Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss


Sexual reproduction in non-vascular plants requires unicellular free-motile sperm to travel from male to female reproductive structures across the terrestrial landscape1. Recent data suggest that microarthropods can disperse sperm in mosses2. However, little is known about the chemical communication, if any, that is involved in this interaction or the relative importance of microarthropod dispersal compared to abiotic dispersal agents in mosses. Here we show that tissues of the cosmopolitan moss Ceratodon purpureus emit complex volatile scents, similar in chemical diversity to those described in pollination mutualisms between flowering plants and insects, that the chemical composition of C. purpureus volatiles are sex-specific, and that moss-dwelling microarthropods are differentially attracted to these sex-specific moss volatile cues. Furthermore, using experimental microcosms, we show that microarthropods significantly increase moss fertilization rates, even in the presence of water spray, highlighting the important role of microarthropod dispersal in contributing to moss mating success. Taken together, our results indicate the presence of a scent-based ‘plant–pollinator-like’ relationship that has evolved between two of Earth’s most ancient terrestrial lineages, mosses and microarthropods.

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Figure 1: Sex-specific volatile profiles.
Figure 2: Differences in volatile composition.
Figure 3: Springtails prefer female moss.
Figure 4: Springtails enhance fertilization in moss microcosms.


  1. 1

    Paolillo, D. J. J. The swimming sperms of land plants. Bioscience 31, 367–373 (1981)

    Article  Google Scholar 

  2. 2

    Cronberg, N., Natcheva, R. & Hedlund, K. Microarthropods mediate sperm transfer in mosses. Science 313, 1255 (2006)

    CAS  Article  Google Scholar 

  3. 3

    Nickrent, D. L., Parkinson, C. L., Palmer, J. D. & Duff, R. J. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol. Biol. Evol. 17, 1885–1895 (2000)

    CAS  Article  Google Scholar 

  4. 4

    Kenrick, P. & Crane, P. R. The origin and early evolution of land plants. Nature 389, 33–39 (1997)

    CAS  Article  ADS  Google Scholar 

  5. 5

    Muggoch, H. & Walton, J. On the dehiscence of the antheridium and the part played by surface tension in the dispersal of spermatocytes in Bryophyta. Proc. R.. Soc. Lond. B 130, 448–461 (1942)

    Article  ADS  Google Scholar 

  6. 6

    Longton, R. E. Reproductive biology and evolutionary potential in bryophytes. J. Hattori Bot. Lab. 41, 205–223 (1976)

    Google Scholar 

  7. 7

    Shaw, A. J. in Bryophyte Biology (eds Shaw, A. J. & Goffinet, B. ) 369–402 (Cambridge Univ. Press, 2000)

    Google Scholar 

  8. 8

    Andrew, N. R., Rodgerson, L. & Dunlop, M. Variation in invertebrate-bryophyte community structure at different spatial scales along altitudinal gradients. J. Biogeogr. 30, 731–746 (2003)

    Article  Google Scholar 

  9. 9

    Rosenstiel, T. N. & Eppley, S. M. Long-lived sperm in the geothermal bryophyte Pohlia nutans. Biol. Lett. 5, 857–860 (2009)

    Article  Google Scholar 

  10. 10

    Shortlidge, E. E., Rosenstiel, T. N. & Eppley, S. M. Tolerance to environmental desiccation in moss sperm. New Phytol. 194, 741–750 (2012)

    Article  Google Scholar 

  11. 11

    Verhoef, H. A., Nagelkerke, C. J. & Joosse, E. N. G. Aggregation pheromones in Collembola. J. Insect Physiol. 23, 1009–1013 (1977)

    Article  Google Scholar 

  12. 12

    Raspotnig, G., Krisper, G., Schuster, R., Fauler, G. & Leis, H. J. Volatile exudates from the oribatid mite, Platynothrus peltifer. J. Chem. Ecol. 31, 419–430 (2005)

    CAS  Article  Google Scholar 

  13. 13

    Bengtsson, G., Erlandsson, A. & Rundgren, S. Fungal odour attracts soil Collembola. Soil Biol. Biochem. 20, 25–30 (1988)

    Article  Google Scholar 

  14. 14

    Knudsen, J. T., Tollsten, L. & Bergstrom, L. G. Floral scents — a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33, 253–280 (1993)

    CAS  Article  Google Scholar 

  15. 15

    Crepet, W. L. Advanced (constant) insect pollination mechanisms: pattern of evolution and implications vis-a-vis angiosperm diversity. Ann. Mo. Bot. Gard. 71, 607–630 (1984)

    Article  Google Scholar 

  16. 16

    Schiestl, F. P. The evolution of floral scent and insect chemical communication. Ecol. Lett. 13, 643–656 (2010)

    Article  Google Scholar 

  17. 17

    Raguso, R. A. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39, 549–569 (2008)

    Article  Google Scholar 

  18. 18

    Ashman, T. L. Sniffing out patterns of sexual dimorphism in floral scent. Funct. Ecol. 23, 852–862 (2009)

