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Wild Bee Pollen Usage and Microbial Communities Co-vary Across Landscapes

  • Invertebrate Microbiology
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Abstract

Bees forage for pollen and nectar at flowers but simultaneously acquire pathogenic, commensal, and likely beneficial microbes from these same flowers. Characterizing pollen usage of wild bees is therefore crucial to their conservation yet remains a challenging task. To understand pollen usage across landscapes and how this affects microbial communities found in the pollen provisions collected from flowers, we studied the generalist small carpenter bee Ceratina australensis. We collected C. australensis nests from three different climatic zones across eastern and southern Australia. To characterize the plant, fungal, and bacterial composition of these pollen provisions, we used a metabarcoding and next-generation sequencing approach. We found that the species richness of plant types, fungi, and bacteria was highest in a subtropical zone compared to a temperate or a grassland zone. The composition of these communities also differentiated by zone, particularly in pollen composition and fungal communities. Moreover, pollen composition strongly correlated with fungal community composition, suggesting that variation in pollen usage across landscapes results in variation in microbial communities. While how these pollen usage and microbial community patterns affect bee health merits additional work, these data further our understanding of how flowering plant community composition affects not only the pollen usage of a generalist bee but also its associated microbial communities.

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References

  1. Beil M, Horn H, Schwabe A (2008) Analysis of pollen loads in a wild bee community (Hymenoptera: Apidae)—a method for elucidating habitat use and foraging distances. Apidologie 39:456–467

    Article  Google Scholar 

  2. Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann Bot 97:141–150. https://doi.org/10.1093/aob/mcj012

    Article  PubMed Central  PubMed  Google Scholar 

  3. Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci U S A 110:555–558. https://doi.org/10.1073/pnas.1208682110

    Article  PubMed  Google Scholar 

  4. Roulston TH, Cane JH (2002) The effect of pollen protein concentration on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera: Apiformes). Evol Ecol 16:49–65. https://doi.org/10.1023/A:1016048526475

    Article  Google Scholar 

  5. Tasei J-N, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39:397–409. https://doi.org/10.1051/apido:2008017

    Article  CAS  Google Scholar 

  6. Roger N, Michez D, Wattiez R et al (2017) Diet effects on bumblebee health. J Insect Physiol 96:128–133. https://doi.org/10.1016/j.jinsphys.2016.11.002

    Article  CAS  PubMed  Google Scholar 

  7. McFrederick QS, Thomas JM, Neff JL et al (2017) Flowers and wild megachilid bees share microbes. Microb Ecol 73:188–200. https://doi.org/10.1007/s00248-016-0838-1

    Article  PubMed  Google Scholar 

  8. Graystock P, Goulson D, Hughes WOH (2015) Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc R Soc B Biol Sci 282:20151371. https://doi.org/10.1098/rspb.2015.1371

    Article  Google Scholar 

  9. McArt SH, Koch H, Irwin RE, Adler LS (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol Lett 17:624–636. https://doi.org/10.1111/ele.12257

    Article  PubMed  Google Scholar 

  10. Roulston T, Goodell K (2010) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312

    Article  CAS  Google Scholar 

  11. Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957–1255957. https://doi.org/10.1126/science.1255957

    Article  CAS  PubMed  Google Scholar 

  12. Ginsberg HS (1983) Foraging ecology of bees in an old field. Ecology 64:165–175. https://doi.org/10.2307/1937338

    Article  Google Scholar 

  13. Kitaoka TK, Nieh JC (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav Ecol Sociobiol 63:501–510. https://doi.org/10.1007/s00265-008-0684-3

    Article  Google Scholar 

  14. Cook SM, Sandoz JC, Martin AP et al (2005) Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour? Physiol Entomol 30:164–174. https://doi.org/10.1111/j.1365-3032.2005.00445.x

    Article  Google Scholar 

  15. 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. https://doi.org/10.1242/jeb.118554

    Article  PubMed  Google Scholar 

  16. Hopkins CY, Jevans AW, Boch R (1969) Occurrence of octadeca-trans-2, cis-9, cis-12-trienoic acid in pollen attractive to the honey bee. Can J Biochem 47:433–436

    Article  CAS  PubMed  Google Scholar 

  17. Kapheim KM, Bernal SP, Smith AR et al (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae). Behav Ecol Sociobiol 65:1179–1190. https://doi.org/10.1007/s00265-010-1131-9

    Article  PubMed Central  PubMed  Google Scholar 

  18. Kapheim KM, Nonacs P, Smith AR et al (2015) Kinship, parental manipulation and evolutionary origins of eusociality. Proc R Soc B Biol Sci 282:20142886. https://doi.org/10.1086/340600

    Article  Google Scholar 

  19. Lawson SP, Helmreich SL, Rehan SM (2017) Effects of nutritional deprivation on development and behavior in the subsocial bee Ceratina calcarata (Hymenoptera: Xylocopinae). J Exp Biol 220:4456–4462. https://doi.org/10.1242/jeb.160531

