Frugivory and seed dispersal role of the Yellow-striped Brush-Finch (Atlapetes citrinellus), an endemic emberizid of Argentina
Román A. Ruggera A B D , M. Daniela Gomez A C and Pedro G. Blendinger A B
+ Author Affiliations
- Author Affiliations
A Consejo Nacional de Investigaciones Científicas y Técnicas, Crisóstomo Álvarez 722, 4000 San Miguel de Tucumán, Tucumán, Argentina.
B Instituto de Ecología Regional, Universidad Nacional de Tucumán, C.C. 34, 4107 Yerba Buena, Tucumán, Argentina.
C Facultad de Ciencias Agrarias, Universidad Nacional de Jujuy, Alberdi 47, 4600 San Salvador de Jujuy, Jujuy, Argentina.
D Corresponding author. Email: raruggera@yahoo.com.ar
Emu 114(4) 343-351 https://doi.org/10.1071/MU14033
Submitted: 25 July 2013 Accepted: 7 June 2014 Published: 19 September 2014
Abstract
The stability and dynamics of multispecies interactions often rely on a small core of species. We examine whether the Yellow-striped Brush-Finch (Atlapetes citrinellus), the only species of bird endemic to the Argentinean Yungas, is a core species for seed dispersal. Of 30 species of fleshy fruit consumed, 16 were dispersed through endozoochory. The Yellow-striped Brush-Finch mostly used the ‘cut or mash’ method of handling fruit, in which reasonably large seeds (>0.04 g) were discarded or swallowed equally. Medium-sized and small seeds were more often swallowed than discarded. Although the fruits consumed were mostly understorey species, there was no difference in the consumption of fruit from forest understorey or canopy when total fruit abundance in vertical strata was considered. By using interaction network metrics, we determined that the role of Yellow-striped Brush-Finches in seed dispersal during the rainy season was more important at higher altitudes and in the southern sector of its distribution. Our findings support the idea that the Yellow-striped Brush-Finch must be considered a core seed-disperser of understorey and canopy fruits. Use of network metrics is an effective way to assess the importance of individual species in a network, allowing restoration and conservation efforts to be focussed on environments in which these species occur.
Additional keywords: avian frugivory, fruit handling, mutualistic networks, network metrics, species strength, subtropical Andean forests.
References
Alarcón, R., Waser, N. M., and Ollerton, J. (2008). Year-to-year variation in the topology of a plant pollinator interaction network. Oikos 117, 1796–1807.| Year-to-year variation in the topology of a plant pollinator interaction network.Crossref | GoogleScholarGoogle Scholar |
Bascompte, J., and Jordano, P. (2006). The structure of plant–animal mutualistic networks. In ‘Ecological Networks: Linking Structure to Dynamics in Food Webs’. (Eds M. Pascual and J. Dunne.) pp. 143–159. (Oxford University Press: Oxford, UK.)
Bascompte, J., Jordano, P., Melián, C. J., and Olesen, J. M. (2003). The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100, 9383–9387.
| The nested assembly of plant–animal mutualistic networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtlyktLY%3D&md5=4aa01c218c04d8abcad5a91982178822CAS | 12881488PubMed |
Bascompte, J., Jordano, P., and Olesen, J. M. (2006). Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433.
| Asymmetric coevolutionary networks facilitate biodiversity maintenance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslSktb4%3D&md5=099a06b513477383aa508713d668a7eaCAS | 16627742PubMed |
Bastolla, U., Fortuna, M. A., Pascual-García, A., Ferrera, A., Luque, B., and Bascompte, J. (2009). The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020.
| The architecture of mutualistic networks minimizes competition and increases biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvFKhtL8%3D&md5=c76409052f71ed2d90a26ea8bf1ad15bCAS | 19396144PubMed |
Blake, J. G., and Rougès, M. (1997). Variation in capture rates of understory birds in El Rey National Park, northwestern Argentina. Ornitologia Neotropical 8, 185–193.
Blake, J. G., Loiselle, B. A., Moermond, T., Levey, D. J., and Denslow, J. S. (1990). Quantifying abundance of fruits for birds in tropical habitats. Studies in Avian Biology 13, 73–79.
Blendinger, P. G., and Álvarez, M. E. (2009). Aves de la Selva Pedemontana de las Yungas australes. In ‘Selva Pedemontana de las Yungas. Historia Natural, Ecología y Manejo de un Ecosistema en Peligro’. (Eds A. D. Brown, P. G. Blendinger, T. Lomáscolo and P. García-Bes.) pp. 233–272. (Ediciones del Subtrópico: Yerba Buena, Argentina.)
