Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-11T01:43:19.813Z Has data issue: false hasContentIssue false
  • English
  • Français

Pollination syndromes and interaction networks in hummingbird assemblages in El Triunfo Biosphere Reserve, Chiapas, Mexico

Published online by Cambridge University Press:  30 July 2018

Ruth Partida-Lara ,
Paula L. Enríquez ,
José Raúl Vázquez-Pérez ,
Esteban Pineda-Diez de Bonilla ,
Miguel Martínez-Ico  and
José L. Rangel-Salazar
Ruth Partida-Lara
Affiliation:
Programa de Posgrado en Ecología y Desarrollo Sustentable, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, 29290, San Cristóbal de las Casas, Chiapas, México
Paula L. Enríquez*
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, 29290, San Cristóbal de las Casas, Chiapas, México Centro de Investigaciones Biológicas del Noroeste. Av. Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, 23096 La Paz, Baja California Sur, México
José Raúl Vázquez-Pérez
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, 29290, San Cristóbal de las Casas, Chiapas, México
Esteban Pineda-Diez de Bonilla
Affiliation:
Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas, 1 Sur Poniente No. 1460, Col. Centro, 29000, Tuxtla Gutiérrez, Chiapas, México
Miguel Martínez-Ico
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, 29290, San Cristóbal de las Casas, Chiapas, México
José L. Rangel-Salazar
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, Barrio de María Auxiliadora, 29290, San Cristóbal de las Casas, Chiapas, México
*
*Corresponding author. Email: penrique@ecosur.mx
Get access Rights & Permissions [Opens in a new window]

Abstract:

Plant–animal mutualistic interactions through ecological network systems and the environmental conditions in which they occur, allow us to understand patterns of species composition and the structure and dynamics of communities. We evaluated whether flower morphologies with different pollination syndromes (ornithophilous and non-ornithophilous) are used by hummingbirds and whether these characteristics affect the structure (core-peripheral species) of hummingbird networks. Observations were made in flowering patches, where plant–hummingbird interactions were recorded at three altitudes (300–2500 m) during three seasons (dry, rainy and post-rainy) from 2015 to 2016 at El Triunfo Biosphere Reserve, Chiapas, Mexico. We recorded 15 hummingbird species interacting with 58 plant species, and the greatest number of interacting hummingbird species (11; 14) and plant species (28; 40) were found at middle altitudes and during the dry season, respectively. In all study sites, most of the plant species visited by hummingbirds had an ornithophilous syndrome (67%) at high altitudes (22 plant species) and during the dry season (26 plant species), but more individual hummingbirds visited non-ornithophilous plant species. The hummingbird species at high altitudes exhibited the greatest level of specialization towards plants (H2′ = 0.74), but the networks of plant-hummingbird interactions were generalist (H2′ = 0.25); i.e. visiting plants with both syndromes, at low altitudes. The core generalist hummingbird species remained constant with altitude and season, but the core generalist plant species varied between different altitudes and seasons according to the phenology of the species.