    Article  PubMed  Google Scholar 

  20. Lawson SP, Ciaccio KN, Rehan SM (2016) Maternal manipulation of pollen provisions affects worker production in a small carpenter bee. Behav Ecol Sociobiol 70:1891–1900. https://doi.org/10.1007/s00265-016-2194-z

    Article  Google Scholar 

  21. Durrer S, Schmid-Hempel P (1994) Shared use of flowers leads to horizontal pathogen transmission. Proc R Soc B Biol Sci 258:299–302

    Article  Google Scholar 

  22. Evison SEF, Roberts KE, Laurenson L et al (2012) Pervasiveness of parasites in pollinators. PLoS One 7:e30641. https://doi.org/10.1371/journal.pone.0030641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. McFrederick QS, Wcislo WT, Taylor DR et al (2012) Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol 21:1754–1768. https://doi.org/10.1111/j.1365-294X.2012.05496.x

    Article  PubMed  Google Scholar 

  24. McFrederick QS, Mueller UG, James RR (2014) Interactions between fungi and bacteria influence microbial community structure in the Megachile rotundata larval gut. Proc R Soc B Biol Sci 281:20132653

    Article  Google Scholar 

  25. McFrederick QS, Rehan SM (2016) Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee. Mol Ecol 25:2302–2311. https://doi.org/10.1111/mec.13608

    Article  CAS  PubMed  Google Scholar 

  26. McFrederick QS, Cannone JJ, Gutell RR et al (2013) Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl Environ Microbiol 79:1803–1812. https://doi.org/10.1128/AEM.03681-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Dew RM, Rehan SM, Schwarz MP (2016) Biogeography and demography of an Australian native bee Ceratina australensis (Hymenoptera, Apidae) since the last glacial maximum. J Hymenopt Res 49:25–41. https://doi.org/10.3897/JHR.49.8066

    Article  Google Scholar 

  28. Engel P, James RR, Koga R et al (2013) Standard methods for research on Apis mellifera gut symbionts. J Apic Res 52:1–24. https://doi.org/10.3896/IBRA.1.52.4.07

    Article  Google Scholar 

  29. Hawkins J, de Vere N, Griffith A et al (2015) Using DNA metabarcoding to identify the floral composition of honey: a new tool for investigating honey bee foraging preferences. PLoS One 10:e0134735. https://doi.org/10.1371/journal.pone.0134735

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Smith DP, Peay KG (2014) Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One 9:e90234. https://doi.org/10.1371/journal.pone.0090234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Rothman JA, Carroll MJ, Meikle WG et al (2018) Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb Ecol 274:1–11. https://doi.org/10.1007/s00248-018-1151-y

    Article  CAS  Google Scholar 

  32. Meeus I, De Graaf DC, Jans K, Smagghe G (2010) Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109:107–115. https://doi.org/10.1111/j.1365-2672.2009.04635.x

    Article  CAS  PubMed  Google Scholar 

  33. Bourgeois AL, Rinderer TE, Beaman LD, Danka RG (2010) Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. J Invertebr Pathol 103:53–58. https://doi.org/10.1016/j.jip.2009.10.009

    Article  CAS  PubMed  Google Scholar 

  34. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  37. Abarenkov K, Henrik Nilsson R, Larsson K-H et al (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x

    Article  PubMed  Google Scholar 

  38. Bell KL, Loeffler VM, Brosi BJ (2017) An rbcL reference library to aid in the identification of plant species mixtures by DNA metabarcoding. Appl Plant Sci 5:1600110. https://doi.org/10.3732/apps.1600110

    Article  Google Scholar 

  39. Cole JR, Wang Q, Cardenas E et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. https://doi.org/10.1093/nar/gkn879

    Article  CAS  PubMed  Google Scholar 

  40. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1006/jmbi.1990.9999

    Article  CAS  PubMed  Google Scholar 

  41. Atlas of Living Australia (2018) Available at: https://www.ala.org.au. Accessed 28 March 2018

  42. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289–300

    Google Scholar 

  43. Mandal S, Van Treuren W, White RA et al (2015) Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis 26:27663

    PubMed  Google Scholar 

  44. Oksanen J, Blanchet FG, Kindt R, et al (2017) vegan: community ecology package

  45. Herrera CM, Pozo MI, Medrano M (2013) Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–279

    Article  PubMed  Google Scholar 

  46. Vannette RL, Fukami T (2017) Dispersal enhances beta diversity in nectar microbes. Ecol Lett 20:901–910

    Article  PubMed  Google Scholar 

  47. McFrederick QS, Vuong HQ, Rothman JA (2018) Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers. Int J Syst Evol Microbial 68:1879–1884. https://doi.org/10.1099/ijsem.0.002758

    Article  CAS  Google Scholar 

  48. de Vega C, Herrera CM (2013) Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinated plant. Am J Bot 100:792–800

