pp 1–10 | Cite as

Pollinator or pedigree: which factors determine the evolution of pollen nutrients?

  • Fabian A. Ruedenauer
  • Johannes Spaethe
  • Casper J. van der Kooi
  • Sara D. LeonhardtEmail author
Behavioral ecology – original research


A prime example of plant–animal interactions is the interaction between plants and pollinators, which typically receive nectar and/or pollen as reward for their pollination service. While nectar provides mostly carbohydrates, pollen represents the main source of protein and lipids for many pollinators. However, the main function of pollen is to carry nutrients for pollen tube growth and thus fertilization. It is unclear whether pollinator attraction exerts a sufficiently strong selective pressure to alter the nutritional profile of pollen, e.g., through increasing its crude protein content or protein-to-lipid ratio, which both strongly affect bee foraging. Pollen nutritional quality may also be merely determined by phylogenetic relatedness, with pollen of closely related plants showing similar nutritional profiles due to shared biosynthetic pathways or floral morphologies. Here, we present a meta-analysis of studies on pollen nutrients to test whether differences in pollen nutrient contents and ratios correlated with plant insect pollinator dependence and/or phylogenetic relatedness. We hypothesized that if pollen nutritional content was affected by pollinator attraction, it should be different (e.g., higher) in highly pollinator-dependent plants, independent of phylogenetic relatedness. We found that crude protein and the protein-to-lipid ratio in pollen strongly correlated with phylogeny. Moreover, pollen protein content was higher in plants depending mostly or exclusively on insect pollination. Pollen nutritional quality thus correlated with both phylogenetic relatedness and pollinator dependency, indicating that, besides producing pollen with sufficient nutrients for reproduction, the nutrient profile of zoophilous plants may have been shaped by their pollinators’ nutritional needs.


Foraging Nutrition Meta-analysis Plant–insect interactions Pollen quality Pollination Resource use 



We thank the many authors who analyzed pollen nutritional content and thus made this meta-analysis possible. We are also very grateful for the constructive comments provided by three anonymous reviewers, which significantly improved the presentation of this study.

Author contribution statement

SDL, JS, and FAR conceived the study. The data set was compiled and edited by FAR. Statistics were designed and performed by SDL and FAR. FAR, SDL, CJvdK, and JS wrote the manuscript. All authors discussed the results, commented on the paper, and agreed to the final version.


Our work was supported by the Deutsche Forschungsgemeinschaft (LE 2750/5-1 and SP 1380/1-1). CJvdK was supported by a Veni Grant (number 016.Veni.181.025) from the Dutch NWO.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

For this type of study formal consent is not required.

Supplementary material

442_2019_4494_MOESM1_ESM.docx (110 kb)
Supplementary material 1 (DOCX 99 kb)


