Abstract
Phenology is the basis for understanding the life cycle of plants or animals throughout the year. Thus, we surveyed diurnal anthophilous fauna on plant species in the Brazilian Chaco to determine (1) groups of floral visitors and occurrence; (2) richness and abundance of fauna in relation to flowering flora and meteorological variables; (3) groups of visitors that pollinate or thieving flora; (4) distribution of herbaceous and woody strata throughout the year of flowering; (5) variation in flowering as a whole community, in the context of abiotic factors; and (6) the predominant plant families and species. We sampled eight groups of floral visitors, totalling 105 sampled species and 644 specimens. The flies and bees were the richest groups, with bees forming the most abundant group. The phenology of the fauna and flora was not clustered and exhibited a continuous and bimodal flowering. The abundance and richness of floral visitors were positively related to the quantity of plant species and flowering, as well as rainfall. Herbaceous and woody strata are important for the maintenance of anthophilous fauna throughout the year. Plant species with the highest abundance and the longest flowering period presented the highest richness and/or abundance of floral visitors. The percentage of pollination was higher than that of resource theft. Bees and flies were the main groups of pollinators, whereas flies were the main thieves. The present survey is only a starting point for future studies on the networks of interactions between plants and their floral visitors in the Brazilian Chaco.


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Amaral-Neto LP, Westerkamp C, Melo GAR (2015) From keel to inverted keel flowers: functional morphology of ‘‘upside down’’ papilionoid flowers and the behavior of their bee visitors. Plant Syst Evol 301:2161–2178. doi:10.1007/s00606-015-1221-2
Anacleto DA, Marchini LC (2005) Análise faunística de abelhas (Hymenoptera, Apoidea) coletadas no cerrado do Estado de São Paulo. Acta Sci Biol Sci 27:277–284. doi:10.4025/actascibiolsci.v27i3.1315
Andena SR, Bego LR, Mechi MR (2005) A comunidade de abelhas (Hymenoptera, Apoidea) de uma área de cerrado (Corumbataí, SP) e suas visitas às flores. Ver Bras de Zooc 7:55–91
Antonini Y, Martins RP (2003) The flowering-visiting bees at the Ecological Station of the Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Neotrop. Entomol 32:565–575. doi:10.1590/S1519-566X2003000400006
Aoki C, Sigrist MR (2006) Inventário dos visitantes florais no Complexo Aporé-Sucuriú. In: Pagoto TCS, Souza PR (eds) Biodiversidade do Complexo Aporé-Sucuriú. Subsídios à conservação e ao manejo do Cerrado, Editora da Universidade Federal de Mato Grosso do, SulCampo Grande, pp 143–162
APG IV, Byng JW, Chase MW, Christenhusz MJM, Fay MF, Judd WS, Mabberley DJ, Sennikov AN, Soltis DE, Soltis PS, Stevens PF et al (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593. doi:10.1146/annurev.ecolsys.38.091206.095818
Buchmann SL (1987) The ecology of oil flowers and their bees. Ann Rev Ecol Syst 18:343–69. doi:10.1146/annurev.es.18.110187.002015
Burnham KP, Anderson DR (2002) Model selection and multimodel inference—a practical-theoretic approach. Springer, Verlag
Camarotti-de-Lima MF, Martins CF (2005) Biologia de nidificação e aspectos ecológicos de Anthodioctes lunatus (Smith) (Hymenoptera: Megachilidae, Anthidiini) em área de tabuleiro nordestino, PB. Neotrop Entomol 34:375–380. doi:10.1590/S1519-566X2005000300003
Carvalho FS, Sartori ÂL (2014) Reproductive phenology and seed dispersal syndromes of woody species in the Brazilian Chaco. J Veg Sci 26:302–311. doi:10.1111/jvs.12227
Dupont YL, Hansen DM, Olesen JM (2003) Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife Canary Islands. Ecography 26:301–310. doi:10.1034/j.1600-0587.2003.03443.x
Ebeling A, Klein AM, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117:1808–1815. doi:10.1111/j.1600-0706.2008.16819.x
Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge
Erhardt A (1993) Pollination of the edelweiss, Leontopodium alpinum. Bot J Linn Soc 111:229–240. doi:10.1006/bojl.1993.1016
Etcheverry AV, Alemán MM, Fleming TF (2008) Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae). Ann Bot 102:305–316. doi:10.1093/aob/mcn106
Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, London
Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. Disponível em: http://floradobrasil.jbrj.gov.br/. Acesso em 10 Ago 2016
Fontaine C, Dajoz I, Mreiguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135
Freitas L, Sazima M (2006) Pollination biology in a tropical high-altitude grassland in Brazil: interactions at the community level. Ann Mo Bot Gard 93:465–516. doi:10.2307/40035488
Freitas TG, Souza CS, Aoki C, Arakaki LMM, Stefanello TH, Sartori ALB, Sigrist MR (2013) Flora of Brazilian humid Chaco: composition and reproductive phenology. Checklist 9:973–979
Galetto L, Bernardello L (2003) Nectar sugar composition in angiosperms from Chaco and Patagonia (Argentina): an animal visitor’s matter? Plant Syst Evol 238:69–86. doi:10.1007/s00606-002-0269-y
Galetto L, Bernardello L (2004) Floral nectaries, nectar production dynamics and chemical composition in six Ipomoea species (Convolvulaceae) in relation to pollinators. Ann Bot 94(2):269–280. doi:10.1093/aob/mch137
Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304. doi:10.1111/j.1365-2745.2006.01098.x
Herrera J (1988) Pollination relationships in southern Spanish Mediterranean shrublands. J Ecol 76:274–287
Imperatriz-fonseca VL, Canhos DAL, Alves DA, Saraiva AM (2012) Polinizadores do Brasil: contribuições e perspectivas para a biodiversidade, uso sustentável, conservação e serviços ambientais. Edusp, São Paulo
Inoue T, Kato M, Kakutani T, Suka T, Itino T (1990) Insect-flower relationship in the temperate deciduous forest of Kibune, Kyoto: an overview of the flowering phenology and the seasonal pattern of insect visits. Contrib Biol Lab Kyoto Univ 27:377–464
Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253. doi:10.2307/1936841
Kato M (2000) Anthophilous insect community and plant-pollinator interactions on Amami Islands in the Ryukyu Archipelago, Japan. Contributions from the Biological Laboratory, Kyoto University 29(2):157–254. http://hdl.handle.net/2433/156116
Kato M, Miura R (1996). Flowering phenology and anthophilous insect community at a threatened natural lowland marsh at Nakaikemi in Tsuruga, Japan. Contributions from the Biological Laboratory, Kyoto University 29:1. http://hdl.handle.net/2433/156114
Kato M, Kakutani T, Inoue T, Itino T (1990) Insect-flower relationship in the primary beech forest of Ashu, Kyoto: an overview of the flowering phenology and the seasonal pattern of insect visits. Contributions from the Biological Laboratory, Kyoto University 27:309–375. http://hdl.handle.net/10091/13206
Kearns CA (2001) North American dipteran pollinators: assessing their value and conservation status. Conserv Ecol 5:1–5
Kovach WL (2004) Oriana for Windows, version 2.0. Kovach Computer Services, Pentraeth
Lopes LA, Blochtein B, Ott AP (2007) Diversidade de insetos antófilos em áreas de reflorestamento de eucalipto, Município de Triunfo, Rio Grande do Sul, Brasil. Iheringia Ser Zool 97:181–193. doi:10.1590/S0073-47212007000200008
Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–376. doi:10.1093/aob/mch152
Machado ICS, Barros LM, Sampaio EVSB (1995) Phenology of Caatinga species at Serra Talhada, PE, Northeastern Brazil. Biotropica 29:57–68. doi:10.1111/j.1744-7429.1997.tb00006.x
Morellato LPC, Leitão Filho HF (1996) Reproductive phenology of climbers in a Southeastern Brazilian forest. Biotropica 28:180–191. doi:10.2307/2389073
Morellato LPC, Alberton B, Alvarado ST, Borges B, Buisson B, Camargo MGG, Cancian LF, Carstensen DW, Escobar DFE, Leite PTP, Mendoza I, Rocha NMWB, Soares NC, Silva TSF, Staggemeier VG, Streher AS, Vargas BC, Peres CA (2016) Linking plant phenology to conservation biology. Biol Conserv 195:60–72. doi:10.1016/j.biocon.2015.12.033
Musicante ML, Galetto L (2008) Biología reproductiva de Cologania broussonetii (Fabaceae, Faboideae). Darwiniana 46:7–16
Newstron LE, Frankie GW, Baker HG, Cowell RK (1994) Diversity of long-term flowering patterns. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva, Ecology and natural history of a neotropical rain forest. Chicago University Press, Chicago, pp 142–160
