Mutualisms can change when conditions change

Although individuals of two or more species might interact in a way that allows both to receive fitness benefits, we need to recognize that each individual participates in the mutualism to improve its own fitness, not that of its partner. Therefore, when conditions alter the costs and benefits for each species, the interaction can change to something that is no longer a mutualism.

From Positive to Negative Interactions

When one species in a relationship provides a benefit to another species at some cost but no longer receives a benefit in return, the interaction can shift from a positive, mutualistic interaction to a negative interaction such as herbivory, predation, or parasitism. For example, we discussed the role that mycorrhizal fungi play in helping plants obtain nutrients. In an experiment with citrus trees in highly fertile soils, researchers examined the effect of eliminating the mycorrhizal fungi by treating the soil with a fungicide. They found that eliminating the fungus made the trees grow up to 17 percent faster. This suggests that the fungus posed a cost to the tree without providing a benefit. Because the soil was fertile, the citrus trees were not dependent on the fungi to provide nutrients. The trees could grow well by collecting nutrients on their own but, because the fungi still existed in the soil, the trees still provided the fungi with the products of photosynthesis. The normally mutualistic relationship had changed into a parasitic interaction.

A similar situation exists for cleaner fish. You may recall that cleaner fish remove ectoparasites from larger fish. Both species benefit and the interaction is a mutualism. However, it turns out that cleaner fish also like to consume mucus and scales of larger fish, which is harmful to the larger fish because mucus and scales are costly to produce and may offer protection against infection. Researchers working on coral reefs in the Caribbean examined whether the feeding decisions of a cleaner fish, the Caribbean cleaning goby (Elacatinus evelynae), changed when there were differences in the number of ectoparasites carried by the longfin damselfish (Stegastes diencaeus). They sampled the number of ectoparasites on the damselfish off the coasts of six different islands, and then observed the cleaner fish to determine the percentage of mucus and scales in their diet. You can see their data in Figure 17.17. When damselfish populations had a high number of parasites, the cleaner fish ingested a small percentage of mucus and scales. However, when the damselfish had a low number of parasites, the cleaner fish ingested a much higher percentage of mucus and scales. Therefore, when the parasites are rare on the damselfish, the cleaner fish switch from being mutualistic to predatory and consume a higher percentage of mucus and scales.

Figure 17.17 Switching from mutualism to predation. In populations of damselfish where ectoparasites are abundant, the cleaner fish primarily consume parasites of the damselfish and very little of the damselfish’s mucus and scales. This is a mutualistic interaction. In populations of damselfish where the ectoparasites are not abundant, the diet of the cleaner fish includes a substantial percentage of the mucus and scales from the damselfish. This becomes more of a predatory interaction. Error bars are standard errors.
Data from K. L. Cheney and I. M. Côté, Mutualism or parasitism? The variable outcome of cleaning symbioses, Biology Letters 1 (2005): 162–165.

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Dealing With Cheaters

A mutualistic relationship can evolve over time into a relationship in which one species receives a benefit but does not provide one in return—a behavior known as cheating. Natural selection would favor cheating as long as it provides a net increase in the cheater’s fitness, although we would also expect natural selection to favor mechanisms that enable organisms to defend themselves against cheaters. We saw an example of this with yuccas and yucca moths. When a moth lays so many eggs that the hatching larvae will eat all of the developing seeds, some species of yucca can respond by aborting the flower, thereby killing the moth larvae. In this way, the yucca punishes yucca moths that act as cheaters.

A similar situation exists in relationships between plants and mycorrhizal fungi. When they operate as mutualists, both species provide a benefit at some cost. If a fungus reduces the benefit it provides to a plant, the plant should respond by providing a smaller benefit to the fungus. In 2009, researchers conducted a study to see if a plant could discriminate between different fungi and send products of photosynthesis to the most beneficial fungal mutualist. To test this question, the researchers planted individual wild onion (Allium vineale) plants in two pots; half of the plant’s roots went into a pot of soil containing a fungal species that provides large benefits to the plant and the other half of the roots went into a second pot containing a fungal species that provides no benefit to the plant. This experiment is illustrated in Figure 17.18a. After the onion roots grew for 9 weeks, researchers measured how much photosynthetic product the plant was sending to each fungus. They did this by placing a bag around each plant and pumping in a special form of CO2 that contained a rare isotope of carbon known as 14C. Using this radioactive form of carbon, they could track the movement of carbon from the plant to each fungal species. They found that onion plants sent more products of photosynthesis to the beneficial fungi, as you can see in Figure 17.18b. This means that plants can discriminate among different fungi and preferentially provide greater benefits to the most beneficial fungi.

Figure 17.18 Favoring the most beneficial partner. (a) In an experiment, the wild onion plant was grown with its roots into two separate pots: one contained a beneficial mycorrhizal fungus and the other contained a nonbeneficial mycorrhizal fungus. After 9 weeks of growth, researchers were able to determine whether the plant allocates more of its photosynthetic products to the beneficial or nonbeneficial fungus. (b) Because the plant can distinguish between the two fungal species, it is able to allocate more of its photosynthetic products to the more beneficial fungus. Error bars are standard errors.
Data from J. D. Bever et al., Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism, Ecology Letters 12 (2009): 13–21.