Keywords

altitudecore speciesmutualismnon-ornithophilous plantsperipheral speciesplant–animal interactionspecialization
Type
Research Article
Information
Journal of Tropical Ecology , Volume 34 , Issue 5 , September 2018 , pp. 293 - 307
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ABRAHAMCZYK, S. & KESSLER, M. 2010. Hummingbird diversity, food niche characters, and assemblage composition along a latitudinal precipitation gradient in the Bolivian lowlands. Journal of Ornithology 151:615–625.Google Scholar
AIZEN, M. A. 2003. Down-facing flowers, hummingbirds and rain. Taxon 52:675–680.Google Scholar
AIZEN, M. A. & EZCURRA, C. 1998. High incidence of plant-animal mutualisms in the woody flora of the temperate forest of southern South America: biogeographical origin and present ecological significance. Ecología Austral 8:217–236.Google Scholar
ARAUJO, A. C. & SAZIMA, M. 2003. The assemblage of flowers visited by hummingbirds in the “capões” of Southern Pantanal, Mato Grosso do Sul, Brazil. Flora 198:427–435.Google Scholar
ARIZMENDI, M. C. & ORNELAS, J. F. 1990. Hummingbirds and their floral resources in a tropical dry forest in Mexico. Biotropica 22:172–180.Google Scholar
ARMBRUSTER, W. S. 1992. Phylogeny and the evolution of plant-animal interactions. BioScience 42:12–20.Google Scholar
BASCOMPTE, J., JORDANO, P., MELIÁN, C. J. & OLESEN, J. M. 2003. The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences 100:9383–9387.Google Scholar
BASCOMPTE, J., JORDANO, P., & OLESEN, J. M. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312: 431–433.Google Scholar
BENADI, G., HOVESTADT, T., POETHKE, H. & BLÜTHGEN, N. 2014. Specialization and phenological synchrony of plant–pollinator interactions along an altitudinal gradient. Journal of Animal Ecology 83:639–650.Google Scholar
BENDER, I. M. A., KISSLING, W. D., BÖHNING-GAESE, K., HENSEN, I., KÜHN, I., WIEGAND, T., DEHLING, D. M. & SCHLEUNING, M. 2017. Functionally specialized birds respond flexibly to seasonal changes in fruit availability. Journal of Animal Ecology 86:800–811.Google Scholar
BLEIWEISS, R. 1998. Origin of hummingbird faunas. Biological Journal of the Linnean Society 65:77–97.Google Scholar
BLÜTHGEN, N. & KLEIN, A. M. 2011. Functional complementarity and specialization: The role of biodiversity in plant–pollinator interactions. Basic and Applied Ecology 12:282–291.Google Scholar
BLÜTHGEN, N., MENZEL, F. & BLÜTHGEN, N. 2006. Measuring specialization in species interaction networks. BMC Ecology 6:9.Google Scholar
BOBERG, E., ALEXANDERSSON, R., JONSSON, M., MAAD, J., ÅGREN, J. & NILSSON, L. A. 2014. Pollinator shifts and the evolution of spur length in the moth-pollinated orchid Platanthera bifolia. Annals of Botany 113:267–275.Google Scholar
BRUNEAU, A. 1997. Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae). American Journal of Botany 84:54–71.Google Scholar
BUZATO, S. 2000. Hummingbird-pollinated floras at three Atlantic forest sites. Biotropica 32:824–841.Google Scholar
COTTON, P. A. 2007. Seasonal resource tracking by Amazonian hummingbirds. Ibis 149:135–142.Google Scholar
CRONK, Q. & OJEDA, I. 2008. Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59:715–727.Google Scholar
CRUDEN, R. W. 1972. Pollinators in high-elevation ecosystems: relative effectiveness of birds and bees. Science 176:1439–1440.Google Scholar
CSERMELY, P., LONDON, A., WU, L.-Y. & UZZI, B. 2013. Structure and dynamics of core/periphery networks. Journal of Complex Networks 1:93–123.Google Scholar
DALSGAARD, B., MARTÍN GONZÁLEZ, A. M., OLESEN, J. M., 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 159:757–766.Google Scholar
DALSGAARD, B., MAGÅRD, E., FJELDSÅ, J., MARTÍN GONZÁLEZ, A. M., RAHBEK, C., OLESEN, J. M., OLLERTON, J., ALARCÓN, R., ARAUJO, A. C., COTTON, P. A., LARA, C., MACHADO, C. G., SAZIMA, I., SAZIMA, M., TIMMERMANN, A., WATTS, S., SANDEL, B., SUTHERLAND, W. J. & SVENNING, J. C. 2011. Specialization in plant-hummingbird networks is associated with species richness, contemporary precipitation and quaternary climate-change velocity. PLoS ONE 6 (10): e25891.Google Scholar
DÃTTILO, W., GUIMARÃES, P. R. & IZZO, T. J. 2013. Spatial structure of ant-plant mutualistic networks. Oikos 122:1643–1648.Google Scholar
DEL HOYO, J., COLLAR, N. J., CHRISTIE, D. A., ELLIOTT, A. & FISHPOOL, L. D. C. 2014. Handbook of the birds of the world and BirdLife International Checklist of the Birds of the World. Volume 1: Non-passerines. Lynx Edicions, Barcelona and BirdLife International, Cambridge. 904 pp.Google Scholar
DUPONT, Y. L., HANSEN, D. M. & OLESEN, J. M. 2003. Structure of a plant-flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography 26:301–310.Google Scholar
