Different foraging preferences of hummingbirds on artificial and natural flowers reveal mechanisms structuring plant-pollinator interactions

Journal of Animal Ecology

Volumn 84, Issue 3, 2015, Pages 655-664

  Maglianesi, María A ^a,b   Böhning Gaese, Katrin ^a,c   Schleuning, Matthias ^a  

^a SENCKENBERG DEUTSCHES ENTOMOLOGISCHES INSTITUT   (Germany)

^b UNIVERSIDAD ESTATAL A DISTANCIA   (Costa Rica)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Artificial feeders; Biotic interactions; Costa rica; Floral morphology; Floral traits; Foraging preferences; Hummingbirds; Interaction niche; Morphological constraints; Resource partitioning

Indexed keywords

BIRD; FLORAL TRAIT; MORPHOLOGY; NECTAR; NICHE PARTITIONING; PLANT-POLLINATOR INTERACTION; PREY PREFERENCE; TROPHIC INTERACTION;

COSTA RICA;

EUPHERUSA NIGRIVENTRIS; LAMPORNIS CALOLAEMUS; PHAETHORNIS GUY; TROCHILIDAE;

NECTAR;

ADAPTATION; ANATOMY AND HISTOLOGY; ANIMAL; APPETITE; BEAK; BIRD; COSTA RICA; FLOWER; NECTAR; PHENOTYPE; PHYSIOLOGY; POLLINATION; SPECIES DIFFERENCE;

ADAPTATION, BIOLOGICAL; ANIMALS; APPETITIVE BEHAVIOR; BEAK; BIRDS; COSTA RICA; FLOWERS; PHENOTYPE; PLANT NECTAR; POLLINATION; SPECIES SPECIFICITY;

EID: 84928128646     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12319     Document Type: Article

References (65)

