Floral biology, breeding system and effective pollinators of the epiphytic bromeliad Tillandsia limbata
DOI:
https://doi.org/10.17129/botsci.3582Keywords:
Florivory, nectar secretion, ornithophily, pollen limitation, reproductive success, self-incompatibilityAbstract
Background: The Bromeliaceae family has undergone one of the most remarkable adaptive radiations within angiosperms, partly due to its diversity of reproductive strategies. However, pollinators are known for only 4 % of its more than 3,800 species.
Questions: What is the flowering pattern like? Which are the characteristics of nectar? What is the breeding system? Which are the effective pollinators?
Studied species: Tillandsia limbata Schldl.
Study site and dates: The study was carried out in Catemaco, Veracruz, Mexico, from April to October, 2021.
Methods: Phenology was determined by recording daily the number of open flowers and their characteristics at different stages of anthesis. Nectar secretion was evaluated by extractions during anthesis. Identification of floral visitors was carried out through recordings and direct observations. The breeding system and pollinator effectiveness were determined using controlled pollination experiments.
Results: Tillandsia limbata produces on average 2.6 flowers per day, with a constant nectar secretion during the day and a self-incompatibility system with high xenogamous capacity. Ten species of floral visitors were recorded, of which the most frequent were the bee Trigona fulviventris and the hummingbird Anthracothorax prevostii.
Conclusions: The effective pollinators of T. limbata are hummingbirds, as they favor the most fruit and seed production. Bees are secondary pollinators; however, they steal pollen and nectar, consume floral parts and displace hummingbirds from flowers, which negatively affects the reproductive success of this bromeliad.
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References
Ackerman JD, Rodríguez-Robles JA, Meléndez EJ. 1994. A meager nectar offering by an epiphytic orchid is better than nothing. Biotropica 26: 44-49. DOI: http://dx.doi.org/10.2307/2389109 DOI: https://doi.org/10.2307/2389109
Aguilar-Rodríguez PA, Krömer T, García-Franco JG, MacSwiney GMC. 2016. From dusk till dawn: Nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae). Plant Biology 18: 37-45. DOI: https://doi.org/10.1111/plb.12319 DOI: https://doi.org/10.1111/plb.12319
Aguilar-Rodríguez PA, Krömer T, Tschapka M, García-Franco JG, Escobedo-Sarti J, MacSwiney GMC. 2019. Bat pollination in Bromeliaceae. Plant Ecology and Diversity 12:1-19. DOI: https://doi.org/10.1080/17550874.2019.1566409 DOI: https://doi.org/10.1080/17550874.2019.1566409
Ashworth L, Aguilar R, Martén-Rodríguez S, Lopezaraiza-Mikel M, Avila-Sakar G, Rosas-Guerrero V, Quesada M. 2015. Pollination Syndromes: A Global Pattern of Convergent Evolution Driven by the Most Effective Pollinator. In: Pontarotti P. ed. Evolutionary Biology: Biodiversification from Genotype to Phenotype. Cham: Springer. 203-224 pp. ISBN: 978-3-319-19932-0 DOI: https://doi.org/10.1007/978-3-319-19932-0_11 DOI: https://doi.org/10.1007/978-3-319-19932-0_11
Bertness MD, Shumway SW. 1992. Consumer driven pollen limitation of seed production in marsh grasses. American Journal of Botany 79: 288-293. DOI: https://doi.org/10.2307/2445017 DOI: https://doi.org/10.1002/j.1537-2197.1992.tb14550.x
Baker HG. 1975. Sugar concentrations in nectars from hummingbird flowers. Biotropica 7: 37-41. DOI: https://doi.org/10.2307/2989798 DOI: https://doi.org/10.2307/2989798
Becker T, Voss N, Durka W. 2011. Pollen limitation and inbreeding depression in an “old rare” bumblebee-pollinated grassland herb. Plant Biology 13: 857-864. DOI: https://doi.org/10.1111/j.1438-8677.2011.00452.x DOI: https://doi.org/10.1111/j.1438-8677.2011.00452.x
