Plant–Pollinator Interactions and Floral Convergence in Two Species Of

Oecologia DOI 10.1007/s00442-011-2043-8 PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Plant–pollinator interactions and floral convergence in two species of Heliconia from the Caribbean Islands Silvana Marteń-Rodrı´guez • W. John Kress • Ethan J. Temeles • Elvia Meleńdez-Ackerman Received: 4 April 2010 / Accepted: 26 May 2011 Ó Springer-Verlag 2011 Abstract Variation in interspecific interactions across nectar chambers and long corollas, whereas on Hispaniola, geographic space is a potential driver of diversification and H. bihai flowers resembled those of H. caribaea with local adaptation. This study quantitatively examined vari- longer nectar chambers and shorter corolla tubes. Mor- ation in floral phenotypes and pollinator service of Heli- phological variation in floral traits corresponded with conia bihai and H. caribaea across three Antillean islands. geographic differences or similarities in the major pollin- The prediction was that floral characters would correspond ators on each island. The Hispaniolan mango, Anthraco- to the major pollinators of these species on each island. thorax dominicus, is the principal pollinator of both Analysis of floral phenotypes revealed convergence among H. bihai and H. caribaea on Hispaniola; thus, the similarity species and populations of Heliconia from the Greater of floral phenotypes between Heliconia species suggests Antilles. All populations of H. caribaea were similar, parallel selective regimes imposed by the principal polli- characterized by long nectar chambers and short corolla nator. Likewise, divergence between H. bihai populations tubes. In contrast, H. bihai populations were strongly from Dominica and Hispaniola corresponded with differ- divergent: on Dominica, H. bihai had flowers with short 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 Communicated by Steven Johnson. and the evolution of locally-adapted plant variants across a geographic mosaic of pollinator species. 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. Keywords Convergent evolution Á Heliconia Á Hummingbird Á Islands Á Pollination S. Marteń-Rodrı´guez Á W. John Kress Department of Botany, National Museum of Natural History, MRC-166, Smithsonian Institution, Washington DC 20013-7012, USA Introduction Present Address: Variation in selective regimes imposed by pollinators S. Marteń-Rodrı´guez (&) Departamento de Biologıá Evolutiva, Instituto de Ecologıá, across plant populations is thought to be a key element AC, Ap. postal 63, 91070 Xalapa, VER, Me´xico driving floral diversification (Johnson 1997, 2006; Boyd e-mail: [email protected]; [email protected] 2002; Herrera et al. 2006; Nattero and Cocucci 2007). As with local adaptation to the abiotic environment (e.g., E. J. Temeles Department of Biology, Amherst College, Amherst, different soil ecotypes; Wright et al. 2006), selection on Massachusetts 01002-5000, USA floral traits that enhance reproductive performance under particular pollination environments can drive the evolution E. Meleńdez-Ackerman of locally-adapted floral variants or pollination ecotypes Institute for Tropical Ecosystem Studies, University of Puerto Rico at Rio Piedras, P.O. Box 70377, San Juan, (Johnson 2006; Harder and Johnson 2009). If populations PR 00936-8377, USA are geographically isolated, limited gene flow between 123 Oecologia ecotypes could ultimately lead to species divergence pollinator assemblages on three islands that have different associated with shifts in pollination systems (Grant and pollinator communities: Dominica (Lesser Antilles), His- Grant 1965; Grant 1992; Johnson 2006). Local adaptation paniola and Puerto Rico (Greater Antilles). of species using the same pollinators could also drive Extending the study of Heliconia floral variation to the convergence of floral traits in sympatric species, although Greater Antilles, where the purple-throated carib is absent, this phenomenon has seldom been documented (but see allows us to start assessing the hypothesis that floral traits Anderson and Johnson 2009). Therefore, placing the study in Caribbean Heliconia have diversified under selective of plant–pollinator interactions within a geographic context regimes imposed by local pollinator faunas. Accordingly, is important to gain insights into the conditions that have we expect to find an association between Heliconia floral promoted floral diversification and convergence. trait variation and variation in bill characteristics of the Oceanic archipelagos offer ideal settings to assess the major pollinators of Heliconia on each island. This cor- role of geographic variation and local adaptation on plant relative approach is the first