Log in

Neglecting nocturnal pollinators has long masked hawkmoth pollination in Rhododendron

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dudareva N, Pichersky E (2006) Biology of Floral Scent. CRC, Boca Raton, Florida, USA

    Book  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Eggli U, Giorgetta M (2015) Flowering phenology and observations on the pollination biology of south American cacti. 2. Cereus aethiops. Haseltonia 21:19–40

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Grant V (1983) The systematic and geographical distribution of hawkmoth flowers in the temperate north American flora. Bot Gaz 144:439–449

    Article  Google Scholar 

  • Hendel-Rahmanim K, Masci T, Vainstein A, Weiss D (2007) Diurnal regulation of scent emission in rose flowers. Planta 226:1491–1499

    Article  CAS  PubMed  Google Scholar 

  • Huang Z-H, Song Y-P, Huang S-Q (2017) Evidence for passerine bird pollination in Rhododendron species. AoB PLANTS 9:plx062

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lu Q-B, Liu C-Q, Huang S-X (2021) Moths pollinate four crops of Cucurbitaceae in Asia. J Appl Entomol 145:499–507

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mejías JA, Arroyo J, Ojeda F (2002) Reproductive ecology of Rhododendron Ponticum (Ericaceae) in relict Mediterranean populations. Bot J Linn Soc 140:297–311

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Ortiz PL, Arista M, Talavera S (2000) Pollination and breeding system of Putoria calabrica (Rubiaceae), a Mediterranean dwarf shrub. Plant Biol 2:325–330

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Souza CS, Oliveira PE, Rosa BB, Maruyama PK (2022) Integrating nocturnal and diurnal interactions in a neotropical pollination network. J Ecol 110:2145–2155

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Stout JC (2007) Reproductive biology of the invasive exotic shrub, Rhododendron Ponticum L. (Ericaceae). Bot J Linn Soc 155:373–381

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vogel S (1954) Blütenbiologische Typen als Elemente Der Sippengliederung: dargestellt anhand Der Flora Südafrikas. Bot Studien 1:1–338

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton & London

    Book  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Chang-Qiu Liu.

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.

Online Resource 1 A visit to Rhododendron excellens by a bumblebee, its tarsi contacting the stigma

Online Resource 2 A bumblebee visiting Rhododendron excellens with a hanging viscin thread

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11829-024-10065-6

Keywords

Navigation