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Bird visits and resource use in Butia odorata (Arecaceae) palm groves in southern Brazil

Visitas de pássaros e uso de recursos em palmares de Butia odorata (Arecaceae) no sul do Brasil

ABSTRACT

We evaluated avian use of a palm grove of Butia odorata (Barb. Rodr.) Noblick in the Brazilian Pampa. We recorded bird species richness, frequency of visits, and feeding behavior in palms trees with different flower and fruit availability. From January 2018 to February 2019, we observed 1,094 bird visits in 347 palm trees and identified 53 species. The most frequent visitors were Sicalis flaveola (Linnaeus, 1766), Myiopsitta monachus (Boddaert, 1783) and Zonotrichia capensis (Statius Muller, 1776). Perching was the most frequent use of palm trees by the birds (79%). Our hypothesis that an increase in the availability of flowers and fruits will be followed by a larger number of visits by insectivorous and frugivorous birds was not corroborated. In addition, there was a higher number of species visiting palm trees with no resources. The species composition and the number of guilds of visiting birds varied seasonally, but independently from resources availability. Bird richness, number of visits, and time length of visits did not vary between flowering/fruiting and resourceless palm trees. Based on this we argue that the main contribution of Butia odorata to the establishment of bird assemblages in palm groves is their role in offering perching, sheltering, and nesting sites.

KEYWORDS
Ecological interaction; frugivory; palm grove; avifauna

RESUMO

Visitas de pássaros e uso de recursos em palmares de Butia odorata (Arecaceae) no sul do Brasil. Avaliamos as visitas das aves nas palmeiras Butia odorata (Barb. Rodr.) Noblick. em um palmar localizado no Pampa brasileiro. Registramos as espécies de aves, a frequênc ia de visitas, e seu comportamento alimentar em palmeiras com diferentes disponibilidades de flores e frutos. Entre janeiro de 2018 e fevereiro de 2019 observamos 1.094 visitas em 347 palmeiras e registramos 53 espécies de aves. As visitas mais frequentes foram feitas por Sicalis flaveola (Linnaeus, 1766), Myiopsitta monachus (Boddaert, 1783) e Zonotrichia capensis (Statius Muller, 1776). O principal uso das palmeiras foi o uso como poleiro (79%). Nossa hipótese de que o aumento de oferta de flores e frutos seria acompanhado por um maior número de visitas de aves insetívoras e frugívoras não foi corroborada. Além disso, houve um maior número de espécies visitando as palmeiras sem recursos do que as com recursos. A riqueza de espécies, o número de visitas, bem como a duração das visitas não variaram entre as palmeiras com e sem flores ou frutos. Com isso nós acreditamos que a principal contribuição da Butia odorata no palmar para o estabelecimento da avifauna está relaciona com a oferta de poleiros, abrigos e sítios para nidificação.

PALAVRAS-CHAVE
Interação ecológica; frugivoria; palmar; avifauna

The presence of birds in ecosystems is generally influenced by resource supply, such as food availability, shelters, perches and nesting sites, which allow their survival, protection and reproduction (Herrera, 1985Herrera, C. M. 1985. Habitat-consumer interactions in frugivorous birds. In: Cody, M. L. ed. Habitat selection in birds. Orlando, Academic Press , p. 341-359., 2004Herrera, C. M. 2004. Ecología de los pájaros frugivores ibéricos. In: Tellería, J. L. ed. La ornitología hoy: homenaje al profesor Francisco Bernis Madrazo. Madrid, Editorial Complutense, Universidad Complutense, p. 127-153.; Terborgh, 1986aTerborgh, J. 1986a. Community aspects of frugivory. In: Estrada, A. & Fleming, T. H. eds. Tropical forests. In frugivores and seed dispersal. Dordrecht, Dr. W. Junk Publishers, p. 371-384. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Galetti & Aleixo, 1998Galetti, M. & Aleixo, A. 1998. Effects of palm heart harvesting on avian frugivores in the Atlantic Rain Forest of Brazil. Journal of Applied Ecology 35:286-293. ; Alves et al., 2012Alves, A. S.; Vecchi, M. B.; Tomaz, V. C. & Piratelli, A. J. 2012. O impacto de vertebrados terrestres sobre a comunidade vegetal: aves como exemplos de estudos. In: Del-Claro, K. & Torezan-Silingardi, H. M. eds. Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. Rio de Janeiro, Technical Books, p. 89-110. ; Morellato et al., 2016Morellato, L. P. C.; Alberton, B.; Alvarado, S. T.; Borges, B. D.; Buisson, E.; Camargo, M. G. G.; Cancian, L. F.; Carstensen, D. W.; Escobar, D. F. E.; Leite, P. T. P.; Mendoza, I.; Rocha, N. M. W. B.; Soares, N. C.; Silva, T. S. F. & Staggemeier, V. G. 2016. Linking plant phenology to conservation biology. Biological Conservation 195:60-72. ). Many ecosystems such as savannas, steppes, and arid regions, have plants that are considered key species due to their great ecological and nutritional relevance for many species (Terborgh, 1986aTerborgh, J. 1986a. Community aspects of frugivory. In: Estrada, A. & Fleming, T. H. eds. Tropical forests. In frugivores and seed dispersal. Dordrecht, Dr. W. Junk Publishers, p. 371-384. ; Peres, 1994aPeres, C. A. 1994a. Composition, density, and fruiting phenology of arborescent palms in an Amazonian Forest. Biotropica 26:285-294. ,bPeres, C. A. 1994b. Primate responses to phenological changes in an Amazonian Terra Firme Forest. Biotropica 26:98-112.; Henderson, 1995Henderson, A. 1995. The palms of the Amazon. New York, Oxford University Press. 388p.; Henderson et al., 1995Henderson, A.; Galeano, G. & Bernal, R. 1995. Field guide to the palms of the Americas. New Jersey, Princeton University. 502p., 2000Henderson, A.; Fischer, B.; Scariot, A.; Pacheco, M. A. W. & Pardini, R. 2000. Flowering phenology of a palm community in a central Amazon Forest. Brittonia 52:149-159. ; Galetti et al., 1999Galetti, M.; Zipparro, V. B. & Morellato, P. C. 1999. Fruiting phenology and frugivory on the palm Euterpe edulis in a lowland Atlantic Forest of Brazil. Ecotropica 5:115-122. ). In general, in tropical forests, there is a high diversity of plants and, consequently, a huge supply of resources for fauna so that it is not always a particular species that stands out as the pivot of the local trophic plot. Still, a seasonal, conspicuous, and large biomass supply may represent an expressive increase in the food chain to which the fauna is linked (WheelWright, 1991WheelWright, N. T. 1991. How Long do fruit-eating birds stay in the plants. Biotropica 23(1):29-40. ; Paise & Vieira, 2005Paise, G. & Vieira, E. M. 2005. Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma floresta ombrófila mista no Rio Grande do Sul, Brasil. Revista Brasileira de Botânica 28:615-625. ; Vieira & Iob, 2009Vieira, E. M. & Iob, G. 2009. Dispersão e predação de sementes da araucária (Araucaria angustifolia). In: Fonseca, C. R.; Souza, A. F.; Leal-Zanchet, A. M.; Dutra, T.; Backes, A. & Ganade, G. eds. Floresta de araucária: ecologia, conservação e desenvolvimento sustentável. Ribeirão Preto, Holos, p. 85-95.). Some palm trees, for example, present long and abundant fruiting periods, which make them strong candidates for key plants of trophic webs in phytosociological formations known as palm groves (Dransfield, 1978Dransfield, J. 1978. Growth rates of rain forest palms. In: Tomlinson, P. B. & Zimmermann, M. H. eds. Tropical trees as living systems. New York, Cambridge University Press, p. 247-268.; Terborgh, 1986bTerborgh, J. 1986b. Keystone plant resources in the tropical forest. In: Soule, M. E. ed. Conservation biology, the science of scarcity and diversity. Sunderland, Sinauer Associates, p. 330-344. ; Galetti & Aleixo, 1998Galetti, M. & Aleixo, A. 1998. Effects of palm heart harvesting on avian frugivores in the Atlantic Rain Forest of Brazil. Journal of Applied Ecology 35:286-293. ; Galetti et al., 1999Galetti, M.; Zipparro, V. B. & Morellato, P. C. 1999. Fruiting phenology and frugivory on the palm Euterpe edulis in a lowland Atlantic Forest of Brazil. Ecotropica 5:115-122. ; Beck, 2006Beck, H. 2006. A Review of peccary-palm interactions and their ecological ramifications across the Neotropics. Journal of Mammalogy 87(3):519-530. ).

