Mycorrhizal Symbiosis and Biological Markets in Plants

The symbiosis between fungal mycorrhizae and plants provides a good example of how plants trade resources with their mutualists from fungi to animals. As explained in Sect. 7.4 in Chap. 7, plants trade carbohydrates for fungal growth and survival in exchange for mineral nutrients and protection. This exchange of resources can be viewed as a biological market in which both plants and fungi try to optimise resource utilisation (Werner et al. 2014). Core assumptions about biological markets are that both plants and the consumers trade resources and services so as to maximise their respective benefits and that there is partner choice among the distinct classes of plants and consumers. Crucially, the quality of different potential partners varies, and there can be competition over which will be the preferred trading partner for other players. Finally, supply and demand govern the exchange value of resources for services, and all players can advertise the resources they offer. Market theory offers a good perspective from which to understand the dynamic interactions between plants, fungi and animals.

This mycorrhizal mutualism evolved long before plants engaged in mutualisms with insects and vertebrates and contributed to plants’ colonisation of the land. Conforming to fundamental assumptions in biological markets, experimental studies demonstrated that plants could detect variation in nutritional returns provided by fungi, discriminate the best fungal partners and reward them (Kiers et al. 2011). Likewise, fungal partners increase nutrient transfer only to those roots that provide more carbohydrates in return. More specifically, the supply of carbohydrates by plants triggers nutrient uptake and transport by fungi in this symbiosis. Only when plants deliver carbohydrates across the mycorrhizal interface do fungi increase nutrient transport, but not when they can obtain carbohydrates directly (Fellbaum et al. 2012). That each partner attempts to optimise nutritional returns by choosing the best partner leads to bidirectional control, which in turn stabilises the mutualism through reciprocal rewards. This distinguishes biological markets from obligate symbiosis, where at least one partner has lost the outside option, which can lead to domestication as in endosymbionts.

The fundamental principle of partner choice does not only apply to mycorrhizae but also occurs in the biological markets of pollination and seed dispersal (Stournaras et al. 2015). Most animals are sensitive to variation in the nutritional rewards offered by plants. Seed-dispersing birds, for example, can discriminate 1-2% differences in the carbohydrate contents of fruits and perceive variation in the composition of amino acids (Schaefer et al. 2003a). Importantly, animals can use a simple self-serving strategy to direct their interactions to more rewarding partners and thereby reduce the fitness of less rewarding ones. A good example are hawkmoths, which reduce probing time on less rewarding flowers to increase their foraging efficiency and thereby reduce the pollination and seed set of relatively unrewarding flowers (Brandenburg et al. 2012). Self-serving behaviour is an effective strategy only if the fitness effects of multiple, repeated interactions between two partners have a pronounced influence on the fitness of each, but a single interaction does not strongly determine their fitness (Schaefer et al. 2014). This is the case for seed dispersal and for pollination.

The dynamics between plants and mycorrhi- zae differ, however, from those of pollination and seed dispersal because plants have greater control over partner choice among mycorrhizal fungi than among animals that disperse their genes. In other words, only animals, not plants, can apply self-serving behaviour to choose optimal partners in pollination and seed dispersal. As stated earlier, plants influence partner choice through their biochemistry. Plants may be able to adjust biochemicals to achieve optimal partner choice in tight coevolutionary interactions with animals over evolutionary time spans. However, coevolutionary interactions incur high risks of being interrupted in communities with high species turnover, such as those occurring during glacial and anthropogenic changes. This leads to a higher probability of deviations from optimal partner choice in pollination and seed dispersal than in mycorrhizal symbiosis.