Local bird traits match fruit traits of two alien plants in urban fruit-frugivore interactions
DOI:
https://doi.org/10.25260/EA.23.33.1.0.1947Keywords:
seed dispersal, invasive species, frugivoryAbstract
Bird-mediated seed dispersal enhances invasions of many alien plant species. Typically, this mutualism is composed of a generalist assemblage of frugivorous birds in which morphological trait matching between bird and plant species is often thought to be poor due to low reciprocal adaptation. Despite this longheld notion, trait matching between local birds and alien plants has not been investigated. Here, we assessed trait matching by comparing functional traits in multidimensional space for local birds (bill, wing and tarsus size) and two alien invasive plants (fruit and seed size, fruit and seed shape) in an urban area. To do this, we measured bird functional traits in museum specimens and plant functional traits in individuals located in the study area. We found significant trait matching between birds and alien invasive plants (i.e., frugivorous birds interacted with morphologically corresponding invasive plant species). In addition, we detected a positive correlation between morphological and functional specialization of bird species so that extreme morphologies played specialized functional roles. Contrary to the idea that alien plant mutualisms are mediated by generalized seed dispersers without a close match between bird and alien plant traits, our results indicate that species with different morphologies forage on distinct plant species. These findings highlight the importance of studying the functional role of local birds in mutualistic interactions with alien invasive plants, and how these functional roles may promote invasion processes.
References
Aguirre-Acosta, N., E. Kowaljow, and R. Aguilar. 2014. Reproductive performance of the invasive tree Ligustrum lucidum in a subtropical dry forest: does habitat fragmentation boost or limit invasion? Biol Invasions 16:1397-1410. https://doi.org/10.1007/s10530-013-0577-x.
Aragón, R., and J. M. Morales. 2003. Species composition and invasion in NW Argentinian secondary forests: effects of land use history, environment and landscape. J Veg Sci 14:195-204. https://doi.org/10.1111/j.1654-1103.2003.tb02144.x.
Ayup, M. M., L. Montti, R. Aragón, and H. R. Grau. 2014. Invasion of Ligustrum lucidum (Oleaceae) in the southern Yungas: changes in habitat properties and decline in bird diversity. Acta Oecol 54: 72-81. https://doi.org/10.1016/j.actao.2013.03.006
Bhatt, A., S. Gairola, Y. Govender, and P. R. de Moura Souza-Filho. 2021. The invasive Melia azedarach in Durban (South Africa): impacts on tree community structure. Folia Geobot 56:139-147. https://doi.org/10.1007/s12224-021-09397-5.
Bender, I. M., W. D. Kissling, P. G. Blendinger, K. Böhning‐Gaese, I. Hensen, Kühn, I., M. C. Muñoz, E. L. Neuschulz, L. Nowak, M. Quitián, F. Saavedra, V. Santillán, T. Töpfer, T. Wiegand, D. M. Dehling, and M. Schleuning. 2018. Morphological trait matching shapes plant-frugivore networks across the Andes. Ecography 41:1910-1919. https://doi.org/10.1111/ecog.03396.
Benavidez, A., F. X. Palacio, L. O. Rivera, A. L. Echevarria, and N. Politi. 2018. Diet of Neotropical parrots is independent of phylogeny but correlates with body size and geographical range. Ibis 160:742-754. https://doi.org/10.1111/ibi.12630.
Bitani, N., D. A. E. Smith, Y. C. E. Smith, and C. T. Downs. 2020. Functional traits vary among fleshy-fruited invasive plant species and their potential avian dispersers. Acta Oecol 108:103651. https://doi.org/10.1016/j.actao.2020.103651.
Blanco, G., C. Bravo, E. C. Pacifico, D. Chamorro, K. L. Speziale, S. A. Lambertucci, F. Hiraldo, and J. L. Tella. 2016. Internal seed dispersal by parrots: an overview of a neglected mutualism. PeerJ 4:e1688. https://doi.org/10.7717/peerj.1688.
Buckley, Y. M., S. Anderson, C. P. Catterall, R. T. Corlett, T. Engel, C. R. Gosper, R. Nathan, D. M. Richardson, M. Setter, O. Spiegel, G. Vivian-Smith, F. A. Voigt, J. E. S. Weir, and D. A. Westcott. 2006. Management of plant invasions mediated by frugivore interactions. J App Ecol 43:848-857. https://doi.org/10.1111/j.1365-2664.2006.01210.x.
