Functional role of the invasive European Starling, Sturnus vulgaris, in Argentina
Facundo X. Palacio A D , René E. Maragliano B and Diego Montalti CA Unidad Ejecutora Lillo-CONICET, Fundación Miguel Lillo, Miguel Lillo 251, T4000JFE-San Miguel de Tucumán, Tucumán, Argentina.
B Instituto de Formación Docente y Técnica N° 35, Amat 279, B1842, Monte Grande, Buenos Aires, Argentina.
C Sección Ornitología, División Zoología Vertebrados, Facultad de Ciencias Naturales y Museo-CONICET, Paseo del Bosque s/n, B1900FWA–La Plata, Buenos Aires, Argentina.
D Corresponding author. Email: facundo_palacio@yahoo.com.ar
Emu 116(4) 387-393 https://doi.org/10.1071/MU16021
Submitted: 3 November 2015 Accepted: 3 June 2016 Published: 12 July 2016
Abstract
The introduction of exotic species may have severe effects on native ecosystems by disrupting communities and ecosystem services. Consequently, assessing the functional role of a species newly added to a community is an important task in order to identify native species at risk. In Argentina, the ecology of the invasive European Starling (Sturnus vulgaris) is poorly known and studies addressing its ecological role in bird communities are still lacking. We assessed the functional role of the European Starling by sampling bird communities across four vegetation types (Solanum grassland, Cynodon grassland, flood plain and forest patches) and making comparisons of body mass, and dietary and foraging traits of European Starling with native and other introduced bird species in east-central Argentina. The European Starling was functionally most similar to two widespread, generalist native passerines – the Bay-winged Cowbird (Agelaioides badius) and the Chalk-browed Mockingbird (Mimus saturninus) – and to the invasive House Sparrow (Passer domesticus), which together defined a functional group of terrestrial and foliage omnivores. European Starlings were more abundant in Solanum grasslands than in other vegetation types and showed significant vegetation-type overlap with functionally similar species. Moreover, abundance of European Starlings was positively correlated with bird abundance and diversity. Our results identify native species that are functionally equivalent to European Starlings, and, consequently, potentially subject to ecological impacts.
Additional keywords: biodiversity, competition, foraging, invasive species.
References
Bates, D., Maechler, M., Bolker, B., and Walker, S. (2015). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–8. Available at http://CRAN.R-project.org/package=lme4 [Verified 3 March 2016].Beissinger, S. R., and Osborne, D. R. (1982). Effects of urbanization on avian community organization. The Condor 84, 75–83.
| Effects of urbanization on avian community organization.Crossref | GoogleScholarGoogle Scholar |
Beveridge, F. M., and Deag, J. M. (1987). The effects of sex, temperature and companions on looking up and feeding in single and mixed species flocks of House Sparrows (Passer domesticus), Chaffinches (Fringila coelebs), and Starlings (Sturnus vulgaris). Behaviour 100, 303–319.
| The effects of sex, temperature and companions on looking up and feeding in single and mixed species flocks of House Sparrows (Passer domesticus), Chaffinches (Fringila coelebs), and Starlings (Sturnus vulgaris).Crossref | GoogleScholarGoogle Scholar |
Blackburn, T. M., Lockwood, J. L., and Cassey, P. (2009). ‘Avian Invasions. The Ecology and Evolution of Exotic Birds.’ (Oxford University Press: Oxford.)
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., and White, J. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.
| Generalized linear mixed models: a practical guide for ecology and evolution.Crossref | GoogleScholarGoogle Scholar |
Clergeau, P., and Quenot, F. (2007). Roost selection flexibility of European starlings aids invasion of urban landscape. Landscape and Urban Planning 80, 56–62.
| Roost selection flexibility of European starlings aids invasion of urban landscape.Crossref | GoogleScholarGoogle Scholar |
Cueto, V. R., and López de Casenave, J. (2000). Seasonal changes in bird assemblages of coastal woodlands in east-central Argentina. Studies on Neotropical Fauna and Environment 35, 173–177.
| Seasonal changes in bird assemblages of coastal woodlands in east-central Argentina.Crossref | GoogleScholarGoogle Scholar |
Dame, E. A., Eth, K., and En, P. (2006). Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Animal Behaviour 71, 1165–1173.
| Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus).Crossref | GoogleScholarGoogle Scholar |
De Cáceres, M., Sol, D., Lapiedra, O., and Legendre, P. (2011). A framework for estimating niche metrics using the resemblance between qualitative resources. Oikos 120, 1341–1350.
| A framework for estimating niche metrics using the resemblance between qualitative resources.Crossref | GoogleScholarGoogle Scholar |
Dehling, D. M., Jordano, P., Schaefer, H. M., Böhning-Gaese, K., and Schleuning, M. (2016). Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. Proceedings. Biological Sciences 283, 20152444.
| Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions.Crossref | GoogleScholarGoogle Scholar |
del Hoyo, J., Elliott, A., and Sargatal, J. (1992). ‘Handbook of the Birds of the World. Vol. 1: Ostrich to Ducks.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Sargatal, J. (1994). ‘Handbook of the Birds of the World. Vol. 2: New World Vultures to Guineafowl.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Sargatal, J. (1996). ‘Handbook of the Birds of the World. Vol. 3: Hoatzin to Auks.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Sargatal, J. (1997). ‘Handbook of the Birds of the World. Vol. 4: Sandgrouse to Cuckoos.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Sargatal, J. (1999). ‘Handbook of the Birds of the World. Vol. 5: Barn-owls to Hummingbirds.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Sargatal, J. (2002). ‘Handbook of the Birds of the World. Vol. 7: Jacamars to Woodpeckers.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2003). ‘Handbook of the Birds of the World. Vol. 8: Broadbills to Tapaculos.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2004). ‘Handbook of the Birds of the World. Vol. 9: Cotingas to Pipits and Wagtails.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2005). ‘Handbook of the Birds of the World. Vol. 10: Cuckoo-shrikes to Thrushes.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2006). ‘Handbook of the Birds of the World. Vol. 11: Old World Flycatchers to Old World Warblers.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2009). ‘Handbook of the Birds of the World. Vol. 14: Bush-shrikes to Old World Sparrows.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2010). ‘Handbook of the Birds of the World. Vol. 15: Weavers to New World Warblers.’ Lynx Edicions: Barcelona.
del Hoyo, J., Elliott, A., and Christie, D. (2011). ‘Handbook of the Birds of the World. Vol. 16: Tanagers to New World Blackbirds.’ Lynx Edicions: Barcelona.
Devereux, C. L., McKeever, C. U., Benton, T. G., and Whittingham, M. J. (2004). The effect of sward height and drainage on Common Starlings Sturnus vulgaris and Northern Lapwings Vanellus vanellus foraging in grassland habitats. The Ibis 146, 115–122.
| The effect of sward height and drainage on Common Starlings Sturnus vulgaris and Northern Lapwings Vanellus vanellus foraging in grassland habitats.Crossref | GoogleScholarGoogle Scholar |
Devictor, D. V., Julliard, R., Clavel, J., Jiguet, F., Lee, A., and Couvet, D. (2008). Functional biotic homogenization of bird communities in disturbed landscapes. Global Ecology and Biogeography 17, 252–261.
| Functional biotic homogenization of bird communities in disturbed landscapes.Crossref | GoogleScholarGoogle Scholar |
Dunning, J. B. (2008). ‘CRC Handbook of Avian Body Masses.’ (CRC Press: Boca Raton, FL.)
Elton, C. (1958). ‘The Ecology of Invasions by Animals and Plants.’ (Methuen: London.)
Feare, C. (1984). ‘The Starling.’ (Oxford University Press: Oxford.)
Fischl, J., and Caccamise, D. F. (1985). Influence of habitat and season on foraging flock composition in the European Starling (Sturnus vulgaris). Oecologia 67, 532–539.
| Influence of habitat and season on foraging flock composition in the European Starling (Sturnus vulgaris).Crossref | GoogleScholarGoogle Scholar |
Freed, L. A., and Cann, R. L. (2009). Negative effects of an introduced bird species on growth and survival in a native bird community. Current Biology 19, 1736–1740.
| Negative effects of an introduced bird species on growth and survival in a native bird community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCrsrvL&md5=fcd743385d3b0b5fec4b13a62f378f80CAS | 19765990PubMed |
Freed, L. A., Cann, R. L., and Bodner, G. R. (2008). Incipient extinction of a major population of the Hawaii akepa owing to introduced species. Evolutionary Ecology Research 10, 931–965.
