6±0.3 3.2
Chlorostilbon maugeus
F 13.8±0.2 2.9±0.2 Puerto Rico Puerto Rican emerald
Nectar robber/occasional pollinator
SB M 12.5±0.1 2.9±0.2
Coereba flaveola M and F
10.5 9.7±0.1 Hispaniola, Puerto Rico
Bananaquit Nectar robber/pollinator SB Eulampis jugularis F 26.6±0.12 7.9±0.09 Dominica Purple-throated
carib
Pollinator LB
M 19.8±0.36 9.9±0.1
All bird species listed for Hispaniola visited bothHeliconiaspecies. Categories refer to pollinator functional groups based on bill characteristics:
long-billed (LB), short-billed (SB). Measurements of bill length and body mass are drawn from Kodric-Brown et al. (1984), Wunderle (1995), Fumero-Caba´n and Melendez-Ackerman (2007), and Temeles, unpublished data
at El Verde Field Station), in Bosque Estatal Carite, and along road 105 to Maricao; elevation ranged between 350 and 700 m a.s.l. With the exception of the Maricao popu- lation, all sites were within the boundaries of protected forest. On Hispaniola, H. caribaea and H. bihai were studied in various sites across Cordillera Septentrional, Cordillera Central and Sierra de Bahoruco, all located in the Dominican Republic side of the island, between 200 and 600 m a.s.l. These study sites consisted of patches of secondary growth vegetation, nested within a matrix of agricultural land. Specific locations and coordinates are listed in Online Resource 1.
Pollinator visitation
We conducted pollinator observations during March, April, and June 2009 in Puerto Rico, and March and May 2009 in Hispaniola. Pollinator visitation data for H. bihai and H. caribaeafrom Dominica were available from past studies (Temeles and Kress2003; Gowda2009). We observed the plants during clear, cloudy or light rainy weather; no observations were conducted during heavy rain. In Puerto Rico, we observed 13 patches ofH. caribaeafor 12 h each, in sets of 2-h periods; we covered all periods between 0630 and 1830 hours over the course of several days. Patches consisted of one to five distinct clumps of stems. In His- paniola, we observed six patches ofH. caribaeaand six of H. bihaiusing the same methodology as in Puerto Rico. On both islands, observations were conducted during the peak
flowering season. We recorded floral visitors through direct observation and with the help of video cameras (Sony Handycam DCR-SR85), and from both types of observa- tion noted the species and sex (when dimorphic only) of the visitor, the number of inflorescences visited, and the number of flowers probed. Honeybees (Apis mellifera) were observed foraging in two patches of H. caribaeaon Hispaniola; honeybees collected pollen from anthers and spent long periods of time in the flower moving mostly between flowers of the same inflorescence or plant. Over- all, they were rare visitors to Heliconia flowers, although they were common at one site. Honeybees are not native to the Antilles and it is unlikely they have had time to influ- ence the floral evolution of long-livedHeliconiasince their introduction to these islands less than 400 years ago (Cox 1994). Because the goal of this study was to evaluate the role of geographic variation in pollinator communities on the evolution of floral variation in Heliconia, we did not quantify visits by non-native species.
We also recorded the total number of plants, inflores- cences, and open flowers on each patch. Flowers on tall stems were counted using a mirror attached to a pole.
Pollinator visitation frequencies were calculated as the number of visits per flower per patch per hour. The number of visits was then multiplied by 12 (approximate number of daylight hours at these latitudes) to obtain a metric that reflected the number of visits per flower per patch per day.
Since flowers last only 1 day, a minimum of one visit per day is necessary for pollen deposition and removal.
Fig. 1 Floral phenotypes and major hummingbird visitors of Heliconia caribaeaandH. bihai studied on Hispaniola, Dominica, and Puerto Rico.
Note the shorter nectar chambers and longer corollas that characterize flowers ofH.
bihaifrom Dominica. Scale bars20 mm. Hummingbird drawings originally published in Raffaele et al. (1998), and authorized to be used in this publication by Herbert Raffaele
Floral trait variation
We measured six floral characters (nectar chamber length, nectar chamber width, corolla length, corolla width, corolla arc length, and corolla curvature height, in mm; Online Resource 2) on fresh flowers collected from two to nine individuals in two to four populations of eachHeliconia species on each island (Hispaniola, Puerto Rico and Dominica). For each individual plant, we measured one to four flowers and averaged these values to obtain a single value per trait per individual. The traits we measured were expected to be under selection by pollinators based on our previous studies of floral trait variation (Temeles et al.
2000; Temeles and Kress 2003; Gowda 2009). Curvature height provides an indirect measure of curvature; the greater values of height indicate greater curvature.
