Abstract
Insufficient investigation of nocturnal floral visitors may bias our understanding of floral diversification in many plant lineages. Here we re-examined the pollination ecology of Rhododendron excellens, which lacks a narrow floral tube characteristic of many hawkmoth flowers and has been considered a bee specialist with daytime observations alone. We used five temporally sequential proxies (i.e. visitation rate, pollen deposition, fruit production, seed production, and seed viability) covering the entire process of reproduction to track the relative importance of the two floral visitor groups that were active by day and by night respectively. We then quantified the floral syndrome and tested the mating system with hand pollination treatments. Both bumblebees and hawkmoths regularly visited R. excellens in two flowering seasons. Hawkmoths’ relative importance increased step-by-step from being inferior to bumblebees (floral visitation and pollen deposition) to making over three times the contribution by bumblebees (seed viability). This is probably because they differ in the ability to deliver outcross pollen for this partially self-compatible species. Correspondingly, R. excellens exhibits a floral syndrome associated with a particular subdivision of sphingophily. We revealed a distinctive pollination mode that mainly involves nocturnal pollinators and is likely to have repeatedly evolved in Rhododendron. Our findings also highlight the need to consider the ‘quality’ of pollen deposited onto stigmas, whose effect on plant fecundity may significantly expand over the course of sexual reproduction.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11829-024-10065-6/MediaObjects/11829_2024_10065_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11829-024-10065-6/MediaObjects/11829_2024_10065_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11829-024-10065-6/MediaObjects/11829_2024_10065_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11829-024-10065-6/MediaObjects/11829_2024_10065_Fig4_HTML.png)
Similar content being viewed by others
References
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Brunet J, Sweet HR (2006) Impact of insect pollinator group and floral display size on outcrossing rate. Evolution 60:234–246
Chain-Guadarrama A, Martínez-Salinasab A, Aristizábalcd N, Rickettscd TH (2019) Ecosystem services by birds and bees to coffee in a changing climate: a review of coffee berry borer control and pollination. Agric Ecosyst Environ 280:53–67
Chen G, Jürgens A, Shao L-D, Liu Y, Sun W-B, **a C-F (2015) Semen-like floral scents and pollination biology of a sapromyophilous plant Stemona Japonica (Stemonaceae). J Chem Ecol 41:244–252
Culley T, Weller S, Sakai A, Rankin A (1999) Inbreeding depression and selfing rates in a self-compatible, hermaphroditic species, Schiedea membranacea (Caryophyllaceae). Am J Bot 86:980–987
de Avila RS, Freitas L (2011) Frequency of visits and efficiency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia Itatiaiae (Rubiaceae). Aust J Bot 59:176–184
Dellinger AS, Scheer LM, Artuso S, Fernández-Fernández D, Sornoza F, Penneys DS, Tenhaken R, Dötterl S, Schönenberger J (2019) Bimodal pollination systems in Andean Melastomataceae involving birds, bats, and rodents. Am Nat 194:104–116
Diller C, Castañeda-Zárate M, Johnson SD (2022) Why honeybees are poor pollinators of a mass-flowering plant: experimental support for the low pollen quality hypothesis. Am J Bot 209:1305–1312
Diniz UM, Fischer NLS, Aguiar LMS (2022) Changing the main course: strong bat visitation to the ornithophilous mistletoe Psittacanthus Robustus (Loranthaceae) in a neotropical savanna. Biotropica 54:478–489
Dudareva N, Pichersky E (2006) Biology of Floral Scent. CRC, Boca Raton, Florida, USA
Dudash MR (1990) Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L.(Gentianaceae): a comparison in three environments. Evolution 44:1129–1139
