Abstract
In high mountain environments, the availability of pollinators may decrease as elevation increases, affecting plant reproductive success. Floral volatile organic compounds (VOCs) are relevant to pollinator attraction; however, few studies have explored the variation of floral VOCs at different elevational sites. We analyzed the floral VOCs, flower size and nectar volume in Bidens triplinervia (a species with a generalized pollination system) and Penstemon roseus (with bee and bird pollination system) at three elevations (2800, 3300, and 3700 m) in the Nevado de Colima Volcano in Mexico. We recorded visitation rate and the identity of pollinators and explored the relationships between floral traits and pollinator visitation. The floral scent profile (composition and relative amounts of VOCs) of B. triplinervia and P. roseus differed between the three elevations. The highest number of VOCs and the largest flowers were found at high elevation, which had the lower visitation rate. Nectar volume was higher at low elevation and nectar concentration was lower at middle elevation. In B. triplinervia, Bombus ephippiatus was the main pollinator at low and middle elevation, while Musca domestica predominated at the highest elevation. Penstemon roseus was visited by hummingbirds and bumblebees, which were the most frequent pollinators at all three elevations. The floral traits (i.e., flower size, floral VOCs and nectar) were significantly associated with pollinator visitation. This study provides evidence of floral VOCs variation at different elevations, which was correlated with the visitation rate of local pollinators. The larger flowers at higher elevations may increase the attraction of pollinators where the environment is more extreme and erratic.
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References
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured publishing corporation, Carol Stream
Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97. https://doi.org/10.1002/j.1537-2197.1982.tb13237.x
Arroyo MTK, Armesto JJ, Primack RB (1985) Community studies in pollination ecology in the high temperate Andes of central Chile II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol 149:187–203. https://doi.org/10.1007/BF00983305
Basnett S, Ganesan R, Devy SM (2019) Floral traits determine pollinator visitation in Rhododendron species across an elevation gradient in the Sikkim Himalaya. Alp Bot 129:81–94
Bergamo PJ, Telles FJ, Arnold SEJ, de Brito VLG (2018) Flower color within communities shifts from over dispersed to clustered along an alpine altitudinal gradient. Oecologia 188:223–235
Braunschmid H, Mükisch B, Rupp T et al (2017) Interpopulation variation in pollinators and floral scent of the lady’s-slipper orchid Cypripedium calceolus L. Arthropod Plant Interac 11:363–379. https://doi.org/10.1007/s11829-017-9512-x
Byers KJ, Bradshaw HD Jr, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623. https://doi.org/10.1242/jeb.092213
Cardona J, Lara C, Ornelas JF (2020) Pollinator divergence and pollination isolation between hybrids with different floral color and morphology in two sympatric Penstemon species. Sci Rep 10:8126
Chapurlat E, Ågren J, Anderson J, Friberg M, Sletvold N (2019) Conflicting selection on floral scent emission in the orchid Gymnadenia conopsea. New Phytol 222:2009–2022. https://doi.org/10.1111/nph.15747
Corbet SA (2003) Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34:1–10
Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59:715–727
Cuevas E, Martínez-Díaz Y, Montes AD, Espinosa-Gacía FJ (2023) Floral and leaf-trap volatiles and their relationship to pollinator and prey attraction in Pinguicula moranensis (Lentibulariaceae). Arthropod-Plant Interac 17:687–694. https://doi.org/10.1007/s11829-023-09984-7
Delle-Vedove R, Schatz B, Dufay M (2017) Understanding intraspecific variation of floral scent in light of evolutionary ecology. Ann Bot 120:1–20. https://doi.org/10.1093/aob/mcx055
Dellinger AS, Pérez-Barrales R, Michelangeli FA, Penneys DS, Fernández-Fernández DM, Schönenberger J (2021) Low bee visitation rates explain pollinator shifts to vertebrates in tropical mountains. New Phytol 231:864–877. https://doi.org/10.1111/nph.17390
Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton, pp 147–198
El-Sayed AM, Sporle A, Colhoun K, Furlong J, White R, Suckling DM (2018) Scents in orchards: Floral volatiles of four stone fruit crops and their attractiveness to pollinators. Chemoecology 28:39–49
El-Sayed AM (2021) The Pherobase: Database of pheromones and semiochemicals. http://www.pherobase.com. Accessed 20 October 2021
Erhardt A (1993) Pollination of the edelweiss, Leontopodium alpinum. Bot J Linn Soc 111:229–240
Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2013) Floral volatile organic compounds: Between attraction and deterrence of visitors under global change. Perspect Plant Ecol Evol Sys 15:56–67
