SHORT COMMUNICATIONSORNITOLOGIA NEOTROPICAL 18: 133–138, 2007
© The Neotropical Ornithological Society

OBSERVATIONS OF HUMMINGBIRD FEEDING BEHAVIOR AT
FLOWERS OF HELICONIA BECKNERI AND H. TORTUOSA IN
SOUTHERN COSTA RICA
Joseph Taylor1 & Stewart A. WhiteDivision of Environmental and Evolutionary Biology, Graham Kerr Building, University ofGlasgow, Glasgow, CB23 6DH, UK.
Observaciones de la conducta de alimentación de colibríes con flores de Heliconia beckneri y H.
tortuosa en El Sur de Costa Rica.
Key words: Pollination, sympatric, cloud forest, Cloudbridge Nature Reserve, Green Hermit, Phaethornis
guy, Violet Sabrewing, Campylopterus hemileucurus, Green-crowned Brilliant, Heliodoxa jacula.

INTRODUCTION
Interactions between closely related sympatricflowering plants may involve competition forpollinators, interspecific pollen loss andhybridization (e.g., Feinsinger 1987). These
processes drive the divergence of genetically
based floral phenotypes that influence pollinator assemblages and behavior. However,floral convergence may be favored if theincreased nectar supplies and flower densities,
for example, increase the regularity and rateof flower visitation for all species concerned(Schemske 1981). Sympatric hummingbirdpollinated plants probably face strong selection pressures against simultaneous pollinator
sharing, since the mobility of birds combinedwith their high energy needs may result inthem visiting several widely scattered nectar______________
1

Current address: Cambridgeshire and PeterboroughBiological Records Centre, The Manor House,
Broad Street, Cambourne, Cambridge, CB3 6DH,
UK. E-mail: joe.taylor@cpbrc.org.uk

sources in a single foraging bout (Stiles 1978).
The flower preferences shown by hummingbirds (Trochilidae) are influenced by a complex array of factors including their bill
dimensions, body size, habitat preference andrelative dominance, as influenced by age andsex, and how these interact with the morphological, caloric and visual properties of flowers (e.g., Stiles 1976).
Hummingbirds are the primary pollinators of most Heliconia species (Heliconiaceae)(Linhart 1973), which are medium to large
clone-forming herbs that usually produce
brightly colored floral bracts (Stiles 1975).
Some species of hummingbirds are known tovisit several Heliconia species, probably resulting in substantial interspecific pollen transfer(Kress 1983). Many Heliconia species are sympatric; however the number of naturally
occurring hybrids is small in proportion tothe number of sympatric associations. Interactions between Heliconia species will probably favor a divergence in spatial and temporal
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flowering patterns (Stiles 1979). Mechanicalisolation may occur through deposition ofpollen from different species in different
places on a given species of hummingbird,
through variation in corolla morphology andpositioning of the anthers (Stiles 1975, 1979;
Kress 1983). The ultimate mechanisms preventing hybridization in Heliconia species may
be pre-fertilization barriers such as the inhibition of foreign pollen tubes, and these areprobably favored by pollinator sharing (Kress1983).
On the Pacific slope of the Cordillera
Talamanca, in southern Costa Rica, Heliconia
beckneri R. R. Smith, a species endemic to thismountain range and probably of hybrid origin(Daniels & Stiles 1979), and H. tortuosa Griggs
occur together in mid-elevation habitats. The
flowering peaks of these two species overlap
in June and July (Daniels & Stiles 1979), andthey are predicted to share the same primaryand secondary pollinators (Stiles 1979), but
hybridization apparently does not occur. Stiles(1979) identifies the Green Hermit (Phaethornis guy) as the primary pollinator of both species, and the Violet Sabrewing (Campylopterus
hemileucurus) as the secondary pollinator of H.
tortuosa and the possible secondary pollinatorof H. beckneri. In addition, the Rufous-tailed
Hummingbird (Amazilia tzacatl) is given as anoccasional pollinator of H. tortuosa. If the services of pollinators are indeed shared it might
be expected that selection has favored mechanisms that reduce the chances of hybridization and pollen loss between these species.
The aim of this research was to investigate theextent of pollinator sharing and the presenceof such mechanisms.