Benzing DH. 2000. Bromeliaceae: Profile of an Adaptive Radiation. Cambridge, UK: Cambridge University Press. ISBN: 0-521-43031-3
Bernardello LM, Galetto L, Juliani HR. 1991. Floral nectar, nectary structure and pollinators in some Argentinean Bromeliaceae. Annals of Botany 67: 401-411. DOI: https://doi.org/10.1093/oxfordjournals.aob.a088156 DOI: https://doi.org/10.1093/oxfordjournals.aob.a088174
Bhat DM, Murali KS. 2001. Phenology of understorey species of tropical moist forest of Western Ghats region of Uttara Kannada district in South India. Current Science 81:799-805
Canela MBF, Sazima M. 2003. Aechmea pectinata: a hummingbird-dependent bromeliad with inconspicuous flowers from the rainforest in south-eastern Brazil. Annals of Botany 92: 731-737. DOI: https://doi.org/10.1093/aob/mcg192 DOI: https://doi.org/10.1093/aob/mcg192
Canela MBF, Sazima M. 2005. The pollination of Bromelia antiacantha (Bromeliaceae) in southeastern Brazil: Ornithophilous versus melittophilous features. Plant Biology 7: 411-416. DOI: https://doi.org/10.1055/s-2005-865619 DOI: https://doi.org/10.1055/s-2005-865619
Cascante-Marín A, Núñez-Hidalgo S. 2023. A review of breeding systems in the pineapple family (Bromeliaceae, Poales). Botanical Review 89: 308-329. DOI: https://doi.org/10.1007/s12229-023-09290-0 DOI: https://doi.org/10.1007/s12229-023-09290-0
Cascante-Marín A, Wolf JHD, Oostermeijer JGB. 2009. Wasp florivory decreases reproductive success in an epiphytic bromeliad. Plant Ecology 203: 149-153. DOI: https://doi.org/10.1007/s11258-008-9522-y DOI: https://doi.org/10.1007/s11258-008-9522-y
Cascante-Marín A, Oostermeijer JGB, Wolf JHD, den Nijs JCM. 2005. Reproductive biology of the epiphytic bromeliad Werauhia gladioliflora in a premontane tropical forest. Plant Biology 7: 203-209. DOI: https://doi.org/10.1055/s-2005-837584 DOI: https://doi.org/10.1055/s-2005-837584
da Cruz DD, Mello MA, Van Sluys M. 2006. Phenology and floral visitors of two sympatric Heliconia species in the Brazilian Atlantic Forest. Flora-Morphology, Distribution, Functional Ecology of Plants 201: 519-527. DOI: https://doi.org/10.1016/j.flora.2005.12.001 DOI: https://doi.org/10.1016/j.flora.2005.12.001
Dafni A. 1992. Pollination Ecology. A Practical Approach. Oxford UK: Oxford University Press. ISBN: 0-19-963298-7
Dafni A, Motta MM. 1998. A rapid and simple procedure to determine stigma receptivity. Sexual Plant Reproduction 11: 177-180. DOI: https://doi.org/10.1007/s004970050138 DOI: https://doi.org/10.1007/s004970050138
de Queiroz PV, Varassin IG. 2007. Interaction network and the relationships between bromeliads and hummingbirds in an area of secondary Atlantic rain forest in southern Brazil. Journal of Tropical Ecology 23: 663-671. DOI: https://doi.org/10.1017/S026646740700449X DOI: https://doi.org/10.1017/S026646740700449X
Díaz-Infante S, Lara C, Arizmendi MC. 2020. Temporal dynamics of the hummingbird-plant interaction network of a dry forest in Chamela, Mexico: a 30 year follow up after two hurricanes. PeerJ 8: e8338. DOI: https://doi.org/10.7717/peerj.8338 DOI: https://doi.org/10.7717/peerj.8338
Dirzo R, García MC. 1992. Rates of deforestation in Los Tuxtlas, a neotropical area in southeast México. Conservation Biology 6: 84-90. DOI: https://doi.org/10.1046/j.1523-1739.1992.610084.x
do Carmo RM, Franceschinelli EV, da Silveira FA. 2004. Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral re-source taken by native pollinators. Biotropica 36: 317-376. DOI: http://doi.org/10.1646/03094 DOI: https://doi.org/10.1111/j.1744-7429.2004.tb00329.x
Espejo-Serna A, Gómez-Escamilla IN, Ballesteros-Barrera C. 2017. Tillandsia limbata (flor de incienso). Registros de presencia usados para elaborar el mapa de distribución potencial. http://www.conabio.gob.mx/informacion/gis/?vns=gis_root/biodiv/distpot/dpplant/dppliliopd/tli008dpgw (accessed June 11, 2024).