ELZINGA, J. A., ATLAN, A., BIERE, A., GIGORD, L., WEIS, A. E. & BERNASCONI, G. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology and Evolution 22:432–439.Google Scholar
FAEGRI, K. & VAN DER PIJL, L. 1979. The principles of pollination ecology. Pergamon Press, Oxford. 244 pp.Google Scholar
GRAHAM, C. H., PARRA, J. L., RAHBEK, C. & MCGUIRE, J. A. 2009. Phylogenetic structure in tropical hummingbird communities. Proceedings of the National Academy of Sciences USA 17:19673–19678.Google Scholar
GUIMARÃES, P. R., JORDANO, P. & THOMPSON, J. N. 2011. Evolution and coevolution in mutualistic networks. Ecology Letters 14:877–885.Google Scholar
HERRERA, C. M. 1988. Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35:95–125.Google Scholar
HOWELL, S. N. G. & WEBB, S. 1995. A guide to the birds of Mexico and northern Central America. Oxford University Press, New York. 851 pp.Google Scholar
JORDANO, P., BASCOMPTE, J. & OLESEN, J. M. 2003. Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6:69–81.Google Scholar
JUNKER, R. R., BLÜTHGEN, N., BREHM, T., BINKENSTEIN, J., PAULUS, J., SCHAEFER, H. M. & STANG, M. 2013. Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology 27:329–341.Google Scholar
KESSLER, D., DIEZEL, C., & BALDWIN, I. T. 2010. Changing pollinators as a means of escaping herbivores. Current Biology 20:237–242.Google Scholar
LANGE, D., DÃTTILO, W. & DEL-CLARO, K. 2013. Influence of extrafloral nectary phenology on ant–plant mutualistic networks in a neotropical savanna. Ecological Entomology 38:463–469.Google Scholar
MAGLIANESI, A. M., BLÜTHGEN, N., BÖHNING-GAESE, K. & SCHLEUNING, M. 2014. Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics. Ecology 95:3325–3334.Google Scholar
MAGLIANESI, M. A., BLÜTHGEN, N., BÖHNING-GAESE, K. & SCHLEUNING, M. 2015. Functional structure and specialization in three tropical plant–hummingbird interaction networks across an elevational gradient in Costa Rica. Ecography 38:001–010.Google Scholar
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.Google Scholar
MARTÍN GONZÁLEZ, A. M., DALSGAARD, B., NOGUÉS-BRAVO, D., GRAHAM, C. H., SCHLEUNING, M., MARUYAMA, P. K., ABRAHAMCZYK, S., ALARCÓN, R., ARAUJO, A. C., ARAÚJO, F. P., AZEVEDO, S. M., BAQUERO, A. C., COTTON, P. A., INGVERSEN, T. T., KOHLER, G., LARA, C., GUEDES LAS-CASAS, F. M., MACHADO, A. O., MACHADO, C. G., MAGLIANESI, M. A., MCGUIRE, J. A., MOURA, A. C., OLIVEIRA, G. M., OLIVEIRA, P. E., ORNELAS, J. F., DA CRUZ RODRIGUES, L., ROSERO-LASPRILLA, L., RUI, A. M., SAZIMA, M., TIMMERMANN, A., VARASSIN, I. G., VIZENTIN-BUGONI, J., WANG, Z., WATTS, S., RAHBEK, C. & MARTINEZ, N. D. 2015. The macroecology of phylogenetically structured hummingbird–plant networks. Global Ecology and Biogeography 24:1212–1224.Google Scholar
OLESEN, S. M. & JORDANO, P. 2002. Geographic patterns in plant–pollinator mutualistic networks. Ecology 83:2416–2424.Google Scholar
OLESEN, J. M., STEFANESCU, C. & TRAVESET, A. 2011. Strong, long-term temporal dynamics of an ecological network. PLoS ONE 6 (11): e26455. doi: 10.1371/journal.pone.0026455.Google Scholar
PARTIDA-LARA, R. ENRIQUEZ, P.L., VÁZQUEZ PÉREZ, J.R. & PINEDA DIEZ DE BONILLA, E. 2018. Estructura espacio-temporal de la diversidad taxonómica y funcional de colibríes en la Reserva de la Biosfera El Triunfo, Chiapas, México. Ornitología Neotropical 28:37–50.Google Scholar
RICO-GRAY, V., DÍAZ-CASTELAZO, C., RAMÍREZ-HERNÁNDEZ, A., GUIMARÃES, P. R. Jr. & HOLLAND, J. N. 2012. Abiotic factors shape temporal variation in the structure of an ant–plant network. Arthropod-Plant Interactions 6:289–295.Google Scholar
STANG, M., KLINKHAMER, P.G. & VAN DER MEIJDEN, E. 2007. Asymmetric specialization and extinction risk in plant flower visitor webs: a matter of morphology or abundance? Oecologia 151:442–453.Google Scholar
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.Google Scholar
STILES, F.G. 2008. Ecomorphology and phylogeny of hummingbirds: divergence and convergence in adaptations to high elevations. Ornitología Neotropical 19:511–519.Google Scholar
STROUP, W. W. 2013. Generalized linear mixed models, modern concepts, methods and application. CRC Press, New York. 555 pp.Google Scholar
VÁZQUEZ, D. P., MELIÁN, C. J., WILLIAMS, N. M., BLÜTHGEN, N., KRASNOV, B. R. & POULIN, R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127.Google Scholar
VÁZQUEZ, D. P., BLÜTHGEN, N., CAGNOLO, L. & CHACOFF, N. P. 2009. Uniting pattern and process in plant–animal mutualistic networks: a review. Annals of Botany 103:1445–1457.Google Scholar
WASER, N. M., CHITTKA, L., PRICE, M. V., WILLIAMS, N. M. & OLLERTON, J. 1996. Generalization in pollination systems, and why it matters. Ecology 77:1043–1060.Google Scholar