METHODS
Field work was carried out by the principal
researcher (JT) between 22 May and 17 July
2005 at Cloudbridge Nature Reserve, San
Gerardo de Rivas, Pérez Zeledón, Costa Rica134(approx. 09°50’N, 83°55’W). The reserve covers over 200 ha adjacent to the Chirripó
National Park on the southern Pacific slopeof the Talamanca mountain range. H. beckneriand H. tortuosa were often found growing
within metres of one another, in both primary
forest and secondary growth, and were bothflowering abundantly during the study period,
thus there was no indication of staggered
flowering peaks as an isolation mechanism(Stiles 1979).
Focal observations were carried out from06:00 h to 12:00 h (CST), through all conditions, at seven plants or clumps of plants (presumed clones) of both species, each with atleast one fresh inflorescence, resulting in 42 hof observations for each species. Most focal
plants were in oak-dominated lower montane
primary forest, but two clumps of H. tortuosa
plants were watched in secondary growth atsimilar elevations. The elevation range of
focal plants, as measured with a global positioning system, was 1561–1678 m for H. beckneri, and 1560–1607 m for H. tortuosa.
During observations, the observer sat or
stood approximately 4 m away from the focal
plants, and 8×30 binoculars were used. Pollinating flower visits were counted, including
repeat visits to the same flower, and wereclassed as those that probably involved contact with the reproductive parts of flowers.
Insect flower visitors were at least identified
to Order, but to a lower taxonomic level
where possible. All hummingbird flower visitors were identified to species, and where possible the sex of birds was noted at all focal
plants and clumps of H. tortuosa and at five of
the focal plants and clumps of H. beckneri.
Hummingbirds were sexed by differences inplumage (Stiles & Skutch 1989). The primaryand secondary pollinators of each Heliconia
species at Cloudbridge during the study
period were identified in terms of the percentage of all pollinating visits that theyaccounted for. Observations of feeding meth-SHORT COMMUNICATIONSTABLE 1. The proportion (%) of all pollinating flower visits (n) by each taxa observed at sevenplants or clumps of plants each of Heliconia beckneri and H. tortuosa at Cloudbridge NatureReserve, Costa Rica, in June and July 2005.
Taxa of flower visitors

Proportion (%) of all pollinating visits (n)H. beckneri (n = 318)

H. tortuosa (n = 271)

Green Hermit1917

Violet Sabrewing

068

Green-crowned Brilliant

690

Euglossine species

87

Probable Trigona species

48

Apodiformes (Trochilidae)

Hymenoptera

ods were made for most flower visits, sometimes with binoculars, including the angle atwhich hummingbirds inserted their bills into
the corolla and the resulting points of contact
on the hummingbird by the anthers andstigma; that is, the likely pollen deposition
sites.

RESULTS
Focal observations revealed that pollinating
flower visits were carried out at both speciesof Heliconia by hummingbirds and bees(Apoidea) (Table 1). The Green Hermit was
only the secondary pollinator of both Heliconia
species; its services, though, appeared to bepartitioned, with males accounting for 92% of
all flower visits by this species at H. beckneri (n= 24), and females or juveniles accounting for
96% of all flower visits by this species at H.
tortuosa (n = 46). The Violet Sabrewing was
the primary pollinator of H. tortuosa, but was
only seen to visit one clump of H. beckneri insecondary growth during trial observations.
The Green-crowned Brilliant (Heliodoxa jacula)was the primary pollinator of H. beckneri, but
was never seen to approach inflorescences of
H. tortuosa. Euglossine bees and probable

Trigona bees were occasional pollinators ofboth Heliconia species (Table 1).
Observations of feeding behavior suggestthat flower shape influenced the feeding
methods of hummingbirds. The flowers of H.
beckneri are virtually straight from the corolla
entrance to just before the nectar chamber,where there is a slight curvature (Fig. 1) andall the species observed (Table 1), including
the Green Hermit and Violet Sabrewing,
which have long decurved bills, were seen toprobe from in front of the flowers (Figs 2Aand 2B). In contrast, the moderately andevenly curved flowers of H. tortuosa (Fig. 1)
appeared to force birds with long decurved
bills to insert them from above and behindthe flowers (Figs 2C and 2D), and almost certainly excluded the straight bill of the Greencrowned Brilliant. The Green-crowned Brilliant always perched on bracts when feedingfrom H. beckneri flowers and the anthers andstigma appeared to touch its chin, cheeks andthroat (Fig. 2A). In contrast, the Green Hermit was always seen to hover whilst feedingfrom flowers. The anthers and stigma of H.
beckneri appeared to touch its lower mandible
and probably its chin (Fig. 2B), while those ofH. tortuosa appeared to touch its upper mandi135

TAYLOR & WHITE

FIG. 1. Three fresh flowers of Heliconia tortuosa (left) and H. beckneri (right) picked at Cloudbridge NatureReserve, Costa Rica, in July 2005. Photo by Joseph Taylor.

ble and probably its forehead (Fig. 2C). The
Violet Sabrewing usually fed whilst hovering,and rarely perched to feed. At H. tortuosaflowers the anthers and stigma appeared totouch the forehead or crown (Fig. 2D). Trialobservations at a large clump of H. beckneri
plants in secondary growth suggested that theanthers and stigma of this species touched thebird’s chin. It should be noted that there is noquantitative data to support these observations of differing feeding methods, and no
additional fieldwork was carried out to confirm the pollen deposition sites.

