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ORNITOLOGIA NEOTROPICAL 23: 143–149, 2012 © The Neotropical Ornithological Society

FLORAL TRAITS OF VISITED BY THE BEE ( HELENAE)

Bo Dalsgaard1,2, Daniel W. Carstensen3, Arturo Kirkconnell4, Ana M. Martín González1,5, Orestes Martínez García6, Allan Timmermann7, & William J. Sutherland2

1Center for Macroecology, Evolution and Climate, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark. E-mail: [email protected] 2Conservation Science Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, United Kingdom. 3Ecology and Genetics, Department of Bioscience, Aarhus University, Ny Munkegade 114, DK-8000 Aarhus, Denmark. 4Museo Nacional de Historia Natural de , Obispo 61, Habana Vieja, Cuba. 5Pacific Ecoinformatics and Computational Ecology Lab, 1604 McGee Avenue, Berkeley, CA 94703, USA. 6Organo CITMA Ciénaga de Zapata, Carretera Playa Larga Km 26, Matanzas, Cuba. 7Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Ny Munkegade 116, DK-8000 Aarhus C, Denmark.

Características florales de las plantas visitadas por el zunzuncito (Mellisuga helenae).

Key words: , Trochilidae, conservation, hummingbird- interactions, seasonality, , Cuba, West Indies.

INTRODUCTION (Feinsinger & Colwell 1978, Schuchmann 1999, Nicolson & Fleming 2003, Dalsgaard et and their food-plants rely to a al. 2011). Although other than hum- large extent on each other for food supply mingbirds also act as pollinators (Feinsinger and pollination service, respectively. This & Colwell 1978, Rocca & Sazima 2008, Dals- mutual relationship has co-evolved for mil- gaard 2011, Kissling et al. 2011), humming- lions of years and across the involv- -plant interactions are one of the most ing over 330 hummingbird and an striking examples of bird-plant co-evolution, estimated nearly 8000 plant species relying on and the associated morphological adapta- hummingbirds as their principle pollinators tions have been studied intensively (e.g., Snow

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& Snow 1972, Brown et al. 1978, Feinsinger & We here: 1) identify and describe the floral Colwell 1978, Stiles 1981, Feinsinger et al. traits of several food plants the Bee Hum- 1982, Arizmendi & Ornelas 1990, Cotton mingbird uses; 2) report to what extent the 1998, Buzato et al. 2000, Temeles & Kress uses the same as the 2003, Lara 2006, Dalsgaard et al. 2009, Abra- Bee Hummingbird; and 3) compare our data hamczyk & Kessler 2010). These studies have on use with those previously reported, found that plants adapted to hummingbird- and discuss how our results could direct pollination typically are odorless, have a long future studies beneficial for the conservation and narrow conspicuous orange-red tubular of the Bee Hummingbird. corolla, and produce extensive dilute - broadly matching the sensory capabilities, METHODS AND STUDY SITE morphology and energetic demands of hum- mingbirds (Temeles & Kress 2003, Dalsgaard Food plants. Our study was conducted near et al. 2009). Similarly, hummingbirds show an Playa Larga (22°17N, 81°12W) in the out- array of features considered nectar-feeding skirts of the Zapata Swamp in Cuba, West adaptations, such as the capability to hover, a Indies - one of the few remaining core areas specialized tongue, highly specialized and for the Bee Hummingbird (Garrido & Kirk- variable bill morphologies, as well as a minute connell 2000). We focused our fieldwork on body size (Brown et al. 1978). measuring the floral traits (see below) of The smallest of all birds is the Bee Hum- plants known to be visited by the Bee Hum- mingbird (Mellisuga helenae) endemic to the mingbird. All the included food plants were Cuban archipelago, including the main island located in the field by OMG and AM (see of Cuba and Isle of Youth (formerly Isle of acknowledgments), both of whom have over Pines), in the West Indies (AOU 1998, Gar- 30 years of experience as bird guides locating rido & Kirkconnell 2000). Of the 15 hum- the Bee Hummingbird and its flowers in the mingbird species endemic to the West Indies Zapata Swamp, and have studied the Bee (Lack 1973, 1976), the Bee Hummingbird is Hummingbirds reproduction and use of food the only species considered threatened on the plants in the Zapata Swamp (Martínez et al. IUCN red list (BirdLife International 2011). 1998). We only included plants that OMG Although the Bee Hummingbird is the small- and AM knew to be used by the Bee Hum- est bird in the World, is categorized as Near mingbird and only at localities they knew well, Threatened and its population size is clearly i.e., we were certain that the individual plants declining, only very basic information regard- studied had been visited by the Bee Hum- ing its distribution and reproduction has pre- mingbird (which coincide with Kirkconnell’s viously been reported (Martínez et al. 1998, field data). The plants were later identified by Schuchmann 1999, Garrido & Kirkconnell Ramona Oviedo, a botanist from the Institute 2000). Almost nothing is known about its of Ecology and Systematic, Cuba. Although feeding ecology. For instance, apart from the during the fieldwork period we observed the record of some 15 food plants, nothing is Bee Hummingbird visiting some of the iden- reported about its preferred food plants or tified plants (Pavonia paludicola, Lysiloma lati- the overlap in flower use with the larger-sized siliquum, and Cissus obovata), we did not Cuban Emerald ( ricordii) - the attempt to estimate how the relative visitation only other resident Cuban hummingbird rate varied among plant species. We also (Martínez et al. 1998, Schuchmann 1999, report whether the plants were visited by the Garrido & Kirkconnell 2000). Cuban Emerald; this information was likewise