Farré-Armengol G, Filella I, Llusià J, Peñuelas J (2015) Pollination mode determines floral scent. Biochem Syst Ecol 61:44–53
Farré-Armengol G, Fernández-Martínez M, Filella I, Junker RR, Peñuelas J (2020) Deciphering the biotic and climatic factors that influence floral scents: a systematic review of floral volatile emissions. Front Plant Sci. https://doi.org/10.3389/fpls.2020.01154
Friberg M, Schwind C, Roark LC, Raguso RA, Thompson JN (2014) Floral scent contributes to interaction specificity in coevolving plants and their insect pollinators. J Chem Ecol 40:955–965. https://doi.org/10.1007/s10886-014-0497-y
Friberg M, Schwind C, Guimarães P, Raguso R, Thompson J (2019) Extreme diversification of floral volatiles within and among species of Lithophragma (Saxifragaceae). Proc Natl Acad Sci 116:201809007. https://doi.org/10.1073/pnas.1809007116
Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. Am Nat 177:258–272. https://doi.org/10.1086/657993
Gervasi D, Schiestl F (2017) Real-time divergent evolution in plants driven by pollinators. Nat Commun 8:1469. https://doi.org/10.1038/ncomms14691
Gross K, Sun M, Schiestl FP (2016) Why do floral perfumes become different? Region-specific selection on floral scent in a terrestrial orchid. PLoS ONE 11:e0147975. https://doi.org/10.1371/journal.pone.0147975
Guleria N, Nebapure SM, Kamala JPD, Suby SB, Kumar PS (2021) Identification of male-specific active host plant volatiles for maize stem borer, Chilo partellus Swinhoe. Curr Sci 121:578–658
He JD, Xue JY, Gao J, Wang J, Wu Y (2017) Adaptations of the floral characteristics and biomass allocation patterns of Gentiana hexaphylla to the altitudinal gradient of the eastern Qinghai-Tibet Plateau. J Mt Sci 14:1563–1576
Hetherington-Rauth MC, Ramírez SR (2016) Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora. Ann Bot 118:135–148
Johnson SD, Nicolson SW (2008) Evolutionary associations between nectar properties and specificity in bird pollination systems. Biol Lett 4:49–52
Johnson SD, Burgoyne PM, Harder LD, Dötterl S (2011) Mammal pollinators lured by the scent of a parasitic plant. Proc Biol Sci 278:2303–2310. https://doi.org/10.1098/rspb.2010.2175
Junker RR, Gershenzon J, Unsicker S (2011) Floral odor bouquet loses its ant repellent properties after inhibition of terpene biosynthesis. J Chem Ecol 37:1323–1331. https://doi.org/10.1007/s10886-011-0043-0
Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017) Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nat Ecol Evol 1:1502–1510. https://doi.org/10.1038/s41559-017-0298-0
Kearns CA (1992) Anthophilous fly distribution across an elevation gradient. Am Midl Nat 127:172–182. https://doi.org/10.2307/2426332
Kiełtyk P (2021) Patterns of floral allocation along an elevation gradient: variation in Senecio subalpinus growing in the Tatra Mountains. Alp Bot 131:117–124. https://doi.org/10.1007/s00035-021-00247-w
Kim A, Rankin D, Rankin E (2021) What is that smell? Hummingbirds avoid foraging on resources with defensive insect compounds. Behav Ecol Sociobiol 75:132
Knudsen JT (2002) Variation in floral scent composition within and between populations of Geonoma macrostachys (Arecaceae) in the western Amazon. Am J Bot 89:1772–1778
Knudsen JT, Tollsten L, Groth I, Bergström G, Raguso RA (2004) Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa. Bot J Linn Soc 146:191–199. https://doi.org/10.1111/j.1095-8339.2004.00329.x
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120. https://doi.org/10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574. https://doi.org/10.1016/j.tree.2007.09.006
Kudo G (1993) Relationship between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. Am J Bot 80:1300–1304. https://doi.org/10.2307/2445714
Lara C, Ornelas JF (2008) Pollination ecology of Penstemon roseus (Plantaginaceae), an endemic perennial shifted toward hummingbird specialization? Plant Syst Evol 271:223–237. https://doi.org/10.1007/s00606-007-0624-0
Lefebvre V, Villemant C, Fontaine C, Daugeron C (2018) Altitudinal, temporal and trophic partitioning of flower-visitors in alpine communities. Sci Rep 8:4706. https://doi.org/10.1038/s41598-018-23210-y
Linstrom PJ, Mallard WG (2001) The NIST Chemistry WebBook: a chemical data resource on the internet. J Chem Eng Data 46:1059–1063
Liu YB, Zeng ZJ, Barron AB, Ma Y, He YZ, Liu JF, Li Z, Yan WY, He XJ (2022) The involvement of a floral scent in plant-honeybee interaction. Naturwissenschaften 109:30. https://doi.org/10.1007/s00114-022-01802-z. (PMID: 35643865)
Lord JM (2008) A test for phylogenetic conservatism in plant pollinator relationships in Australian and New Zealand alpine floras. N Z J Bot 46:367–372. https://doi.org/10.1080/00288250809509774