  1. Ackerman JD (2000) Abiotic pollen and pollination: ecological, functional, and evolutionary perspectives. Plant Syst Evol 222:167–185. CrossRefGoogle Scholar
  2. Auclair JL, Jamieson CA (1948) A qualitative analysis of amino acids in pollen collected by bees. Science 108:357–358. CrossRefGoogle Scholar
  3. Baidya DK, Sasaki M, Matsuka M (1993) Effect of pollen-substitute feeding site on brood rearing in honeybee colonies. Appl Entomol Zool 28:590–592CrossRefGoogle Scholar
  4. Baker HG, Baker I (1979) Starch in angiosperm pollen grains and its evolutionary significance. Am J Bot 66:591–600CrossRefGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc: Ser B (Methodol) 57:289–300Google Scholar
  6. Berenbaum M et al (1986) Insect-plant interactions. Springer, New YorkGoogle Scholar
  7. Bernays EA (1989) Insect-plant interactions. CRC Press, Boca RatonGoogle Scholar
  8. Camazine S, Sneyd J (1991) A model of collective nectar source selection by honey bees: self-organization through simple rules. J Theor Biol 149:547–571. CrossRefGoogle Scholar
  9. Chichiriccò G, Pacini E, Lanza B (2019) Pollenkitt of some monocotiledons: lipid composition and implications in pollen germination. Plant Biol. Google Scholar
  10. DeGroot AP (1953) Protein and amino acid requirements of the honey bee (Apis mellifica L.). Physiol Comp Oecol 3:197–285Google Scholar
  11. Faegri K, Van der Pijl L (2013) Principles of pollination ecology. Elsevier, AmsterdamGoogle Scholar
  12. Friedman J, Barrett SCH (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann Bot 103:1515–1527. CrossRefGoogle Scholar
  13. Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598. CrossRefGoogle Scholar
  14. Haydak MH (1970) Honey bee nutrition. Annu Rev Entomol 15:143–156CrossRefGoogle Scholar
  15. Herbert EW, Shimanuki H, Caron D (1977) Optimum protein levels required by honey bees (Hymenoptera, Apidae) to initiate and maintain brood rearing. Apidologie 8:141–146. CrossRefGoogle Scholar
  16. Hopper S (1980) Bird and Mammal pollen vectors in Banksia communities at Cheyne Beach, Western Australia. Aust J Bot 28:61–75. CrossRefGoogle Scholar
  17. Ibrahim SH (1974) Composition of pollen gathered by honeybees from some major sources. Albohouth Azziraiya 52:121–123Google Scholar
  18. Jones CG, Lawton JH, Shachak M (1996) Organisms as ecosystem engineers. Ecosystem management: selected readings. Springer, New York, pp 130–147Google Scholar
  19. Junker RR et al (2017) Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications. New Phytol. Google Scholar
  20. Kitaoka TK, Nieh JC (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav Ecol Sociobiol 63:501–510. CrossRefGoogle Scholar
  21. Kriesell L, Hilpert A, Leonhardt SD (2017) Different but the same: bumblebee species collect pollen of different plant sources but similar amino acid profiles. Apidologie 48:102–116CrossRefGoogle Scholar
  22. Külheim C, Hui Yeoh S, Maintz J, Foley WJ, Moran GF (2009) Comparative SNP diversity among four Eucalyptus species for genes from secondary metabolite biosynthetic pathways. BMC Genomics 10:452. CrossRefGoogle Scholar
  23. Labandeira CC, Currano ED (2013) The fossil record of plant-insect dynamics. Annu Rev Earth Planet Sci 41:287–311. CrossRefGoogle Scholar
  24. Labarca C, Loewus F (1973) The nutritional role of pistil exudate in pollen tube wall formation in Lilium longiflorum II. Production and utilization of exudate from stigma and stylar canal. Plant Physiol 52:87–92CrossRefGoogle Scholar
  25. Lau TC, Stephenson AG (1993) Effects of soil nitrogen on pollen production, pollen grain size, and pollen performance in Cucurbita pepo (Cucurbitaceae). Am J Bot 80:763–768CrossRefGoogle Scholar
  26. Leonhardt SD, Blüthgen N (2012) The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43:449–464. CrossRefGoogle Scholar
  27. Lewis AC (1986) Memory constraints and flower choice in Pieris rapae. Science 232:863–865. CrossRefGoogle Scholar
  28. Loper GM, Berdel RL (1980) A nutritional bioassay of honeybee brood-rearing potential. Apidologie 11:181–189CrossRefGoogle Scholar
  29. Manning R, Rutkay A, Eaton L, Dell B (2007) Lipid-enhanced pollen and lipid-reduced flour diets and their effect on the longevity of honey bees (Apis mellifera L.). Aust J Entomol 46:251–257. CrossRefGoogle Scholar
  30. McCall C, Primack RB (1992) Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am J Bot 79:434–442. CrossRefGoogle Scholar
  31. McCullagh P (2018) Generalized linear models. CRC Press, Boca RatonGoogle Scholar
  32. Nicholls E, Hempel de Ibarra N (2016) Assessment of pollen rewards by foraging bees. Funct Ecol. Google Scholar
