Floral ecology of Puya ctenorhyncha (Bromeliaceae) an endemic plant of Bolivia

keywords: Ecological interactions, floral syndrome, hummingbirds, nectar, reproductive phenology, Yungas

Abstract

Background: The terrestrial bromeliad Puya ctenorhyncha is a near-threatened endemic species that grows between 2,500-4,050 m asl.

Hypotheses: Hummingbirds are the most important visitors of this plant given its morphological and floral traits.

Study site: The study was carried out along the “Death Road”, located in the Yungas montane cloud forest, La Paz, Bolivia.

Methods: We monitored an average of 216 individuals monthly for two years (2018-2019). Besides we conducted direct observations of focal plants to quantify the visits of animals.

Results: The reproductive season lasted from April to August in the first year and from May to June in the second. The mean nectar volume was 8.09 ± 1.59 μL per flower and its composition included fructose, glucose, and 86 % of water. With 341 hours of observations, we determined that Coeligena torquata (Trochilidae) is the main visitor and putative pollinator, followed by C. violifer. Males of both species were more frequent visitors than females. Coeligena torquatashowed the highest activity during the afternoon while C. violifer was more active in the morning.

Conclusions: Floral phenology seems to be annual and unimodal. Although the main pollinators seem to be hummingbirds, the nectar concentration and composition is more similar to bromeliad species of other genera which are pollinated by bats or passerine birds. It is important to evaluate, in future studies, the dependence of both hummingbirds and their behavioural response towards the plant.

Downloads

Download data is not yet available.
Floral ecology of <em>Puya ctenorhyncha</em> (Bromeliaceae) an endemic plant of Bolivia

References

Abrahamczyk S, Kessler M, Hanley D, Karger DN, Müller MPJ, Knauer AC, Keller F, Schwerdtfeger M, Humphreys AM. 2017. Pollinator adaptation and the evolution of floral nectar sugar composition. Journal of Evolutionary Biology 30: 112-127. DOI: https://doi.org/10.1111/jeb.12991

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.

Aguilar-Rodríguez PA, MacSwiney GMC, Krömer T, García-Franco JG, Knauer A, Kessler M. 2014. First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae). Annals of Botany 113: 1047-1055. DOI: https://doi.org/10.1093/aob/mcu031

Altshuler DL. 2003. Flower color, hummingbird pollination, and habitat irradiance in four Neotropical forests. Biotropica 35: 344-355. DOI: https://doi.org/10.1111/j.1744-7429.2003.tb00588.x

Aquino W, Condo F, Romero J, Yllaconza R. 2018. Distribución geográfica y poblacional de Puya raimondii Harms en el distrito de Huarochirí, provincia de Huarochirí, Lima, Perú. The Biologist (Lima) 16: 25-33. DOI: https://doi.org/10.24039/rtb2018161219

Bach K, Schawe M, Beck S, Gerold G, Gradstein SR, Moraes RM. 2003. Vegetación, suelos y clima en los diferentes pisos altitudinales de un bosque montano de Yungas, Bolivia: Primeros resultados. Ecología en Bolivia 38: 3-14.

Baker HG, Baker I. 1990. The predictive value of nectar chemistry to the recognition of pollinator types. Israel Journal of Botany 39: 157-166.

Baker HG, Baker I, Hodges SA. 1998. Sugar composition of nectars and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30: 559-586. DOI: https://doi.org/10.1111/j.1744-7429.1998.tb00097.x

Barnes K, Nicolson SW, Van Wyk B-E. 1995. Nectar sugar composition in Erica. Biochemical Systematics and Ecology 23: 419-423. DOI: https://doi.org/10.1016/0305-1978(95)00024-O

Benzing DH. 2000. Bromeliaceae: profile of an adaptative radiation. Cambridge, United Kingdom: Cambridge University Press. ISBN: 0-521-43031-3

Bribiesca R, Herrera-Alsina L, Ruiz-Sanchez E, Sánchez-González LA, Schondube JE. 2019. Body mass as a supertrait linked to abundance and behavioral dominance in hummingbirds: A phylogenetic approach. Ecology and Evolution 9: 1623-1637. DOI: https://doi.org/10.1002/ece3.4785