Espejo-Serna A, López-Ferrari AR. 2018. La familia Bromeliaceae en México. Botanical Sciences 96: 533-554. DOI: https://doi.org/10.17129/botsci.1918 DOI: https://doi.org/10.17129/botsci.1918
Espejo-Serna A, López-Ferrari AR, Ramírez-Morillo I. 2005. Bromeliaceae. Flora de Veracruz. 136: 1-307
Faegri K, van der Pijl L. 1979. The principles of pollination ecology. Oxford, UK: Pergamon Press. ISBN: 978-0-08-021338-5
Faria RR, Araújo AC. 2010. Flowering phenology and pollination of ornithophilous species in two habitats of Serra da Bodoquena, Mato Grosso do Sul, Brazil. Anais Da Academia Brasileira De Ciências 82: 843-855. DOI: https://doi.org/10.1590/S0001-37652010000400006 DOI: https://doi.org/10.1590/S0001-37652010000400006
Feinsinger P, Colwell RK. 1978. Community organization among Neotropical nectar-feeding birds. American Zoologist 18: 779-795. DOI: https://doi.org/10.1093/icb/18.4.779 DOI: https://doi.org/10.1093/icb/18.4.779
Feinsinger P, Chaplin SB. 1975. On the relationship between wing disc loading and foraging strategy in hummingbirds. The American Naturalist 109: 217-224. DOI: https://doi.org/10.1086/282988 DOI: https://doi.org/10.1086/282988
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD, Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35: 375-403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347 DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Freeman CE, Reid WH, Becvar JE, Scogin R. 1984. Similarity and apparent convergence in the nectar-sugar composition of some hummingbird-pollinated flowers. Botanical Gazette 145: 132-135. DOI: https://doi.org/10.1086/337436 DOI: https://doi.org/10.1086/337436
Freitas L. 2018. Precisamos falar sobre o uso impróprio de recursos florais. Rodriguésia 68: 2223-2228. DOI: https://doi.org/10.1590/2175-7860201869446 DOI: https://doi.org/10.1590/2175-7860201869446
García-Franco JG, Rico-Gray V. 1991. Reproductive biology of Tillandsia deppeana (Bromeliaceae) in Veracruz, Mexico. Brenesia 35: 61-79.
Gardner CS. 1986. Inferences about pollination in Tillandsia (Bromeliaceae). Selbyana 9: 76-97.
Gentry AH. 1974. Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6: 64-68. DOI: https://doi.org/10.2307/2989698 DOI: https://doi.org/10.2307/2989698
Givnish TJ, Barfuss MHJ, van EB, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Sytsma KJ. 2014. Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Molecular Phylogenetics and Evolution 71: 55-78. DOI: https://doi.org/10.1016/j.ympev.2013.10.010 DOI: https://doi.org/10.1016/j.ympev.2013.10.010
Gouda EJ, Butcher D, Gouda CS. 2023. Encyclopaedia of Bromeliads, Version 5. Utrecht, Nederland: Utrecht University Botanic Gardens. http://bromeliad.nl/encyclopedia/ (accessed June 13, 2024).