Gavareski, C. A. (1976). Relation of park size and vegetation to urban bird populations in Seattle, Washington. The Condor 78, 375–382.
| Relation of park size and vegetation to urban bird populations in Seattle, Washington.Crossref | GoogleScholarGoogle Scholar |
Gavett, A. P., and Wakeley, J. S. (1986). Diets of House Sparrows in urban and rural habitats. The Wilson Bulletin 98, 137–144.
Girini, J. M., Palacio, F. X., del Huerto, M. C., and Kuzmanich, N. (2014). Selección de dormideros por el Estornino Pinto (Sturnus vulgaris) en La Plata, Buenos Aires, Argentina. Hornero 29, 23–28.
Gitay, H., Wilson, J. B., and Lee, W. G. (1996). Species redundancy: a redundant concept? Journal of Ecology 84, 121–124.
| Species redundancy: a redundant concept?Crossref | GoogleScholarGoogle Scholar |
Gowaty, P. A. (1984). House Sparrows kill Eastern Bluebirds. Journal of Field Ornithology 55, 378–380.
Gower, J. C. (1971). A general coefficient of similarity and some of its properties. Biometrics 27, 857–874.
| A general coefficient of similarity and some of its properties.Crossref | GoogleScholarGoogle Scholar |
Hidasi-Neto, J., Barlow, J., and Cianciaruso, M. V. (2012). Bird functional diversity and wildfires in the Amazon: the role of forest structure. Animal Conservation 15, 407–415.
| Bird functional diversity and wildfires in the Amazon: the role of forest structure.Crossref | GoogleScholarGoogle Scholar |
Hill, M. O. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.
| Diversity and evenness: a unifying notation and its consequences.Crossref | GoogleScholarGoogle Scholar |
Horlent, N., Juárez, M. C., and Arturi, M. (2003). Incidencia de la estructura del paisaje sobre la composición de especies de aves de los talares del noreste de la provincia de Buenos Aires. Ecología Austral 13, 173–182.
Ibañez, L. M. (2015). Invasión del Estornino Pinto Sturnus vulgaris en el Noreste de la provincia de Buenos Aires: análisis de la competencia con aves nativas y potencialidad como transmisor de parásitos. Ph.D. Thesis, Universidad Nacional de La Plata, La Plata, Argentina.
Ifran, N. R., and Fiorini, V. D. (2010). European Starling (Sturnus vulgaris): population density and interactions with native species in Buenos Aires parks. Ornitologia Neotropical 21, 507–518.
Ingold, D. J. (1994). Influence of nest-site competition between European Starlings and woodpeckers. The Wilson Bulletin 106, 227–241.
Ingold, D. J. (1996). Delayed nesting decreases reproductive success in Northern Flickers: implications for competition with European Starlings. Journal of Field Ornithology 67, 321–326.
Kark, S., Iwaniuk, A., Schalaimtzek, A., and Banjer, E. (2007). Living in the city: can anyone become an ‘urban exploiter’? Journal of Biogeography 34, 638–651.
| Living in the city: can anyone become an ‘urban exploiter’?Crossref | GoogleScholarGoogle Scholar |
Kerpez, T. A., and Smith, N. S. (1990). Competition between European starlings and native woodpeckers for nest cavities in saguaros. The Auk 107, 367–375.
| Competition between European starlings and native woodpeckers for nest cavities in saguaros.Crossref | GoogleScholarGoogle Scholar |
Kiesecker, J. M., Blaustein, A. R., Miller, C. L., Iesecker, J. O. M. K., and Laustein, A. N. R. B. (2001). Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82, 1964–1970.
| Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs.Crossref | GoogleScholarGoogle Scholar |
Koenig, W. D. (2003). European starlings and their effect on native cavity-nesting birds. Conservation Biology 17, 1134–1140.
| European starlings and their effect on native cavity-nesting birds.Crossref | GoogleScholarGoogle Scholar |
Kruskal, J. B., and Wish, M. (1978). ‘Multidimensional Scaling.’ (Sage Publications: Sage, CA.)