Eggli U, Giorgetta M (2015) Flowering phenology and observations on the pollination biology of south American cacti. 2. Cereus aethiops. Haseltonia 21:19–40
Escaravage N, Pornon A, Doche B, Till-Bottraud I (1997) Breeding system in an alpine species: Rhododendron ferrugineum L. (Ericaceae) in the French northern Alps. Can J Bot 75:736–743
Fang M-Y, Fang R-C, He M-Y, Hu L-C, Yang H-P, Qin H-N, Min T-L, Chamberlain DC, Stevens PF, Wallace GD, Anderberg A (2005) Ericaceae. Flora of China, vol 14. Science Press and Missouri Botanical Garden, Bei**g and St. Louis, Missouri, China and USA, pp 242–517
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403
Filipowicz N, Schaefer H, Renner SS (2014) Revisiting Luffa (Cucurbitaceae) 25 years after C. Heiser: species boundaries and application of names tested with plastid and nuclear DNA sequences. Syst Bot 39:205–215
Funamoto D, Sugiura S (2021) Relative importance of diurnal and nocturnal pollinators for reproduction in the early spring flowering shrub Stachyurus praecox (Stachyuraceae). Plant Species Biol 36:94–101
Grant V (1983) The systematic and geographical distribution of hawkmoth flowers in the temperate north American flora. Bot Gaz 144:439–449
Hendel-Rahmanim K, Masci T, Vainstein A, Weiss D (2007) Diurnal regulation of scent emission in rose flowers. Planta 226:1491–1499
Huang Z-H, Song Y-P, Huang S-Q (2017) Evidence for passerine bird pollination in Rhododendron species. AoB PLANTS 9:plx062
Jaca J, Nogales M, Traveset A (2020) Effect of diurnal vs. nocturnal pollinators and flower position on the reproductive success of Echium simplex. Arthropod Plant Interact 14:409–419
Koski MH, Ison JL, Padilla A, Pham AQ, Galloway LF (2018) Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant-pollinator mutualism. Proc R Soc Lond B 285:20180635
Liu C-Q, Huang S-Q (2013) Floral divergence, pollinator partitioning and the spatiotemporal pattern of plant–pollinator interactions in three sympatric Adenophora species. Oecologia 173:1411–1423
Liu C-Q, Niu Y, Lu Q-B, Chen Z, Cai B, Fang Y, Gao Y-D (2019) Floral adaptations of two lilies: implications for the evolution and pollination ecology of huge trumpet-shaped flowers. Am J Bot 106:622–632
Liu C-Q, Niu Y, Lu Q-B, Chen Z, Cai B, Fang Y, Gao Y-D (2022) Papilio butterfly vs. hawkmoth pollination explains floral syndrome dichotomy in a clade of Lilium. Bot J Linn Soc 199:678–693
Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. N Z J Bot 24:135–162
Lombardi GC, Peter CI, Turner RC, Midgley JJ (2017) The unusual, closed flowers of Erica Lanuginosa (Ericaceae) are adapted for rodent-pollination and not cleistogamy. S Afr J Bot 111:189–193
Lopezaraiza–Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol Lett 10:539–550
Lu Q-B, Liu C-Q, Huang S-X (2021) Moths pollinate four crops of Cucurbitaceae in Asia. J Appl Entomol 145:499–507
Matsuki Y, Tateno R, Shibata M, Isagi Y (2008) Pollination efficiencies of flower-visiting insects as determined by direct genetic analysis of pollen origin. Am J Bot 95:925–930
Mejías JA, Arroyo J, Ojeda F (2002) Reproductive ecology of Rhododendron Ponticum (Ericaceae) in relict Mediterranean populations. Bot J Linn Soc 140:297–311
Miller TJ, Raguso RA, Kay KM (2014) Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors. Ann Bot 113:317–329
Mitchell TC, Dötterl S, Schaefer H (2015) Hawk-moth pollination and elaborate petals in Cucurbitaceae: the case of the Caribbean endemic Linnaeosicyos amara. Flora 216:50–56
Ng SC, Corlett RT (2000) Comparative reproductive biology of the six species of Rhododendron (Ericaceae) in Hong Kong, South China. Can J Bot 78:221–229
Ohashi K, Jürgens A (2021) Three options are better than two: compensatory nature of different pollination modes in Salix caprea L. J Pollinat Ecol 28:75–90
Ortiz PL, Arista M, Talavera S (2000) Pollination and breeding system of Putoria calabrica (Rubiaceae), a Mediterranean dwarf shrub. Plant Biol 2:325–330