Calder WA. 1979. On the temperature-dependency of optimal nectar concentrations for birds. Journal of Theoretical Biology 78: 185-196. DOI: https://doi.org/10.1016/0022-5193(79)90263-7

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

Chen CCW, Welch KC. 2014. Hummingbirds can fuel expensive hovering flight completely with either exogenous glucose or fructose. Functional Ecology 28: 589-600. DOI: https://doi.org/10.1111/1365-2435.12202

Corbet SA, 2003. Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34: 1-10. DOI: https://doi.org/10.1051/apido:2002049

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

Fenner M. 1998. The phenology of growth and reproduction in plants. Perspectives in Plant Ecology, Evolution and Systematics 1: 78-91. DOI: https://doi.org/10.1078/1433-8319-00053

Franco-Saldarriaga A, Bonilla-Gómez MA. 2021. Sexual reproductive strategies of Puya nitida (Bromeliaceae) in a Colombian paramo, a tropical high-elevation ecosystem. Journal of Tropical Ecology 36: 258-266. DOI: https://doi.org/10.1017/S0266467420000218

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

Galetto L, Bernardello LM. 1992. Extrafloral nectaries that attract ants in Bromeliaceae: structure and nectar composition. Canadian Journal of Botany 70: 1101-1106. DOI: https://doi.org/10.1139/b92-136

García-Meneses P, Ramsay PM. 2012. Pollinator response to within-patch spatial context determines reproductive output of a giant rosette plant. Basic and Applied Ecology 13: 516-523. DOI: https://doi.org/10.1016/j.baae.2012.08.011

García MTA, Hoc PS. 1998. Biología floral de Passiflora foetida (Passifloraceae). Revista de Biología Tropical 46: 191-202.

Gonzalez O, Díaz C, Britto B. 2019. Assemblage of nectarivorous birds and their floral resources in an Elfin forest of the central Andes of Peru. Ecología Aplicada 18: 21-35. DOI: https://doi.org/10.21704/rea.v18i1.1302

Gonzalez O, Loiselle BA. 2016. Species interactions in an Andean bird-flowering plant network: phenology is more important than abundance or morphology. PeerJ 4: 1-22. DOI: https://doi.org/10.7717/peerj.2789

Hölscher D, Brand S, Wenzler M, Schneider B. 2008. NMR-Based metabolic profiling of Anigozanthos floral nectar. Journal of Natural Products 71: 251-257. DOI: https://doi.org/10.1021/np0705514

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

Hornung-Leoni C, Sosa V. 2005. Morphological variation in Puya (Bromeliaceae): an allometric study. Plant Systematics and Evolution 256: 35-53. DOI: https://doi.org/10.1007/s00606-005-0302-z

Jabaily RS, Sytsma KJ. 2013. Historical biogeography and life-history evolution of Andean Puya (Bromeliaceae). Botanical Journal of the Linnean Society 171: 201-224. DOI: https://doi.org/10.1111/j.1095-8339.2012.01307.x

Janeba Z. 2017. A new species of Puya (Bromeliaceae) from Coastal Peru. Cactus and Succulent Journal 89: 176-184. DOI: https://doi.org/10.2985/015.089.0406

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

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

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36: 467-497. DOI: https://doi.org/10.1146/annurev.ecolsys.36.102403.115320

Krömer T. 2000. Distribution of terrestrial bromeliads along the La Paz to Caranavi road in. The Bromeliad Society 50: 158-164.

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

Krömer T, Kessler M, Holst BK, Luther HE, Gouda EJ, Ibisch PL, Till W, Vásquez R. 1999. Checklist of Bolivian Bromeliaceae with notes on species distribution and levels of endemism. Selbyana 20: 201-223.