Loiselle, B. A., Blendinger, P. G., Blake, J. G., and Ryder, T. B. (2007). Ecological redundancy in seed dispersal systems: a comparison between Manakins (Aves: Pipridae) in two tropical forests. In ‘Frugivory and Seed Dispersal: Theory and Applications in a Changing World’. (Eds A. J. Dennis, E. W. Schupp, R. Green, and D. Westcott.) pp. 178–195. (CAB International: Wallingford, UK.)
Lowe, S., Browne, M., Boudjelas, S., and De Poorter, M. (2000). ‘100 of the World’s Worst Invasive Alien Species: a Selection from the Global Invasive Species Database.’ (The Invasive Specialist Group: Auckland.)
Maragliano, R. E., Marti, L. J., Ibañez, L. M., and Montalti, D. (2009). Comunidades de aves urbanas de Lavallol, Buenos Aires, Argentina. Acta Zoológica Lilloana 53, 108–114.
Martín-Albarracín, V. L., Amico, G. C., Simberloff, D., and Nuñez, M. A. (2015). Impact of non-native birds on native ecosystems: a global analysis. PLoS One 10, e0143070.
| Impact of non-native birds on native ecosystems: a global analysis.Crossref | GoogleScholarGoogle Scholar | 26576053PubMed |
Mazzulla, J. (2013). Primeros registros de estornino pinto Sturnus vulgaris (Linnaeus 1758) (Aves, Passeriformes, Sturnidae) en Uruguay. Novedades Ornitológicas 3, 13–17.
Milsom, T. P., Hart, J. D., Parkin, W. K., and Peel, S. (2002). Management of coastal grazing marshes for breeding waders: the importance of surface topography and wetness. Biological Conservation 103, 199–207.
| Management of coastal grazing marshes for breeding waders: the importance of surface topography and wetness.Crossref | GoogleScholarGoogle Scholar |
Montalti, D., and Kopij, G. (2001). Bird community of inner La Plata city, Argentina. Acta Ornithologica 36, 161–164.
| Bird community of inner La Plata city, Argentina.Crossref | GoogleScholarGoogle Scholar |
Mooney, H. A., and Cleland, E. E. (2001). The evolutionary impacts of invasive species. Proceedings of the National Academy of Sciences of the United States of America 98, 5446–5451.
| The evolutionary impacts of invasive species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Wgurw%3D&md5=4727f82a7a6d183904483e5f6437dcf1CAS | 11344292PubMed |
Morisita, M. (1959). Measuring of the dispersion and analysis of distribution patterns. Memories of the Faculty of Science, Kyushu University, Series E. Biology (Basel) 2, 215–235.
Oksanen, J., Blanchett, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H. (2015). vegan: community ecology package. R package version 2.3–0. Available at http://CRAN.R-project.org/package=vegan [Verified 3 March 2016].
Olden, J. D., and Rooney, T. P. (2006). On defining and quantifying biotic homogenization. Global Ecology and Biogeography 15, 113–120.
| On defining and quantifying biotic homogenization.Crossref | GoogleScholarGoogle Scholar |
Ortega-Álvarez, R., and MacGregor-Fors, I. (2009). Living in the big city: effects of urban land-use on bird community structure, diversity, and composition. Landscape and Urban Planning 90, 189–195.
| Living in the big city: effects of urban land-use on bird community structure, diversity, and composition.Crossref | GoogleScholarGoogle Scholar |
Palacio, F. X., and Montalti, D. (2013). Seasonal variation and effect of non-native invasive vegetation on two bird communities in northeast of Buenos Aires province, Argentina. Ornitologia Neotropical 24, 157–168.
