Do predators always reduce the benefits of mutualists?

What we found:

You might expect that mutualisms are often disrupted by predators that eat mutuallists such as bees or fish, but it’s not always true. In our new paper led by Holly Moeller, Adrian Stier, and Roger Nisbet, we showed that it really depends on how animals interact when you have diverse sets of animals that all mutualistically interact and compete with one another. We used a mathematical model to investigate the effects of predation on mutualism function in coral reefs. We found that predators can have both positive and negative effects on mutualistic relationships between coral and their symbiotic partners. Specifically, when predators preferentially consume competitively dominant but lower quality mutualists, this can allow higher quality mutualists to dominate and enhance the performance of the coral host. This suggests that the relationship between predators and mutualism is more complex than previously thought, and that the direction and strength of predator effects depend on various factors such as competition, service provision, and predation vulnerability. We suggest that changes in predator populations (such as those caused by human activities) can lead to dynamic responses in mutualist communities, with potentially nonmonotonic effects on host provisioning to their symbionts

Motivation

Mutualisms are special relationships between different species where both parties benefit. For example, pollinators help spread pollen from plant to plant, and in return, plants offer nectar as a reward. Scientists study these relationships because they can be very complex and involve multiple species. In the past, scientists only studied positive interactions between two species, but now they are looking at how these relationships are connected to other ecological processes such as competition and predation.

Predators can have a big impact on mutualistic relationships. For example, if a predator eats a pollinator, it can decrease the amount of pollen being spread which can negatively affect a plant's growth. However, sometimes predation can also have a positive impact on mutualistic relationships, like when a predator eats a less effective pollinator, the plant may benefit from the remaining, more efficient pollinators.

Here we used mathematical models to predict how predators affect mutualistic relationships. They study how different factors, like the quality of mutualistic partners or their susceptibility to predation, affect the relationship. These models can be based on specific examples like coral reef fishes, but the results can also be applied to other types of mutualistic relationships. The goal is to understand how predators can alter the services and performance of multispecies mutualisms, and the conditions under which higher trophic level can have positive impacts on mutualistic partners.

Our Approach

To construct our mathematical model, we drew inspiration from a real biological system in which a multispecies mutualism is exposed to variable predation pressure. Tropical coral reefs are populated by dozens of fish species. Some of these species live on or among the interstices of branching corals where they receive protection from predation . These coral-dwelling fishes excrete nitrogen-rich waste products, typically in the form of ammonium and/or urea, which can be taken up by the coral and are transferred to and used by the photosynthetic algae living inside of the coral animal's tissue . The photosynthate produced by these algae feeds the coral, stimulating coral growth.

A model for the coral–fish–predator mutualism system. We model a population of corals C (here, one coral colony is shown for illustrative convenience) which hosts two coral-dwelling fishes: damselfish D and hawkfish H. Both fish species are vulnerable to predation by a mesopredator P, which is itself susceptible to fishing pressure. Depending upon the mutualists' traits, coral area exhibits divergent responses to increasing predator abundances. Illustration by Emma Vogan.

A model for the coral–fish–predator mutualism system. We model a population of corals C (here, one coral colony is shown for illustrative convenience) which hosts two coral-dwelling fishes: damselfish D and hawkfish H. Both fish species are vulnerable to predation by a mesopredator P, which is itself susceptible to fishing pressure. Depending upon the mutualists' traits, coral area exhibits divergent responses to increasing predator abundances.

Benefits provided by two coral-dwelling fishes to corals are well studied in the lagoons surrounding the island of Moorea, French Polynesia. Both hawkfish (Paracirrhites arcatus) and yellow-tailed damselfish (Dascyllus flavicaudus) colonize branching colonies of the coral genus Pocillopora. While hawkfish—mesopredators that occasionally prey on damselfish—are the dominant competitors, corals that host damselfish grow significantly faster than those with hawkfish. Both fishes are preyed upon by transient predatory fishes (e.g., longface emperor Lethrinus olivaceus), though predation rates in Moorea are not well known and vary significantly across sites.

What we found

We used a computer simulation to study how the number of predatory fish in coral reefs affects the growth of coral. We imagined a situation where the number of predators increased every five years. In the absence of predators, our simulation showed that the coral was mostly dominated by a fish called the hawkfish and another fish called the damselfish was not able to compete with them. As the number of predators increased, they hunted and eliminated the hawkfish. This change in competition between the fish had a different effect on the coral growth depending on the scenario. In some cases, the overall reduction in fish that live on the coral caused the coral to shrink. However, in other cases, the change in competition allowed the damselfish to thrive, which caused the coral to grow faster. In both cases, as the number of predators continued to increase, they eventually hunted all the fish that live on the coral, which had a negative impact on the coral growth.

In order for predators to indirectly benefit the growth of foundation species, three criteria must be met:

1. Damselfish must be higher quality mutualists than hawkfish

2. Hawkfish must be stronger competitors than damselfish, such that damselfish are competitively excluded in the absence of predators.

3. Hawkfish must be more susceptible to predation than damselfish

More generally, predators mediate indirect benefits when their activity reduces the competitive dominance of a lower quality mutualist. Predators do not benefit foundation species when:

1. they prefer the higher quality mutualist, because in this case predators reduce the population of the best partner and have a net negative effect on mutualist goods provisioning, or

2. they prefer the weaker competitor, because in this case predators do not alter the outcome of competition.

Why does this matter?

Because predators consume prey, their presence is generally thought to reduce benefits conferred by mutualist prey to their partners. However, here we show that under certain circumstances predators can in fact enhance the performance of multispecies mutualisms, with cascading impacts on the growth of foundation species. Our model predicts that the indirect benefits of predators on foundation species can occur under specific conditions: namely, when predators preferentially target a dominant competitor that is also a weaker mutualist. Under these circumstances, predators alter the outcome of competition in ways that enhance the overall delivery of mutualist goods. These results corroborate previous research documenting the importance of third-party species interactions in driving the performance of mutualist guilds and point to significant empirical opportunities to better integrate mutualisms into networks embedded with diverse sets of species interactions.

If fishing alters predation pressure on coral reefs either by reducing the abundance of large predatory fishes or increasing the abundance of highly carnivorous mid food web predators, this may modify the dominant mutualist fish found in certain corals and restructure the services imbued by these diverse coral occupants. Additional research should consider how these potential shifts might integrate with ongoing research examining how fishing potentially alters the supply of nutrients from fishes to coral reefs. In extreme cases, these fisheries-induced shifts in mutualist identity and density may have significant consequences for the growth and survival of corals.

Conclusion

The idea that predation is a critical process governing the coexistence of species and altering the abundance of foundation species is central to our understanding of biological communities. Long-standing theories predict that predators can maintain the biodiversity in systems and by altering the abundance and behavior of prey they can alter the abundance of habitat-forming species. While the role of predation in modifying consumer–resource interactions is well established, the theoretical and empirical link between predation and diverse mutualist communities is in its infancy. The next step is to further characterize how predators interact with diverse guilds of mutualists in nature, paying particular attention to the covariance structure predation, competition, and the services mutualists provide. Moreover, the theory developed here provides a foundation to develop new models linking predation and mutualism, such as consideration for how predator–mutualist dynamics shift as the architecture of species interactions change in shape and the consequences for the resilience of natural systems.