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Niche partitioning between hummingbirds and well-matched flowers is independent of hummingbird traits

Published online by Cambridge University Press:  04 August 2021

Raquel de Oliveira Bueno*
Affiliation:
Departamento de Biodiversidade e Conservação da Natureza, Universidade Tecnológica Federal do Paraná, Via Rosalina Maria dos Santos 1233, CEP: 87301-899, Campo Mourão, Paraná, Brazil
Thais Bastos Zanata
Affiliation:
Departamento de Botânica e Ecologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Cuiabá, Brazil
Isabela Galarda Varassin
Affiliation:
Laboratório de Interações e Biologia Reprodutiva, Departamento de Botânica, Centro Politécnico, Universidade Federal do Paraná, Rua Alcides Vieira Arcoverde s/n.º, 81.531-990, Caixa Postal 19031, Jardim das Américas, Curitiba, Paraná, Brazil
*
Author for correspondence: Raquel de Oliveira Bueno, Email: quelloliveira@gmail.com

Abstract

Among nectarivorous birds, the highest niche partitioning occurs between hummingbirds and plants. Although hummingbirds tend to visit morphologically well-matched resources, as ornithophilous species, they can also visit flowers with other traits. Here, we investigated whether the niche partitioning in hummingbird-plant interactions is also observed with ornithophilous species only. We also explored if hummingbird traits predicted resources use. We recorded a plant-ornithophilous species network in a semi-deciduous forest in Brazil. We quantified interaction partitioning through network connectance, complementary specialisation, and modularity. The influence of hummingbirds’ traits into their visits was investigated through methods of functional ecology and ecological networks. We recorded 948 interactions between nine hummingbirds and seven ornithophilous plants. We detected similar patterns of niche partitioning between hummingbirds and ornithophilous plants in comparison to networks considering the entire plant community. However, hummingbird species with the most specialised interactions are different from those when the whole system is evaluated. Therefore, we cannot downscale the patterns from one scale to the other. The pattern of interaction with ornithophilous plants was not related to hummingbirds’ traits. Therefore, the coexistence of species with shared traits might be occurring through facilitative and competitive processes, leading to trait mismatching and maintaining niche partitioning among ornithophilous plants.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Abrahamczyk, S and Kessler, M (2010) Hummingbird diversity, food niche characters, and assemblage composition along a latitudinal precipitation gradient in the Bolivian lowlands. Journal of Ornithology 151, 615625.CrossRefGoogle Scholar
Bergamo, PJ, Wolowski, M, Maruyama, PK, Vizentin-Bugoni, J and Sazima, M (2018) Trait patterns across space and time suggest an interplay of facilitation and competition acting on Neotropical hummingbird-pollinated plant communities. Oikos 127, 16901700.CrossRefGoogle Scholar
Berns, CM and Adams, DC (2010) Bill shape and sexual shape dimorphism between two species of temperate hummingbirds: black chinned hummingbird (Archilochus alexandri) and ruby throated hummingbird (A. colubris). The Auk 127, 626635.CrossRefGoogle Scholar
Blüthgen, N (2010) Why network analysis is often disconnected from community ecology: a critique and an ecologist’s guide. Basic and Applied Ecology 11, 185195.CrossRefGoogle Scholar
Blüthgen, N, Menzel, F and Blüthgen, N (2006) Measuring specialization in species interaction networks. BioMed Central Ecology 6, 112.Google ScholarPubMed
Borcard, D, Gillet, F and Legendre, P (2011) Unconstrained ordination. In: Numerical ecology with R. New York, NY: Springer, pp. 115151.CrossRefGoogle Scholar
Brown, JH and Bowers, MA (1985) Community organization in hummingbirds: relationships between morphology and ecology. The Auk 102, 251269.CrossRefGoogle Scholar
Brown, JH and Kodric-Brown, A (1979) Convergence, competition, and mimicry in a temperate community of hummingbird-pollinated flowers. Ecology 60, 10221035.CrossRefGoogle Scholar
Chacoff, NP, Vazquez, DP, Lomascolo, SB, Stevani, EL, Dorado, J and Padron, B (2012) Evaluating sampling completeness in a desert plant-pollinator network. Journal of Animal Ecology 81, 190200.CrossRefGoogle Scholar
Chao, A (1984) Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265270.Google Scholar
Colwell, RK and Coddington, JA (1994) Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B: Biological Sciences 345, 101118.Google ScholarPubMed