Guevara S, Laborde J, Sánchez-Ríos J. 2004. Los Tuxtlas. El paisaje de la sierra. Xalapa, México: Instituto de Ecología, AC. ISBN: 970-709-043-X
Hargreaves AL, Harder LD, Johnson SD. 2009. Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biological Reviews 84: 259-276. https://doi.org/10.1111/j.1469-185X.2008.00074.x DOI: https://doi.org/10.1111/j.1469-185X.2008.00074.x
Hornung-Leoni CT, González-Gómez PL, Troncoso AJ. 2013. Morphology, nectar characteristics and avian pollinators in five Andean Puya species (Bromeliaceae). Acta Oecologica 51: 54-61. DOI: https://doi.org/10.1016/j.actao.2013.05.010 DOI: https://doi.org/10.1016/j.actao.2013.05.010
Irwin RE, Bronstein JL, Manson JS, Richardson L. 2010. Nectar robbing: ecological and evolutionary perspectives. Annual Review of Ecology, Evolution, and Systematics 41: 271-292 DOI: https://doi.org/10.1146/annurev.ecolsys.110308.120330 DOI: https://doi.org/10.1146/annurev.ecolsys.110308.120330
Jaeger S, Girvin C, Demarest N, LoPresti E. 2023. Secondary pollinators contribute to reproductive success of a pink-flowered sand verbena population. Ecology 104: e3977. DOI: https://doi.org/10.1002/ecy.3977 DOI: https://doi.org/10.1002/ecy.3977
Janzen DH. 1967. Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21: 620-637. DOI: https://doi.org/10.2307/2406621 DOI: https://doi.org/10.1111/j.1558-5646.1967.tb03416.x
Juárez R, Huffstater K, Arizmendi MC, Rodríguez-Flores CI, Soberanes-González CA. 2022. Green-breasted Mango (Anthracothorax prevostii). Version 2.0. Birds of the World Ithaca, NY, USA: Cornell Lab of Ornithology DOI: https://doi.org/10.2173/bow.gnbman.02
Kamke R, Schmid S, Zillikens A, Lopes BC, Steiner J. 2011. The importance of bees as pollinators in the short corolla bromeliad Aechmea caudata in southern Brazil. Flora 206: 749-756. DOI: https://doi.org/10.1016/j.flora.2010.12.004 DOI: https://doi.org/10.1016/j.flora.2010.12.004
Kearns CA, Inouye DW. 1993. Techniques for pollination biologists. Denver, Colorado: University Press of Colorado. ISBN: 978-0-87081-281-1
Kessler M, Abrahamczyk S, Krömer T. 2020. The role of hummingbirds in the evolution and diversification of Bromeliaceae: Unsupported claims and untested hypotheses. Botanical Journal of the Linnean Society 192: 592-608. DOI: https://doi.org/10.1093/botlinnean/boz100 DOI: https://doi.org/10.1093/botlinnean/boz100
Kessler M, Krömer T. 2000. Patterns and ecological correlates of pollination modes among bromeliad communities of Andean forests in Bolivia. Plant Biology 2: 659-669. DOI: https://doi.org/10.1055/s-2000-16642 DOI: https://doi.org/10.1055/s-2000-16642
Krauss SL, Phillips RD, Karron JD, Johnson SD, Roberts DG, Hopper SD. 2017. Novel consequences of bird pollination for plant mating. Trends in Plant Science 22: 395-410. DOI: https://doi.org/10.1016/j.tplants.2017.03.005 DOI: https://doi.org/10.1016/j.tplants.2017.03.005
Krömer T, Acebey A. 2007. The bromeliad flora of the San Martin Tuxtla volcano, Veracruz, Mexico. Journal of Bromeliad Society 57: 62-69.
Krömer T, Espejo-Serna A, López-Ferrari AR, Acebey AR, García-Cruz J, Mathieu G. 2020. Las angiospermas epífitas del estado de Veracruz, México: Diversidad y distribución. Revista Mexicana de Biodiversidad 91: e913415. DOI: https://doi.org/10.22201/ib.20078706e.2020.91.3415 DOI: https://doi.org/10.22201/ib.20078706e.2020.91.3415
Krömer T, Kessler M, Herzog SK. 2006. Distribution and flowering ecology of bromeliads along two climatically contrasting elevational transects in the Bolivian Andes. Biotropica 38: 183-195. DOI: https://doi.org/10.1111/j.1744-7429.2006.00124.x DOI: https://doi.org/10.1111/j.1744-7429.2006.00124.x
Krömer T, Kessler M, Lohaus G, Schmidt-Lebuhn AN. 2008. Nectar sugar composition and concentration in relation to pollination syndromes in Bromeliaceae. Plant Biology 10: 502-511. DOI: https://doi.org/10.1111/j.1438-8677.2008.00058.x DOI: https://doi.org/10.1111/j.1438-8677.2008.00058.x
Larson BMH, Barrett SCH. 2000. A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69: 503-520. DOI: https://doi.org/10.1006/bijl.1999.0372 DOI: https://doi.org/10.1111/j.1095-8312.2000.tb01221.x
Lieberman D, Lieberman M. 1984. The causes and consequences of synchronous flushing in a dry tropical forest. Biotropica 16: 193-201. DOI: https://doi.org/10.2307/2388052 DOI: https://doi.org/10.2307/2388052
Martén-Rodríguez S, Fenster CB. 2008. Pollination ecology and breeding systems of five Gesneria species from Puerto Rico. Annals of Botany 102: 23-30. DOI: https://doi.org/10.1093/aob/mcn056 DOI: https://doi.org/10.1093/aob/mcn056
Martinelli G. 1994. Reproductive biology of Bromeliaceae in the Atlantic Rainforest of Southeastern Brazil. PhD Thesis. University of St Andrews.
