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University of Copenhagen Plant-hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size Dalsgaard, Bo; Martín González, Ana M; Olesen, Jens; Ollerton, Jeff; Timmermann, Allan; Andersen, Laila Hanghøj; Tossas, Adrianne G Published in: Oecologia DOI: 10.1007/s00442-008-1255-z Publication date: 2009 Document version Publisher's PDF, also known as Version of record Citation for published version (APA): Dalsgaard, B., Martín González, A. M., Olesen, J., Ollerton, J., Timmermann, A., Andersen, L. H., & Tossas, A. G. (2009). Plant-hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size. Oecologia, 159, 757-66. https://doi.org/10.1007/s00442-008-1255-z Download date: 23. Sep. 2021 Oecologia (2009) 159:757–766 DOI 10.1007/s00442-008-1255-z PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Plant–hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size Bo Dalsgaard Æ Ana M. Martı´n Gonza´lez Æ Jens M. Olesen Æ Jeff Ollerton Æ Allan Timmermann Æ Laila H. Andersen Æ Adrianne G. Tossas Received: 26 March 2008 / Accepted: 3 December 2008 / Published online: 9 January 2009 Ó Springer-Verlag 2008 Abstract Floral phenotype and pollination system of a had flowers with long corolla tube, large amounts of nectar plant may be influenced by the abiotic environment and the and showy orange-red colouration. These attracted few or local pollinator assemblage. This was investigated in seven no insect species, whereas plants pollinated by small, short- plant–hummingbird assemblages on the West Indian billed hummingbirds were frequently pollinated by insects, islands of Grenada, Dominica and Puerto Rico. We report particularly lepidopterans. The separation of plants related all hummingbird and insect pollinators of 49 hummingbird- to environmental factors showed that species in the wet and pollinated plant species, as well as six quantitative and cold highlands produced large amounts of dilute nectar, semi-quantitative floral characters that determine visitor possessed no or a weak odour, and were associated with restriction, attraction and reward. Using nonmetric multi- few insects, particularly few hymenopterans, compared to dimensional scaling analysis, we show that hummingbird- plants in the dry and warm lowlands. The most specialised pollinated plants in the West Indies separate in floral hummingbird-pollinated plants are found in the West phenotypic space into two gradients—one associated with Indian highlands where they are pollinated by mainly large, the abiotic environment and another with hummingbird long-billed hummingbirds. At the other extreme, highly size. Plants pollinated by large, long-billed hummingbirds generalised plants growing in the dry and warm lowlands are pollinated by small, short-billed hummingbirds and numerous insect species. This illustrates that, even within Communicated by Florian Schiestl. the hummingbird-pollinated flora, pollination syndrome Electronic supplementary material The online version of this and the degree of specialisation may vary tremendously article (doi:10.1007/s00442-008-1255-z) contains supplementary depending on pollinator morphology and environment. material, which is available to authorized users. Keywords Floral phenotype Á Insect pollinator Á B. Dalsgaard (&) Á J. M. Olesen Á A. Timmermann Á L. H. Andersen Ornithophilous syndrome Á Plant–pollinator interaction Á Department of Biological Sciences, University of Aarhus, Specialisation gradient Ny Munkegade, Building 1540, 8000 Aarhus, Denmark e-mail: [email protected] B. Dalsgaard Á A. M. Martı´n Gonza´lez Introduction Unit of Ecology and Center for Ecological Research and Forestry Applications (CREAF), Autonomous University Plant–pollinator interactions have often been stated to be of Barcelona, 08193 Bellaterra, Barcelona, Spain highly coevolved, resulting in certain floral phenotypes or J. Ollerton ‘‘pollination syndromes’’, which are expected to be spe- Landscape and Biodiversity Research Group, cialisations to particular types of pollinators (Faegri and School of Applied Sciences, University of Northampton, van der Pijl 1979). However, during the last decade, the Park Campus, Northampton NN2 7AL, UK concept of pollination syndromes has been reassessed (e.g. A. G. Tossas Waser et al. 1996; Hingston and Mcqillan 2000; Ollerton Villas del Rı´o, 1100 Bambu´, Mayagu¨ez, PR, USA and Watts 2000; Fenster et al. 2004; Wilson et al. 2004; 123 758 Oecologia (2009) 159:757–766 Ollerton et al. 2009). Although in a number of cases pol- may modify corolla morphology, nectar reward and col- linator type can be predicted from floral phenotype ouration, causing changes in hummingbird and insect (Ollerton et al. 2009), pollinator preference often seems accessibility