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

Krömer T, Ibisch PL, Vásquez R, Kessler M, Holst B, Luther HE. 2014. Bromeliaceae. In: Jørgensen PM, Nee MH, Beck SG, Arrázola S, Saldias M, eds. Catálogo de las Plantas Vasculares de Bolivia. St. Louis, USA: Missouri Botanical Garden Press.p. 418-439. ISBN: 978-1-930723-71-9

Machado CG, Semir J. 2006. Fenologia da floração e biologia floral de bromeliáceas ornitófilas de uma área da Mata Atlântica do Sudeste brasileiro. Revista Brasileira de Botânica 29: 163-174. DOI: https://doi.org/10.1590/s0100-84042006000100014

Maruyama PK, Oliveira GM, Ferreira C, Dalsgaard B, Oliveira PE. 2013. Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds. Naturwissenschaften 100: 1061-1068. DOI: https://doi.org/10.1007/s00114-013-1111-9

Mercado Ustariz J, Krömer T, Fuentes Claros A, Meneses R, Beck S. 2020. Puya ctenorhyncha. In: The IUCN Red List of Threatened Species (Vol. 8235). DOI: https://doi.org/10.2305/IUCN.UK.2020-1.RLTS.T131347588A131347652.es

Nicolson SW, Fleming PA. 2003. Nectar as food for birds: the physiological consequences of drinking dilute sugar solutions. Plant Systematics and Evolution 238: 139-153. DOI: https://doi.org/10.1007/s00606-003-0276-7

Ornelas JF, Ordano M, De-Nova AJ, Quintero ME, Garland JRT. 2007. Phylogenetic analysis of interspecific variation in nectar of hummingbird-visited plants. Journal of Evolutionary Biology 20: 1904-1917. DOI: https://doi.org/10.1111/j.1420-9101.2007.01374.x

Pereira FRDL, Quirino ZGM. 2008. Fenologia e biologia floral de Neoglaziovia variegata (Bromeliaceae) na Caatinga Paraibana. Rodriguésia. 59: 835-844. DOI: https://doi.org/10.1590/2175-7860200859412

Pool-Chalé M, Ramírez-Morillo I, Carnevali Fernández-Concha G, Hornung-Leoni CT. 2018. Reproductive biology of Aechmea bracteata (Sw.) Griseb. (Bromelioideae: Bromeliaceae). Plant Biology 20: 113-120. DOI: https://doi.org/10.1111/plb.12645

Rees WE, Roe NA. 1980. Puya raimondii (Pitcairnioideae, Bromeliaceae) and birds: an hypothesis on nutrient relationships. Canadian Journal of Botany 58: 1262-1268. DOI: https://doi.org/10.1139/b80-157

Restrepo-Chica M, Bonilla-Gómez MA. 2017. Dinámica de la fenología y visitantes florales de dos bromelias terrestres de un páramo de Colombia. Revista Mexicana de Biodiversidad 88: 636-645. DOI: https://doi.org/10.1016/j.rmb.2017.07.008

Ribera-Arismendi MO. 1995. Aspectos ecológicos, del uso e la tierra y conservación en el parque nacional y área natrual de manejo integrado Cotapata. In: Morales C, eds., Caminos de Cotapata. La Paz, Bolivia: Artes Gráficas Latina. pp 1-84.

Rodrigues Marques A, De Lemos Filho JP. 2008. Fenologia reprodutiva de espécies de bromélias na Serra da Piedade, MG, Brasil. Acta Botanica Brasilica 22: 417-424. DOI: https://doi.org/10.1590/S0102-33062008000200011

Salinas L, Arana C, Suni M. 2007. El néctar de especies de Puya como recurso para picaflores Altoandinos de Ancash, Perú. Revista Peruana de Biología 14: 129-134. DOI: https://doi.org/10.15381/rpb.v14i1.2166

Schmidt-Lebuhn AN, Schwerdtfeger M, Kessler M, Lohaus G. 2007. Phylogenetic constraints vs. ecology in the nectar composition of Acanthaceae. Flora: Morphology, Distribution, Functional Ecology of Plants 202: 62-69. DOI: https://doi.org/10.1016/j.flora.2006.02.005

Scogin R, Freeman CE. 1984. Floral pigments and nectar constituents in the genus Puya (Bromeliaceae). Aliso: A Journal of Systematic and Evolutionary Botany 10: 617-619. DOI: https://doi.org/10.5642/aliso.19841004.10

Serrudo-Gonzáles V, Arteaga-Voigt D, Fuentes-Bazán S, García-Estigarribia E, Luna-Barrón R. 2012. Estrategias de forrajeo de cuatro especies de picaflores (Aves, Trochilidae) en la ceja de monte yungueña (La Paz, Bolivia). Ecología en Bolivia 47: 143-147.

