Abstract
Birds are common visitors of bromeliads, despite the scarcity of studies on the association of these plants with bird communities, especially for terrestrial and rupicolous species. In the present study we first address the association of a bird community with rupicolous bromeliads (Encholirium spectabile) in rocky outcrops of the Brazilian semi-arid region. The observations were made monthly between 2014 and 2018. The species of birds which used bromeliads were recorded, as well as the abundance of individuals and the interaction (guilds) between bird species and bromeliads. We also test the possible effects of seasonality on the richness and composition of bird species recorded between the dry and rainy seasons. Twenty-one species in 12 families that used bromeliads regularly were recorded and this number rises to 31 species in 16 families when considering the opportunistic records. Birds used bromeliads as a feeding site for either nectar or small animals, and as a place for nesting or resting. There were no significant differences as to the richness or abundance of bird species between seasons, but the species composition changed between them. The study shows that E. spectabile is an important kind of bromeliad for the bird community, as it plays a key role in inhabiting their surroundings. Therefore, the conservation of these bromeliads directly impacts the conservation of birds that use them. We suggest the clumps of E. spectabile as a place for bird watching in the semi-arid region of Brazil.
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References
Ab’saber AN (1974) O domínio morfoclimático semi-árido das caatingas brasileiras. Geomorfologia 43:1–39
Benzing DH (2000) Bromeliaceae: Profile of an adaptive radiation. Cambridge University Press. 690 pp. https://doi.org/10.1017/S0960428602240159
Blondel J (2003) Guilds or functional groups: Does it matter? Oikos 100:223–231. https://doi.org/10.1034/j.1600-0706.2003.12152.x
Bodrati A, Cockle KL (2017) Nest, eggs and reproductive behavior of greenish schiffornis (Schiffornis virescens). Rev Brasil Ornitol 25:273–276. https://doi.org/10.1007/BF03544407
Boechat RF, Silva BF, Nunes-Freitas AF (2019) Bird-epiphyte interactions in three Atlantic Forest environments in southeastern Brazil. Rev Brasil Ornitol 27:108–114. https://doi.org/10.1007/BF03544454
Butcher D, Gouda E (2017) The new bromeliad taxon list. University Botanic Gardens, Utrecht, Netherlands
Canela MBF, Sazima M (2003) Florivory by the crab Armases angustipes (Grapsidae) influences hummingbird visits to Aechmea pectinata (Bromeliaceae). Biotropica 35:289–294. https://doi.org/10.1111/j.1744-7429.2003.tb00287.x
Cestari C (2009) Epiphyte plants use by birds in Brazil. Oecol Bras 13:689–712. https://doi.org/10.4257/oeco.2009.1304.12
Cestari C, Pizo MA (2008) Utilization of epiphytes by birds in a Brazilian Atlantic Forest. Ornitol Neotrop 19:97–107
Cruz-Angon A, Greenberg R (2005) Are epiphytes important for birds in coffee plantations? An experimental assessment. J Appl Ecol 42:150–159. https://doi.org/10.1111/j.1365-2664.2004.00983.x
Develey PF (2021) Bird conservation in Brazil: challenges and practical solutions for a key megadiverse country. Perspect Ecol Conserv 19:171–178. https://doi.org/10.1016/j.pecon.2021.02.005
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics software package for education and data analysis. Paleontol Electron 4:1–9
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373. https://doi.org/10.2307/3545850
Jorge JS, Santos RL, Almeida EA, Freire EMX (2014) First record of Hemidactylus agrius (Squamata, Gekkonidae) in thickets of Encholirium spectabile (Bromeliaceae) in the Brazilian semi-arid. Biota Amazon 4:176–179
Jorge JS, Sales RFD, Kokubum MNK, Freire EMX (2015) On the natural history of the Caatinga horned frog, Ceratophrys joazeirensis (Anura: Ceratrophryidae), a poorly known species of northeastern Brazil. Phyllomedusa 14:147–156. https://doi.org/10.11606/issn.2316-9079.v14i2p147-156
Jorge JS, Rocha LHS, Rocha JPS, Sousa PHP, Santos RL, Freire EMX (2018) Floral visitors and potential pollinators of a rupicolous bromeliad (Pitcairnioideae) in the Brazilian semi-arid. Neotrop Biol Conserv 13:101–110. https://doi.org/10.4013/nbc.2018.132.02