and attractiveness (Bradshaw et al. 1995; weak (Pleasants and Waser 1985), ecological generalisa- Bradshaw and Schemske 2003; Wilson et al. 2006). Hence, tion on multiple pollinators may be the rule rather than the floral phenotype of hummingbird-pollinated plants may be exception (Waser et al. 1996) and clear-cut predictions of adaptations to a mixture of hummingbird and insect for- pollinator type based on pollination syndromes seem aging (Stiles 1981; Hurlbert et al. 1996; Mayfield et al. therefore hazardous and cannot replace field observations 2001; Castellanos et al. 2004). Indeed, as most researchers (Johnson and Steiner 2000; Ollerton et al. 2009). studying plant–hummingbird interactions have observed, Moreover, plant–pollinator interactions change with hummingbirds and insects, in particular lepidopterans and environment, at both species and community level (e.g. bees, often pollinate the same plants (e.g. Snow and Snow Cruden 1972; Primack and Inouye 1993; Hingston and 1972; Feinsinger and Colwell 1978; Carpenter 1979; Stiles Mcqillan 2000; Olesen and Jordano 2002; Aizen 2003; 1981; Feinsinger et al. 1982; Arizmendi and Ornelas 1990; Medel et al. 2007; Devoto et al. 2005). For instance, pol- Mayfield et al. 2001; Medel et al. 2007; Dalsgaard et al. linator species richness and composition vary with 2008). This may especially be the case for plants pollinated elevation, rainfall and temperature (Arroyo et al. 1982; by small hummingbirds (e.g. Stiles 1981; Feinsinger et al. Olesen and Jordano 2002; Aizen 2003; Devoto et al. 2005), 1982; Arizmendi and Ornelas 1990; Dalsgaard et al. 2008), affecting specialisation level (Elberling and Olesen 1999) plants in dry lowland habitats where insects are reliable and and pollinator mode (Cruden 1972; Stiles 1978; Aizen and effective pollinators (Cruden 1972; Bleiweiss 1998), and Ezcurra 1998; Aizen 2003; Kessler and Kro¨mer 2000; Kay on islands, where pollination systems are expected to be and Schemske 2003; Kro¨mer et al. 2006). Insects, espe- more generalised than on comparable mainland (e.g. Lin- cially hymenopterans, have low species richness in areas hart and Feinsinger 1980; Feinsinger et al. 1982; Olesen with cold and rainy weather (Cruden 1972; Aizen and et al. 2002; Rivera-Marchand and Ackerman 2006; Tim- Ezcurra 1998; Devoto et al. 2005), whereas vertebrates are mermann et al. 2008). expected to be less affected by these environmental factors Floral phenotype may consequently vary with environ- (Stiles 1978; Bleiweiss 1998). In Central and South ment, local pollinator assemblage and size of hummingbird America, where hummingbirds are part of the pollinator pollinator. Thus, hummingbird-pollinated flowers might fauna, many plant species are specialised on hummingbird– not fit into a single category, such as the traditional or- pollination in cold and rainy environments, often prevailing nithophilous pollination syndrome (Ollerton et al. 2009). In at high elevations (Cruden 1972; Stiles 1978; Aizen and this study, we examine the relationships between floral Ezcurra 1998; Bleiweiss 1998; Kessler and Kro¨mer 2000; phenotype, hummingbird type, insect generalisation level Aizen 2003; Kro¨mer et al. 2006). As an example, in the and environment in seven plant–hummingbird assemblages cold highlands and in wet areas of the eastern Andes, varying in altitude, rainfall and temperature on the West bromeliads are primarily hummingbird-pollinated, whereas Indian islands of Grenada, Dominica and Puerto Rico. We in arid habitats they are mainly insect-pollinated (Kessler ask: (1) can we separate the plant species in floral pheno- and Kro¨mer 2000;Kro¨mer et al. 2006). Similarly, in the typic space in relation to the type of hummingbird visitor tropical highlands, Costus species are pollinated by hum- and environment, i.e. can we identify gradients associated mingbirds, whereas lowland species are pollinated by with hummingbird size and environment? (2) How is floral either euglossine bees or hummingbirds (Kay and Schem- phenotypic separation related to insect visitor fauna, and ske 2003). how is insect species richness related to hummingbird size Plant species adapted to hummingbird–pollination often and environment? (3) Finally, we identify representatives have flowers that are showy orange-red, scentless, have a of the most specialised and generalised plant species, and long, narrow, tubular corolla and produce a large amount of discuss the pros and cons of having a generalised pollina- dilute nectar, which broadly correspond to hummingbird tion system in the West Indies. sensory capabilities, morphology and high energetic demands. However, floral phenotype may vary among populations within
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