Cronk, Q and Ojeda, I (2008) Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59, 715727.CrossRefGoogle Scholar
Dalsgaard, B, Magard, E, Fjeldsa, J, Martın Gonzalez, AM, Rahbek, C, Olesen, JM and Svenning, JC (2011) Specialization in plant-hummingbird networks is associated with species richness, contemporary precipitation and quaternary climate-change velocity. PLoS ONE 6, e25891.CrossRefGoogle ScholarPubMed
Dehling, DM, Jordano, P, Schaefer, HM, Böhning-Gaese, K and Schleuning, M (2016) Morphology predicts species’ functional roles and their degree of specialization in plant-frugivore interactions. Proceedings of the Royal Society B 283, 20152444.CrossRefGoogle ScholarPubMed
Dormann, CF and Strauss, R (2014) A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5, 9098.CrossRefGoogle Scholar
Dormann, CF, Frueund, J, Blüthgen, N and Gruber, B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2, 724.Google Scholar
Etcheverry, AV and Alemán, CET (2005) Reproductive biology of Erythrina falcata (Fabaceae: Papilionoideae). Biotropica 37, 5463.CrossRefGoogle Scholar
Faegri, K and van der Pijl, L (1971) The Principles of Pollination Ecology. Oxford, UK: Pergamon Press.Google Scholar
Fleming, TH and Muchhala, N (2008) Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems. Journal of Biogeography 35, 764780.Google Scholar
Guimarães, PR, Jordano, P and Thompson, JN (2011) Evolution and coevolution in mutualistic networks. Ecology Letters 14, 877885.Google ScholarPubMed
Hatschbach, GG and Ziller, SR (1995) Lista Vermelha de Espécies Ameaçadas de Extinção no estado do Paraná. Curitiba, Brazil: Secretaria Estadual do Meio Ambiente de Curitiba, Biblioteca Nacional do Paraná. 139 pp.Google Scholar
HCF - Herbário da Universidade Tecnológica Federal do Paraná Campus Campo Mourão, Available at INCT - Herbário Virtual da Flora e dos Fungos <http://inct.splink.org.br>. Access on 25 March 2021..+Access+on+25+March+2021.>Google Scholar
Hsieh, TC, Ma, KH and Chao, A (2014) CRAN - Package iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0. Available at: <http://chao.stat.nthu.edu.tw/blog/software-download>. Access on 11 March 2021..+Access+on+11+March+2021.>Google Scholar
IAP/DIBAP - Instituto Ambiental do Paraná / Diretoria de Biodiversidade e Áreas Protegidas (2005) Plano de Manejo do Parque Estadual Lago Azul. Curitiba, PR.Google Scholar
Kaehler, M, Varassin, IG and Goldenberg, R (2005) Polinização em uma comunidade de bromélias em Floresta Atlântica Alto-Montana no Estado do Paraná, Brasil. Revista Brasileira de Botânica 28, 219228.Google Scholar
Lunau, K, Papiorek, S, Eltz, T and Sazima, M (2011) Avoidance of chromatic colours by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214, 16071612.CrossRefGoogle Scholar
Maglianesi, MA, Blüthgen, N, Bohning-Gaese, K and Schleuning, M (2014) Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology 95, 33253334.CrossRefGoogle Scholar
Maglianesi, MA, Blüthgen, N, Bohning-Gaese, K and Schleuning, M (2015) Functional structure and specialization in three tropical plant hummingbird interaction networks across an elevational gradient in Costa Rica. Ecography 38, 11191128.CrossRefGoogle Scholar
Maruyama, PK, Sonne, J, Vizentin-Bugoni, J, Martín González, AM, Zanata, TB, Abrahamczyk, S, Alarcón, R, Araujo, AC, Araújo, FP, Baquero, AC, Chávez-González, E, Coelho, AG, Cotton, PA, Dehling, DM, Fischer, E, Kohler, G, Lara, C, Las-Casas, FMG, Machado, AO, Machado, CG, Maglianesi, MA, Malucelli, TS, Marín-Gómez, OH, Oliveira, PE, Ornelas, JF, Ortiz-Pulido, R, Ramírez-Burbano, MB, Rocca, MA, Rodrigues, LC, Rosero-Lasprilla, L, Rui, AM, Sandel, B, Svenning, JC, Tinoco, BA, Varassin, IG, Watts, S, Rahbek, C, Sazima, M, Schleuning, M and Dalsgaard, B (2018) Functional diversity mediates macroecological variation in plant-hummingbird interaction networks. Global Ecology and Biogeography 27, 11861199.CrossRefGoogle Scholar
Maruyama, PK, Vizentin-Bugoni, J, Oliveira, GM, Oliveira, PE and Dalsgaard, B (2014) Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica 46, 740747.CrossRefGoogle Scholar
Matias, R, Maruyama, PK and Consolaro, H (2016) A non-hermit hummingbird as main pollinator for ornithophilous plants in two isolated forest fragments of the Cerrados. Plant Systematics and Evolution 302, 12171226.CrossRefGoogle Scholar
McGuire, JA, Witt, CC, Remsen, JV, Corl, A, Rabosky, DL, Altshuler, DL and Dudley, R (2014) Molecular phylogenetics and the diversification of hummingbirds. Current Biology 24, 910916.Google ScholarPubMed