South American palm groves of Butia odorata are phytophysiognomies formed by grasslands with the presence of palm trees in relatively high density (Bondar, 1964Bondar, G. 1964. Palmeiras do Brasil. Boletim do Instituto de Botânica de São Paulo 2:1-159.; Oliveira et al., 2007Oliveira, M. L. A. A.; Senna, R. M.; Neves, M. T. M. B.; Blank, M. & Bordrin, I. I. 2007. Flora e vegetação. In: Becker, F. G.; Ramos, R. A. & Moura, L. de A. eds. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 85-102.; Geymonat & Rocha, 2009Geymonat, G. & Rocha, N. 2009. M´botiá. Ecosistema único en el mundo. Castillos, Casa Ambiental. 93p.; Rivas & Barbieri, 2014Rivas, M. & Barbieri, R. L. 2014. Boas práticas de manejo para o extrativismo sustentável do butiá. Pelotas, Embrapa Clima Temperado . 59p.; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.). In the biome Pampa, there are few remnants of palm groves of the species Butia odorata (Oliveira et al., 2007Oliveira, M. L. A. A.; Senna, R. M.; Neves, M. T. M. B.; Blank, M. & Bordrin, I. I. 2007. Flora e vegetação. In: Becker, F. G.; Ramos, R. A. & Moura, L. de A. eds. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 85-102.; MMA, 2007MMA - Ministério do Meio Ambiente. 2007. Áreas prioritárias para conservação, uso sustentável e repartição de benefícios da biodiversidade brasileira: atualização. Portaria MMA n° 9, de 23 de janeiro de 2007. Brasília, Secretaria de Biodiversidade e Florestas. 300p.; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.), and the species is currently included in the list of endangered species of the flora of the state of Rio Grande do Sul due to the development of several human activities, such as agriculture, forestry, livestock and urban expansion (FZB, 2014FZB - Fundação Zoobotânica do Rio Grande do Sul. 2014. Lista vermelha de espécies da flora do Rio Grande do Sul ameaçadas de extinção. 21p. Available at <Available at http://www.fzb.rs.gov.br/upload/20141208161010anexo_i_taxons_da_flora_nativa_do_estado_rio_grande_do_sul_ameacadas_de_extincao_1_.pdf >. Accessed on 27 November 2017.
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; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.). The coastal plain of Rio Grande do Sul, more specifically in the municipalities of Tapes and Barra do Ribeiro, harbors the largest groupings of B. odorata groves in southern Brazil (Oliveira et al., 2007Oliveira, M. L. A. A.; Senna, R. M.; Neves, M. T. M. B.; Blank, M. & Bordrin, I. I. 2007. Flora e vegetação. In: Becker, F. G.; Ramos, R. A. & Moura, L. de A. eds. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 85-102.; Costa et al., 2017Costa, F. A.; Barbieri, R. L.; Sosinski, E. E. & Heiden, G. 2017. Caracterização e discriminação espectral de butiazeiros (Butia odorata, Arecaceae) utilizando técnicas de sensoriamento remoto. Comunicado Técnico 355. Pelotas, Embrapa Clima Temperado . 7p.). Even so, details about the participation and influence of B. odorata on the trophic plot in which it is inserted are still poorly known. It is estimated that the fruits of B. odorata are still a relevant food source for many animals that inhabit and visit these palms in the Pampa (Barbieri, 2015Barbieri, R. L. 2015. Vida no Butiazal. Pelotas, Embrapa Clima Temperado. 200p.; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.).

Birds are the animals that are most often observed visiting palm groves to use their resources (Bencke et al., 2007Bencke, G. A.; Burger, M. I.; Dotto, J. C. P.; Guadagnin, D. L.; Leite, T. O. & Menegheti, J. O. 2007. Aves. In: Becker, F. G.; Ramos, F. G. & Moura, L. de A. orgs. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 317-355.; Barbieri, 2015Barbieri, R. L. 2015. Vida no Butiazal. Pelotas, Embrapa Clima Temperado. 200p.; EMBRAPA, 2015EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária. 2015. Projeto manejo e conservação de butiazais no Rio Grande do Sul. Embrapa Clima Temperado. Video: Amamos Butiá. Available at <Available at https://www.youtube.com/watch?v=pwq7DnX6dqI >. Accessed on 27 November 2017.
https://www.youtube.com/watch?v=pwq7DnX6...
; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.). Besides fruits, insects attracted by the palm flowers are also important food sources for birds, being another potential for bird gathering in palm groves. It is worth remembering that insects are important resources not only for insectivorous species but also for omnivores (Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.; Wilman et al., 2014Wilmann, H.; Belmaker, J.; Simpson, J.; De La Rosa, C.; Rivadeneira, M. M. & Jetz, W. 2014. Eltontraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95(7):2027-2027. Available at <Available at https://esapubs.org/archive/ecol/E095/178/ >. Accessed on 27 November 2017.
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), which consequently increases the attractiveness of palm trees. However, birds can often make random visits to the branches of plants just to perch and occupy new territories (McClanahan & Wolfe, 1993McClanahan, T. R. & Wolfe, R. W. 1993. Accelerating forest succession in a fragmented landscape: the role of birds and perches. Conservation Biology 7(2):279-288. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Athiêa & Diasb, 2016Athiêa, S. & Diasb, M. M. 2016. Use of perches and seed dispersal by birds in an abandoned pasture in the Porto Ferreira state park, southeastern Brazil. Brazilian Journal of Biology 76(1):80-92. ; Portugal et al., 2017Portugal, S. J.; Sivess, L.; Martin, G. R.; Butler, P. J. & White, C. R. 2017. Perch height predicts dominance rank in birds. Ibis 156(2):456-462. ).

