Biological Market example
underground nutrient trade
rhizobium-nodules on Acacia roots
(photo: Frank Brunner)
The cover of the 'microbial markets' paper by Werner et al (2014)
You can hear (and see) the quite amazing Toby Kiers talking about "mycorrhizal markets" and more here:
TED-talk (2019) "Lessons from fungi on markets and economics"
Mushroom revival podcast (2021) "The Mycorrizal Market Economy"
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.
Reviews contemplating 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
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)
Bragazzi, N., Woldegerima, W. A. & Siri, A. (2024). Economic microbiology: Exploring microbes as agents in economic systems. Frontiers in Microbiology, 15
... 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 these authors:
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
---------------------------------------------------------------------
In 2018, I published a review together with Toby Kiers in which we tried to tackle the question of what exactly is a 'trader' on an underground market (Noë, R. & Kiers, E. T. (2018). Mycorrhizal markets, firms, and co-ops. Trends in Ecology & Evolution, 33(10), 777-789. pdf). This is a hairy question (see also 'the agency problem' on the page 'microbial markets'), notably in the case of arbuscular mycorrhizal fungi (AMFs): which entity is the trading agent that decides about how much to trade and with whom and at what price? And, if plants indeed exert partner choice among their AMF-partners, what is the entity they choose: the whole fungal network (the mycelium, or fungal individual, if one can speak of individuals in this case)? Or, do they choose at the level of single arbuscules, the trading sites inside the root cells that are formed by both fungal and plant tissues? The answer is probably a bit of both: small groups of fungal nuclei, which we called 'co-ops', perhaps determine what happens at the level of single arbuscules, but the whole mycelium also directs the nutrients it trades over long distances to patches where it fetches a better price, as is described in several other papers from the Kiers-lab. Here a few examples:
Whiteside, M.D., Werner, G.D.A., Caldas, V.E.A., van’t Padje, A., Dupin, S.E., Elbers, B.,Bakker, M., Wyatt, G.A.K., Klein, M., Hink, M.A., Postma, M., Vaitla, B., Noë, R., Shimizu, T.S., West, S.A., Kiers, E.T. (2019). Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Current Biology, 29(12), 2043-2050.e2048 open access
The economist Loch-Temzelides used the results of this study in his paper in PNAS (2021): "Walrasian equilibrium behavior in nature" (see the page Biological Market models)
van’t Padje, A., Oyarte Galvez, L., Klein, M., Hink, M. A., Postma, M., Shimizu, T. & Kiers, E. T. (2020). Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. The ISME Journal open access
van ’t Padje, A., Werner, G. D. A. & Kiers, E. T. (2020). Mycorrhizal fungi control value of phosphorus in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability. New Phytologist (this is an exceptionally interesting paper from a BMT viewpoint)
---------------------------------------------------------------------
In the fall of 2020 Prescott and colleagues published a paper in which they claimed that an organism does not (or cannot?) use a substance it produces as a commodity that can be traded against other commodities with mutualistic partners when this substance is a waste product - in this case surplus C produced by plants which is either stored in, or exudated by, their roots. I reacted to this paper with a short 'Letter' in the same journal, because I have the expression that this is a wide-spread fallacy in this particular sub-field of mutualism research.
Prescott CE, Grayston SJ, Helmisaari H-S, Kaštovská E, Körner C, Lambers H, Meier IC, Millard P, Ostonen I (2020) Surplus carbon drives allocation and plant–soil interactions. Trends in Ecology and Evolution 35 1110-1118
Noë R (2021) Waste can be traded with mutualistic partners. Trends in Ecology & Evolution, 36 (3) 175-176 pdf
---------------------------------------------------------------------
Brian Steidinger published an clever extension to BMT in which he develops a model that would explain how mycoheterotrophic plants (plants that are assumed to take up both carbon and other nutrients from fungi) could take part on markets by buying a nutrient from one partner and selling that same nutrient for a better price to another, which in economic jargon is called 'arbitrage'. This also contradicts the paper by Walder and Van der Heijden (2015) mentioned above, by showing that 'arbitrage' is an alternative to the source-sink story, which is more a description than an explanation anyway.
Steidinger, B. S. (2024). Mycorrhizal arbitrage, a hypothesis: How mycoheterotrophs could profit from inefficiencies in the biological marketplace. Functional Ecology
A lot more information on mycorrhizal fungi, and the networks they form, can be found here: SPUN
Till about 2015 the literature in this field developed more or less independently from the literature on markets in vertebrates, but there were 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 68(9), 2603-2618
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 pdf
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 19:648–656
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 a comment 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
van ’t Padje, A., Oyarte Galvez, L., Klein, M., Hink, M. A., Postma, M., Shimizu, T. & Kiers, E. T. (2020). Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. The ISME Journal open access
van ’t Padje, A., Werner, G. D. A. & Kiers, E. T. (2020). Mycorrhizal fungi control value of phosphorus in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability. New Phytologist 299, 2933-2944
Whiteside, M.D., Werner, G.D.A., Caldas, V.E.A., van’t Padje, A., Dupin, S.E., Elbers, B.,Bakker, M., Wyatt, G.A.K., Klein, M., Hink, M.A., Postma, M., Vaitla, B., Noë, R., Shimizu, T.S., West, S.A., Kiers, E.T. (2019). Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Current Biology, 29(12), 2043-2050.e2048 open access
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
Weber, S. E., Bascompte, J., Kahmen, A. & Niklaus, P. A. (2024). Plant choice between arbuscular mycorrhizal fungal species results in increased plant P acquisition. PLOS ONE, 19(1), e0292811
Westhoek, A., Clark, L. J., Culbert, M., Dalchau, N., Griffiths, M., Jorrin, B., . . . Turnbull, L. A. (2021). Conditional sanctioning in a legume–Rhizobium mutualism. Proceedings of the National Academy of Sciences, 118(19), e2025760118
last update: 26 JUN 24