Burns, K. C. 2013. What causes size coupling in fruit-frugivore interaction webs? Ecology 94:295-300. https://doi.org/10.1890/12-1161.1.
Cordlandwehr, V., R. L. Meredith, W. A. Ozinga, R. M. Bekker, J. M. van Groenendael, and J. P. Bakker. 2013. Do plant traits retrieved from a database accurately predict on‐site measurements? J Ecol 101:662-670. https://doi.org/10.1111/1365-2745.12091.
Corlett, R. T. 2005. Interactions between birds, fruit bats and exotic plants in urban Hong Kong, South China. Urban Ecosyst 8:275-283. https://doi.org/10.1007/s11252-005-3260-x.
Cribari-Neto, F., and A. Zeileis. 2010. Beta regression in R. J Stat Softw 34:1-24. https://doi.org/10.18637/jss.v034.i02.
de la Peña, M. R. 2001. Observaciones de campo en la alimentación de las aves. Rev FAVE 15:99-107. https://doi.org/10.14409/fave.v15i1.
de Paula, A. 1987. La ciudad de La Plata, sus tierras y su arquitectura. Banco de la Provincia de Buenos Aires, La Plata, Argentina.
Dehling, D. M., P. Jordano, H. M. Schaefer, K. Böhning-Gaese, and M. Schleuning. 2016. Morphology predicts species’ functional roles and their degree of specialization in plant-frugivore interactions. Proc R Soc B 1823:2015-2444. https://doi.org/10.1098/rspb.2015.2444.
Douma, J. C., and J. T. Weedon. 2019. Analysing continuous proportions in ecology and evolution: a practical introduction to beta and Dirichlet regression. Methods Ecol Evol 10:1412-1430. https://doi.org/10.1111/2041-210X.13234.
Dray, S., and A. Dufour. 2007. The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1-20. https://doi.org/10.18637/jss.v022.i04.
Fernández, R. D., P. Castro‐Díez, R. Aragón, and N. Pérez‐Harguindeguy. 2021. Changes in community functional structure and ecosystem properties along an invasion gradient by Ligustrum lucidum. J Veg Sci 32:e13098. https://doi.org/10.1111/jvs.13098.
Fernández, R. D., S. J. Ceballos, R. Aragón, A. Malizia, L. Montti, J. I. Whitworth-Hulse, P. Castro-Díez, and H. R. Grau. 2020. A global review of Ligustrum lucidum (Oleaceae) invasion. Bot Rev 86:93-118. https://doi.org/10.1007/s12229-020-09228-w.
Frutos, A. E., C. F. Reales, and A. L. Ronchi-Virgolini. 2014. Presencia del Calancate Cara Roja (Aratinga mitrata) en la provincia de Entre Ríos. Natura Neotropicalis 45:97-101. https://doi.org/10.14409/natura.v1i45.4360.
García, D., D. Martínez, D. B. Stouffer, and J. M. Tylianakis. 2014. Exotic birds increase generalization and compensate for native bird decline in plant-frugivore assemblages. J Anim Ecol 83:1441-1450. https://doi.org/10.1111/1365-2656.12237.
Ghersa, C. M., E. de la Fuente, S. Suárez, and R. J. León. 2002. Woody species invasion in the Rolling Pampa grasslands, Argentina. Agric Ecosyst and Envir 88(3):271-278. https://doi.org/10.1016/S0167-8809(01)00209-2.
González-Castro, A., S. Yang, M. Nogales, and T. A. Carlo. 2015. Relative importance of phenotypic trait matching and species’ abundances in determining plant-avian seed dispersal interactions in a small insular community. AoB Plants 7:plv017. https://doi.org/10.1093/aobpla/plv017.
Gosper, C. R., C. D. Stansbury, and G. Vivian-Smith. 2005. Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Diversity Distrib 11:549-558. https://doi.org/10.1111/j.1366-9516.2005.00195.x.
Heleno, R. H., J. M. Olesen, M. Nogales, P. Vargas, and A. Traveset. 2013a. Seed dispersal networks in the Galápagos and the consequences of alien plant invasions. Proc R Soc B 1750:2012-2112. https://doi.org/10.1098/rspb.2012.2112.