    Article  Google Scholar 

  19. 19

    Shaw, A. J. & Gaughan, J. F. Control of sex-ratios in haploid populations of the moss, Ceratodon purpureus. Am. J. Bot. 80, 584–591 (1993)

    Article  Google Scholar 

  20. 20

    Stark, L. R., McLetchie, D. N. & Eppley, S. M. Sex ratios and the shy male hypothesis in Bryum argenteum (Bryaceae). Bryologist 113, 788–797 (2010)

    Article  Google Scholar 

  21. 21

    Bisang, I. & Hedenäs, L. Sex ratio patterns in dioicous bryophytes re-visited. J. Bryol. 27, 207–219 (2005)

    Article  Google Scholar 

  22. 22

    Hemborg, A. M. & Bond, W. J. Different rewards in female and male flowers can explain the evolution of sexual dimorphism in plants. Biol. J. Linn. Soc. 85, 97–109 (2005)

    Article  Google Scholar 

  23. 23

    Varga, S. & Kytoviita, M. M. Sex-specific responses to mycorrhiza in a dioecious species. Am. J. Bot. 95, 1225–1232 (2008)

    Article  Google Scholar 

  24. 24

    Voigt, C. C., Caspers, B. & Speck, S. Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. J. Mamm. 86, 745–749 (2005)

    Article  Google Scholar 

  25. 25

    Pankow, J. F. et al. Volatilizable biogenic organic compounds (VBOCs) with two dimensional gas chromatography-time of flight mass spectrometry (GC×GC–TOFMS): sampling methods, VBOC complexity, and chromatographic retention data. Atmos. Meas. Tech. Discuss. 4, 3647–3684 (2011)

    Article  Google Scholar 

  26. 26

    Thimm, T. & Larink, O. Grazing preferences of some collembola for endomycorrhizal fungi. Biol. Fertil. Soils 19, 266–268 (1995)

    Article  Google Scholar 

  27. 27

    Sadaka-Laulan, N., Ponge, J. F., Roquebert, M. F., Bury, E. & Boumezzough, A. Feeding preferences of the Collembolan Onychiurus sinensis for fungi colonizing holm oak litter (Quercus rotundifolia Lam.). Eur. J. Soil Biol. 34, 179–188 (1998)

    Article  Google Scholar 

  28. 28

    Staaden, S., Milcu, A., Rohlfs, M. & Scheu, S. Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour. Soil Biol. Biochem. 43, 1411–1416 (2011)

    CAS  Article  Google Scholar 

  29. 29

    Lawton, E. Moss Flora of the Pacific Northwest. (Hattori Botanical Laboratory, 1971)

    Google Scholar 

  30. 30

    Fountain, M. T. & Hopkin, S. P. Folsomia candida (Collembola): A “standard” soil arthropod. Annu. Rev. Entomol. 50, 201–222 (2005)

    CAS  Article  Google Scholar 

  31. 31

    Johnson, D. L. & Wellington, W. G. Predation of Apochthonius minimus (Pseudoscorpionida: Chthoniidae) on Folsomia candida (Collembola: Isotomidae) I. Predation rate and size-selection. Res. Popul. Ecol. (Kyoto) 22, 339–352 (1980)

    Article  Google Scholar 

  32. 32

    Xu, J., Ke, X., Krogh, P. H., Wang, Y., Lou, Y.-M. & Song, J. Evaluation of growth and reproduction as indicators of soil metal toxicity to the Collembolan, Sinella curvis. Insect Sci. 16, 57–63 (2009)

    Article  Google Scholar 

  33. 33

    Steidle, J. L. M. & Schöller, M. Olfactory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J. Insect Behav. 10, 331–342 (1997)

    Article  Google Scholar 

  34. 34

    Mishler, B. D. Reproductive biology and species distinctions in the moss genus Tortula, as represented in Mexico. Syst. Bot. 15, 86–97 (1990)

    Article  Google Scholar 

  35. 35

    van Dam, N. M. & Poppy, G. M. Why plant volatile analysis needs bioinformatics-detecting signals from noise in increasingly complex profiles. Plant Biol. 10, 29–37 (2008)

    CAS  Article  Google Scholar 

  36. 36

    SAS Institute. JMP for Windows. Release 10.0.0. (SAS Institute, 2012)

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We are grateful to W. Luo and L. Isabelle for analytical assistance, to C. Rupert for assistance with the preference assays, and to L. Stark and N. McLetchie for plant material. Funding was provided by the 3M Corporation and the National Science Foundation (DEB-0743461 to S.M.E. and IOS-0719570 to T.N.R).

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S.M.E. and T.N.R. coordinated and planned the project. E.E.S., S.M.E., and T.N.R. initiated and carried out the experiments. A.N.M., J.F.P.. and T.N.R. were responsible for the gas chromatography data and analyses. All authors contributed to the writing of the manuscript.

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Correspondence to Sarah M. Eppley.

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The authors declare no competing financial interests.

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Rosenstiel, T., Shortlidge, E., Melnychenko, A. et al. Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature 489, 431–433 (2012).

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