Matallana G, Godinho MAS, Guilherme FAG, Belisario M, Coser TS, Wendt T. 2010. Breeding systems of Bromeliaceae species: Evolution of selfing in the context of sympatric occurrence. Plant Systematics and Evolution 289: 57-65. DOI: https://doi.org/10.1007/s00606-010-0332-z DOI: https://doi.org/10.1007/s00606-010-0332-z
McCall AC. 2008. Florivory affects pollinator visitation and female fitness in Nemophila menziesii. Oecologia 155: 729-737. DOI: https://doi.org/10.1007/s00442-007-0934-5 DOI: https://doi.org/10.1007/s00442-007-0934-5
McCall AC, Irwin RE. 2006. Florivory: the intersection of pollination and herbivory. Ecology Letters 9: 1351-1365. DOI: https://doi.org/10.1111/j.1461-0248.2006.00975.x DOI: https://doi.org/10.1111/j.1461-0248.2006.00975.x
Missagia CCC, Mendes CJO, Alves MAS. 2023. Performance of pollinators of the tropical bromeliad Tillandsia stricta Sol. (Bromeliaceae) in the Atlantic Forest, Rio de Janeiro. Plant Ecology & Diversity 16: 179-188. DOI: https://doi.org/10.1080/17550874.2023.2261927 DOI: https://doi.org/10.1080/17550874.2023.2261927
Moreira X, Castagneyrol B, Abdala-Roberts L, Traveset A. 2019. A meta-analysis of herbivore effects on plant attractiveness to pollinators. Ecology 100: e02707. DOI: https://doi.org/10.1002/ecy.2707 DOI: https://doi.org/10.1002/ecy.2707
Newstrom LE, Frankie GW, Baker HG. 1994. A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26: 141-159. DOI: https://doi.org/10.2307/2388804 DOI: https://doi.org/10.2307/2388804
Ohashi K, Thomson JD. 2009. Trapline foraging by pollinators: its ontogeny, economics and possible consequences for plants. Annals of Botany 103: 1365-1378. DOI: https://doi.org/10.1093/aob/mcp088 DOI: https://doi.org/10.1093/aob/mcp088
Orozco-Ibarrola OA, Flores-Hernández PS, Victoriano-Romero E, Corona-López AM, Flores-Palacios A. 2015. Are breeding system and florivory associated with the abundance of Tillandsia species (Bromeliaceae)? Botanical Journal of the Linnean Society 177: 50-65. DOI: https://doi.org/10.1111/boj.12225 DOI: https://doi.org/10.1111/boj.12225
Paton DC. 1993. Honeybees Apis mellifera in the Australian environment: Does Apis melifera disrupt or benefit native biota? Bioscience 43: 95-103. DOI: https://doi.org/10.2307/1311970 DOI: https://doi.org/10.2307/1311970
Piacentini VQ, Varassin IG. 2007. Interaction network and the relationships between bromeliads and hummingbirds in an area of secondary Atlantic rain forest in southern Brazil. Journal of Tropical Ecology 23: 663-671. DOI: https://doi.org/10.1017/S026646740700449X DOI: https://doi.org/10.1017/S026646740700449X
Pierce S, Gottsberger RA. 2001. Bromeliad flowers, and attractive meal for weevils at Cerro Jefe, Panama. Journal of the Bromeliad Society 51: 172-177.