Statistical analyses
Differences in pollinator visitation were tested with ANOVA using PROC GLIMMIX in SAS v.9.2 (SAS Institute 2008). The model included pollinator functional group (long-billed hummingbird, short-billed humming- bird, and bananaquit), island (Puerto Rico or Hispaniola), Heliconia species (H. bihai and H. caribaea), and all possible interactions as predictor variables. Neither the island9species interaction, nor the three-way interaction were possible because native populations of H. bihai are absent from Puerto Rico. Covariation in visitation of the same patches by each functional group of pollinators was accounted for in a random residual statement (patch was specified as subject and option unordered was used for the covariance matrix). A Poisson distribution was specified in the model statement with a link=log option. Back- transformation of means was obtained by theilinkoption under thelsmeans statement. A priori contrasts were used to compare visitation rates among Heliconia populations and among pollinators.
To assess variation of flowers as integrated phenotypes across islands, we performed a canonical discriminant analysis using the CANDISC procedure in SAS v.9.2 (SAS Institute2008). This analysis generates linear combinations of variables (e.g., floral traits) that have the highest mul- tiple correlations with the classes (e.g., populations of Heliconia from different islands). It also estimates the contribution of individual traits to the generated canonical variables as standardized canonical coefficients. Two canonical axes were selected for plotting floral phenotypes because the third axis of variation did not contribute to any distinct separation among clusters. The traits that contrib- uted most to variation in CAN1 were nectar chamber length and corolla length, whereas the traits that contrib- uted most to variation in CAN2 were corolla width and
corolla height (an indirect measure of curvature; i.e., greater heights indicate greater curvatures).
Results
Pollinator visitation
Visitation rates differed significantly among pollinator functional groups and between islands (Table2). On His- paniola,H. bihaiandH. caribaeawere pollinated primarily by the long-billed Hispaniolan mango (males and females), accounting for 90% of the visits; other visitors included bananaquits and the short-billed Hispaniolan emerald (Fig.2).On Puerto Rico,H. caribaeaplants received visits by two species of long-billed hummingbirds (the green mango and the green-throated carib, 41% of all visits), bananaquits (40% of all visits), and the short-billed Puerto Rican emerald (19% of all visits; Fig. 2). Short-billed hummingbirds were primarily nectar thieves, failing to contact the reproductive organs of the flower (Marte´n- Rodrı´guez, unpublished data). Bananquits acted both as nectar robbers, by piercing a hole at the level of the nectar chamber, and as pollinators, by directly contacting repro- ductive organs and picking-up pollen on different parts of head and chest while taking nectar accumulated in the corolla pouch. While bananaquits are known to effectively transfer pollen among Heliconia flowers (Mele´ndez-Ack- erman, unpublished data), the large variation in feeding behaviors makes bananaquits unlikely agents of directional or stabilizing selection on floral traits. Visitation occurred throughout the day in both Heliconia species. The only temporal pattern observed was that long-billed humming- birds were primary visitors during early morning hours (0600–0800 hours), whereas bananaquits and short-billed hummingbirds became frequent visitors after 0900 hours, coinciding with the time when nectar accumulation reached the top of the nectar chamber in unvisited flowers.
Floral trait variation
On both Hispaniola and Puerto Rico, corollas of H. cari- baea were relative short with long nectar chambers, com- parable to the flowers of that species on Dominica (Table3). In contrast, floral phenotypes of H. bihai dif- fered among islands. Corollas of H. bihai on Dominica were approximately 10 mm longer than on Hispaniola, whereas nectar chambers of H. bihai on Dominica were approximately 10 mm shorter than on Hispaniola (Table3). Significant canonical correlations were found among floral traits underlying the clustering of floral phe- notypes (Wilks k, F(24, 405)=48.8, P\0.0001). Floral phenotypes of Heliconia segregated in two clusters: one
that containedH. bihaifrom Dominica, and the other that included all other populations ofHeliconia(Fig.3). Clus- tering of floral phenotypes along canonical axis 1 (CAN1) was associated with variation in nectar chamber length, corolla length, and corolla width (Table3). Along canon- ical axis 2 (CAN2), populations of Heliconia were more dispersed; thus, floral trait variation associated with this axis did not contribute to cluster separation (Fig.3).
Discussion
In the Neotropics, the genusHeliconiahas flowers adapted to bird pollination; therefore, variation in floral traits among species is not associated with major transitions in pollination syndromes (e.g., birds vs. bat). Instead, floral traits reflect variation in the bill characteristics of the particular hummingbird pollinators of each Heliconia species (Stiles 1975; Temeles and Kress 2003; Temeles et al. 2010). Geographic differences in hummingbird assemblages thus have the potential to influence the evo- lution of locally-adapted floral phenotypes in Heliconia.
The results of this study support the idea that geographic variation in pollinator composition and service underlies
the phenotypic similarities and differences observed among flowers of CaribbeanHeliconia.