    Article  CAS  PubMed  Google Scholar 

  49. Rering CC, Beck JJ, Hall GW et al (2017) Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytol 40:6–12. https://doi.org/10.1111/nph.14809

    Article  CAS  Google Scholar 

  50. Vannette RL, Fukami T (2016) Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption by pollinators. Ecology 97:1410–1419. https://doi.org/10.1890/15-0858.1

    Article  PubMed  Google Scholar 

  51. Vannette RL, Gauthier M (2013) Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proc R Soc B Biol Sci 280:20122601. https://doi.org/10.1098/rspb.2012.2601

    Article  Google Scholar 

  52. Herrera CM, García IM, Pérez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–2376

    Article  PubMed  Google Scholar 

  53. Klinger EG, James RR, Youssef NN, Welker DL (2013) A multi-gene phylogeny provides additional insight into the relationships between several Ascosphaera species. J Invertebr Pathol 112:41–48. https://doi.org/10.1016/j.jip.2012.10.011

    Article  CAS  PubMed  Google Scholar 

  54. Batra L, Batra S, Bohart G (1973) The mycoflora of domesticated and wild bees (Apoidea). Mycopathologia 49:13–44

    Google Scholar 

  55. James RR, McGuire MR, Leland JE (2012) Susceptibility of adult alfalfa leafcutting bees and honey bees to a microbial control agent, Beauveria bassiana. Southwest Entomol 37:13–21. https://doi.org/10.3958/059.037.0102

    Article  Google Scholar 

  56. Hammer TJ, Janzen DH, Hallwachs W et al (2017) Caterpillars lack a resident gut microbiome. Proc Natl Acad Sci U S A 114:9641–9646. https://doi.org/10.1073/pnas.1707186114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Ambika Manirajan B, Ratering S, Rusch V et al (2016) Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environ Microbiol 18:5161–5174. https://doi.org/10.1111/1462-2920.13524

    Article  PubMed  Google Scholar 

  58. Fridman S, Izhaki I, Gerchman Y, Halpern M (2011) Bacterial communities in floral nectar. Environ Microbiol Rep 4:97–104. https://doi.org/10.1111/j.1758-2229.2011.00309.x

    Article  PubMed  Google Scholar 

  59. McFrederick QS, Wcislo WT, Hout MC, Mueller UG (2014) Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol Ecol 88:398–406. https://doi.org/10.1111/1574-6941.12302

    Article  CAS  PubMed  Google Scholar 

  60. Jojima Y, Mihara Y, Suzuki S (2004) Saccharibacter floricola gen. nov., sp. nov., a novel osmophilic acetic acid bacterium isolated from pollen. Int J Syst Evol Microbiol 54:2263–2267. https://doi.org/10.1099/ijs.0.02911-0

    Article  CAS  PubMed  Google Scholar 

  61. Lenaerts M, Lenaerts M, Álvarez-Pérez S et al (2014) Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar. Syst Appl Microbiol 37:402–411. https://doi.org/10.1016/j.syapm.2014.03.002

    Article  CAS  PubMed  Google Scholar 

  62. Mendonça-Hagler LC, AHOS, 1993 (1993) Phylogeny of Metschnikowia species estimated from partial rRNA sequences. Int J Syst Bacteriol 43:368–373. https://doi.org/10.1099/00207713-43-2-368

    Article  PubMed  Google Scholar 

  63. Rosa CA, Lachance MA (1998) The yeast genus Starmerella gen. nov. and Starmerella bombicola sp. nov., the teleomorph of Candida bombicola (Spencer, Gorin & Tullock) Meyer & Yarrow. Int J Syst Bacteriol 48:1413–1417

    Article  PubMed  Google Scholar 

  64. Schaeffer RN, Mei YZ, Andicoechea J et al (2017) Consequences of a nectar yeast for pollinator preference and performance. Funct Ecol 31:613–621. https://doi.org/10.1111/1365-2435.12762

    Article  Google Scholar 

  65. Rehan SM, Richards MH, Schwarz MP (2010) Social polymorphism in the Australian small carpenter bee, Ceratina (Neoceratina) australensis. Insect Soc 57:403–412. https://doi.org/10.1007/s00040-010-0097-y

    Article  Google Scholar 

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Acknowledgements

We thank Wyatt Shell and Rebecca Dew (UNH) for assistance with nest collections as well as Laura Leger (UCR) for assistance with pathogen screens.

Funding

US Department of Agriculture NIFA Hatch funds (CA-R-ENT-5109-H) to QSM and (NC1173) to SMR, National Science Foundation MSB-ECA award #1638728 to QSM and National Science Foundation IOS-Behavior #1456296 to SMR, as well as National Geographic (9659-15) to SMR supported this research.

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Correspondence to Quinn S. McFrederick.

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McFrederick, Q.S., Rehan, S.M. Wild Bee Pollen Usage and Microbial Communities Co-vary Across Landscapes. Microb Ecol 77, 513–522 (2019). https://doi.org/10.1007/s00248-018-1232-y

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