Pinzón JP, Ramírez-Morillo IM, Carnevali G, Till W, Butcher D, Ortiz-Díaz JJ. 2019. Taxonomic treatment of the Tillandsia utriculata complex (Bromeliaceae). Annals of the Missouri Botanical Garden 104: 262-323. DOI: https://doi.org/10.3417/2019315 DOI: https://doi.org/10.3417/2019315
Raguso RA, Llorente-Bousquets J. 1991. The butterflies (Lepidoptera) of the Tuxtlas Mts., Veracruz, Mexico, revisited: species-richness and habitat disturbance. Journal of Research on the Lepidoptera 29: 105-133. DOI: https://doi.org/10.5962/p.266622 DOI: https://doi.org/10.5962/p.266622
Ramírez N, Brito Y. 1990. Reproductive biology of tropical palm swamp community in the Venezuelan Llanos. American Journal of Botany 77: 1260-1271. DOI: https://doi.org/10.2307/2444587 DOI: https://doi.org/10.1002/j.1537-2197.1990.tb11378.x
Ramírez-Morillo IM, Chi MF, Carnevali G, May PF. 2009. It takes two to tango: self-incompatibility in the bromeliad Tillandsia streptophylla (Bromeliaceae) in Mexico. Revista de Biología Tropical 57: 761-770. DOI: https://doi.org/10.15517/rbt.v57i3.5490 DOI: https://doi.org/10.15517/rbt.v57i3.5490
Ramírez-Morillo IM, González JU, Chi F, Carnevali G, May F. 2008. Reproductive biology of six species of Tillandsia L. (Bromeliaceae) in Mexico. Journal of the Bromeliad Society 58: 149-155.
Ramírez-Rosas K, Aguirre-Jaimes A, Ramírez-Morillo IM, García-Franco JG. 2020. Floral biology and potential hybridization of three sympatric epiphytic bromeliads in Veracruz, Mexico. Plant Species Biology 35: 197-209. DOI: https://doi.org/10.1111/1442-1984.12279 DOI: https://doi.org/10.1111/1442-1984.12279
Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida, JM, Quesada M. 2014. A quantitative review of pollination syndromes: Do floral traits predict effective pollinators? Ecology Letters 17: 388-400. DOI: https://doi.org/10.1111/ele.12224 DOI: https://doi.org/10.1111/ele.12224
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. Revista Brasileira de Botânica 33: 469-477. DOI: https://doi.org/10.1590/S0100-84042010000300009
Sáyago R, Quesada M, Aguilar R, Ashworth L, Lopezaraiza-Mikel M, Martén-Rodríguez S, 2018. Consequences of habitat fragmentation on the reproductive success of two Tillandsia species with contrasting life history strategies. AoB Plants 10: ply038. DOI: https://doi.org/10.1093/aobpla/ply038 DOI: https://doi.org/10.1093/aobpla/ply038
Schmid S, Schmid VS, Zillikens A, Harter-Marques B, Steiner J. 2011. Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biology 13: 41-50. DOI: https://doi.org/10.1111/j.1438-8677.2010.00348.x DOI: https://doi.org/10.1111/j.1438-8677.2010.00348.x
Serrano-Serrano ML, Rolland J, Clark JL, Salamin N, Perret M. 2017. La polinización de colibríes y la diversificación de las angiospermas: una asociación antigua y exitosa en Gesneriaceae. Actas de la Royal Society: Ciencias Biológicas 284:1852. DOI: https://doi.org/10.1098/rspb.2016.2816 DOI: https://doi.org/10.1098/rspb.2016.2816
Sheldon KS, Nadkarni NM. 2015. Reproductive phenology of epiphytes in Monteverde, Costa Rica. Revista de Biología Tropical 63: 1119-1126. DOI: https://doi.org/10.15517/rbt.v63i4.16583
Sick H. 1997. Ornitologia Brasileira. Rio de Janeiro: Editora Nova Fronteira. 912 pp. ISBN: 8520908160.