Wolfe et al. (2014Wolfe, J. D.; Johnson, M. D. & Ralph, C. J. 2014. Do birds select habitat or food resources? Nearctic-neotropic migrants in Northeastern Costa Rica. PLOS ONE 9(1):1-10.), in a study in Costa Rica, confirmed that the availability of food and structural attributes of the habitat influence its use by birds. These authors showed synchrony between the arrival of migratory birds in a region and the increase in the supply of ripe fruits in the environment. In addition, they observed that frugivorous species are strongly related to fruit availability, while insectivorous species are related to habitat structure (Wolfe et al., 2014Wolfe, J. D.; Johnson, M. D. & Ralph, C. J. 2014. Do birds select habitat or food resources? Nearctic-neotropic migrants in Northeastern Costa Rica. PLOS ONE 9(1):1-10.). Kissling et al. (2011Kissling, W. D.; Sekercioglu, C. H. & Jetz, W. 2011. Bird dietary guild richness across latitudes, environments and biogeographic regions. Global Ecology and Biogeography 21(3):328-340. ), on the other hand, demonstrated that variations in species richness and bird trophic guilds across the latitude gradients are mainly determined by the environment’s net primary productivity and climate variations between different geographical regions (Jetz & Rahbek, 2002Jetz, W. & Rahbek, C. 2002. Geographic range size and determinants of avian species richness. Science (297):1548-1551. ; Hawkins et al., 2003Hawkins, B. A.; Field, R.; Cornell, H. V.; Currie, D. J.; Guégan, J. F.; Kaufman, D. M.; Kerr, J. T.; Mittelbach, G. G.; Oberdoff, T.; O’Brien, E. M.; Porter, E. E. & Turner, J. R. G. 2003. Energy, water, and broad-scale geographic patterns of species richness. Ecology (84):3105-3117. ). In most cases, the increase in the availability of food resources in habitats may also berelated to these factors and influence bird richness and abundance in the environment (Mckey, 1975Mckey, D. 1975. The ecology of coevolved seed dispersal systems. In: Gilbert, L. E. & Raven, P. H. eds. Coevolution of animals and plants. Austin, University Texas Press, p. 159-191.; Pizo, 1997Pizo, M. A. 1997. Seed dispersal and predation in two populations of Cabralea canjerana (Meliaceae) in the Atlantic Forest of Southeastern Brazil. Journal of Tropical Ecology 13:559-578. ; Francisco & Galetti, 2002Francisco, M. R. & Galetti, M. 2002. Aves como potenciais dispersores de sementes de Ocotea pulchella Mart. (Lauraceae) numa área de vegetação de cerrado do sudeste brasileiro. Revista Brasileira de Botânica 25:11-17. ).

The number and time length of bird visits to fruit trees vary according to the size and abundance of fruits in plants as well as their nutritional aspects (WheelWright, 1991WheelWright, N. T. 1991. How Long do fruit-eating birds stay in the plants. Biotropica 23(1):29-40. ; Jordano, 2000Jordano, P. 2000. Frutas e frugivoria. In: Fenner, M. ed. Sementes: a ecologia de regeneração em comunidades vegetais. 2ed. Wallingford, CABI Publ., p. 125-166., 2014Jordano, P. 2014. In: Gallagher, R. S. ed. Seeds: the ecology of regeneration in plant communities. 3ed. London, CAB International. British Library, p. 18-61. ; Lord, 2004Lord, J. M. 2004. Frugivore gape size and the evolution of fruit size and shape in Southern Hemisphere floras. Austral Ecology 29(4):430-436.). This fact may be related to a foraging optimization behavior, adjusting the best way to get resources. The length of the visit to the plant may represent its relevance for bird nutrition. It is also possible that there is a cost/benefit ratio between the bird’s length of visit to the plant and fruit supply. Theoretically, a bird would tend to maximize the number of ingested fruits and, to do so, it would stay longer feeding on the same plant if it has a large fruit supply. On the other hand, a bird would tend to remain less time in each plant when there is a fruit shortage in order to visit as many plants as possible. Those are some of the possible predictions that are present in the Optimal Foraging Theory (Charnov, 1976Charnov, E. L. 1976. Optimal foraging: the marginal value theorem. Theoretical Population Biology 9:129-136. ; Chaves & Alves, 2010Chaves, F. G. & Alves, M. A. S. 2010. Teoria do forrageamento ótimo: premissas e críticas em estudos com aves. Oecologia Australis 14(2):369-380. ). The distance between fruit trees can also be crucial for birds to spend more time feeding on the same plant (Murray, 1987Murray, K. G. 1987. Selection for optimal fruit-crop size in bird-dispersed plants. The American Naturalist 129:18-31. ; Westcott & Graham, 2000Westcott, D. A. & Graham, D. L. 2000. Patterns of movement and seed dispersal of a tropical frugivore. Oecologia 122:249-257. ; Khamcha et al., 2012Khamcha, D.; Savini, T.; Brocleman, W. Y.; Chimchome, V. & Gale, G. A. 2012. Influence of food availability and distribution on the movement patterns of a forest avian frugivore, the puff-throated bulbul (Alophoixus pallidus). Journal of Tropical Ecology (28):1-9. ). In addition, arthropod abundance is also directly affected by seasonal changes in plant productivity, which indirectly influences insectivorous birds due to the increased population of these organisms (Janzen & Schoener, 1968Janzen, D. H. & Schoener, T. W. 1968. Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology 49:96-110. ; Levings & Windsor, 1982Levings, S. & Windsor, D. 1982. Seasonal and annual variation in litter arthropod population. In: Jr. Leigh, E. G.; Rand, A. S. & Windsor, D. M. eds. The ecology of a tropical forest. Washington D. C., Smithsonian Institution Press, p. 355-389.; Del-Claro, 2012Del-Claro, K. 2012. Origens e importância das relações plantas-animais para a ecologia e conservação. In: Del-Claro, K. & Torezan-Silingardi, H. M. eds. Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. Rio de Janeiro, Technical Books , p. 37-49.). In the present study, we evaluated whether the number of visits, length of visits, species composition and use of food resources by birds vary according to the flower and fruit supply in palm trees.

MATERIAL AND METHODS

Study area. The study was carried out between January 2018 and February 2019 in a remnant of Butia odorata palm grove in the municipality of Tapes, Rio Grande do Sul State, Brazil (Fig. 1). Due to the absence of well-preserved palm groves, our sample focused on a single continuous palm grove located in a private property (30°31ʼ49.83ˮS, 51°21ʼ24.62ˮW). The sampled area consists of 840 hectares of natural Pampa biome (Becker et al., 2007Becker, F. G.; Ramos, R. A. & Moura, L. de A. 2007. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente. 385p.; Medeanic et al., 2007Medeanic, S.; Corrêa, I. C. S. & Weschenfelder, J. 2007. Palinomorfos nos sedimentos de fundo da Laguna dos Patos-RS: Aplicação nas reconstruções paleoambientais. Porto Alegre, Gravel., p. 89-102.).

Fig. 1.
1. Study site location at municipality of Tapes, Rio Grande do Sul, Brazil. 2. Photo of an area of the palm grove (Photo by Cyro Menezes da Gloria). 3. Sampling area outlined in red; Map image created in R Studio; Study area in Google Earth, Google (C), 2019 (Edited by Cyro Menezes da Glória).

We considered each palm tree as a sampling unit. To minimize the effects of spatial dependence between the sample sites, we selected three sampling locations of about 22 ha each and with a minimum distance of 500 m from each other (Fig. 3). All three sites have the same average palm density and similar phytophysiognomy (Fig. 2).