Variation in pollinator assemblages across islands was associated with patterns of floral variation, which was particularly evident in the comparison between Dominica and Hispaniola, islands where both Heliconia species are present. On Dominica, the presence of the purple-throated carib hummingbird, with its marked bill dimorphism, has provided opportunities forHeliconiato evolve in response to selection by either male or female hummingbird poll- inators, explaining the large floral differences among Heliconiaspecies on this island (Temeles and Kress2003, and unpublished data). In contrast, both H. bihai and H. caribaea on Hispaniola are subject to selection by a species of hummingbird that lacks the marked sexual dimorphism in bill size and shape of the purple-throated carib (Table2). The striking similarities among flowers of H. bihai and H. caribaea on Hispaniola may thus be the result of floral convergence driven by selection mediated by a common pollinator species.
Floral convergence of closely related sympatric species due to sharing of the same pollinator is a rarely docu- mented phenomenon; however, there are a few well-stud- ied cases (Schemske 1981; Anderson and Johnson 2009).
In one example, the floral tube length of fly-pollinated plants in South Africa reflected convergence between sympatric species and divergence between allopatric populations of the same species, a pattern of floral variation that was associated with variation in the proboscis length of a single fly pollinator species (Anderson and Johnson 2009). The case of CaribbeanHeliconiasprovides a similar example, with the difference that not a single pollinator visited allHeliconia populations in all islands.
In a second well-documented example of floral con- vergence, similarities in nectar production, phenology, and floral morphology of two co-occurringCostusspecies from Barro Colorado Island were attributed to selection to enhance visitation by a single bee pollinator species. This occurred in an environment where low flower density caused by weevil predation resulted in insufficient polli- nator visitation (Schemske 1981). In contrast with the Costus system, facilitation is unlikely to play a role in driving floral convergence of Heliconias on Hispaniola because Heliconia patches are usually monospecific and the two species rarely share the same habitats. Heliconia bihai is found almost exclusively on steep rocky walls of ravines, whereasH. caribaeaoccurs on varied terrain along stream edges, wet forest edges, and gaps. Thus, although the two Heliconia species share the same pollinator, dif- ferent habitat preferences make co-occurrences rare within the island.
The use of different local habitats by H. caribaea and H. bihaion Hispaniola is perhaps a reason why some forms Table 2 ANOVA statistics of pollinator visitation and island for
H. bihaiandH. caribaeafrom Hispaniola and Puerto Rico in 2009
Effect F(numdf, dendf) Pvalue
Pollinator 16.40(2, 75) \0.0001
Island 1.39(1, 75) 0.2511
Species 0.69(1, 75) 0.4016
Pollinator9island 9.59(2, 75) 0.0009
Pollinator9species 0.14(2, 75) 0.8719
Fig. 2 Visitation rates toH. bihaiandH. caribaeafrom Hispaniola and Puerto Rico, March–June 2009, by three pollinator groups. Means with identicallettersare not significantly different from each other (experiment-widea=0.05, Tukey adjusted)
of reproductive isolation involving floral divergence between species are apparently lacking. In theory, when close relatives occur in sympatry and share the same pollinators, floral traits should diverge to promote repro- ductive isolation in order to reduce reproductive losses incurred by hybrid crosses (reinforcement) or to reduce competition for pollinators (character displacement; Grant 1972; Johnson 2006). Floral isolation may occur via changes in flower structure that direct pollen placement onto particular parts of the pollinator’s body (mechanical isolation; Grant1949), or via pollinator’s preferences for particular plant species (ethological isolation; Grant1949).
These two forms of floral isolation may also act in concert (Grant 1992), and in conjunction with other forms of reproductive isolation (Kay and Sargent 2009). In Carib- beanHeliconia, floral isolation is observed on the island of Dominica, where both structural differences in flower morphology and pollinator preferences determine effective pollination by either male or female purple-throated caribs (Temeles et al. 2009). However, this situation does not occur on Hispaniola, where there are no morphological differences betweenHeliconiaspecies that would promote pollen placement on different parts of the pollinator’s body.
These observations suggest that strong selection to enhance pollen transfer by the single pollinator species, coupled with reproductive isolation promoted by different habitat preferences, may be driving floral convergence and pre- venting character displacement.
Other explanations are also possible to explain the observed patterns of floral similarity among species of Heliconia on Hispaniola. For instance, correspondence of morphological traits could reflect common expression of plastic phenotypes in a shared environment (Pigliucci 2001). Phenotypic plasticity is not a very plausible hypothesis, however, because the individuals measured in this study were sampled from populations at different elevations and different regions of Hispaniola, encom- passing wide environmental variations in temperature, precipitation, light and soils. Therefore, the common expression of floral traits cannot be explained by a common response to a set of particular abiotic conditions.