1. Bascompte, J. & Jordano, P. (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38, 567-593.
2. Benadi, G., Hovestadt, T., Poethke, H.-J. & Blüthgen, N. (2014) Specialization and phenological synchrony of plant-pollinator interactions along an altitudinal gradient. Journal of Animal Ecology, 83, 639-650.
3. Blake, J.G. & Loiselle, B.A. (2000) Diversity of birds along an elevational gradient in the Cordillera Central, Costa Rica. Auk, 117, 663-686.
4. Blüthgen, N. (2010) Why network analysis is often disconnected from community ecology: a critique and an ecologist's guide. Basic and Applied Ecology, 11, 185-195.
5. Bolnick, D.I., Svanback, R., Fordyce, J.A., Yang, L.H., Davis, J.M., Hulsey, C.D. et al. (2003) The ecology of individuals: incidence and implications of individual specialization. The American Naturalist, 161, 1-28.
6. Brown, J.H. & Bowers, M.A. (1985) Community organization in hummingbirds: relationships between morphology and ecology. Auk, 102, 251-269.
7. Case, T.J. & Gilpin, M.E. (1974) Interference competition and niche theory. Proceedings of the National Academy of Sciences USA, 71, 3073-3077.
8. Chalcoff, V.R., Aizen, M.A. & Galetto, L. (2006) Nectar concentration and composition of 26 species from the temperate forest of South America. Annals of Botany, 97, 413-421.
9. Colwell, R.K. (1973) Competition and coexistence in a simple tropical community. The American Naturalist, 107, 737-760.
10. Colwell, R.K. & Fuentes, E.R. (1975) Experimental studies of the niche. Annual Review of Ecology, Evolution, and Systematics, 6, 281-310.
11. Corbet, S.A. (2000) Butterfly nectaring flowers: butterfly morphology and flower form. Entomologia Experimentalis et Applicata, 96, 289-298.
12. Cotton, P.A. (1998) Coevolution in an Amazonian hummingbird-plant community. Ibis, 140, 639-646.
13. Dalsgaard, B., Martín Gonzáles, A.M., Olesen, J.M., Ollerton, J., Timmermann, A., Andersen, L.H. et al. (2009) Plant-hummingbird interactions in the West Indies: floral specialization gradients associated with environment and hummingbird size. Oecologia, 159, 757-766.
14. Dehling, D.M., Töpfer, T., Schaefer, H.M., Jordano, P., Böhning-Gaese, K. & Schleuning, M. (2014) Functional relationships beyond species richness patterns: trait matching in plant-bird mutualisms across scales. Global Ecology and Biogeography, 23, 1085-1093.
15. Devictor, V., Clavel, J., Julliard, R., Lavergne, S., Mouillot, D., Thuiller, W. et al. (2010) Defining and measuring ecological specialization. Journal of Applied Ecology, 47, 15-25.
16. Faegri, K. & van der Pijl, L. (1979) The Principles of Pollination Ecology. Pergamon Press, Oxford, UK.
17. Feinsinger, P. (1976) Organization of a tropical guild of nectarivorous birds. Ecological Monographs, 46, 257-291.
18. Feinsinger, P. & Colwell, R.K. (1978) Community organization among neotropical nectar feeding birds. American Zoologist, 18, 779-795.
19. Fründ, J., Linsenmair, K.E. & Blüthgen, N. (2010) Pollinator diversity and specialization in relation to flower diversity. Oikos, 119, 1581-1590.
20. Geerts, S. & Pauw, A. (2009) Hyper-specialization for long-billed bird pollination in a guild of South African plants: the Malachite Sunbird pollination syndrome. South African Journal of Botany, 75, 699-706.
21. Goldblatt, P. & Manning, J.C. (2000) The long-proboscid fly pollination system in southern Africa. Annals of the Missouri Botanical Garden, 87, 146-170.
22. Grant, K.A. & Grant, V. (1968) Hummingbirds and their Flowers. Columbia Univ. Press, New York, USA.
23. Hainsworth, F.R. & Wolf, L.L. (1972) Crop volume, nectar concentration and hummingbird energetics. Comparative Biochemistry and Physiology, 42A, 359-366.
24. Hartshorn, G. & Peralta, R. (1988) Preliminary description of primary forests along the La Selva-Volcan Barva altitudinal transect, Costa Rica. Tropical Rainforests: Diversity and Conservation (eds F. Almeda & C.M. Pringle), pp. 281-295. California Academy of Sciences, San Francisco, California, USA.
25. Holdridge, L.R. (1967) Life Zone Ecology. Tropical Science Center, San José.
26. del Hoyo, J., Elliott, J. & Christie, D.A. (eds) (2005) Handbook of the Birds of the World, vol. 10: Cuckoo-shrikes to Thrushes. Lynx Editions, Barcelona, Spain.
27. Hutchinson, G.E. (1957) Concluding remarks. Cold Spring Harbor Symposia Quantitative Biology, 22, 415-427.
28. Ibanez, S. (2012) Optimizing size thresholds in a plant-pollinator interaction web: towards a mechanistic understanding of ecological networks. Oecologia, 170, 233-242.
29. Inouye, D.W. (1977) Species structure of bumblebee communities in North America and Europe. The Role of Arthropods in Forest Ecosystems (ed W.J. Mattson), pp. 35-40. Springer-Verlag, New York, USA.
30. Inouye, D.W. (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology, 59, 672-678.
31. Inouye, D.W. (1980) The effect of proboscis and corolla tube lengths on patterns and rates of flower visitation by bumblebees. Oecologia, 45, 197-201.
32. Jordano, P., Bascompte, J. & Olesen, J.M. (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters, 6, 69-81.
33. Kershaw, F.L. (2006) The Co-evolution of Hummingbird Bill Morphology and Floral Structures with Regard to Both Native and Non-native Flower Species. Department of Biology, School of Biological Sciences, Leeds University, Leeds, UK.