Bird sampling. The sampling was carried out systematically, been each sampling location sampled once a month. In a same month, all sites were sampled along three consecutive days in order to reduce the effects of climatic changes on activity of birds. Sampling occurred between 6:00 a.m. and 12:00 a.m., and between 2:00 p.m. and 5:00 p.m. when the palm trees were scanned for birds with the aid of binoculars (10x42). Observations started at a randomly selected point at the border of each sampling location and, when a bird was observed on a palm tree, the tree was classified as a focal palm and the data recording process began, lasting 15 minutes (focal observation method; Altmann, 1974Altmann, J. 1974. Observational study of behavior: sampling methods. Behavior 49:227-265. ). Birds were observed at a minimum distance of 15 meters (Pizo & Galetti, 2010Pizo, M. A. & Galetti, M. 2010. Métodos e perspectivas do estudo da frugivoria e dispersão de sementes por aves. In: Accordi, I.; Straube, F. C. & Von Matter, S. eds. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro, Technical Books , p. 492-504.). We called a “visit” the event starting from the first sighting of a bird until it departed from a focal palm tree. For each individual that visited a focal palm tree, we recorded: (a) species, (b) total amount of time spent in the palm, (c) total amount of time dedicated to the consumption of fruits, flowers or insects. The amount of time spent at the palm with no consumption of food was registered as “total amount of time spent perching/resting”. We are considering the broader concept of ‟resource use” which would include not only the use of the palm tree for food (fruits or insects) but also its use as a temporary habitat (e.g., perch). The use of each resource by the same individual during the same visit was computed as one event, regardless of the number of fruit or insects eaten by the bird. We consider as “consumption” the partial or complete use of a food resource (fruits or insects). For palm fruits, we considered as consumption the following events: swallowing of the whole fruit, partial consumption (pulp pieces) of the fruit, mandibulation and suction of pulp juice (Pizo, 1997Pizo, M. A. 1997. Seed dispersal and predation in two populations of Cabralea canjerana (Meliaceae) in the Atlantic Forest of Southeastern Brazil. Journal of Tropical Ecology 13:559-578. ). After 15 minutes of observation, a new search started at a minimum distance of 200 meters from the already evaluated place. The nomenclature followed the standards of the Brazilian Ornithological Records Committee (CBRO, 2015CBRO - Comitê Brasileiro de Registros Ornitológicos. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. 209p. Available at <Available at http://www.cbro.org.br/wp-content/uploads/2020/06/Piacentini-et-al-2015-RBO.pdf >. Accessed on 27 November 2017.
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). Species were classified according to their trophic guilds following Sick (1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.) and Wilmann et al. (2014Wilmann, H.; Belmaker, J.; Simpson, J.; De La Rosa, C.; Rivadeneira, M. M. & Jetz, W. 2014. Eltontraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95(7):2027-2027. Available at <Available at https://esapubs.org/archive/ecol/E095/178/ >. Accessed on 27 November 2017.
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).

Evaluation of flower and fruit supply. We considered flowers and fruits as resources since fruits can be an indirect attraction or be consumed directly by some common birds in the study area [Aramides cajaneus (Statius Muller, 1776), Coereba flaveola (Linnaeus, 1758), Myiopsitta monachus (Boddaert, 1783), Penelope obscura Temminck, 1815, Pyrrhura frontalis (Vieillot, 1817), Tangara sayaca Cabanis, 1847, Turdus rufiventris Vieillot, 1818, among others]. In addition, flowers can be an indirect attraction for many insectivorous birds as flowers attract insects (Moermond & Denslow, 1985Moermond, T. C. & Denslow, J. S. 1985. Neotropical avian frugivores patterns of behavior, morphology, and nutrition, with consequences for fruit selection. In: Buckley, P. A.; Foster, M. S.; Morton, E. S.; Ridgely, R. S. & Buckley, F. G. eds. Neotropical ornithology. Ornithology Monographs 36:865-897.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Chin & Rajathurai, 2005Chin, W. Y. & Rajathurai, S. 2005. Of palms and birds. Nature Watch 13(4):7-11.; Koh, 2008Koh, L. P. 2008. Birds defend oil palms from herbivorous insects. Ecological Applications 18(4):821-825. ; Del-Claro, 2012Del-Claro, K. 2012. Origens e importância das relações plantas-animais para a ecologia e conservação. In: Del-Claro, K. & Torezan-Silingardi, H. M. eds. Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. Rio de Janeiro, Technical Books , p. 37-49.). The evaluation of flower and fruit supply was made in the focal palm (observation palm) and in three adjacent palm trees, called satellite palms (the three closest trees to the focal palm), which are defined to evaluate the flower/fruit supply. For this, we estimated the measures of length (vertical measurement = height) and width (horizontal measurement = diameter) in centimeters of the focal palm and satellite clusters and estimated the percentage of mature flowers or fruits present in the clusters. The bunch dimensions were visually estimated by the approximation of a ruler suspended by a retractable extension cable that served as a reference for the measurements. Based on the length and width of the bunch, its volume (cm³) was calculated by the cylinder volume formula (v = π * r² * h), where, v = bunch volume, r = bunch width / 2, h = bunch length. The same procedure was repeated for focal palms and satellites. The percentage value of flowers and fruits in palm trees was adapted from Fournier (1974Fournier, L. A. 1974. Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba 24:422-423. ), aiming to evaluate the variation in the intensity of flowering and fruiting in the bunches between the estimated proportion categories (Tab. I).

Tab. I.
Evaluation of the intensity of the flowering and fruiting phenophases of palm trees, according to the estimated percentage of ripe fruits and flowers in the bunches.

Data analysis. Because the distribution of the data is not normal, we applied the Kruskal-Wallis test to assess whether there was a significant difference between visit parameters (number of visits and length of visit) in palm trees with flowers, fruits and resources. To minimize the effect of the difference between the number of fruiting and flowering palm trees, bird species richness between these phases was compared by the rarefaction method (Sanders, 1968Sanders, H. 1968. Marine benthic diversity: a comparative study. The American Naturalist 102:243-282. ). Richness was estimated from an extrapolated value for 1000 random repetitions of the samples, calculated by means of the program Estimates 8.2.0 (Colwell, 2009Colwell, R. K. 2009. Estimates: statistical estimation of species richness and shared species from samples. Version 8.2.0. Available at <Available at http://viceroy.eeb.uconn.edu/estimates >. Accessed on 15 November 2018.
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). We evaluated mean and standard deviation and applied the coefficient of variation in cluster volume to detect whether there was a low or high difference in the obtained values ​so that they could be considered relevant for the evaluation of the supply (percentage of fruits and flowers in the bunches). After confirming the high coefficient of variation, we multiplied the volume of the bunch by the percentage value of its phenological supply to obtain the value of the flower or fruit supply index between the focal palms and satellites. Analyses were performed using the programs PAST version 3.18 and BioEstat version 5.3.

Using the program Multiv version 3.55b, we performed a multivariate analysis of variance (MANOVA) to evaluate the variation in the composition of the variables (53 species and six trophic guilds) between the sample units (347 palm trees). Thus, we sought to confirm if there was significant variation (p <0.05) in the composition of trophic species and guilds recorded throughout the evaluated seasons (summer, autumn and spring), having as a sample unit the number of visits of each species, between the evaluated palm trees of each season. To evaluate the composition of trophic species and guilds in relation to the availability of resources in palm trees (flowers and fruits), another similar matrix was created for the same test (MANOVA) to evaluate if there were significant differences (p <0.05) in the composition of trophic species and guilds between flowering, fruiting and resourceless palm trees. When ordering the data, we used, as a measure of similarity, Euclidean Distance to compare sample units and principal coordinate analysis (Pillar & Orlóci, 1996Pillar, V. D. & Orlóci, L. 1996. On randomization testing in vegetation science: multifactor comparisons of relevé groups. Journal of Vegetation Science 7:585-592. ).