Silva MR, Barbosa BC, Faria APG. 2022. Reproductive biology and flower-visitor interactions of two bromeliad species from the Brazilian Atlantic Forest. Plant Ecology and Evolution 155: 16-28. DOI: https://doi.org/10.5091/plecevo.84464 DOI: https://doi.org/10.5091/plecevo.84464
Snow AA, Spira TP, Simpson R, Klips RA. 1996. The ecology of geitonogamous pollination. In: Lloyd DG, Spencer CHB. eds. Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants. Boston, MA: Springer. pp. 191-216. ISBN: 978-1-4612-8494-9 DOI: https://doi.org/10.1007/978-1-4613-1165-2_7
Soto M, Gama L. 1997. Clima. In: González-Soriano ER, Dirzo R, Vogt RC. eds. Historia Natural de Los Tuxtlas. DF, México: Universidad Nacional Autónoma de México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. ISBN: 9683656463
Strauss SY, Irwin RE. 2004. Ecological and evolutionary consequences of multispecies plant-animal interactions. Annual Review of Ecology, Evolution, and Systematics 35: 435-466. DOI: https://doi.org/10.1146/annurev.ecolsys.35.112202.130215 DOI: https://doi.org/10.1146/annurev.ecolsys.35.112202.130215
Stebbins GL. 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: Pollination mechanisms. Annual Review of Ecology and Systematics 1: 307-326. DOI: https://doi.org/10.1146/annurev.es.01.110170.001515 DOI: https://doi.org/10.1146/annurev.es.01.110170.001515
Stiles FG, Freeman CE. 1993. Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25: 191-205. DOI: https://doi.org/10.2307/2389183 DOI: https://doi.org/10.2307/2389183
Talavera S, Bastida F, Ortiz PL, Arista M. 2001. Pollinator attendance and reproductive success in Cistus libanotis L. (Cistaceae). International Journal of Plant Sciences 162: 343-352. DOI: https://doi.org/10.1086/319573 DOI: https://doi.org/10.1086/319573
Toledo VM. 1975. La estacionalidad de las flores utilizadas por los colibríes de una selva tropical húmeda en México. Biotropica 7: 63-70. DOI: https://doi.org/10.2307/2989802 DOI: https://doi.org/10.2307/2989802
JAMOVI [The jamovi project]. 2024. jamovi (Version 2.5) [Computer Software]. Retrieved from https://www.jamovi.org
Thomson JD, Thomson BA. 1992. Pollen presentation and viability schedules in animal-pollinated plants: consequences for reproductive success. In: Wyatt R, ed. Ecology and Evolution of Plant Reproduction: New Approaches. New York: Chapman & Hall. pp. 1-25. ISBN: 0-412-030-217
Tschapka M, Helversen VO. 2007. Phenology, nectar production and visitation behaviour of bats on the flowers of the bromeliad Werauhia gladioliflora in a Costa Rican lowland rain forest. Journal of Tropical Ecology 23: 385-395. DOI: https://doi.org/10.1017/S0266467407004129 DOI: https://doi.org/10.1017/S0266467407004129
Wendt T, Canela MBF, Klein DE, Rios RI. 2002. Selfing facilitates reproductive isolation among three sympatric species of Pitcairnia (Bromeliaceae). Plant Systematics and Evolution 232: 201-212. DOI: https://doi.org/10.1007/s006060200043 DOI: https://doi.org/10.1007/s006060200043
Winkler M, Hülber K, Mehltreter K, García-Franco JG, Hietz P. 2005. Herbivory in epiphytic bromeliads, orchids and ferns in a Mexican montane forest. Journal of Tropical Ecology 21: 147-154. DOI: https://doi.org/10.1017/S0266467404002081 DOI: https://doi.org/10.1017/S0266467404002081
Yamamura N, Fujita N, Hayashi M, Nakamura Y, Yamauchi A. 2007. Optimal phenology of annual plants under grazing pressure. Journal of Theoretical Biology 246: 530-537. DOI: https://doi.org/10.1016/j.jtbi.2007.01.010 DOI: https://doi.org/10.1016/j.jtbi.2007.01.010
Yumoto T. 1987. Pollination ecology in the canopy: two corollaries deduced from the energetics of pollination. In: Kawano S, Connell J, Hidaka T, eds. Evolution and Coadaptation in Biotic Communities Tokio, Japan: University of Tokyo Press, pp. 165-182.
Zanella CM, Janke A, Palma-Silva C, Kaltchuk-Santos E, Pinheiro FG, Paggi GM, Soares LES, Goetze M, Büttow MV, Bered F. 2012. Genetics, evolution and conservation of Bromeliaceae. Genetics and Molecular Biology 35: 1020-1026. DOI: https://doi.org/10.1590/S1415-47572012000600017 DOI: https://doi.org/10.1590/S1415-47572012000600017
Zapata TR, Kalin AMT. 1978. Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10: 221-230. DOI: https://www.doi.org/10.2307/2387907 DOI: https://doi.org/10.2307/2387907
Zotz G. 2013. The systematic distribution of vascular epiphytes-a critical update. Botanical Journal of the Linnean Society 171: 453-481. DOI: https://doi.org/10.1111/boj.12010 DOI: https://doi.org/10.1111/boj.12010
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