144 SHORT COMMUNICATIONS based on the accumulated knowledge by un-bagged and fresh flowers sampled within OMG and AM, although during fieldwork we the first hour of sunrise. Hence, nectar vol- also observed the Cuban Emerald visiting ume estimates express standing crop available several of the identified plants (Forsteronia to hummingbirds and other visitors in the corymbosa, Pavonia paludicola, Lysiloma latisiliq- early morning and not nectar production per se uum, , , and Cissus (Cotton 1998, Dalsgaard et al. 2009). obovata). RESULTS AND DISCUSSION Floral traits. We measured six quantitative and semi-quantitative floral traits, which have Each of the identified ten plant species visited been shown previously to be important in by the Bee Hummingbird belongs to different structuring West Indian hummingbird-plant plant families, of which one species (Antigonon communities into traditional ornithophilous leptopus) was introduced to Cuba. The remain- flowers and more generalistic entomophilous ing nine plant species are either native or syndrome flowers (Dalsgaard et al. 2009). The endemic to Cuba (Table 1). Most of the ten six floral traits can be divided into: two flowers visited by the Bee Hummingbird - of “restriction” traits (corolla depth, corolla which nine were also visited by the Cuban width); two “reward” traits (nectar volume, Emerald, as well as insects, such as bees and nectar concentration); and two “attraction” butterflies (pers. observ.) - have floral traits traits (color, odor). Corolla depth was mea- that fall outside the traditional ornithophilous sured as the internal distance from the open- syndrome, noticeably most flowers had little ing to the base of the flower. When the nectar nectar and a short, white corolla, although was not protected by a tubular corolla, we some had more vivid colors (Table 1, Fig. 1). measured the distance from the start of the This indicates that the Bee Hummingbird floral restriction to the base of the flower. uses plants with generalized pollination sys- Likewise, corolla width was measured as the tems as has also been reported for plants vis- internal width of the opening of the flower. ited by small hummingbirds on Trinidad, Both restriction traits were measured with a Tobago, and other islands in the West Indies digital caliper to nearest mm. Nectar volume (Feinsinger et al. 1982, Dalsgaard et al. 2008, was measured using 1, 5, and 10 µl micropi- 2009). pettes, while nectar concentration (expressed as % sucrose equivalents) was measured with Conclusions. A total of 15 plant species from 15 a refractometer and corrected for tempera- different genera had previously been reported ture. The floral color of each species was to be visited by the Bee Hummingbird, but no assigned as perceived by the human eye. study had described their floral traits (Mar- Where the floral bracts/stems were a major tínez et al. 1998, Schuchmann 1999). Of the part of the color display, as in C. obovata, they herein reported ten food plants, only one spe- were included in the assignment. Finally, the cies (Hamelia patens) occurs in the 15 genera flower of each species was coded according to previously listed as being visited by the Bee their odor, with (1) representing no odor; (2): hummingbird. Many of the previously little; (3): moderate; and (4): strong odor. All reported food plants in the Zapata Swamp floral trait estimates were obtained during 15– were observed in March–June during the 27 July 2010 (i.e., in the rainy season outside breeding season of the Bee Hummingbird of the Bee Hummingbirds breeding season), (Martínez et al. 1998), whereas the food plants and are means of 8–15 flowers measured on we here report bloom in the latter part of July,