Oliveira PE, Gibbs PE (2000) Reproductive biology of wood plants in Cerrado community of Central Brazil. Flora 195:311–329
Ormond WT, Pinheiro MCB, Lima HA, Correia MCR, Pimenta ML (1993) Estudo das recompensas florais das plantas da restinga de Maricá– Itaipuaçu, RJ. I—Nectaríferas. Bradea 6:179–195
Ortega-Baes P, Saravia M, Sühring S, Godínez-Alvarez H, Zamar M (2011) Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators. Plant Biol 13:33–40
Pennington RT, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and quaternary vegetation changes. J Biogeogr 27:261–273. doi:10.1046/j.1365-2699.2000.00397.x
Pinheiro MA, Harter-Marques BE, Miotto STS (2008) Floral resources used by insects in a grassland community in Southern Brazil. Rev Bras Bot 31:469–489. doi:10.1590/S0100-84042008000300011
Proctor M, Yeo P, Lack A (1996) The Natural History of Pollination. Timber Press, Portland
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 20 Jun 2015
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214
Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge
Santos FM, Carvalho CAL, Silva RF (2004) Diversidade de abelhas (Hymenoptera: Apoidea) em uma área de transição Cerrado-Amazônia. Act Amaz 34:319–328. doi:10.1590/S0044-59672004000200018
Sigrist T (2007) Guia de campo—Aves do Brasil oriental. Avis Brasilis, São Paulo
Sigrist MR, Sazima M (2004) Pollination biology of twelve species of Neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Ann Bot 94:33–41. doi:10.1093/aob/mch108
Simpson BB, Neff JL (1981) Floral rewards: alternatives to pollen and nectar. Ann Mo Bot Gard 68:301–322. doi:10.2307/2398800
Smith-Ramírez C, Armesto JJ (1994) Flowering and fruiting patterns in the temperate rainforest of Chiloé, Chile—ecologies and climatic constraints. J Ecol 82:353–365. doi:10.2307/2261303
Smith-Ramírez C, Martinez P, Nuñez M, González C, Armesto JJ (2005) Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloé Island, Chile. Bot J Linn Soc 147:399–416. doi:10.1111/j.1095-8339.2005.00388.x
Struck M (1994) Flowers and their insect visitors in the arid winter rainfall region of southern Africa: observations on permanent plots. composition of the anthophilous insect fauna. J Arid Environ 28:45–50. doi:10.1016/S0140-1963(05)80020-5
Talora DC, Morellato LPC (2000) Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Rev Bras Bot 23:13–26. doi:10.1590/S0100-84042000000100002
Torres C, Galetto L (2008) Importancia de los polinizadores en la reproducción de Asteraceae de Argentina Central. Acta Bot Venez 31:473–494
UNESCO (United Nations Educational, Scientific and Cultural) (1973) Ecology and conservation international classification and mapping of vegetation. UNESCO, Paris
Werneck FP (2011) The diversification of eastern South American open vegetation biomes: historical biogeography and perspectives. Quart Sci Rev 30:1630–1648. doi:10.1016/j.quascirev.2011.03.009
Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18
Wolda H, Broadhead E (1985) Seasonality of Psocoptera in two tropical forests in Panama. J Anim Ecol 54:519–530. doi:10.2307/4496
Zar JH (1999) Biostatistical Analysis. Prentice Hall, New Jersey
Acknowledgements
The authors thanks to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (process: 115037/2012-1; 303084/2011-1), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação de Amparo à Pesquisa do Estado de São Paulo (2011/16621-9) for financial support; Sérgio de Oliveira for access to his ranch Retiro Conceição; and specialists who identified the anthophilous fauna: Ayr de Moura Bello (beetles), Dr. André Victor Lucci Freitas (butterflies), Dr. Manoel Fernando Demétrio (ants), Dr. Maria Antonietta Castro Pivatto (hummingbirds), Ana Gabrielle Lubas Arruda, and Dr. Carlos José Einicker Lamas (flies). The authors also thanks to Fábia Silva de Carvalho and Bárbara Ellen de Medeiros Pinto for the identification of plant species.
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de Souza, C.S., Aoki, C., Alcantara, D.M.C. et al. Diurnal anthophilous fauna in Brazilian Chaco vegetation: phenology and interaction with flora. Braz. J. Bot 40, 203–213 (2017). https://doi.org/10.1007/s40415-016-0338-z
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DOI: https://doi.org/10.1007/s40415-016-0338-z