DISCUSSION
The identities of the primary and secondary
pollinators of H. beckneri and H. tortuosa atCloudbridge did not conform to those that136were expected, however explaining the rolesof species is difficult without a study of theirrelative abundances in the locality. Whilst thepresence of the Green-crowned Brilliant andViolet Sabrewing as the primary pollinators ofthese Heliconia species was probably strongly
influenced by season and elevation, respectively (see Stiles 1979, Stiles & Skutch 1989),
the relative preferences of all three hummingbird species were probably influenced byexploitation competition, flower morphology,
bract and floral coloration, and nectar production (e.g., Stiles 1976). The limited sampling of accumulated nectar in protected
flowers by picking and dissection revealed
that there was a significantly higher energy
content (J flower-1) in those of H. beckneri at
both sampling times of 06:00 h (Mann-Whitney U-test, U = 138.0, P = 0.014, n = 10

SHORT COMMUNICATIONS

FIG. 2. Feeding methods of three hummingbird species at Heliconia flowers as observed at Cloudbridge
Nature Reserve, Costa Rica, between 22 May and 17 July 2005: A) Heliodoxa jacula at H. beckneri; B)
Phaethornis guy at H. beckneri; C) P. guy at H. tortuosa; and D) Campylopterus hemileucurus at H. tortuosa. Arrows
indicate probable pollen deposition sites. Drawings by Joseph Taylor.

flowers per species) and 12:00 h (U = 136.0, P= 0.021, n = 10 flowers per species). The partitioning of the pollination services of theGreen Hermit by sex and possibly age could
be due to the interaction of a dominance hierarchy and the difference in the energy contentof flowers, as female hummingbirds are generally subordinate (Stiles 1976). Although
Euglossine bees were only occasional pollinators of both species, they are thought to promote outcrossing among tropical plants withlow population densities (Janzen, 1971).
Flower mites (Acari: Mesostigmata: Ascidae)
were observed on the flowers of both species
and may contribute to self-pollination(Dobkin 1984).
The data suggest that the pollination services of the Green Hermit and Violet Sabrewing are shared by populations of H. beckneriand H. tortuosa at Cloudbridge to only a limited extent. If interspecific pollen transfer did
take place, hybridization might occur, since H.
tortuosa is known to hybridize with H. latispatha (Stiles 1979), one of the suspected parent species of H. beckneri (Daniels & Stiles
1979). However, the observed differences inflower curvature, feeding methods and thelikely pollen deposition sites, probably reduce
the risk of pollen loss and cross-fertilization.
Thus, there is unlikely to be selection against
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both the sharing of pollinators and simultaneous flowering in these two species. Both of
the Heliconia species studied at Cloudbridge
were abundant in primary forest, and Stiles(1975) noted that under the forest canopy low
light intensity may make it difficult for a species to photosynthesize the metabolic
reserves necessary for flowering. Therefore
simultaneous flowering may create sufficientnectar resources to maintain pollinator traplines (Schemske 1981) where only one species would be unable to. Stiles (1975, 1979)
also noted that, at La Selva, Costa Rica, H.
irrasa and H. umbrophila flowered simultaneously in most years. These species areplants of the forest understory, and simultaneous flowering perhaps allows hermits toextend their foraging routes through the forest more frequently than usual. The different
flower curvatures of H. irrasa and H. umbrophila result in pollen being placed at dorsal
and ventral sites on their shared pollinator,
the Long-tailed Hermit (P. superciliosus) (Stiles
1979). The flower morphologies and resulting
pollen deposition sites noted by Stiles (1975,1979) mirror the observations in the present
study surprisingly closely, suggesting that this
could be a reoccurring pattern in sympatricHeliconia species. Stiles (1975) suggested thatthe less abundant H. umbrophila had converged in flowering season with H. irrasa; achange favored because it would make its
clumps more accessible to traplining hermits.
Further research on whether other sympatricHeliconia species, such as H. beckneri and H.
tortuosa, have influenced one another’s populations may uncover interesting relationships.

ACKNOWLEDGMENTS
Many thanks to I. and G. Giddy for making
this project possible and for their hospitality
and advice. I. Giddy and two anonymous referees made some useful comments on earlier

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drafts of this paper. We are grateful for thehelp and advice kindly provided by E. Kangat Cloudbridge, P. McLaughlin, J. Freel and G.
Hancock at the University of Glasgow, and L.
D. Gómez at Las Cruces Biological Station,Costa Rica.

REFERENCES
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Dobkin, D. S. 1984. Flowering patterns of longlived Heliconia inflorescences: implications forvisiting and resident nectarivores. Oecologia
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Feinsinger, P. 1987. Effects of plant species oneach other’s pollination: Is community structure influenced? Trends Ecol. Evol. 2: 123–126
Janzen, D. H. 1971. Euglossine bees as long-distance pollinators of tropical plants. Science
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Accepted 28 August 2006.