Jorge JS, Sales RFD, Santos RL, Freire EMX (2020) Living among thorns: herpetofaunal community (Anura and Squamata) associated to the rupicolous bromeliad Encholirium spectabile (Pitcairnioideae) in the Brazilian semi-arid Caatinga. Zoologia 37:e46661. https://doi.org/10.3897/zoologia.37.e46661
Jorge JS, Freire EMX, Caliman AC (2021a) The rupicolous bromeliad (Encholirium spectabile) as a keystone species for Brazilian semi-arid biodiversity. Ecology 102:e03357. https://doi.org/10.1002/ecy.3357
Jorge JS, Silva-Jorge JP, Santos RL, Caliman A, Freire EMX (2021b) Association of Strymon serapio (Lycaenidae:Theclinae) and Castnia invaria (Castiniidae: castniini) with the habitat-forming bromeliad Encholirium spectabile (Bromeliaceae: Pitcairnioideae) in the Brazilian Semiarid Caatinga. J Lepid Soc 75:37–43. https://doi.org/10.18473/lepi.75i1.a5
Jorge JS, Sales RFD, Silva VTC, Freire EMX (2021c) Lizards and bromeliads in the Neotropics: literature review and relevance of this association to conservation. Symbiosis 84:119–130. https://doi.org/10.1007/s13199-021-00779-z
Kitching RL (2000) Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press
Krömer T, Kessler M, Herzog SK (2006) Distribution and flowering ecology of bromeliads along two climatically contrasting elevation transects in the Bolivian Andes. Biotropica 38:183–195. https://doi.org/10.1111/j.1744-7429.2006.00124.x
Ladino G, Ospina-Bautista F, Estévez-Varón J, Jerabkova L, Kratina P (2019) Ecosystem services provided by bromeliad plants: a systematic review. Ecol Evol 9:7360–7372. https://doi.org/10.1002/ece3.5296
Leal RLB, Moreira MM, Pinto AR, Ferreira JO, Rodriguez-Girones M, Freitas L (2020) Temporal changes in the most effective pollinator of a bromeliad pollinated by bees and hummingbirds. PeerJ 8:e8836. https://doi.org/10.7717/peerj.8836
Leroy C, Carrias JF, Corbara B, Pélozuelo L, Dézerald O, Brouard O, Céréghino R (2013) Mutualistic ants contribute to tank-bromeliad nutrition. Ann Bot 112:919–926. https://doi.org/10.1093/aob/mct147
Lounibos LP, Frank JH (2009) Insects and allies associated with bromeliads: a review. Terr Arthropod Rev 1:125–153. https://doi.org/10.1163/187498308X414742
Machado CG, Semir J (2009) Fenologia da floração e biologia floral de bromeliáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Rev Bras de Bot 29:163–174. https://doi.org/10.1590/S0100-84042006000100014
Millennium Ecosystem Assessment (2005) Ecosystems and human well-being Synthesis. Island Press, Washington, DC
Pacheco JF, Silveira LF, Aleixo A, Agne CE, Bencke GA, Bravo GA, Brito GRR, Cohn-Haft M, Mauricio GN, Naka LN, Olmos F, Posso S, Lees AC, Figueiredo LFA, Carrano E, Guedes RC, Cesari E, Franz I, Schunck F, Piacentini VQ (2021) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee - second edition. Ornithol Res 29:94–105. https://doi.org/10.1007/s43388-021-00058-x
Queiroz JA, Quirino ZGM, Lopes AV, Machado IC (2016) Vertebrate mixed pollination system in Encholirium spectabile: abromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ 125:21–30. https://doi.org/10.1016/j.jaridenv.2015.09.015
Ramalho M, Batista MA, Silva M (2004) Xylocopa (Monoxylocopa) abbreviata Hurd and Moure (Hymenoptera: Apidae) e Encholirium spectabile (Bromeliaceae): uma associação estreita no semi-árido do Brasil tropical. Neotrop Entomol 33:417–425. https://doi.org/10.1590/S1519-566X2004000400004
Rees WE, Roe NA (1980) Puya raimondii (Pitcairnioideae, Bromeliaceae) and birds: a hypothesis on nutrient relationships. Can J Bot 58:1262–1268. https://doi.org/10.1139/b80-157
Rizzini CT (1997) Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. Âmbito Cultural Edições, Rio de Janeiro
Rocha J (2022) Neotropical bromeliads as food sources for birds: a systematic review and perspectives on the management of ecological interactions. Ibis 165:17–33. https://doi.org/10.1111/ibi.13138
Rocha CFD, Cogliatti-Carvalho L, Nunes-Freitas AF, Rocha-Pessôa TC, Dias ADS, Ariani CV, Morgado LN (2004) Conservando uma larga porção da diversidade biológica através da conservação de Bromeliaceae. Vidalia 2:52–68
Romero GQ, Nomura F, Gonçalves AZ, Dias NY, Mercier H, Conforto EDC, Rossa-Feres DDC (2010) Nitrogen fluxes from treefrogs to tank epiphytic bromeliads: an isotopic and physiological approach. Oecologia 162:941–949. https://doi.org/10.1007/s00442-009-1533-4