34. Linhart, Y.B. (1973) Ecological and behavioral determinants of pollen dispersal in hummingbird-pollinated Heliconia. The American Naturalist, 107, 511-523.
35. Maglianesi, M.A., Böhning-Gaese, K. & Schleuning, M. (2015) Data from "Different foraging preferences of hummingbirds on artificial and natural flowers reveal mechanisms structuring plant-pollinator interactions". Data & Metadata Repository, http://dx.doi.org/10.12761/SGN.2014.4.
36. Maglianesi, M.A., Blüthgen, N., Böhning-Gaese, K. & Schleuning, M. (2014) Morphological traits determine specialization and resource use in plant-hummingbird networks in the Neotropics. Ecology, doi:10.1890/13-2261.1.
37. Maruyama, P.K., Oliveira, G.M., Ferreira, C., Dalsgaard, B. & Oliveira, P.E. (2013) Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds. Naturwissenschaften, 100, 1061-1068.
38. McDade, L.A. (2004) Nectar in Hummingbird-pollinated Neotropical Plants I: patterns of Production and Variability in 12 Species. Biotropica, 36, 196-215.
39. Moran, C. & Catterall, C.P. (2010) Can functional traits predict ecological interactions? A case study using rain forest frugivores and plants in Australia. Biotropica, 42, 318-326.
40. Ollerton, J., Alarcón, R., Waser, N.M., Price, M.V., Watts, S., Cranmer, L. et al. (2009) A global test of the pollination syndrome hypothesis. Annals of Botany, 103, 1471-1480.
41. Ornelas, J.F., Ordano, M., De-Nova, A.J., Quintero, M.E. & Garland, T. Jr (2007) Phylogenetic analysis of interspecific variation in néctar of hummingbird-visited plants. Journal of Evolutionary Biology, 20, 1904-1917.
42. Paton, D.C. & Collins, B.G. (1989) Bills and tongues of nectar-feeding birds: a review of morphology, function and performance, with intercontinental comparisons. Australian Journal of Ecology, 14, 473-506.
43. Pauw, A. (2013) Can pollination niches facilitate plant coexistence? Trends in Ecology and Evolution, 28, 30-37.
44. Peterson, C.H. & Renaud, P.E. (1989) Analysis of feeding preference experiments. Oecologia, 80, 82-86.
45. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
46. Ralph, C.J., Geupel, G.R., Pyle, P., Martin, T. & DeSante, D.F. (1993) Handbook of Field Methods for Monitoring Landbirds. Pacific Southwest Research Station, Albany, California, USA.
47. Robertson, A.W., Kelly, D., Ladley, J.J. & Sparrow, A.D. (1999) Effects of pollinator loss on endemic New Zealand mistletoes (Loranthaceae). Conservation Biology, 13, 499-508.
48. Rodríguez-Flores, C.I. & Stiles, F.G. (2005) Análisis ecomorfológico de una comunidad de colibríes ermitaños (Trochilidae, Phaethorninae) y sus flores en la Amazonia Colombiana. Ornitología Colombiana, 3, 7-27.
49. Snow, B.K. & Snow, D.W. (1972) Feeding niches of hummingbirds in a Trinidad valley. Journal of Animal Ecology, 41, 471-485.
50. Stang, M., Klinkhamer, P.G.L. & van der Meijden, E. (2006) Size constraints and flower abundance determine the number of interactions in a plant-flower visitor web. Oikos, 112, 111-121.
51. Stiles, F.G. (1975) Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species. Ecology, 56, 285-301.
52. Stiles, F.G. (1978) Ecological and Evolutionary Implications of Bird Pollination. American Zoologist, 8, 715-727.
53. Stiles, F.G. (1981) Geographical aspects of Bird-flower coevolution, with particular reference to Central America. Annals of the Missouri Botanical Garden, 68, 323-351.
54. Stiles, F.G. (2004) Phylogenetic constraints upon morphological and ecological adaptation in hummingbirds (Trochilidae): why are there no hermits in the paramo? Ornitología Neotropical, 15, 191-198.
55. Stiles, F.G. & Skutch, A. (1989) A Guide to the Birds of Costa Rica. Comstock Publishing Associates, A division of Cornell University Press, Ithaca, New York, USA.
56. TEAM (2013) Tropical Ecology Assessment and Monitoring Network. Volcán Barba, Heredia.
57. Temeles, E.J., Miller, J.S. & Rifkin, J.L. (2010) Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): a role for ecological causation. Philosophical Transactions of the Royal Society, 365, 1053-1063.
58. Temeles, E.J., Linhart, Y.B., Masonjones, M. & Masonjones, H.D. (2002) The role of flower width in hummingbird bill length-flower length relationships. Biotropica, 34, 68-80.
59. Temeles, E.J., Koulouris, C.R., Sander, S.E. & Kress, W.J. (2009) Effect of flower shape and size on foraging performance and trade-offs in a tropical hummingbird. Ecology, 90, 1147-1161.
60. Tur, C., Vigalondo, B., Trøjelsgaard, K., Olesen, J.M. & Traveset, A. (2014) Downscaling pollen-transport networks to the level of individuals. Journal of Animal Ecology, 83, 306-317.
61. Vizentin-Bugoni, J., Maruyama, P.K. & Sazima, M. (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proceedings of the Royal Society B, 281, 1-8.
62. Wiklund, C., Eriksson, T. & Lundberg, H. (1979) The wood white butterfly, Leptidea sinapsis, and its nectar plants: a case of mutualism or parasitism? Oikos, 33, 358-362.
63. Williams, P. (2005) Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biological Conservation, 122, 33-43.
64. Wolf, L.L. & Stiles, F.G. (1989) Adaptations for the 'fail-safe' pollination of specialized ornithophilous flowers. American Midland Naturalist, 121, 1-10.
65. Wolf, L.L., Stiles, F.G. & Hainsworth, F.R. (1976) Ecological organization of a highland tropical hummingbird community. Journal of Animal Ecology, 45, 349-379.