Table 3 Trait measurements (mean±SEM), one-way ANOVA statistics, and standardized coefficients from Canonical Discriminant Analysis of floral variation inH. caribaeaandH. bihaifrom Hispaniola, Puerto Rico and Dominica
Floral trait Greater Antilles Lesser Antilles ANOVA Standardized
canonical coefficientsa H. caribaea
(n=32) Puerto Rico
H. caribaea (n=14) Hispaniola
H. bihai (n=18) Hispaniola
H. caribaea (n= 31) Dominica
H. bihai (n= 31) Dominica
F(4, 120) P CAN1 CAN2
Nectar chamber length (mm)
20.8±0.24 a 21.9±0.41 a 21.4±0.52 a 17.8±0.33 c 10.6±0.21 b 227.2 \0.0001 2.44 1.02 Nectar chamber
width (mm)
5.6±0.07 a 5.1±0.11 b 5.7±0.13 a 5.0±0.07 b 6.8±0.12 c 53.1 \0.0001 -0.11 0.37 Corolla length
(mm)
37.3±0.35 a 35.7±0.23 a,b 37.5±0.51 a 35.8±0.22 b 47.8±0.43 c 206.1 \0.0001 -1.44 -0.47 Corolla width
(mm)
5.9±0.07 a 5.4±0.10 a 6.7±0.14 b 5.6±0.09 a 9.0±0.13 c 202.1 \0.0001 -1.07 1.62 Corolla arc
length (mm)
42.8±0.39 a 42.3±0.25 a,b 43.1±0.63 a 40.5±0.22 b 54.2±0.51 c 186.9 \0.0001 -0.40 0.92 Corolla height
(mm)
8.7±0.12 a 9.3±0.18 a 7.8±0.15 b 9.1±0.11 a 11.±0.17C 69.7 \0.0001 -0.17 -1.59 Sample sizes (n) refer to the number of individualHeliconiaplants from which flowers were measured. Means followed by identical letters are not significantly different from each other (experiment-widea=0.05, Tukey adjusted)
a Standardized canonical coefficients represent the contribution of each variable to the canonical axes while holding other variables in the model constant
Fig. 3 Canonical discrimant analysis of floral traits for two species of Heliconiawith populations on three Caribbean islands. On axisCan1, populations on the left have flowers with long corollas and short nectar chambers, and populations on therighthave flowers with short corollas and long nectar chambers
A second explanation for the shared floral similarities of H. bihaiandH. caribaeaon Hispaniola is that convergent floral phenotypes evolved in allopatric ancestral popula- tions in other islands and were later assembled in sympatry by chance dispersal. Because flowers most closely resem- blingH. bihaifrom Hispaniola correspond to populations of this species from islands near the coast of South America (Trinidad and Tobago; Kress and Temeles, unpublished data), long-distance dispersal would have to be invoked to support this hypothesis. This explanation, albeit unlikely, cannot be rejected until the phylogeography of CaribbeanHeliconiais better understood. Nevertheless, even if heliconias from Hispaniola did not evolve their actual floral phenotypes in situ,pollinator-mediated selec- tion has probably played an important role in preventing the divergence of floral traits that would be expected under drift or reinforcement.
In summary, both phenotypic divergence and conver- gence appear to have played an important role in the diversification of floral traits in Antillean Heliconia. Pre- vious studies have documented large floral differences betweenH. bihaiandH. caribaeaon Dominica (Temeles and Kress2003). Our study reports a case of divergence between allopatric populations of the same species,H. bi- haion Hispaniola and Dominica, and convergence between two species of Heliconia, H. bihai and H. caribaea, on Hispaniola. The associations between floral characteristics and bills of the principal hummingbird pollinators on each island suggest that adaptation to local pollinator faunas is a major evolutionary force driving floral diversification of CaribbeanHeliconia.
Acknowledgments The authors thank T. Clase, A. Cherenfant, J. Fumero, N. Marte´n, B. Peguero, R. Perez, R. Rodrı´guez, N. Ruiz and M. Vindas for assistance conducting field work. The authors thank P. Acevedo for discussion of ideas and providing useful botanical information, and I. Lopez for generating the distribution map. V. Gowda, S. Johnson, and three anonymous reviewers provided insightful comments on earlier versions of this manuscript. Logistic support for fieldwork was provided by Jardı´n Bota´nico Nacional de Santo Domingo in Dominican Republic, and El Verde Field Station in Puerto Rico. Research permits were awarded by Depto de Recursos Naturales y Ambientales in Puerto Rico, and by the Secretarı´a de Estado de Medio Ambiente y Recursos Naturales in the Dominican Republic, and experiments complied with the current laws of those countries. Funding was provided by Smithsonian Institution grant to SMR, NSF Grant DEB 0614218 to E. Temeles and W.J. Kress.
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