To evaluate the type of foraging behavior in relation to resource supply (flower or fruit), we generated four generalized linear mixed models (Knudson, 2018Knudson, C. 2018. Glmm: Generalized Linear Mixed Models Via Monte Carlo Likelihood Approximation. R Package Version 1.3.0. Cran - Package Glmm.) by means of the program R (R Development Core Team, 2019R Development Core Team 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. 409p.). In all models, each palm tree was considered as a single sampling unit. Time and number of frugivory and insectivory events were considered as response variables. Fruit and flower supply index in focal palm and satellite palms were considered as fixed effects in the model. Since weather conditions of the month may have influenced bird activity, the effect of the sampling month was also included in the models as a random effect. The following models were generated: 1- fruit supply vs. frugivory events, 2- fruit supply vs. frugivory time, 3- fruit and flower supply vs. insectivory events, 4- fruit and flower supply vs. insectivory time.

RESULTS

Number of species. In a total of 348 hours of observations, we recorded 53 bird species distributed in 18 families (Tab. II). We recorded six trophic guilds, with the larger number of species being insectivores (26 species), omnivores (16) and granivores (8) (Fig 2). Perch use was recorded in 52 species (6 trophic guilds) in a total of 987 visits. Insectivory events was observed in 20 species (3 trophic guilds) in a total of 77 visits. We also recorded 8 species in frugivory events (from 4 trophic guilds) in a total of 30 visits (Tab. II). The species with the largest number of visits were Sicalis flaveola (n=236 records; 94% of visits were for perching, 4% for nesting and 2% for insect consumption), Myiopsitta monachus (n=133; 50% of visits were for perching, 47% for nesting and 3% for fruit consumption) and Zonotrichia capensis (n=126; 94% of visits were for perching, 5% for insect consumption and 1% for fruit consumption).

Fig. 2.
The trophic guilds with the larger number of species in palm trees, Tapes, Rio Grande do Sul, Brazil.

Among the birds visiting the palm trees (visitors assembly), 32% of the recorded species richness occur inside forests (17 species, 10 families), while 68% do not occur inside forests (36 species, 16 families). Concerning the trophic guild, among the forest species, ten are insectivorous, four omnivorous, two granivorous and one frugivorous. Among the non-forest species, fifteen are insectivorous, twelve omnivorous, six granivorous, two carnivorous and one scavenger.

The assembly formed by visiting birds in resourceless palm trees was larger than in those with some type of food resource (flower or fruit) (Tabs II, III). The rarefaction method revealed that resourceless palm trees were visited by a larger number of species (between 17 and 26), while in flowering or fruiting palm trees the number of visiting species was smaller and ranged between 16 and 23 (Tab. III). Thus, richness did not vary between flowering, fruiting and resourceless palm trees (Kruskal-Wallis: H20,269 = 2.02, p = 0.3071).

Variation of species composition between seasons and resource supply. We recorded significant variation in species composition between seasons, but the effect of variation was only 1% (MANOVA: R² = 0.01, p = 0.04). Similarly, there was variation in trophic guild composition throughout the seasons but with an effect of only 2% (MANOVA: R² = 0.02, p = 0.004). There was no significant variation in species composition between palm trees with different types of resource supply (flowering, fruiting and resourceless, MANOVA: R² = 0.01, p = 0.257). There was also no significant variation in trophic guild composition between flowering or fruiting palm trees and resourceless palm trees (MANOVA: R² = 0.01, p = 0.318).

Tab. II.
Bird species observed visiting Butia odorata with different resource supply, in southern Brazil. Trophic guilds: O, omnivore; G, granivore; I, insectivore; C, carnivore; S, scavenger; F, frugivore. PE = perch events; FR = frugivory events; IN= insectivory events.

Tab. III.
Variation in the number of absolute and estimated rarefaction records of species in relation to the resource supply in the palms Butia odorata (With Fruit = fruiting palm trees; With Flower = flowering palm trees; FR = frugivory events; IN = insectivory events; NR = non-resource visits) among fruiting, flowering and resourceless palm trees.

Visits and resource supply. We observed 1,094 visits distributed among 347 palm trees (fruiting = 194 visits, flowering = 62, resourceless = 838). On average, each palm received from 3.1 to 3.3 visits during each observation (Tab. III). There was no significant variation in the number of visits between flowering, fruiting and resourceless palm trees (Kruskal-Wallis: H20,269 = 0.3688, p = 0.8248). The average length of visit of birds to the focal palm was 188 seconds (SD = 239.33). The total length of visits of the birds to the palm trees (sum of the length of each visit in each palm tree) did not vary significantly between flowering, fruiting and resourceless palm trees (Kruskal-Wallis: H20,269 = 1.686, p = 0.4304). Likewise, the average length of visit of each bird did not vary significantly between flowering, fruiting and resourceless palm trees (Kruskal-Wallis: H20,269 = 1.53, p = 0.4653).

Variation in foraging events regarding palm resource supply. The result of the Generalized Linear Mixed Model (GLMM) indicated that there was no significant relationship between the number of frugivory events and fruit supply in the focal palm trees (GLMM: F = 0.012713, p = 0.183), nor the satellite palm trees (GLMM: F = -0.018457, p = 0.145). There was a positive and significant relationship between frugivory time and fruit availability in both focal palm trees (GLMM: F = 0.031843, p < 0.001) and satellite palm trees (GLMM: F = -0.019454, p < 0.001). However, the estimated coefficients for fixed effects are less than 0.1, which suggests a weak relationship (Tab. IV).

There was a positive and significant relationship between flower supply in satellite palm trees and insectivory events (GLMM: F = 0.018572, p = 0.001). However, we did not detect a significant relationship between focal palm flower supply and insectivory events (GLMM: F = 0.008169, p = 0.1873). Insectivory time showed a positive and significant relationship with flower supply in both focal palm trees (GLMM: F = 0.010531, p < 0.001) and satellite palm trees (GLMM: F = 0.026525, p < 0.001).

There was no significant relationship between fruit supply and number of insectivory events in either focal palm trees (GLMM: F = -0.00193, p = 0.8322) or satellite palm trees (GLMM: F = -0.00794, p = 0.3943). However, for the evaluation of the relationship between fruit supply and insectivory time, the effect was positive in both focal palm trees (GLMM F = -0.02139, p < 0.001) and satellite palm trees (GLMM: F = - 0.02022, p < 0.001). Overall, insectivory events varied significantly over the year (Tab. IV; Fig. 3).

Fig. 3.
Average indices of flower and ripe fruit supply of Butia odorata and number of frugivory and insectivory events in the evaluated months, Tapes, Rio Grande do Sul, Brazil.

Tab. IV.
Generalized Linear Mixed Model demonstrating the effect of flower and fruit supply of Butia odorata and month on the number and length of frugivory and insectivory events. (FOC, offer on focal palm trees; SAT, offer on satellite palm).