Blendinger, P. G., and Villegas, M. (2011). Crop size is more important than neighborhood fruit availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers. Plant Ecology 212, 889–899.
| Crop size is more important than neighborhood fruit availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers.Crossref | GoogleScholarGoogle Scholar |
Blendinger, P. G., Blake, J. G., and Loiselle, B. A. (2011). Connecting fruit production to seedling establishment in two co-occurring Miconia species: consequences of seed dispersal by birds in upper Amazonia. Oecologia 167, 61–73.
| Connecting fruit production to seedling establishment in two co-occurring Miconia species: consequences of seed dispersal by birds in upper Amazonia.Crossref | GoogleScholarGoogle Scholar | 21400192PubMed |
Blendinger, P. G., Ruggera, R. A., Núñez Montellano, M. G., Macchi, L., Zelaya, P. V., Álvarez, M. E., Martín, E., Osinaga Acosta, O., Sánchez, R., and Haedo, J. (2012). Fine-tuning the fruit-tracking hypothesis: spatiotemporal links between fruit availability and fruit consumption by birds in an Andean mountain forest. Journal of Animal Ecology 81, 1298–1310.
| Fine-tuning the fruit-tracking hypothesis: spatiotemporal links between fruit availability and fruit consumption by birds in an Andean mountain forest.Crossref | GoogleScholarGoogle Scholar | 22742825PubMed |
Blüthgen, N., Fründ, J., Vázquez, D. P., and Menzel, F. (2008). What do interaction network metrics tell us about specialization and biological traits? Ecology 89, 3387–3399.
| What do interaction network metrics tell us about specialization and biological traits?Crossref | GoogleScholarGoogle Scholar | 19137945PubMed |
Brown, A. D., Grau, H. R., Malizia, L. R., and Grau, A. (2001). Argentina. In ‘Bosques Nublados del Neotrópico’. (Eds M. Kappelle and A. D. Brown.) pp. 623–659. (Editorial del Instituto Nacional de Biodiversidad (INBio): Santo Domingo de Heredia, Costa Rica.)
Burgos, E., Ceva, H., Perazzo, R. P. J., Devoto, M., Medán, D., Zimmermann, M., and Delbue, A. M. (2007). Why nestedness in mutualistic networks? Journal of Theoretical Biology 249, 307–313.
| Why nestedness in mutualistic networks?Crossref | GoogleScholarGoogle Scholar | 17897679PubMed |
Cabrera, A. L. (1976). Regiones fitogeográficas argentinas. In ‘Enciclopedia argentina de agricultura y jardinería’. (Ed. W. F. Kugler) Tomo 2, Fascículo 1, pp. 1–85. (Editorial Acme: Buenos Aires, Argentina.)
Carlo, T. A., and Morales, J. M. (2008). Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. Journal of Animal Ecology 96, 609–618.
| Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation.Crossref | GoogleScholarGoogle Scholar |
Chapman, C. A., and Chapman, L. J. (1995). Survival without dispersers: seedling recruitment under parents. Conservation Biology 9, 675–678.
| Survival without dispersers: seedling recruitment under parents.Crossref | GoogleScholarGoogle Scholar |
D’Avila, G., Gomez, A., Canary, A. C., and Bugoni, L. (2010). The role of avian frugivores on germination and potential seed dispersal of the Brazilian Pepper Schinus terebinthifolius. Biota Neotropica 10, 45–51.
| The role of avian frugivores on germination and potential seed dispersal of the Brazilian Pepper Schinus terebinthifolius.Crossref | GoogleScholarGoogle Scholar |
Donatti, C. I., Guimarães, P. R., Galetti, M., Pizo, M. A., Marquitti, F. M. D., and Dirzo, R. (2011). Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecology Letters 14, 773–781.
| Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms.Crossref | GoogleScholarGoogle Scholar | 21699640PubMed |
Fleming, T. H. (2005). The relationship between species richness of vertebrate mutualists and their food plants in tropical and subtropical communities differs among hemispheres. Oikos 111, 556–562.
| The relationship between species richness of vertebrate mutualists and their food plants in tropical and subtropical communities differs among hemispheres.Crossref | GoogleScholarGoogle Scholar |
Fortuna, M. A., and Bascompte, J. (2006). Habitat loss and the structure of plant–animal mutualistic networks. Ecology Letters 9, 281–286.
| Habitat loss and the structure of plant–animal mutualistic networks.Crossref | GoogleScholarGoogle Scholar | 16958893PubMed |
Foster, M. S. (1987). Feeding methods and efficiencies of selected frugivorous birds. Condor 89, 566–580.
| Feeding methods and efficiencies of selected frugivorous birds.Crossref | GoogleScholarGoogle Scholar |
Gentry, A. H. (1993). ‘A Field Guide to the Families and Genera of Woody Plants of Northwest South America.’ (University of Chicago Press: Chicago, IL.)