145 DALSGAARD ET AL. 2 1 3 1 2 3 2 2 1 1 1 Odor red pink white white white white ) all species ) visited Color yellow orange-red orange-red yellow-green Nectar Chlorostilbon ricordii = little; 3 = moderate; and 4 = strong conc. (%) conc. 40.03 ± 5.21 SD 40.03 ± 2.67 SD 15.85 ± 9.41 SD 27.19 ± 2.03 SD 16.64 ± 2.51 SD 26.89 ± 2.65 SD 16.88 ± 0.89 SD 25.91 ± 2.88 SD 22.91 ± 5.55 SD 22.35 35.89 ± 22.14 SD Nectar volume (ml) volume 0.51± 0.41 SD 0.48 ± 0.31 SD 0.48 ± 0.10 SD 0.25 ± 0.93 SD 0.82 ± 1.14 SD 1.26 ± 0.66 SD 1.25 ± 5.30 SD 5.41 ± 0.30 SD 0.37 ± 0.34 SD 0.50 ). The Cuban Emerald ( 29.61 ± 24.37 SD 29.61 Odor: coded as 1–4: 1= no odor; 2 2 odor; no 1= Odor: 1–4: as coded 2 Corolla Mellisuga helenae Mellisuga width (mm) 1.97 ± 0.13 SD 1.09 ± 0.26 SD 1.81 ± 0.30 SD 6.52 ± 0.90 SD 1.12 ± 0.19 SD 0.84 ± 0.15 SD 1.73 ± 0.21 SD 3.47 ± 0.47 SD 1.53 ± 0.14 SD 1.48 ± 0.15 SD Corolla depth(mm) 2.62 ± 0.44 SD 6.79 ± 0.54 SD 4.87 ± 0.44 SD 1.03 ± 0.34 SD 8.88 ± 0.80 SD 3.29 ± 0.38 SD 0.00 ± 0.00 SD 16.83 ± 1.64 SD 16.83 ± 1.27 SD 21.33 ± 1.97 SD 18.20 8 9 8 9 N 15 12 11 11 11 11

1 1 2 2 2 2 2 3 2 2 1 origin Plant ecies visited by the Bee the Hummingbird ( ecies visited by Plant origin: 3 = introduced. 1 = endemic; 2 = native; 1 Cissus obovata Cissus obovata Plant species . Hamelia patens Hamelia Turnera ulmifolia Pavonia paludicola paludicola Pavonia icaco Lysiloma Forsteronia corymbosa Forsteronia Clerodendrum aculeatum hirsutissima Plant family Apocynaceae Boraginaceae Malvaceae Mimosaceae Passifloraceae Polygonaceae Rubiaceae Verbenaceae Vitaceae except except TABLE 1. Floral traitsTABLE of ten plant sp odor. odor.