  33. Pearse WD et al (2015) Pez: phylogenetics for the environmental sciences. Bioinformatics 31:2888–2890. CrossRefGoogle Scholar
  34. Petanidou T, Van Laere A, Ellis WN, Smets E (2006) What shapes amino acid and sugar composition in Mediterranean floral nectars? Oikos 115:155–169. CrossRefGoogle Scholar
  35. R Core Team (2018) R: a language and environment for statistical computing R Foundation for Statistical Computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  36. Raubenheimer D, Simpson SJ (1999) Integrating nutrition: a geometrical approach. Entomol Exp Appl 91:67–82. CrossRefGoogle Scholar
  37. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591–601. CrossRefGoogle Scholar
  38. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209. CrossRefGoogle Scholar
  39. Roulston TaH, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol Monogr 70:617–643.;2 Google Scholar
  40. Ruedenauer FA, Spaethe J, Leonhardt SD (2015) How to know which food is good for you: bumblebees use taste to discriminate between different concentrations of food differing in nutrient content. J Exp Biol 218:2233–2240. CrossRefGoogle Scholar
  41. Ruedenauer FA, Spaethe J, Leonhardt SD (2016) Hungry for quality—individual bumblebees forage flexibly to collect high-quality pollen. Behav Ecol Sociobiol 70:1209–1217. CrossRefGoogle Scholar
  42. Ruedenauer FA, Leonhardt SD, Lunau K, Spaethe J (2019) Bumblebees are able to perceive amino acids via chemotactile antennal stimulation. J Comp Physiol A. Google Scholar
  43. Saffari A, Kevan PG, Atkinson JL (2010) Palatability and consumption of patty-formulated pollen and pollen substitutes and their effects on honeybee colony performance. J Apic Sci 54:63–71Google Scholar
  44. Sargent RD, Kembel SW, Emery NC, Forrestel EJ, Ackerly DD (2011) Effect of local community phylogenetic structure on pollen limitation in an obligately insect-pollinated plant. Am J Bot 98:283–289CrossRefGoogle Scholar
  45. Saunders ME (2018) Insect pollinators collect pollen from wind-pollinated plants: implications for pollination ecology and sustainable agriculture. Insect Conserv Divers 11:13–31. CrossRefGoogle Scholar
  46. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, PrincetonCrossRefGoogle Scholar
  47. Somerville DC (2001) Nutritional value of bee collected pollens—a report for the Rural Industries Research and Development Corporation. RIRDC Publication No. 01/047. NSW AgricultureGoogle Scholar
  48. Somme L et al (2015) Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46:92–106. CrossRefGoogle Scholar
  49. Stanley RG, Linskens HF (1974) Pollen: biology biochemistry management. Springer, BerlinCrossRefGoogle Scholar
  50. Stiles FG (1976) Taste preferences, color preferences, and flower choice in hummingbirds. Condor 78:10–26. CrossRefGoogle Scholar
  51. Todd FE, Bretherick O (1942) The composition of pollens. J Econ Entomol 35:312–317. CrossRefGoogle Scholar
  52. Vallejo-Marín M, Manson JS, Thomson JD, Barrett SCH (2009) Division of labour within flowers: heteranthery, a floral strategy to reconcile contrasting pollen fates. J Evol Biol 22:828–839. CrossRefGoogle Scholar
  53. van der Kooi C, Kevan P, Koski M (2019a) The thermal ecology of flowers. Ann Bot. Google Scholar
  54. van der Kooi CJ, Dyer AG, Kevan PG, Lunau K (2019b) Functional significance of the optical properties of flowers for visual signalling. Ann Bot 123:263–276. CrossRefGoogle Scholar
  55. Vanderplanck M, Michez D, Vancraenenbroeck S, Lognay G (2011) Micro-quantitative method for analysis of sterol levels in honeybees and their pollen loads. Anal Lett 44:1807–1820. CrossRefGoogle Scholar
  56. Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM (2016a) Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. PNAS. Google Scholar
  57. Vaudo AD, Stabler D, Patch HM, Tooker JF, Grozinger CM, Wright GA (2016b) Bumble bees regulate their intake of the essential protein and lipid pollen macronutrients. J Exp Biol. Google Scholar
  58. Waser NM (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, ChicagoGoogle Scholar
  59. Weiner CN, Hilpert A, Werner M, Linsenmair KE, Blüthgen N (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41:476–487. CrossRefGoogle Scholar
  60. Winston ML (1991) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  61. Zanne AE et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Animal Ecology and Tropical Biology, BiozentrumUniversity of WürzburgWürzburgGermany
  2. 2.Department of Behavioral Physiology and Sociobiology, BiozentrumUniversity of WürzburgWürzburgGermany
  3. 3.Groningen Institute for Evolutionary Life SciencesUniversity of GroningenGroningenThe Netherlands

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