DISCUSSION

We recorded 53 bird species visiting Butia odorata, which represent 11% of the Brazilian Pampa species and 22% of the species recorded in the vicinity of the study site (Bencke et al., 2007Bencke, G. A.; Burger, M. I.; Dotto, J. C. P.; Guadagnin, D. L.; Leite, T. O. & Menegheti, J. O. 2007. Aves. In: Becker, F. G.; Ramos, F. G. & Moura, L. de A. orgs. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 317-355.; Develey et al., 2008Develey, P. F.; Setubal, R. B.; Dias, R. A. & Bencke, G. A. 2008. Conservação das aves e da biodiversidade no bioma Pampa aliada a sistemas de produção animal. Revista Brasileira de Ornitologia 16(4):308-315. ). Considering that all records were based exclusively on the observation of birds on a single plant species, the evidence shows that B. odorata palm groves may represent a relevant habitat to the local avifauna. Probably the palm clusters are important for birds because they increase habitat heterogeneity, offering food opportunities, shelter and protected breeding sites (Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Bencke et al., 2007Bencke, G. A.; Burger, M. I.; Dotto, J. C. P.; Guadagnin, D. L.; Leite, T. O. & Menegheti, J. O. 2007. Aves. In: Becker, F. G.; Ramos, F. G. & Moura, L. de A. orgs. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 317-355.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.). Other systems have reported that the ability to access higher strata in the vegetation is a relevant element in microhabitat selection by birds (Cody & Diamond, 1975Cody, M. L. & Diamond, J. M. 1975. Ecology and evolution of communities. Cambridge, Harvard University Press. 560p.; Norberg, 1977Norberg, R. A. 1977. An ecological theory on foraging time and energetic and choice of optimal food-searching method. Journal of Animal Ecology 46:511-529. , 1983Norberg, R. A. 1983. Optimal locomotion modes of foraging birds in trees. Ibis 125:172-180. ; Cody, 1985bCody, M. L. 1985b. Habitat selection in grassland and open-country birds. In: Cody, M. L. ed. Habitat selection in birds. Orlando, Academic Press, p. 191-223.; Gill, 1990Gill, F. B. 1990. Ornithology. New York, W. F. Freeman and Company. 758p.; Azhar et al., 2013Azhar, B.; Lindenmayer, D. B.; Wood, J.; Fischer, J.; Manning, A.; Mcelhinny, C. & Zakaria, M. 2013. The Influence of agricultural system stand structural complexity and landscape context on foraging birds in oil palm landscapes. Ibis 155:297-312.; Castaño-Villa et al., 2014Castaño-Villa, G. J.; Ramos-Valencia, A. S. & Fontúrbel, F. E. 2014. Fine-scale habitat structure complexity determines insectivorous bird diversity in a tropical forest. Acta Oecologica 61:19-23. ). Because this palm grove is an extensive cluster of palm trees that form islands spaced across the grassland, birds can safely move and take refuge among them when crossing wide areas of open habitats.

The species that most frequently searched for some type of palm resource were relatively common in the region: Myiopsitta monachus, Sicalis flaveola and Zonotrichia capensis. Such species are usually abundant and frequently recorded in several ecosystems in southern Brazil, especially in rural environments (Belton, 1985Belton, W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2: Formicariidae through Corvidae. Bulletin of American Museum of Natural History 180(1):1-242.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Azpiroz, 2012Azpiroz, A. B. 2012. Aves de las Pampas y Campos de Argentina, Brasil y Uruguay. Una guía de indentificación. Nueva Helvecia, PRESSUR. 351p.). It is worth noticing that M. monachus, a gregarious species, usually builds collective nests in the palms and often consumes their fruits. We believe that this is one of the species with the widest range of resource use on B. odorata (shelter, nesting and fruit consumption).

The hypothesis that there would be more visits to palm trees with more resources was refuted. In fact, most of the bird visits in the palm trees was limited to perch use. It means that palms were not mainly attractive by their food offering. However, it is possible that, like many other tropical ecosystems, the surrounding ecosystem in which palm trees are inserted offers many food resources. The palm groves of B. odorata occur in an angiosperm-rich field matrix that offers large seed biomass and small fruits and certainly attracts a large number of arthropods, offering abundant resources especially for omnivorous and insectivorous birds (Becker et al., 2007Becker, F. G.; Ramos, R. A. & Moura, L. de A. 2007. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente. 385p.; Oliveira et al., 2007Oliveira, M. L. A. A.; Senna, R. M.; Neves, M. T. M. B.; Blank, M. & Bordrin, I. I. 2007. Flora e vegetação. In: Becker, F. G.; Ramos, R. A. & Moura, L. de A. eds. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 85-102.; Barbieri, 2015Barbieri, R. L. 2015. Vida no Butiazal. Pelotas, Embrapa Clima Temperado. 200p.; Barbieri et al., 2016Barbieri, R. L.; Chomenko, L.; Sosinski, E. E.; Costa, F. A.; Gomes, G. C.; Marchil, M. M.; Mistura, C. C.; Heiden, G.; Matos J. Z.; Carneiro, A. M.; Nilson, A. D.; Ramos, R. A. & Farias-Singer, R. 2016. Butiás: conservação e uso sustentável de Butia odorata na região do litoral médio do Rio Grande do Sul. Natureza em Revista 14:10-15.). This hypothesis is reinforced by the fact that most of the recorded species are insectivorous, omnivorous or granivorous, which can find food in several other habitats (Cody, 1985aCody, M. L. 1985a. Habitat selection in birds (Physiological Ecology). Orlando, Academic Press. 541p.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Wilman et al., 2014Wilmann, H.; Belmaker, J.; Simpson, J.; De La Rosa, C.; Rivadeneira, M. M. & Jetz, W. 2014. Eltontraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95(7):2027-2027. Available at <Available at https://esapubs.org/archive/ecol/E095/178/ >. Accessed on 27 November 2017.
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). Thus, the presence of flowers and fruits in these palms would not represent such a significant increase in regional productivity to the point that we could detect an increase in the number of visits to palm trees. For a better assessment of the role of palms in the observed bird food chain, a complementary approach would be needed, including the use of tools such as stable isotope analysis to verify the carbon source (primary source) that supports the trophic web of birds (Peterson & Fry, 1987Peterson, B. J. & Fry, B. 1987. Stable isotopes in ecosystem studies. Annual Reviews of Ecology and Systematics 18:293-320. ). Our data also showed that palm trees without flowers or fruits (without measured resources) were visited by a larger number of species than those with resources. Despite going against our premises, this fact reinforces the idea that the presence of birds in palm trees is not related to aspects of fruit consumption but rather to search for shade, shelter, refuge and nesting place (Cody & Diamond, 1975Cody, M. L. & Diamond, J. M. 1975. Ecology and evolution of communities. Cambridge, Harvard University Press. 560p.; Howe, 1979Howe, H. F. 1979. Fear and frugivory. American Naturalist 114(6):925-931.; Gill, 1990Gill, F. B. 1990. Ornithology. New York, W. F. Freeman and Company. 758p.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Chin & Rajathurai, 2005Chin, W. Y. & Rajathurai, S. 2005. Of palms and birds. Nature Watch 13(4):7-11.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.; Azhar et al., 2013Azhar, B.; Lindenmayer, D. B.; Wood, J.; Fischer, J.; Manning, A.; Mcelhinny, C. & Zakaria, M. 2013. The Influence of agricultural system stand structural complexity and landscape context on foraging birds in oil palm landscapes. Ibis 155:297-312.).