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FIG. 1. The flowers of ten plant species visited by the Bee Hummingbird: a) Forsteronia corymbosa (Apocy- naceae); B) Tournefortia hirsutissima (Boraginaceae); C) Chrysobalanus icaco (Chrysobalanaceae); D) Pavonia palu- dicola (Malvaceae); E) Lysiloma latisiliquum (Mimosaceae); F) Turnera ulmifolia (Passifloraceae); G) Antigonon leptopus (Polygonaceae); H) Hamelia patens (Rubiaceae); I) Clerodendrum aculeatum (Verbenaceae); J) Cissus ob- ovata (Vitaceae). Note that the photos of each flower have a different scale. For the actual size of each flower, see Table 1 (photos: Bo Dalsgaard).

147 DALSGAARD ET AL. outside the breeding season of the Bee Hum- ing useful comments improving the manu- mingbird. In Cuba, the dry season extends script. BD was supported by The Carlsberg from November to April, whereas the wettest Foundation, The Danish Research Council | months are from June to October (Garrido & Natural Sciences and Weis-Fogh Fund at Kirkconnell 2000). Therefore, it seems likely Department of Zoology, University of Cam- that the flower community largely changes bridge, DWC by The Faculty of Science and between the dry and the rainy season, roughly Technology at Aarhus University, AMMG by coinciding with the termination of the Bee the Spanish Ministry of Education, and WJS Hummingbirds breeding season. by Arcadia. This study is a first step in identifying the floral niche of the Bee Hummingbird. We rec- REFERENCES ommend that a quantitative field study be undertaken to evaluate the floral overlap in Abrahamczyk, S., & M. Kessler. 2010. Humming- the context of floral use and availability, and bird diversity, food niche characters, and behavioral interactions with the Cuban assemblage composition along a latitudinal pre- Emerald (Vaurie 1957) and insect-pollinators, cipitation gradient in the Bolivian lowlands. J. such as the potential negative impact of the Ornithol. 151: 615–625. AOU. 1998. Check-list of North American Birds. non-native honeybee (Apis mellifera). Compar- 7th ed. American Ornithologists Union, Wash- ing the herein reported food plants of the Bee ington, D.C., USA. Hummingbird with the plant species reported Arizmendi, M. D. C., & J. F. Ornelas. 1990. Hum- by Martínez et al. (1998), indicates that it mingbirds and their floral resources in a tropi- would be essential to examine both dry sea- cal dry forest in Mexico. Biotropica 22: 172– son and rainy season floral overlap and 180. behavior. It would also be interesting to study BirdLife International. 2011. IUCN Red List for the effect of introduced plants, forest loss and birds. Downloaded on 2 August 2011 from degradation on the feeding behavior of the http://www.birdlife.org. Bee Hummingbird (BirdLife International Bleiweiss, R. 1998. Origin of hummingbird faunas. 2011). Finally, we recommend that field stud- Biol. J. Linn. Soc. 65: 77–97. Brown, J. H., W. A. III Calder, & A. Kodric-Brown. ies are also conducted in other areas than the 1978. Correlates and consequences of body Zapata Swamp, e.g., in the Bee Humming- size in nectar-feeding birds. Am. Zool. 18: 687– birds strongholds in the lowlying Guanaha- 700. cabibes peninsula in western Cuba and in the Brown, J. H., & M. A. Bowers. 1985. Community eastern mountains of Cuchillas del Toa and organization in hummingbirds: relationship Sierra Cristal. This should prove valuable for between morphology and ecology. Auk 102: the conservation of the Bee hummingbird, an 251–269. endemic and threatened species of the Cuban Buzato, S., M. Sazima, & I. Sazima. 2000. Hum- archipelago, West Indies. mingbird-pollinated floras at three Atlantic for- est sites. Biotropica 32: 824–841. ACKNOWLEDGMENTS Cotton, P. A. 1998. in an Amazonian hummingbird-plant community. Ibis 140: 639– 646. Thanks to Ramona Oviedo for identifying the Dalsgaard, B., A. M. Martín González, J. M. Ole- plants, to Angel Martínez and Lazara Reina sen, A. Timmermann, L. H. Andersen, & J. Rodriquez Gazmury for help in the field, and Ollerton. 2008. Pollination networks and func- to Joseph M. Wunderle, André Weller, Gary F. tional specialization: a test using Lesser Anti- Stiles, and an anonymous reviewer for provid- llean plant-hummingbird assemblages. Oikos