Giannini, N. P. (1999). La interacción de aves-murciélagos-plantas en el sistema de frugivoría y dispersión de semillas en San Javier, Tucumán, Argentina. Ph.D. Thesis, Universidad Nacional de Tucumán, Tucumán, Argentina.
Heleno, R. H., Ross, G., Everard, A., Memott, J., and Ramos, J. A. (2011). The role of the avian ‘seed predators’ as seed dispersers. Ibis 153, 199–203.
| The role of the avian ‘seed predators’ as seed dispersers.Crossref | GoogleScholarGoogle Scholar |
Herrera, C. M. (1995). Plant–vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annual Review of Ecology and Systematics 26, 705–727.
Hulme, P. E. (2002). Seed-eaters: seed dispersal, destruction and demography. In ‘Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation’. (Eds D. J. Levey, W. R. Silva and M. Galetti.) pp. 257–273. (CAB International: Cambridge, UK.).
Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forest. American Naturalist 104, 501–528.
| Herbivores and the number of tree species in tropical forest.Crossref | GoogleScholarGoogle Scholar |
Jordano, P. (1995). Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant–animal interactions. American Naturalist 145, 163–191.
| Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant–animal interactions.Crossref | GoogleScholarGoogle Scholar |
Jordano, P., and Schupp, E. W. (2000). Determinants of seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecological Monographs 70, 591–615.
| Determinants of seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb.Crossref | GoogleScholarGoogle Scholar |
Levey, D. J. (1987). Seed size and fruit-handling techniques of avian frugivores. American Naturalist 129, 471–485.
| Seed size and fruit-handling techniques of avian frugivores.Crossref | GoogleScholarGoogle Scholar |
Lewinsohn, T. M., Prado, P. I., Jordano, P., Bascompte, J., and Olesen, J. M. (2006). Structure in plant–animal interaction assemblages. Oikos 113, 174–184.
| Structure in plant–animal interaction assemblages.Crossref | GoogleScholarGoogle Scholar |
Loiselle, B. A., and Blake, J. G. (1990). Diets of understory fruit-eating birds in Costa Rica. Studies in Avian Biology 13, 91–103.
Loiselle, B. A., Blake, J. G., Blendinger, P. G., and Ryder, T. B. (2007). Ecological redundancy in seed dispersal systems: a comparison between manakins (Pipridae) in two tropical forests. In ‘Seed Dispersal and Frugivory: Ecology, Evolution and Conservation’. (Eds D. J. Levey, W. R. Silva and M. Galetti.) pp. 178–196. (CAB International: Cambridge, UK.)
Malizia, L. R. (2001). Seasonal fluctuation of birds, fruits and flowers in a subtropical forest of Argentina. Condor 103, 45–61.
| Seasonal fluctuation of birds, fruits and flowers in a subtropical forest of Argentina.Crossref | GoogleScholarGoogle Scholar |
Manhães, M. A. (2003). Dieta de traupíneos (Passeriformes, Emberizidae) no Parque Estadual do Ibitipoca, Mina Gerais, Brasil. Iheringia – Série Zoologia Porto Alegre 93, 59–73.
Martín González, A. M., Dalsgaard, B., and Olesen, J. M. (2010). Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity 7, 36–43.
| Centrality measures and the importance of generalist species in pollination networks.Crossref | GoogleScholarGoogle Scholar |
Mello, M. A. R., Bezerra, E. L. S., and Machado, I. C. (2013). Functional roles of Centridini oil bees and Malpighiaceae oil flowers in biome-wide pollination networks. Biotropica 45, 45–53.
| Functional roles of Centridini oil bees and Malpighiaceae oil flowers in biome-wide pollination networks.Crossref | GoogleScholarGoogle Scholar |
Murray, K. G. (2000). The importance of different bird species as seed dispersers. In ‘Monteverde: Ecology and Conservation of a Tropical Cloud Forest’. (Eds N. Nadakami and N. T. Wheelwright.) pp. 294–295. (Oxford University Press: New York.).
Olesen, J. M., Bascompte, J., Dupont, Y. L., and Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 104, 19 891–19 896.
| The modularity of pollination networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitFSqtw%3D%3D&md5=eb811bd32d9a23e0b5ad02b650f85d09CAS |
Olrog, C. C. (1984). ‘Las Aves Argentinas: Una Guía de Campo.’ (Administración de Parques Nacionales: Buenos Aires, Argentina.)
