Biological Market examples:

Nutrient exchange symbiosis: mycorrhiza and rhizobia



rhizobium-nodules on Acacia roots

(photo: Frank Brunner)


cover Werner et al. 2014
(click to enlarge)

The cover of the 'microbial markets' paper by Werner et al (2014)


The mutualistic interactions between plants and mycorrhizal fungi and rhizobia (bacteria) provide ideal examples for tests of the biological market paradigm with traders belonging to two clear cut classes: plants and either fungi or bacteria.

The commodities exchanged on this sort of markets are nutrients, which makes it possible to quantify exchanges, at least for those who know how to do this. These systems are also ideally suited for experiments: nutrients can be added, the same individual can interact with different partners in split-root experiments, nodules formed by root tissue and symbionts can be isolated and so forth.

A review of the possibilities of applying biological market theory (BMT) to 'underground markets' can be found here:

  • Werner GDA, Strassmann JE, Ivens ABF, Engelmoer DJP, Verbruggen E, Queller DC, Noë R, Johnson NC, Hammerstein P, Kiers ET (2014) Evolution of microbial markets. Proceedings of the National Academy of Sciences 111:1237-1244. pdf
... and a 'state of the art' review of mycorrhizal markets:
  • Werner, G. D. A., & Kiers, E. T. (2015). Partner selection in the mycorrhizal mutualism. New Phytologist 205: 1437-1442 open access ( This paper appeared in a special issue of New Phytologist in which you can find more comments on the application of BMT to mycorrhiza)
... and a more critical review:
  • Walder, F., & van der Heijden, M. G. A. (2015). Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants, 1, 15159
Toby Kiers and colleagues came to (verbal) blows with the authors of this review (see also my comments on ScoopIt - entry of May 4, 2016):
  • Kiers, E. T., West, S. A., Wyatt, G. A. K., Gardner, A., Bücking, H., & Werner, G. D. A. (2016). Misconceptions on the application of biological market theory to the mycorrhizal symbiosis. Nature Plants, 2, 16063
  • van der Heijden, M. G. A., & Walder, F. (2016). Reply to ‘Misconceptions on the application of biological market theory to the mycorrhizal symbiosis’. Nature Plants, 2, 16062

Till recently the literature in this field developed more or less independently from the literature on markets in vertebrates, but there are regular cross-references. The following papers describe market models based on these nutrient exchange mutualisms:

  • Hoeksema, J. D. & Schwartz, M. W. 2003. Expanding comparative-advantage biological market models: contingency of mutualism on partners’ resource requirements and acquisition trade-offs. Proceedings of the Royal Society B-Biological Sciences, 270, 913-919
  • Kummel, M. & Salant, S. W. 2006. The economics of mutualisms: optimal utilization of mycorrhizal mutualistic partners by plants. Ecology, 87, 892-902
  • Schwartz, M. W. & Hoeksema, J. D. 1998. Specialization and resource trade: biological markets as a model of mutualisms. Ecology, 79, 1029-1038
  • Wyatt, G. A. K., Kiers, E. T., Gardner, A., & West, S. A. (2014). A biological market analysis of the plant-mycorrhizal symbiosis. Evolution


Sanctioning, a drastic form of partner choice

A phenomenon often described here is 'sanctioning', i.e. breaking off the relationship with a partner. An example would be a plant cutting off supplies to a nodule with rhizobia that are less productive than others. 'Sanctioning' is a form of partner choice with usually more drastic results than 'punishment', which is more likely to occur on markets with less extreme power differentials between partners.

The idea of sanctioning as a selective force goes back to a seminal paper by Bull & Rice (1991) on selective abortion of figs. My first paper on the subject (Noë 1990) was cited by these authors, but I have little doubts that they would have had their brain wave without me too. A decade later the idea of sanctioning was further developed by Denison and colleagues.