Heleno, R. H., J. A. Ramos, and J. Memmott. 2013b. Integration of exotic seeds into an Azorean seed dispersal network. Biol Invasions 15:1143-1154. https://doi.org/10.1007/s10530-012-0357-z.
Højsgaard, S., and U. Halekoh. 2020. doBy: groupwise statistics, Lsmeans, linear contrasts, utilities. R package version 4.6.8. URL: cran.r-project.org/package=doBy.
Ibáñez, L. M., J. M. Girini, F. X. Palacio, and D. Montalti. 2014. Nidificación y alimentación de psittácidos introducidos en el noreste de la provincia de Buenos Aires, Argentina. Hornero 29:13-22.
Ibáñez, L. M., S. M. Zalba, A. Scorolli, D. Forcelli, and D. Montalti. 2016. El estornino pinto en Argentina: desafíos y prioridades. Revista del Museo de La Plata 1:159-169. https://doi.org/10.24215/25456377e010.
Jordaan, L. A., S. D. Johnson, C. T. Downs. 2012. Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi) as a potential dispersal agent for fleshy-fruited invasive alien plants: effects of handling behaviour on seed germination. Biol Invas 14:959-968. https://doi.org/10.1007/s10530-011-0131-7.
Jordano, P., J. Bascompte, and J. M. Olesen. 2003. Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6:69-81. https://doi.org/10.1046/j.1461-0248.2003.00403.x.
Lódola, A. and R. Brigo. 2011. Diagnóstico socioeconómico de La Plata y sus centros comunales. Facultad de Ciencias Económicas, Universidad Nacional de La Plata, La Plata.
Mabberley, D. J. 1984. A monograph of Melia in Asia and the Pacific. The history of white cedar and Persian lilac. Gard Bull 37:49-64.
McNeil, R., and M. A. Martínez. 1967. Asymétrie bilatérale des os longs des membres du pigeon Columba livia et du perroquet Amazona amazonica. Rev Can Biol 26:273-386.
Miles, D. B., and R. E. Ricklefs. 1984. The correlation between ecology and morphology in deciduous forest passerine birds. Ecology 65:1629-1640. https://doi.org/10.2307/1939141.
Montaldo, N. H. 1993. Avian dispersal and reproductive success of 2 species of Ligustrum (Oleaceae) in a subtropical forest relict in Argentina. Rev Chil Hist Nat 66:75-85.
Montaldo, N. H. 2005. Aves frugívoras de un relicto de selva subtropical ribereña en Argentina: manipulación de frutos y destino de las semillas. Hornero 20:163-172.
Montalti, D., and G. Kopij. 2001. Bird community of inner La Plata city, Argentina. Acta Ornithol 36:161-164. https://doi.org/10.3161/068.036.0209.
Oksanen, J. 2018. Vegan: community ecology package. R package version 2.5-6. URL: cran.r-project.org/web/packages/vegan/index.html.
Palacio, F. X., M. J. Apodaca, and J. V. Crisci. 2020. Análisis multivariado para datos biológicos: teoría y su aplicación utilizando el lenguaje R. Vázquez-Mazzini Editores, Buenos Aires, Argentina.
Palacio, F. X., and D. Montalti. 2013. Seasonal variation and effect of non-native invasive vegetation on two bird communities in northeast of Buenos Aires province, Argentina. Ornitol Neotrop 24:157-168.
Palacio, F. X., R. E. Maragliano, and D. Montalti. 2016. Functional role of the invasive European Starling, Sturnus vulgaris, in Argentina. Emu 116:387-393. https://doi.org/10.1071/MU16021.
Palacio, F. X., M. Valoy, F. Bernacki, M. S. Sánchez, M. G. Núñez-Montellano, O. Varela, and M. Ordano. 2017. Bird fruit consumption results from the interaction between fruit-handling behaviour and fruit crop size. Ethol Ecol and Evol 29:24-37. https://doi.org/10.1080/03949370.2015.1080195.
Perchivale, P., and R. F. Lucero. 2011. Notas de algunos hábitos de Aratinga leucophtalmus (Müller, 1776) en la provincia de Buenos Aires. Hist Nat 3:99-102.