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117: 789–793. Lack, D. 1976. Island biology illustrated by the land Dalsgaard, B., A. M. Martín González, J. M. Ole- birds of . Blackwell, Oxford, UK. sen, J. Ollerton, A. Timmermann, L. H. Ander- Lara, C. 2006. Temporal dynamics of flower use by sen, & A. G. Tossas. 2009. Plant-hummingbird hummingbirds in a highland temperate forest in interactions in the West Indies: floral specialisa- Mexico. Ecoscience 13: 23–29. tion gradients associated with environment and Martínez García, O., L. Bacallao Mesa, & E. Nieves hummingbird size. Oecologia 159: 757–766. Lorenzo. 1998. Estudio preliminary de la con- Dalsgaard, B. 2011. Nectar-feeding and pollination ducta reproductive de Mellisuga helenae (Aves, by the Cuban Green Woodpecker (Xiphidiopicus ) en condiciones naturals. El percussus) in the West Indies. Ornitol. Neotrop. Pitirre 11: 102–106. 22: 447–451. Nicolson, S. W., & P. A. Fleming. 2003. Nectar as Dalsgaard, B., E. Magård, J. Fjeldså, A. M. Martín food for birds: the physiological consequences González, C. Rahbek, J. M. Olesen, J. Ollerton, of drinking dilute sugar solutions. Plant Syst. R. Alarcón, A. C. Araujo, P. A. Cotton, C. Lara, Evol. 238: 139–153. C. G. Machado, I. Sazima, M. Sazima, A. Tim- Rocca, M. A., & M. Sazima. 2008. Ornithophilous mermann, S. Watts, B. Sandel, W. J. Sutherland, canopy species in the Atlantic rain forest of & J.-C. Svenning. 2011. Specialization in plant- southeastern Brazil. J. Field Ornithol. 79: 130– hummingbird networks is associated with spe- 137. cies richness, contemporary precipitation and Schuchmann, K. L. 1999. Family Trochilidae Quaternary climate-change velocity. PLoS (Hummingbirds). Pp. 468–680 in del Hoyo, J., ONE 6: e25891. A. Elliott, & J. Sargatal (eds). Handbook of the Feinsinger, P., & R. K. Colwell. 1978. Community birds of the world. Volume 5: Barn-owls to organization among neotropical nectar-feeding hummingbirds. Lynx Edicions, Barcelona, birds. Am. Zool. 18: 779–796. Spain. Feinsinger, P., J. A. Wolfe, & L. A. Swarm. 1982. Snow, B. K., & D. W. Snow. 1972. Feeding niches of Island ecology: reduced hummingbird diversity hummingbirds in a Trinidad valley. J. Anim. and the pollination biology of plants, Trinidad Ecol. 41: 471–485. and Tobago, West Indies. Ecology 63: 494– Stiles, F. G. 1981. Geographical aspects of bird- 506. flower coevolution, with particular reference to Garrido, O. H., & A. Kirkconnell. 2000. Field guide Central America. Ann. Mo. Bot. Gard. 68: 323– to the birds of Cuba. Cornell Univ. Press, New 351. York, New York, USA. Temeles, E. J., & J. Kress. 2003. Adaptation in a Kissling, D. W., C. H. Sekercioglu, & W. Jetz. 2011. plant-hummingbird association. Science 300: Bird dietary guild richness across latitudes, 630–633. environments and biogeographic regions. Glo- Vaurie, C. 1957. Field notes on some Cuban birds. bal Ecol. Biogeogr. 21: 328–340. Wilson Bull. 69: 301–313. Lack, D. 1973. The number of species of hum- mingbirds in the West Indies. Evolution 27: Accepted 14 March 2012. 326–337.

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