Maad J, Armbruster WS, Fenster CB (2013) Floral size variation in Campanula rotundifolia (Campanulaceae) along altitudinal gradients: patterns and possible selective mechanisms. Nord J Bot 31:361–371. https://doi.org/10.1111/j.1756-1051.2013.01766.x
Majetic CJ, Raguso RA, Ashman TL (2009) The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Funct Ecol 23:480–487. https://doi.org/10.1111/j.13652435.2008.01517.x
McCabe LM, Cobb NS (2021) From bees to flies: global shift in pollinator communities along elevation gradients. Front Ecol Evol 8:626124. https://doi.org/10.3389/fevo.2020.626124
O’hara M, Higashi S (1994) Effects of inflorescence size on visits from pollinators and seed set of corydalis ambigua (Papaveraceae). Oecologia 98:25–30. https://doi.org/10.1007/BF00326086
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Oksanen MJ (2013) Package ‘vegan’. Community ecology package, version, 2, 1–295
Parachnowitsch AL, Raguso RA, Kessler A (2012) Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytol 195:667–675. https://doi.org/10.1111/j.1469-8137.2012.04188.x
Peeters L, Totland Ø (1999) Wind to insect pollination ratios and floral traits in five alpine Salix species. Canad J Bot 77:556–563. https://doi.org/10.1139/b99-003
Pi HQ, Quan QM, Wu B, Lv XW, Shen LM, Huang SQ (2021) Altitude-related shift of relative abundance from insect to sunbird pollination in Elaeagnus umbellata (Elaeagnaceae). J Syst Evol 59:1266–1275. https://doi.org/10.1111/plb.13493
Proffit M, Lapeyre B, Buatois B, Deng X, Arnal P, Gouzerh F, Carrasco D, Hossaert-McKey M (2020) Chemical signal is in the blend: bases of plant-pollinator encounter in a highly specialized interaction. Sci Rep 10:10071. https://doi.org/10.1038/s41598-020-66655-w
Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569
Rzedowski GC, Rzedowski J (2001) Flora fanerogámica del Valle de México, 2nd edn. Instituto de Ecología y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Pátzcuaro
Sargent RD, Goodwillie C, Kalisz S, Ree RH (2007) Phylogenetic evidence for a flower size and number trade-off. Am J Bot 94:2059–2062
Souto-Vilarós D, Proffit M, Buatois B, Rindos M, Sisol M, Kuyaiva T, Segar ST (2018) Pollination along an elevational gradient mediated both by floral scent and pollinator compatibility in the fig and fig-wasp mutualism. J Ecol 106:2256–2273. https://doi.org/10.1111/1365-2745.12995
Sun M, Gross K, Schiestl FP (2014) Floral adaptation to local pollinator guilds in a terrestrial orchid. Ann Bot 113:289–300. https://doi.org/10.1093/aob/mct219
Sunoj S, Subhashree SN, Dharani S, Igathinathane C, Franco JG, Mallinger RE, Prasifka JR, Archer D (2018) Sunflower floral dimension measurements using digital image processing. Comput Electron Agric 151:403–415. https://doi.org/10.1016/j.compag.2018.06.026
Takkis K, Tscheulin T, Petanidou T (2018) Differential effects of climate warming on the nectar secretion of early- and late-flowering mediterranean plants. Front Plant Sci 9:1664–2462. https://doi.org/10.3389/fpls.2018.00874
Trunschke J, Stöcklin J (2017) Plasticity of flower longevity in alpine plants is increased in populations from high elevation compared to low elevation populations. Alp Bot 127:41–51. https://doi.org/10.1007/s00035-016-0176-4
Weber MG, Cacho NI, Phan MJQ, Disbrow C, Ramirez SR, Strauss SY (2018) The evolution of floral signals in relation to range overlap in a clade of California jewelflowers (Streptanthus s.l.). Evolution 72:798–807. https://doi.org/10.1111/evo.13456
Wright GA, Schiestl FP (2009) The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honest signaling of floral rewards. Funct Ecol 23:841–851. https://doi.org/10.1111/j.1365-2435.2009.01627.x
Zhao R, Zhang H, An L (2019) Plant size influences abundance of floral visitors and biomass allocation for the cushion plant Thylacospermum caespitosum under an extreme alpine environment. Ecol Evol 9:5501–5511. https://doi.org/10.1002/ece3.5147
Acknowledgements
We thank the staff of Nevado de Colima Volcano for their support during the development of this research, especially José Villa. L. Ramírez, E. Medina, and S. Pozas for field support. Funding was provided by CONAHCYT-Mexico (postdoctoral fellowship 741128 and 769349 to YMD; Laboratorio Nacional de Análisis y Síntesis Ecológica 299033 to SMR and EC), and Universidad Nacional Autónoma de México (DGAPA-PAPIIT IV200418).
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Figure S1. The flower morphology of studied species, a) Bidens triplinervia (Asteraceae) and b) Penstemon roseus (Plantaginaceae)
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Martínez-Díaz, Y., Espinosa-García, F.J., Martén-Rodríguez, S. et al. Floral attractants in an alpine environment: linking floral volatiles, flower size and pollinators. Alp Botany (2023). https://doi.org/10.1007/s00035-023-00303-7
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DOI: https://doi.org/10.1007/s00035-023-00303-7