Piccolo, A. L. G., and M. I. Gregolim. 1980. Phenology of Melia azedarach in S. Brazil. Turrialba 30:107-109.
Pigot, A. L., C. H. Trisos, and J. A. Tobias. 2016. Functional traits reveal the expansion and packing of ecological niche space underlying an elevational diversity gradient in passerine birds. Proc Royal Soc B: Biol Sci 283:20152013. https://doi.org/10.1098/rspb.2015.2013.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: R-project.org.
Ramaswami, G., M. Kaushik, S. Prasad, R. Sukumar, and D. Westcott. 2016. Dispersal by generalist frugivores affects management of an invasive plant. Biotropica 48:638-644. https://doi.org/10.1111/btp.12343.
Rasband, W. S. 1997. ImageJ. US National Institutes of Health, Bethesda, MD.
Richardson, D. M., P. Pyšek, M. Rejmánek, M. G. Barbour, F. D. Panetta, and C. J. West. 2000. Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93-107. https://doi.org/10.1046/j.1472-4642.2000.00083.x.
Rougès, M., and J. G. Blake. 2001. Tasas de captura y dietas de aves del sotobosque en el Parque Biológico Sierra de San Javier, Tucumán. Hornero 16:7-15.
Scheffer, M., L. Cremaschi, D. Montalti, and P. Grilli. 2015. Los loros exóticos del Parque Provincial Pereyra Iraola y comentarios sobre su presencia en la Ribera Platense. Nuestras Aves 60:3-8.
Sperry, J. H., D. O’Hearn, D. R. Drake, A. M. Hruska, S. B. Case, J. Vizentin-Bugoni, C. Arnett, and C. E. Tarwater. 2021. Fruit and seed traits of native and invasive plant species in Hawai ‘i: implications for seed dispersal by non-native birds. Biol Invas 23:1819-1835. https://doi.org/10.1007/s10530-021-02473-z.
Spotswood, E. N., J. Meyer, and J. W. Bartolome. 2012. An invasive tree alters the structure of seed dispersal networks between birds and plants in French Polynesia. J Biogeogr 39:2007-2020. https://doi.org/10.1111/j.1365-2699.2012.02688.x.
Thakur, S., S. Choudhary, A. Singh, K. Ahmad, G. Sharma, A. Majeed, and P. Bhardwaj. 2016. Genetic diversity and population structure of Melia azedarach in North-Western Plains of India. Trees 30:1483-1494. https://doi.org/10.1007/s00468-016-1381-x.
Tella, J. L., A. Baños-Villalba, D. Hernández-Brito, A. Rojas, E. Pacífico, J. A. Díaz-Luque, M. Carrete, G. Blanco, and F. Hiraldo. 2015. Parrots as overlooked seed dispersers. Front Ecol Environ 13:338-339. https://doi.org/10.1890/1540-9295-13.6.338.
Tella, J. L., G. Blanco, F. V. Dénes, and F. Hiraldo. 2019. Overlooked parrot seed dispersal in Australia and South America: insights on the evolution of dispersal syndromes and seed size in Araucaria trees. Frontiers Ecol Evol 7:82. https://doi.org/10.3389/fevo.2019.00082.
Traveset, A., and D. M. Richardson. 2006. Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208-216. https://doi.org/10.1016/j.tree.2006.01.006.
Vázquez, D. P., N. P. Chacoff, and L. Cagnolo. 2009. Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90:2039-2046. https://doi.org/10.1890/08-1837.1.
Vergara‐Tabares, D. L., P. G. Blendinger, A. Tello, S. I. Peluc, and P. A. Tecco. 2021. Fleshy‐fruited invasive shrubs indirectly increase native tree seed dispersal. Oikos 2:e08311. https://doi.org/10.1111/oik.08311.
Voigt, F. A., N. Farwig, and S. D. Johnson. 2011. Interactions between the invasive tree Melia azedarach (Meliaceae) and native frugivores in South Africa. J Trop Ecol 27:355-363. https://doi.org/10.1017/S0266467410000702.
Wheelwright, N. T. 1985. Fruit‐size, gape width, and the diets of fruit‐eating birds. Ecology 66:808-818. https://doi.org/1940542.
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