Pittaway AR, Kitching IJ (2018) Sphingidae of the Eastern Palaearctic (including Siberia, the Russian Far East, Mongolia, China, Taiwan, the Korean Peninsula and Japan). http://tpittaway.tripod.com/china/china.htm
R Core Team (2018) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Reynolds RJ, Westbrook MJ, Rohde AS, Cridland JM, Fenster CB, Dudash MR (2009) Pollinator specialization and pollination syndromes of three related north American Silene. Ecology 90:2077–2087
Skogen KA, Jogesh T, Hilpman ER, Todd SL, Rhodes MK, Still SM, Fant JB (2016) Land-use change has no detectable effect on reproduction of a disturbance-adapted, hawkmoth-pollinated plant species. Am J Bot 103:1950–1963
Song Y-P, Huang Z-H, Huang S-Q (2019) Pollen aggregation by viscin threads in Rhododendron varies with pollinator. New Phytol 221:1150–1159
Souza CS, Oliveira PE, Rosa BB, Maruyama PK (2022) Integrating nocturnal and diurnal interactions in a neotropical pollination network. J Ecol 110:2145–2155
Stevens PF (1976) The altitudinal and geographical distributions of flower types in Rhododendron section Vireya, especially in the papuasian species, and the significance. Bot J Linn Soc 72:1–33
Stout JC (2007) Reproductive biology of the invasive exotic shrub, Rhododendron Ponticum L. (Ericaceae). Bot J Linn Soc 155:373–381
Tian X-L (2011) The reproductive biology of Rhododendron excellens Hemsl. et. Wils. Master’s thesis. Nan**g Forestry University, Nan**g, China
Van der Niet T, Cozien RJ (2022) Hawkmoth pollination of the scented South African fynbos endemic Erica Cylindrica Thunb. (Ericaceae) Flora 292:152088
Vogel S (1954) Blütenbiologische Typen als Elemente Der Sippengliederung: dargestellt anhand Der Flora Südafrikas. Bot Studien 1:1–338
Walton RE, Sayer CD, Bennion H, Axmacher JC (2020) Nocturnal pollinators strongly contribute to pollen transport of wild flowers in an agricultural landscape. Biol Lett 16:20190877
Wang X-Y, Chen Y, Li Y (2023) Features of floral odor and nectar in the distylous Luculia pinceana (Rubiaceae) promote compatible pollination by hawkmoths. Ecol Evol 13:e9920
Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton & London
Yang L-E, Peng D-L, Li Z-M, Huang L, Yang J, Sun H (2020) Cold stratification temperature light GA3 and KNO3 effects on seed germination of Primula beesiana from Yunnan China Plant Divers 42:168–173
Young HJ (2002) Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). Am J Bot 89:433–440
Acknowledgements
We thank the staff in Malipo-Laoshan Provincial Nature Reserve, who helped us during fieldwork, Gao Chen and Zhen Yu for their help in the collection and analysis of floral scents, Ji-Bai He and Zhuo-Heng Jiang for identification of hawkmoths, Huan-Li Xu for identification of bumblebees, and Zhe Chen for his advice on statistical analysis. The study was supported by Science and Technology Plans of Guangxi (grant no. AD19245113 to CQL), Basic Expenses for Scientific Research of Guangxi Academy of Sciences (grant no. CQZ-E-1917 to C.-Q. Liu), National Natural Science Foundation of China (grant no. 31971563 to CQL. and 32060079 to DLP), and the Light of West China Program of the Chinese Academy of Sciences (grant no. [2020]59), Guangxi Key Laboratory Construction Project (grant no. 22–035–26).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Isabel Alves dos Santos.
Communicated by: Ray Ming.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
11829_2024_10065_MOESM3_ESM.pdf
Online Resource 3 Average relative amounts (mean ? SE %) of floral scent compounds from individuals of Rhododendron excellens
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cai, B., Peng, DL., Liu, CQ. et al. Neglecting nocturnal pollinators has long masked hawkmoth pollination in Rhododendron. Arthropod-Plant Interactions (2024). https://doi.org/10.1007/s11829-024-10065-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11829-024-10065-6