We did not record a significant change in species composition or trophic guilds of birds in relation to changes in flower and fruit supply in palm trees, despite several studies reinforcing that seasonal variation in the availability of food resources and the breeding period influence the composition of birds in the environment (Alves & Cavalcanti, 1996Alves, A. S. & Cavalcanti, R. B. 1996. Sentinel behaviour, seasonality, and the structure of bird flocks in Brazilian savanna. Ornitologia Neotropical 7:43-51. ; Machado, 1999Machado, C. G. 1999. Estrutura, composição e dinâmica de bandos mistos de aves na Mata Atlântica do Alto da Serra do Paranapiacaba, no sudeste brasileiro. Revista Brasileira de Biologia 59(1):75-85.; Develey & Peres, 2000Develey, P. F. & Peres, C. A. 2000. Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic forest of southeastern Brazil. Journal of Tropical Ecology 16:33-53. ). We assume, therefore, that the abundance of resources in the palm grove areas is not wholly dependent on the palm trees and is scattered over several associated microhabitats.

Another important element linked to foraging resources (food demand, habitat dispersal) concerns the reproductive period. Reproductive cycles directly affect the intensity and way species look for resources in space and consequently affect species composition in the environment (Cody & Diamond, 1975Cody, M. L. & Diamond, J. M. 1975. Ecology and evolution of communities. Cambridge, Harvard University Press. 560p.; Snow, 1981Snow, D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1-14. ; Cody, 1985aCody, M. L. 1985a. Habitat selection in birds (Physiological Ecology). Orlando, Academic Press. 541p.; Belton, 1985Belton, W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2: Formicariidae through Corvidae. Bulletin of American Museum of Natural History 180(1):1-242.; Alves & Cavalcanti, 1996Alves, A. S. & Cavalcanti, R. B. 1996. Sentinel behaviour, seasonality, and the structure of bird flocks in Brazilian savanna. Ornitologia Neotropical 7:43-51. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.). Our data suggest a slight tendency in the variation of species composition and trophic guilds between seasons but the percentage of species that explains this variation is low. There is possibly the influence of the fact that there are more insectivorous species in the environment, among which few are migratory (Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Bencke et al., 2007Bencke, G. A.; Burger, M. I.; Dotto, J. C. P.; Guadagnin, D. L.; Leite, T. O. & Menegheti, J. O. 2007. Aves. In: Becker, F. G.; Ramos, F. G. & Moura, L. de A. orgs. Biodiversidade: Regiões da Lagoa do Casamento e dos Butiazais de Tapes, Planície Costeira do Rio Grande do Sul. Brasília, Ministério do Meio Ambiente , p. 317-355.; Donatelli et al., 2017Donatelli, R. J.; Matos-Martins, R.; Sementili-Cardoso, G.; Vianna, R. M.; Gerotti, R. W. & Rodrigues, F. G. 2017. Categorias alimentares, estratificação e sazonalidade da comunidade de aves do Parque das Neblinas e seu entorno, município de Bertioga, São Paulo. Atualidades Ornitológicas 197:58-65. ). On the other hand, it is possible that reproduction-related aspects, in addition to seasonal variation of arthropods and climatic conditions, may also be influencing trophic species and guild composition in some way (Belton, 1985Belton, W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2: Formicariidae through Corvidae. Bulletin of American Museum of Natural History 180(1):1-242.; Poulin et al., 1994Poulin, B.; Lefebvre, G. & Mcneil, R. 1994. Characteristics of feeding guilds and variation in diets of bird species of three adjacent tropical sites. Biotropica 26(2):187-197. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Brereton & Taylor, 2000Brereton, R. N. & Taylor, R. J. 2000. Composition, seasonal occurrences and habitat use of bird assemblages in wet forests on the Central Plateau of Tasmania. Papers and Proceedings of the Royal Society of Tasmania 134:35-43. ; Khamcha et al., 2012Khamcha, D.; Savini, T.; Brocleman, W. Y.; Chimchome, V. & Gale, G. A. 2012. Influence of food availability and distribution on the movement patterns of a forest avian frugivore, the puff-throated bulbul (Alophoixus pallidus). Journal of Tropical Ecology (28):1-9. ; Donatelli et al., 2017Donatelli, R. J.; Matos-Martins, R.; Sementili-Cardoso, G.; Vianna, R. M.; Gerotti, R. W. & Rodrigues, F. G. 2017. Categorias alimentares, estratificação e sazonalidade da comunidade de aves do Parque das Neblinas e seu entorno, município de Bertioga, São Paulo. Atualidades Ornitológicas 197:58-65. ). In general, changes in temperature, humidity and precipitation tend to affect the abundance of arthropods, which in turn influence the presence of birds in ecosystems (Wolda, 1988Wolda, H. 1988. Insect seasonality, why? Annual Review of Ecology and Systematics 19:1-18.; Oliveira et al., 2006Oliveira, E. A.; Zardo, C. M. L. & Nascimento, L. V. 2006. Abundância e padrão sazonal da entomofauna de restinga de uma ilha do estuário da laguna Lagoa dos Patos, Rio Grande, RS, Brasil. Estudos de Biologia PUC-PR 28(64):27-35. ; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.). In our data, we recorded a significant variation in insectivory events over the year, possibly due to seasonal arthropod variation in the environment, in addition to the variation in the energy demand of birds due to the metabolic changes in their natural cycles (Janzen & Schoener, 1968Janzen, D. H. & Schoener, T. W. 1968. Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology 49:96-110. ; Payne, 1972Payne, R. B. 1972. Mechanisms and control of moult. In: FARNER, D. S. & KING, J. R. eds. Avian Biology. New York, Academic Press, p. 104-155.; Levings & Windsor, 1982Levings, S. & Windsor, D. 1982. Seasonal and annual variation in litter arthropod population. In: Jr. Leigh, E. G.; Rand, A. S. & Windsor, D. M. eds. The ecology of a tropical forest. Washington D. C., Smithsonian Institution Press, p. 355-389.; Wolda, 1988Wolda, H. 1988. Insect seasonality, why? Annual Review of Ecology and Systematics 19:1-18.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.). In addition, insectivory was more related to the supply of satellite palm flowers around the focal area (local scale), which may indicate that there is an influence of environmental conditions regarding the offer of this resource in the palm to increase insectivory (Wolda, 1988Wolda, H. 1988. Insect seasonality, why? Annual Review of Ecology and Systematics 19:1-18.; Oliveira et al., 2006Oliveira, E. A.; Zardo, C. M. L. & Nascimento, L. V. 2006. Abundância e padrão sazonal da entomofauna de restinga de uma ilha do estuário da laguna Lagoa dos Patos, Rio Grande, RS, Brasil. Estudos de Biologia PUC-PR 28(64):27-35. ). Among the bird species that fed on palm arthropods, Troglodytes musculus, Colaptes melanochloros, Tangara sayaca and Zonotrichia capensis stood out in our study.

