Transient dehydration of pollen carried by hot bees impedes fertilization

  • Sarah A. Corbet
  • Fei-Fei Chen
  • Fang-Fang Chang
  • Shuang-Quan HuangEmail author
Original Paper


In the intense solar radiation of an alpine climate, small black bees often experience extremely high thoracic temperatures when they are foraging on flowers, but flies forage at lower temperatures. To explore the hypothesis that seed set could be depressed by transient dehydration of pollen at the high temperatures reached by hot bees foraging in sunshine, we compared the effectiveness of single visits by different pollinators to a bowl-shaped flower Potentilla lancinata in alpine meadows, SW China. The ratio of seed set to pollen transferred in individual flowers was monitored over 2 years, indicating that pollen deposited on stigmas by halictid bees produced lower seed set than pollen carried by flies. Scopal pollen applied to stigmas by hand gave good seed set, but in germination tests it burst more frequently than pollen from anthers, implying dehydration. Pollen grains freshly taken from the scopae of solitary bees foraging in sunshine were smaller than those taken from anthers or foraging bees in early-morning overcast conditions, implying dehydration. The effect was reversible: hand pollination showed that scopal pollen was no less effective than fly pollen after removal from the bee. Pollen carried by such bees foraging in intense sunlight in flowers became dehydrated, causing an osmotic mismatch between the pollen and the stigmas. Transient heat-induced dehydration of pollen represents a novel pathway by which climate warming may disrupt plant reproduction, and helps us understand why flies could be more effective pollinators than bees in cool, high-radiation arctic or high-altitude sites.


Bees Flies Environmental effects on pollen performance Scopal pollen Humidity Temperature Seed set Potentilla lancinata 



We thank Director Z.-D. Fang for making available the facilities of the Shangri-La Alpine Botanic Garden, and Jim Cane, John Hobart and two referees for valued comments. This work was supported by the National Science Foundation of China (Grants Nos. U1402267, 31730012).

Supplementary material

11829_2019_9726_MOESM1_ESM.doc (1.4 mb)
Supplementary material 1 (DOC 1450 kb)