step to investigate whether and animal diversification. For instance, adaptive radia- local adaptation to pollinator assemblages is potentially tions in archipelagoes reflect repeated opportunities for driving floral diversification of heliconias on the Caribbean speciation in response to environmental selective mosaics, Islands. To evaluate our predictions we: (1) quantified resulting in wide phenotypic diversification and conver- patterns of pollinator visitation for H. bihai and H. cari- gence (e.g., Grant 1986; Losos 1992; Givnish et al. 2009). baea on Hispaniola and Puerto Rico, (2) characterized However, knowledge of spatial variation in plant–pollina- variation of floral traits important for pollination in Heli- tor interactions across islands of oceanic archipelagoes is conia populations from Hispaniola, Puerto Rico (Greater limited. This paucity of information is particularly true for Antilles) and Dominica (Lesser Antilles), and (3) examined the Caribbean Islands where strict characterization of the association between pollinator assemblages and floral plant–pollinator interactions over a range of island popu- variation across the three islands. lations has only been attempted for the genus Heliconia (e.g., Temeles and Kress 2003; Gowda 2009). Accordingly, we examined floral and pollination system variation in Materials and methods Heliconia populations from three Antillean islands. Caribbean Heliconia offer an ideal study system for vari- Study system ous reasons. First, only two species of Heliconia are native to the Antilles, but these species display great variation in The plants floral traits across islands (Berry and Kress 1991). Second, the Caribbean Islands are moderately isolated from each Heliconia bihai (L.) Griggs and H. caribaea Lamarck are other; therefore, limited gene flow among islands might two closely related species that comprise the only native favor the evolution of stable, locally-adapted variants. representatives of the genus Heliconia in the Antilles. Third, comprehensive studies of plant–pollinator interac- Heliconia caribaea is distributed across the Antilles, from tions, floral ecology, and hummingbird behavior are Eastern Cuba to Saint Vincent, with populations present on available for various islands of the Lesser Antilles, pro- all mountainous islands (Anderson 1981). Heliconia bihai viding baseline information for comparative studies is distributed from northern South America through the (Temeles et al. 2000, 2005, 2009; Temeles and Kress 2003; Lesser Antilles, and is also present on Hispaniola (Greater Gowda 2009. Antilles). Heliconia bihai has also been reported from Earlier studies on the islands of St Lucia and Dominica Puerto Rico (Acevedo and Strong 2010); however, it is showed a strong association between Heliconia floral known only from one collection (Acevedo, personal com- phenotypes and the bills and energy requirements of their munication), and we were not able to find it in our survey sexually-dimorphic hummingbird pollinator, the purple- across the island. For this reason, we report data for both throated carib (Eulampis jugularis) (Temeles et al. 2000; Heliconia species from Hispaniola and Dominica, but only Temeles and Kress 2003). Heliconia bihai has long, curved for H. caribaea from Puerto Rico. flowers that are pollinated by female purple-throats, Heliconia plants are large perennial herbs mostly whereas H. caribaea has shorter and straighter flowers that occurring in disturbed habitats, along roads, trails, rivers, are pollinated primarily by male purple-throats (Temeles and in forest gaps. They have rhizomatous growth, a mu- and Kress 2003; Fig. 1). The geographic range of the soid growth habit, and produce multiple inflorescences purple-throated carib is restricted to the Lesser Antilles each of which can last from 1 to 3 months. Flowering (Raffaele et al. 1998), but the native ranges of H. bihai and seasons for both species of Heliconia on Hispaniola and for H. caribaea extend to the Greater Antilles (Berry and Kress H. caribaea on Puerto Rico ranged from February through 1991). Here, we assess floral variation in relation to July, with peak flowering in April–May. Inflorescences are 123 Oecologia Table 1 Floral visitors of Heliconia caribaea and H. bihai in Hispaniola and Puerto Rico Species Sex Bill length Body Island Common name Behavior Category (mm) mass (g) Anthracothorax F 24.5 ± 0.3 5.4 ± 0.5 Hispaniola Hispaniolan Pollinator LB dominicus M 22.6 ± 0.2 6.2 ± 0.5 mango Anthracothorax F 25.1 ± 0.2 6.2 ± 0.3 Puerto Rico Green mango Pollinator LB viridis M 23.1 ± 0.2 6.6 ± 0.3 Eulampis F 23.3 ± 0.3 – Puerto Rico Green-throated Pollinator LB holocericeus

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