Romero GQ, Gonçalves-Souza T, Roslin T, Marquis RJ, Marino NAC, Novotny V, Cornelissen T, Orivel J, Sui S, Aires G, Antoniazzi R, Dáttilo W, Breviglieri CPB, Busse A, Gibb H, Izzo TJ, Kadlec T, Kemp V, Kersch-Becker M, Koricheva J (2022) Climate variability and aridity modulate the role of leaf shelters for arthropods: a global experiment. Glob Change Biol 28:3694–3710. https://doi.org/10.1111/gcb.16150
Sabagh LT, Ferreira RB, Rocha CFD (2017) Host bromeliads and their associated frog species: further considerations on the importance of species interactions for conservation. Symbiosis 73:201–211. https://doi.org/10.1007/s13199-017-0500-9
Sales RF, Andrade MJ, Jorge JDS, Kolodiuk MF, Ribeiro MM, Freire EMX (2015) Geographic distribution model for Mabuya agmosticha (Squamata: Scincidae) in northeastern Brazil. Zoologia 32:71–76. https://doi.org/10.1590/S1984-46702015000100011
Santana CS, Machado CG (2010) Fenologia de floração e polinização de espécies ornitófilas de bromeliáceas em uma área de campo rupestre da Chapada Diamantina, BA, Brasil. Rev Bras Bot 33:469–477. https://doi.org/10.1590/S0100-84042010000300009
Sazima I, Buzato S, Sazima M (1995) The saw-billed hermit Ramphodon naevius and its flowers in southeastern. Brazil J Ornithol 136:195–206. https://doi.org/10.1007/BF01651241
Sazima I, Buzato S, Sazima M (1996) An assemblage of hummingbird-pollinated flowers in a montane forest in southeastern. Acta Bot Brazil 109:149–160. https://doi.org/10.1111/j.1438-8677.1996.tb00555.x
Sazima M, Buzato S, Sazima I (1999) Bat-pollinated flower assemblages and bat visitors at two Atlantic Forest sites in Brazil. Ann Bot 83:705–712. https://doi.org/10.1006/anbo.1999.0876
Schmid S, Schmid VS, Kamke R et al (2010) Association of three species of Strymon hubner (Lycaenidae: Theclinae: Eumaeini) with bromeliads in southern Brazil. J Res Lepid 42:50–55. https://doi.org/10.5962/p.266514
Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro
Sillett TS, James A, Sillett KB (1997) Bromeliad foraging specialization and diet selection of Pseudocolaptes lawrencii (Furnariidae). Ornithol Monogr 48:733–742. https://doi.org/10.2307/40157564
Silva HR, Carvalho ALG, Bittencourt-Silva GB (2011) Selecting a hiding place: anuran diversity and the use of bromeliads in threatened coastal sand dune habitat in Brazil. Biotropica 4:218–227. https://doi.org/10.1111/j.1744-7429.2010.00656.x
Srivastava DS, Kolasa J, Bengtsson J et al (2004) Are natural microcosms useful model systems for ecology? Trends Ecol Evol 19:379–384. https://doi.org/10.1016/j.tree.2004.04.010
Ulloa CU, Acevedo-Rodríguez P, Beck S, Belgrano MJ, Bernal R, Berry PE, Gradstein SR (2017) An integrated assessment of the vascular plant species of the Americas. Science 358:1614–1617. https://doi.org/10.1126/science.aao0398
Velloso AL, Sampaio ESB, Pareyn FGC (2002) Ecorregiões propostas para o bioma Caatinga. Associação Plantas do Nordeste, Instituto de Conservação Ambiental, The Nature Conservancy Brasil, Recife 76 pp
Whelan CJ, Sekercioglu ÇH, Wenny DG (2015) Why birds matter: from economic ornithology to ecosystem services. J Ornithol 156:227–238. https://doi.org/10.1007/s10336-015-1229-y
Zima PVQ, Perrella DF, Francisco MR (2019) First nest description of the azure-shouldered tanager (Thraupis cyanoptera, Thraupidae). Rev Brasil Ornitol 27:122–125. https://doi.org/10.1007/BF03544456
Zizka A, Azevedo J, Leme E, Neves B, Costa AF, Caceres D, Zizka G (2020) Biogeography and conservation status of the pineapple family (Bromeliaceae). Divers Distrib 26:183–195. https://doi.org/10.1111/ddi.13004
Acknowledgements
This study was supported by research grants from the National Council for Scientific and Technological Development (CNPq) to JSJ (Process130363/2014-6) and EMXF (Process 313661/2017-0) and from the Coordination for the Improvement of Higher Education Personnel (CAPES). We also thank the employees of Fazenda Tanques for their support in the field and all others who helped by giving feedback to improve the manuscript. We also thank Matheus Rocha, two anonymous reviewers and the editors for helpful comments on the manuscript.
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Jorge, J.S., Sousa, P.H.P., de Albuquerque França, B.R. et al. Among flowers and thorns: birds associated with Encholirium spectabile, a keystone bromeliad in a Brazilian semi-arid region. Ornithol. Res. 31, 93–102 (2023). https://doi.org/10.1007/s43388-023-00129-1
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DOI: https://doi.org/10.1007/s43388-023-00129-1