In general, the increase in supply did not influence the number of birds consuming fruit on palm trees but favored an increased length of visit during foraging. In addition, we observed more fruit consumption events in the period of lower supply. A possible explanation for this is the fact that, under low fruit supply in the region, there would be a higher concentration of frugivory events in a smaller number of palm trees, enhancing their observation. In other words, the few palm trees with fruit supply would have a greater focus on foraging and, thus, would concentrate frugivory events on the palm. Following this logic, in a period with greater fruit availability, frugivory would occur in a dispersed way in the habitat, being recorded less frequently by our method of recording (observation of focal palm). Fruit weight and seed size are known to influence frugivory rate, with light (less than 3.5 g) and small fruits generally being the most consumed by birds (Herrera, 1985Herrera, C. M. 1985. Habitat-consumer interactions in frugivorous birds. In: Cody, M. L. ed. Habitat selection in birds. Orlando, Academic Press , p. 341-359.; WheelWright, 1985WheelWright, N. T. 1985. Fruit size gape width, and the diets of fruit-eating birds. Ecology 66(3):808-818. , 1991WheelWright, N. T. 1991. How Long do fruit-eating birds stay in the plants. Biotropica 23(1):29-40. ). Because the fruits of this palm species are fibrous and relatively heavy (7 to 14 g; Rivas & Barbieri, 2014Rivas, M. & Barbieri, R. L. 2014. Boas práticas de manejo para o extrativismo sustentável do butiá. Pelotas, Embrapa Clima Temperado . 59p.), few bird species in this palm grove may be able to consume them since the vast majority are small passerine birds (Passeriformes), among which few have the beak adapted for the effective consumption of this type of fruit (Snow, 1971Snow, D. W. 1971. Evolutionary aspects of fruit-eating by birds. Ibis 113:194-202. , 1981Snow, D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1-14. ; Moermond & Denslow, 1985Moermond, T. C. & Denslow, J. S. 1985. Neotropical avian frugivores patterns of behavior, morphology, and nutrition, with consequences for fruit selection. In: Buckley, P. A.; Foster, M. S.; Morton, E. S.; Ridgely, R. S. & Buckley, F. G. eds. Neotropical ornithology. Ornithology Monographs 36:865-897.; Gautier-Hion et al., 1985Gautier-Hion, A.; Duplantier, J.; Quris, R.; Feer, F.; Sourd, C.; Decoux, J.; Dubost, G.; Emmons, L.; Erard, C.; Hecketsweiler, P.; Moungazi, A.; Roussilhon, C. & Thiollay, J. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324-337. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.). Fruit consumption was characterized by species (n = 5) that plucked pieces and macerated the pulp, and by species (n = 3) that drilled and sucked the pulp, both cases without ingestion of the seed. Among these records, only two species (T. sayaca and M. monachus) were observed transporting the fruit away from the mother plant. We recorded a total of eight species feeding on fruits, among which the following four included the largest number of recorded frugivory events: Coereba flaveola, Myiopsitta monachus, Tangara sayaca and Pyrrhura frontalis. Villalobos & Bagno (2012Villalobos, M. P. & Bagno, M. A. 2012. Avian frugivores feeding on Mauritia flexuosa (Arecaceae) fruits in Central Brazil. Revista Brasileira de Ornitologia 20(1):26-29.), in their study on Mauritia flexuosa L.f. frugivory by birds, recorded eight bird species feeding on the fruits of this palm (buriti), where parrot species were their main consumers and dispersers. Likewise, in our study, the two recorded parrot species (M. monachus and P. frontalis) stood out as the main consumers of Butia odorata fruits, which is possibly due to the adaptive and evolutionary aspects of their beak type, which enables them to pull off pieces of the fruit fibers from palm trees, as well as their ability to handle the fruit with their feet while feeding during foraging (Snow, 1971Snow, D. W. 1971. Evolutionary aspects of fruit-eating by birds. Ibis 113:194-202. ; Herrera, 1985Herrera, C. M. 1985. Habitat-consumer interactions in frugivorous birds. In: Cody, M. L. ed. Habitat selection in birds. Orlando, Academic Press , p. 341-359.; Moermond & Denslow, 1985Moermond, T. C. & Denslow, J. S. 1985. Neotropical avian frugivores patterns of behavior, morphology, and nutrition, with consequences for fruit selection. In: Buckley, P. A.; Foster, M. S.; Morton, E. S.; Ridgely, R. S. & Buckley, F. G. eds. Neotropical ornithology. Ornithology Monographs 36:865-897.; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Ares, 2007Ares, R. A. 2007. Aves: vida y conducta. Buenos Aires, Vázquez Mazzini Editores. 288p.). Weight and size of fruits as well the beak morphology could limit the consumption by birds (WheelWright, 1991WheelWright, N. T. 1991. How Long do fruit-eating birds stay in the plants. Biotropica 23(1):29-40. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.; Jordano, 2000Jordano, P. 2000. Frutas e frugivoria. In: Fenner, M. ed. Sementes: a ecologia de regeneração em comunidades vegetais. 2ed. Wallingford, CABI Publ., p. 125-166., 2014Jordano, P. 2014. In: Gallagher, R. S. ed. Seeds: the ecology of regeneration in plant communities. 3ed. London, CAB International. British Library, p. 18-61. ; Lord, 2004Lord, J. M. 2004. Frugivore gape size and the evolution of fruit size and shape in Southern Hemisphere floras. Austral Ecology 29(4):430-436.). Most of the birds observed in this study did not have a specialized beak for the consumption of Butia odorata fruit (Rivas & Barbieri, 2014Rivas, M. & Barbieri, R. L. 2014. Boas práticas de manejo para o extrativismo sustentável do butiá. Pelotas, Embrapa Clima Temperado . 59p.), and the majority of species are insectivorous or omnivorous (Snow, 1981Snow, D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1-14. ; Gautier-Hion et al., 1985Gautier-Hion, A.; Duplantier, J.; Quris, R.; Feer, F.; Sourd, C.; Decoux, J.; Dubost, G.; Emmons, L.; Erard, C.; Hecketsweiler, P.; Moungazi, A.; Roussilhon, C. & Thiollay, J. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324-337. ; WheelWright, 1991WheelWright, N. T. 1991. How Long do fruit-eating birds stay in the plants. Biotropica 23(1):29-40. ; Sick, 1997Sick, H. 1997. Ornitologia Brasileira. 2ed. Rio de Janeiro, Nova Fronteira. 912p.). The results of this study indicated that many birds that are not potential consumers of the fruits of Butia odorata used palm groves. Thus, we consider that other factors of the palm may be more relevant to the presence of birds, such as other food opportunities, shelter and protected breeding sites. However, more studies need to be carried out to infer with greater precision these observed issues concerning the main attractive factors for birds in the Butia odorata palms.

Our results shown a seasonal variation in the number of bird visits in the palms. Insectivorous species were the most frequent observed species. Among the most used resources along the visit, we highlighted the use of palms trees as perch, shelter and nesting site. This suggests the importance of formation of the palm groves of Butia odorata to the establishment of avifauna, whatever was their feeding behavior.

Acknowledgments

Several people participated in laboratory work and manuscript advice, especially Glayson Ariel Bencke, Juliano Morales de Oliveira, Fernanda Ávila and Edna Bertin. We also thank Carmen Heller Barros for allowing us to access the study site. We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the support obtained through the master’s scholarship.

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Publication Dates

  • Publication in this collection
    08 Dec 2021
  • Date of issue
    2021

History

  • Received
    01 May 2021
  • Accepted
    12 Nov 2021
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