  1. Ballantyne G, Baldock K, Willmer P (2015) Constructing more informative plant-pollinator networks: visitation and pollen deposition networks in a heathland plant community. Proc R Soc B 282(1814):20151130CrossRefGoogle Scholar
  2. Bassani M, Pacini E, Franchi GG (1994) Humidity stress reponse in pollen of anemophilous and entomophilous species. Grana 33:146–150CrossRefGoogle Scholar
  3. Bolten AB, Feinsinger P, Baker HG, Baker I (1979) On the calculation of sugar concentration in flower nectar. Oecologia 41:301–304CrossRefGoogle Scholar
  4. Corbet SA (1990) Pollination and the weather. Israel J Bot 39:13–30Google Scholar
  5. Corbet SA, Huang SQ (2016) Small bees overheat in sunlit flowers: do they make cooling flights? Ecol Entomol 41:344–350CrossRefGoogle Scholar
  6. Corbet SA, Plumridge JR (1985) Hydrodynamics and the germination of oil-seed rape pollen. J Agric Sci (Cambridge) 104:445–451CrossRefGoogle Scholar
  7. Grubb PJ (1977) The maintenance of species richness in plant communities: the importance of the regeneration niche. Biol Rev 52:107–145CrossRefGoogle Scholar
  8. Haverkamp A, Li X, Hansson BS, Baldwin IT, Knaden M, Yon F (2018) Flower movement balances pollinator needs and pollen protection. Ecology. CrossRefPubMedGoogle Scholar
  9. Herrera CM (1997) Thermal biology and foraging responses of insect pollinators to the forest floor irradiance mosaic. Oikos 78:601–611CrossRefGoogle Scholar
  10. Herrera CM (2000) Flower-to-seedling consequences of different pollination regimes in an insect-pollinated shrub. Ecology 81:15–29CrossRefGoogle Scholar
  11. Inouye DW (2015) Flies and flowers III: ecology of foraging and pollination. J Pollinat Ecol 16:115–133Google Scholar
  12. Kevan PG (1975) Suntracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723–726CrossRefGoogle Scholar
  13. Keys RN, Buchmann SL, Smith S (1995) Pollination effectiveness and pollination efficiency of insects foraging Prosopis velutina in south-eastern Arizona. J Appl Ecol 32:519–527CrossRefGoogle Scholar
  14. King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol 4:811–818CrossRefGoogle Scholar
  15. Loupassaki M, Vasilakakis M, Androulakis I (1997) Effect of pre-incubation humidity and temperature treatment on the in vitro germination of avocado pollen grains. Euphytica 94:247–251CrossRefGoogle Scholar
  16. Luza J, Polito VS (1987) Effects of desiccation and controlled rehydration on germination in vitro of pollen of walnut (Juglans spp.). Plant Cell Environ 10:487–492CrossRefGoogle Scholar
  17. Mao YY, Huang SQ (2009) Pollen resistance to water in 80 angiosperm species: flower structures protect rain-susceptible pollen. New Phytol 183:892–899CrossRefGoogle Scholar
  18. Michener C (2000) The bees of the world. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  19. Ne’eman G, Jurgens A, Newstrom-Lloyd L, Potts S, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451PubMedGoogle Scholar
  20. Nepi M, Franchi G, Pacini E (2001) Pollen hydration status at dispersal: cytophysiological features and strategies. Protoplasma 216:171–180CrossRefGoogle Scholar
  21. Pisanty G, Afik O, Wajnberg E, Mandelik YD (2016) Watermelon pollinators exhibit complementarity in both visitation rate and single-visit pollination efficiency. J Appl Ecol 53:360–370CrossRefGoogle Scholar
  22. Reynolds R, Fenster C (2008) Point and interval estimation of pollinator importance: a study using pollination data of Silene caroliniana. Oecologia 156:325–332CrossRefGoogle Scholar
  23. Rodriguez-Riano T, Dafni A (2000) A new procedure to assess pollen viability. Sex Plant Reprod 12:241–244CrossRefGoogle Scholar
  24. Rosbakh S, Pacini E, Nepi M, Poschlod P (2018) An unexplored side of regeneration niche: seed quantity and quality are determined by the effect of temperature on pollen performance. Front Plant Sci 9:1036CrossRefGoogle Scholar
  25. Song B, Chen G, Stöcklin J, Peng DL, Niu Y, Li ZM, Sun H (2014) A new pollinating seed-consuming mutualism between Rheum nobile and a fly fungus gnat, Bradysia sp., involving pollinator attraction by a specific floral compound. New Phytol 203:1109–1118CrossRefGoogle Scholar
  26. Tiusanen M, Hebert PDN, Schmidt NM, Roslin T (2016) One fly to rule them all—muscid flies are the key pollinators in the Arctic. Proc R Soc B 283:20161271CrossRefGoogle Scholar
  27. Totland Ø (1994) Intraseasonal variation in pollination intensity and seed set in an alpine population of Ranunculus acris in Southwestern Norway. Ecography 17:159–165CrossRefGoogle Scholar
  28. Totland Ø (1996) Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): effects on flower temperature, insect visitation, and seed production. Am J Bot 83:452–458CrossRefGoogle Scholar
  29. Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507CrossRefGoogle Scholar
  30. Yates I, Sparks D (1989) Hydration and temperature influence in vitro germination of pecan pollen. J Am Soc Hortic Sci 114:599–605Google Scholar
  31. Zinn K, Tunc-Ozdemir M, Harper J (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exper Bot 61:1959–1968CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sarah A. Corbet
    • 1
    • 2
  • Fei-Fei Chen
    • 3
  • Fang-Fang Chang
    • 3
  • Shuang-Quan Huang
    • 3
    Email author
  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK
  2. 2.PenzanceUK
  3. 3.School of Life Sciences, Institute of Evolution and EcologyCentral China Normal UniversityWuhanChina

Personalised recommendations