Moeller, DA (2004). Facilitative interactions among plants via shared pollinators. Ecology 85, 32893301.CrossRefGoogle Scholar
Olesen, JM, Bascompte, J, Dupont, YL and Jordano, P (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences 104, 1989119896.Google ScholarPubMed
Patefield, WM (1981) Algorithm AS 159: An efficient method of generating random RxC tables with given row and column totals. Journal of the Royal Statistical Society 30, 9197.Google Scholar
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at <https://www.r-project.org/>. Access on 11 March 2021..+Access+on+11+March+2021.>Google Scholar
Roderjan, CV, Galvão, F, Kuniyoshi, YS and Hatschback, G (2002) As unidades fitogeográficas do estado do Paraná. Ciência e Ambiente 24, 7592.Google Scholar
Rodríguez-Flores, CI, Ornelas, JF, Wethington, S, Arizmendi, MdC (2019) Are hummingbirds generalists or specialists? Using network analysis to explore the mechanisms influencing their interaction with nectar resources. PLoS ONE 14, e0211855.CrossRefGoogle ScholarPubMed
Sargent, RD and Ackerly, DD (2008) Plant–pollinator interactions and the assembly of plant communities. Trends in Ecology & Evolution 23, 123130.CrossRefGoogle ScholarPubMed
Schleuning, M, Fründ, J, Klein, AM, Abrahamczyk, S, Alarcón, R, Albrecht, M, Andersson, GKS, Bazarian, S, Böhning-Gaese, K, Bommarco, R, Dalsgaard, B, Dehling, DM, Gotlieb, A, Hagen, M, Hickler, T, Holzschuh, A, Kaiser-Bunbury, CN, Kreft, H, Morris, RJ, Sandel, B, Sutherland, WJ, Svenning, JC, Tscharntke, T, Watts, S, Weiner, CN, Werner, M, Williams, NM, Winqvist, C, Dormann, CF and Blüthgen, N (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology 22, 19251931.CrossRefGoogle ScholarPubMed
Sick, H (2001) Ornitologia brasileira. Rio de Janeiro, Brazil: Nova Fronteira. 862 pp.Google Scholar
Sonne, J, Zanata, TB, Martín González, AM, Torres, NLC, Fjeldså, J, Colwell, RK, Tinoco, BA, Rahbek, C and Dalsgaard, B (2019). The distributions of morphologically specialized hummingbirds coincide with floral trait matching across an Andean elevational gradient. Biotropica 51, 205218.CrossRefGoogle Scholar
Souza, DGS (2004) Todas as aves do Brasil: guia de campo para identificação. Feira de Santana, Brazil: Dall. 350 pp.Google Scholar
Stiles, FG (1975). Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species. Ecology 56, 285301.CrossRefGoogle Scholar
Temeles, EJ, Linhart, YB, Masonjones, M and Masonjones, HD (2002) The role of flower width in hummingbird bill length-flower length relationships. Biotropica 34, 6880.Google Scholar
Thompson, JN (2005) The geographic mosaic of coevolution. Chicago, Illinois: University of Chicago Press. 400 pp.CrossRefGoogle Scholar
Thomson, JD and Wilson, P (2008) Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. International Journal of Plant Sciences 169, 2338.CrossRefGoogle Scholar
Tinoco, BA, Graham, CH, Aguilar, JM and Schleuning, M (2017) Effects of hummingbird morphology on specialization in pollination networks vary with resource availability. Oikos 126, 5260.CrossRefGoogle Scholar
Tripp, EA and McDade, LA (2013) Time-calibrated phylogenies of hummingbirds and hummingbird-pollinated plants reject a hypothesis of diffuse co-evolution. Aliso: A Journal of Systematic and Evolutionary Botany 31, 89103.CrossRefGoogle Scholar
Vizentin-Bugoni, J, Maruyama, PK and 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, 20132397.CrossRefGoogle Scholar
Weinstein, BG and Graham, CH (2017) Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbird-plant interactions. Ecology Letters 20, 326335.CrossRefGoogle ScholarPubMed
Zanata, TB, Dalsgaard, B, Passos, FC, Cotton, PA, Roper, JJ, Maruyama, PK, Fischer, E, Schleuning, M, Martín González, AM, Vizentin-Bugoni, J, Franklin, DC, Abrahamczyk, S, Alárcon, R, Araujo, AC, Araújo, FP, Azevedo-Junior, SM, Baquero, AC, Böhning-Gaese, K, Carstensen, DW, Chupil, H, Coelho, AG, Faria, RR, Hořák, D, Ingversen, TT, Janeček, S, Kohler, G, Lara, C, Las-Casas, FMG, Lopes, AV, Machado, AO, Machado, CG, Machado, IC, Maglianesi, MA, Malucelli, TS, Mohd-Azlan, J, Moura, AC, Oliveira, GM, Oliveira, PE, Ornelas, JF, Riegert, J, Rodrigues, LC, Rosero-Lasprilla, L, Rui, AM, Sazima, M, Schmid, B, Sedláček, O, Timmermann, A, Vollstädt, MGR, Wang, Z, Watts, S, Rahbek, C and Varassin, IG (2017) Global patterns of interaction specialization in bird–flower networks. Journal of Biogeography 44, 18911910.CrossRefGoogle Scholar
Zanata, TB, Dalsgaard, B, Rahbek, C and Varassin, IG (2019) Bill measurements of hummingbirds in the ecological network database. Figshare. Fileset.Google Scholar
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