  • Bull, J. J. & Rice, W. R. 1991. Distinguishing mechanisms for the evolution of co-operation. Journal of Theoretical Biology, 149, 63-74
  • Denison, R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist, 156, 567-576
  • Kiers, E. T. & Denison, R. F. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annual Review of Ecology, Evolution, and Systematics, 39, 215-236
  • Noë, R. 1990. A Veto game played by baboons: a challenge to the use of the Prisoner's Dilemma as a paradigm for reciprocity and cooperation. Animal Behaviour, 39, 78-90
  • West, S. A., Kiers, E. T., Simms, E. L. & Denison, R. F. 2002. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceedings of the Royal Society B-Biological Sciences, 269, 685- 694

Beautiful examples of these underground nutrient exchange markets, based on technically challenging experiments and inspired by biological market logic are given in: 

  • Argüello, A., O'Brien, M. J., van der Heijden, M. G. A., Wiemken, A., Schmid, B., & Niklaus, P. A. (2016). Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism. Ecology Letters (in press)
  • Fellbaum, C. R., Mensah, J. A., Cloos, A. J., Strahan, G. E., Pfeffer, P. E., Kiers, E. T., & Bücking, H. (2014). Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytologist 203, 646-656
  • Franklin, O., Näsholm, T., Högberg, P., & Högberg, M. N. (2014). Forests trapped in nitrogen limitation – an ecological market perspective on ectomycorrhizal symbiosis. New Phytologist, 203, 657–666 pdf (see also coment on this paper in the same issue: Kuyper, T. W., & Kiers, E. T. (2014). The danger of mycorrhizal traps? New Phytologist, 203, 352-354 pdf)
  • Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., Fellbaum, C. R., Kowalchuk, G. A., Hart, M. M., Bago, A., Palmer, T. M., West, S. A., Vandenkoornhuyse, P., Jansa, J. & Bücking, H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333, 880-882

There are many more high-quality empirical papers on nutrient exchange markets, however, of which I list just a few that I found personally most appealing, especially because they give proper attention to partner choice.

  • Bever, J. D., Richardson, S. C., Lawrence, B. M., Holmes, J. & Watson, M. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters, 12, 13-21
  • Cowden, C. C. & Peterson, C. J. 2009. A multi-mutualist simulation: Applying biological market models to diverse mycorrhizal communities. Ecological Modelling, 220, 1522-1533
  • Grman, E., Robinson, T. M. P. & Klausmeier, C. A. 2012. Ecological specialization and trade affect the outcome of negotiations in mutualism. The American Naturalist, 179, 567-581
  • Gubry-Rangin, C., Garcia, M. & Béna, G. 2010. Partner choice in Medicago Truncatula–Sinorhizobium symbiosis. Proceedings of the Royal Society B: Biological Sciences, 277, 1947-1951
  • Heath, K. D. & Tiffin, P. 2007. Context dependence in the coevolution of plant and rhizobial mutualists. Proceedings of the Royal Society B: Biological Sciences, 274, 1905-1912
  • Heath, K. D. & Tiffin, P. 2009. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution, 63, 652-662
  • Kiers, E. T. & van der Heijden, M. G. A. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: Exploring hypotheses of evolutionary cooperation. Ecology, 87, 1627-1636
  • Peay, K., Bruns, T. & Garbelotto, M. 2010. Testing the ecological stability of ectomycorrhizal symbiosis: effects of heat, ash and mycorrhizal colonization on Pinus muricata seedling performance. Plant and Soil, 330, 291-302
  • Simms, E. L., Taylor, D. L., Povich, J., Shefferson, R. P., Sachs, J. L., Urbina, M. & Tausczik, Y. 2006. An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proceedings of the Royal Society B-Biological Sciences, 273, 77-81
  • Verbruggen, E., Mouden, C. E., Jansa, J., Akkermans, G., Bücking, H., West, S. A. & Kiers, E. T. 2012. Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism. The American Naturalist, 179, E133-E146