Parker, I. M., Simberloff, D., Lonsdale, W. M., Goodell, K., Wonham, M., Kareiva, P. M., Williamson, M. H., Von Holle, B., Moyle, P. B., Byers, J. E., and Goldwasser, L. (1999). Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1, 3–19.
| Impact: toward a framework for understanding the ecological effects of invaders.Crossref | GoogleScholarGoogle Scholar |
Peck, H. L., Pringle, H. E., Marshall, H. H., Owens, I. P. F., and Lord, A. M. (2014). Experimental evidence of impacts of an invasive parakeet on foraging behavior of native birds. Behavioral Ecology 25, 582–590.
| Experimental evidence of impacts of an invasive parakeet on foraging behavior of native birds.Crossref | GoogleScholarGoogle Scholar | 24822022PubMed |
Pell, A. S., and Tidemann, C. R. (1997). The impact of two exotic hollow-nesting birds on two native parrots in savannah and woodland in eastern Australia. Biological Conservation 79, 145–153.
| The impact of two exotic hollow-nesting birds on two native parrots in savannah and woodland in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Peris, S. A., Soave, G. E., Camperi, A. R., Darrieu, C. A., and Aramburu, R. M. (2005). Range expansion of the European Starling Sturnus vulgaris in Argentina. Ardeola 52, 359–364.
Petchey, O. L., Evans, K. L., Fishburn, I. S., and Gaston, K. J. (2007). Low functional diversity and no redundancy in British avian assemblages. Journal of Animal Ecology 76, 977–985.
| Low functional diversity and no redundancy in British avian assemblages.Crossref | GoogleScholarGoogle Scholar | 17714276PubMed |
Pimentel, D., Lach, L., Zuniga, R., and Morrison, D. (2000). Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65.
| Environmental and economic costs of nonindigenous species in the United States.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org [Verified 3 March 2016].
Remsen, J. V., Jr, Areta, J. I., Cadena, C. D., Jaramillo, A., Nores, M., Pacheco, J. F., Pérez-Emán, J., Robbins, M. B., Stiles, F. G., Stotz, D. F., and Zimmer, K. J. (2016). A classification of the bird species of South America. American Ornithologists’ Union. Available at http://www.museum.lsu.edu/~Remsen/SACCBaseline.htlm [Verified 9 June 2016].
Ridgely, R. S., and Tudor, G. (2009). ‘Field Guide to the Songbirds of South America: The Passerines.’ (University of Texas Press: Austin, TX.)
Sibley, D. A. (2001). ‘The Sibley Guide to Birds.’ (Alfred A. Knopf: New York.)
Skaug, H., Fournier, D., Bolker, B., Magnusson, A., and Nielsen, A. (2014). Generalized Linear Mixed Models using AD Model Builder. R package version 0.8.0. Available at http://glmmadmb.r-forge.r-project.org/ [Verified 3 March 2016].
Slater, P. (1994). Factors affecting the efficiency of the area search method of censusing birds in open forests and woodlands. Emu 94, 9–16.
| Factors affecting the efficiency of the area search method of censusing birds in open forests and woodlands.Crossref | GoogleScholarGoogle Scholar |
Stachowicz, J. J., and Byrnes, J. E. (2006). Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Marine Ecology Progress Series 311, 251–262.
| Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors.Crossref | GoogleScholarGoogle Scholar |
Vega, M. R. (2004). Fotografías curiosas y novedades de aves silvestres. Nuestras Aves 47, 10.
Walker, B. H. (1992). Biodiversity and ecological redundancy. Conservation Biology 6, 18–23.
| Biodiversity and ecological redundancy.Crossref | GoogleScholarGoogle Scholar |
Wauters, L., Tosi, G., Gurnell, J., and Martinoli, A. (2002). Interspecific competition between native Eurasian red squirrels and alien grey squirrels: does resource partitioning occur? Behavioral Ecology and Sociobiology 52, 332–341.
| Interspecific competition between native Eurasian red squirrels and alien grey squirrels: does resource partitioning occur?Crossref | GoogleScholarGoogle Scholar |
Williamson, P., and Gray, L. (1975). Foraging behavior of the Starling (Sturnus vulgaris) in Maryland. The Condor 77, 84–89.
| Foraging behavior of the Starling (Sturnus vulgaris) in Maryland.Crossref | GoogleScholarGoogle Scholar |
Zhang, J. (2013). spaa: SPecies Association Analysis. R package version 0.2.1. Available at: http://CRAN.R-project.org/package=spaa [Verified 3 March 2016].
Zuur, A., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M. (2009). ‘Mixed Effects Models and Extensions in Ecology with R.’ (Springer: New York.)