R Development Core Team (2011). R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org [Verified 1 August 2014].
Ridgely, R. S., and Tudor, G. (1989). ‘The Birds of South America. Vol. 1: The Oscine Passerines.’ (University of Texas Press: Austin, TX.)
Rougès, M. (2003). Bird community dynamics along an altitudinal gradient in subtropical montane forests. Ph.D. Thesis, University of Missouri-St Louis, St Louis.
Rougès, M., and Blake, J. G. (2001). Tasas de captura y dietas de aves del sotobosque en el parque biológico Sierra de San Javier, Tucumán. Hornero 16, 7–15.
Ruggera, R. A. (2013). Equivalencia ecológica en mutualismos de dispersión-frugivoría y su relación con la estructura y función de las comunidades en las Yungas australes. Ph.D. Thesis, Universidad Nacional de Tucumán, Tucumán, Argentina.
Santos, T., Tellería, J. S., and Virgós, E. (1999). Dispersal of Spanish Juniper Juniperus thurifera by birds and mammals in a fragmented landscape. Ecography 22, 193–204.
| Dispersal of Spanish Juniper Juniperus thurifera by birds and mammals in a fragmented landscape.Crossref | GoogleScholarGoogle Scholar |
Schleuning, M., Blüthgen, N., Flörchinger, M., Braun, J., Schaefer, M., and Böhning-Gaese, K. (2011). Specialization and interaction strength in a tropical plant–frugivore network differ among forest strata. Ecology 92, 26–36.
| Specialization and interaction strength in a tropical plant–frugivore network differ among forest strata.Crossref | GoogleScholarGoogle Scholar | 21560673PubMed |
Schupp, E. W., Jordano, P., and Gómez, J. M. (2010). Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333–353.
| Seed dispersal effectiveness revisited: a conceptual review.Crossref | GoogleScholarGoogle Scholar | 20673283PubMed |
Shanahan, M., and Compton, S. G. (2001). Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different? Plant Ecology 153, 121–132.
| Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different?Crossref | GoogleScholarGoogle Scholar |
Sheldon, K. S., and Nadkarni, N. M. (2013). Spatial and temporal variation of seed rain in the canopy and on the ground of a tropical cloud forest. Biotropica 45, 549–556.
| Spatial and temporal variation of seed rain in the canopy and on the ground of a tropical cloud forest.Crossref | GoogleScholarGoogle Scholar |
Silva, W. R., De Marco, P. Jr, Hasui, É., and Gomes, V. S. M. (2002). Patterns of fruit–frugivore interactions in two Atlantic forest bird communities of south-eastern Brazil: implications for conservation. In ‘Seed Dispersal and Frugivory: Ecology, Evolution and Conservation’. (Eds D. J. Levey, W. R. Silva and M. Galetti.) pp. 423–435. (CAB International: Cambridge, UK.)
Vázquez, D. P., Morris, W. F., and Jordano, P. (2005). Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8, 1088–1094.
| Interaction frequency as a surrogate for the total effect of animal mutualists on plants.Crossref | GoogleScholarGoogle Scholar |
Vázquez, D. P., Melián, C. J., Williams, N. M., Blüthgen, N., Krasnov, B. R., and Poulin, R. (2007). Species abundance and asymmetric interaction strength in ecological networks. Oikos 116, 1120–1127.
| Species abundance and asymmetric interaction strength in ecological networks.Crossref | GoogleScholarGoogle Scholar |
Vázquez, D. P., Chacoff, N. P., and Cagnolo, L. (2009). Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90, 2039–2046.
| Evaluating multiple determinants of the structure of plant–animal mutualistic networks.Crossref | GoogleScholarGoogle Scholar | 19739366PubMed |
Wenny, D. G., and Levey, D. J. (1998). Directed seed dispersal by Bellbirds in a tropical cloud forest. Proceedings of the National Academy of Sciences of the United States of America 95, 6204–6207.
| Directed seed dispersal by Bellbirds in a tropical cloud forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtlKntbY%3D&md5=4fbcb59415db585e72e8b1d9b699696fCAS | 9600942PubMed |
Wheelwright, N. T., and Orians, G. H. (1982). Seed dispersal by animals – contrasts with pollen dispersal, problems of terminology, and constraints on coevolution. American Naturalist 119, 402–413.
| Seed dispersal by animals – contrasts with pollen dispersal, problems of terminology, and constraints on coevolution.Crossref | GoogleScholarGoogle Scholar |