Smith LB. 1969. The Bromeliaceae of Bolivia. Rhodora 71: 35-57. DOI: http://www.jstor.org/stable/23311188

Smith LB, Downs RJ. 1974. Pitcairnioideae (Bromeliaceae). Flora Neotropica. Monograph. No. 14, Part 1. Hafner Press, New York.

Stiles FG. 1978. Temporal organization of flowering among the hummingbird foodplants of a Tropical Wet Forest. Biotropica 10: 194-210. DOI: https://doi.org/10.2307/2387905

Stoddard MC, Eyster HN, Hogan BG, Morris DH, Soucy ER, Inouye DW. 2020. Wild hummingbirds discriminate nonspectral colors. Proceedings of the National Academy of Sciences of the United States of America 117: 15112-15122. DOI: https://doi.org/10.1073/pnas.1919377117

van Wyk B-E. 1993. Nectar sugar composition in Southern African Papilionoideae (Fabaceae). Biochemical Systematics and Ecology 21: 271-277. DOI: https://doi.org/10.1016/0305-1978(93)90045-S

Varadarajan GS, Brown GK. 1988. Morphological variation of some floral features of the subfamily Pitcairnioideae (Bromeliaceae) and their significance in pollination biology. Botanical Gazette 149: 82-91. DOI: https://doi.org/10.1086/337694

Vázquez DP, Morris WF, Jordano P. 2005. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8: 1088-1094. DOI: https://doi.org/10.1111/j.1461-0248.2005.00810.x

Velásquez-Noriega P, Cuba E, Paca-Condori AC, Lozada-Gobilard S, Gómez MI. 2023. An annotated bird checklist of two touristic trails in the Yungas of Bolivia. Cotinga. 45: 2-12.

Velásquez-Noriega P, Mayta C, Cuba E, García EE, Montaño-Centellas F, Krömer T. 2020. Floral ecology and floral visitors of Puya atra (Bromeliaceae), a Bolivian endemic plant. Ecología en Bolivia 55: 36-45.

Wenzler M, Hölscher D, Oerther T, Schneider B. 2008. Nectar formation and floral nectary anatomy of Anigozanthos flavidus: A combined magnetic resonance imaging and spectroscopy study. Journal of Experimental Botany 59: 3425-3434. DOI: https://doi.org/10.1093/jxb/ern191

Wolf LL, Stiles FG, Hainsworth FR. 1976. Ecological organization of a tropical, highland hummingbird community. The Journal of Animal Ecology 45: 349-379. DOI: https://doi.org/10.2307/3879

Woods S, Ortiz-Crespo F, Ramsay PM. 1998. Presence of giant hummingbird Patagona gigas and Ecuadorian hillstar Oreotrochilus chimborazo jamesoni at the Ecuador - Colombia border. Cotinga 10: 37-40.

Woods S, Ramsay PM. 2001. Variability in nectar supply: implications for high- altitude humminbirds. In: Ramsay PM, eds. The ecology of Volcán Chiles: High-Altitude Ecosystems on the Ecuador-Colombia border. Plymouth, United Kingdom: Pebble & Shell Publications, University of Plymouth. pp. 209-217. ISBN: 0953913406

Published
2023-11-22
How to Cite
Velásquez-Noriega, P., Krömer, T., & Pacheco, L. F. (2023). Floral ecology of Puya ctenorhyncha (Bromeliaceae) an endemic plant of Bolivia. Botanical Sciences, 102(1), 68-82. https://doi.org/10.17129/botsci.3393
Section
ECOLOGY / ECOLOGÍA