Pollination mutualisms increase diversity, stability, and function in complex ecosystems

“Aside from their pollination function, pollinators consume and are consumed by other members of ecological communities, which influences the controversial effects of pollinators on ecological networks. Here the authors show that when mutualists such as pollinators are introduced into food webs, they increase ecosystem biodiversity, stability, and function.” – Editor’s Summary

The role of mutualism in ecological and other systems (e.g., cooperation in business and economic systems, host-microbiome systems) has been controversial since at least the 1970s when Robert May famously argued for its destabilizing influence due to the positive feedbacks between species. This theoretical instability contradicts the rich diversity of mutualisms observed in nature including those of indispensable agricultural significance between plants and their pollinators, in which animals forage for nectar and pollen rewards produced by plants and provide reproductive services in the process.

We developed a novel consumer-resource theory that synthesizes mechanisms of mutualisms and other feeding interactions like predation, parasitism, and herbivory in what we believe is the most comprehensive investigation of the role of mutualism in complex ecosystems yet conducted. Specifically, we studied the effect of pollination mutualisms on ecosystem stability and function by interconnecting the structure and dynamics of mutualistic networks and food webs, and calculated bioenergetic dynamics using species’ body size. In the model, the production of floral rewards like nectar and pollen is coupled to plants’ production of vegetative biomass. When plants have a high rewards production rate, pollinators are attracted to feed on this resource (which is insulated from competition with other herbivores), providing reproductive services in the process. Even if producing rewards is energetically costly, this feedback permits plant vegetative biomass to grow and in turn support more production of floral rewards. Together, these processes increase the total primary production of biomass, which propagates though the food web to support more stable, diverse, and abundant communities of animals at higher trophic levels (omnivores and carnivores).

This highlights the critically important role of rewards biomass in supporting diversity and function of terrestrial ecosystems. Perhaps because of its crypticity (hidden in flowers) or because of its association with mutualisms, rewards biomass has traditionally been ignored by trophic ecology. Yet, recent estimates suggest that nectar alone can account for up to 5-10% of net primary productivity of meadows in the UK (Baude et al. 2016).

We also found that when floral rewards production rate is insufficient to support pollinators, ecosystems with pollination mutualisms are less diverse, productive, and stable than ecosystems with no mutualism at all. This is because the dynamics of competition for insufficient floral rewards cause crashes in pollinator populations, which in turn destabilizes higher trophic levels that rely on pollination mutualisms for sufficient or steady food sources. However, these effects can be ameliorated when pollinators have additional food available to them in the form of other plant and animal resources. Floral rewards are thought to have declined in natural ecosystems over the last century with only recent trends of partial recovery (Baude et al. 2016; Hicks et al. 2016), and our results suggest that these systems could face collapse of both pollination mutualisms and higher trophic levels if this recovery is insufficient.

Our findings make a significant advance towards resolving contradictions between classical theory and empirical observations. Additionally our work advances towards the prominent goal of unifying ecological research by integrating multiple types of species interactions into a common conceptual framework based on multiplex networks, one of the most active frontiers of ecological network research and in network science more generally.

Citation: Hale, K. R. S., Valdovinos, F. S., & Martinez, N. D. (2020). Mutualism increases diversity, stability, and function of multiplex networks that integrate pollinators into food webs. Nature Communications 11:1–14. https://doi.org/10.1038/s41467-020-15688-w

Abstract: Ecosystems are composed of complex networks of many species interacting in different ways. While ecologists have long studied food webs of feeding interactions, recent studies increasingly focus on mutualistic networks including plants that exchange food for reproductive services provided by animals such as pollinators. Here, we synthesize both types of consumer-resource interactions to better understand the controversial effects of mutualism on ecosystems at the species, guild, and whole-community levels. We find that consumer-resource mechanisms underlying plant-pollinator mutualisms can increase persistence, productivity, abundance, and temporal stability of both mutualists and non-mutualists in food webs. These effects strongly increase with floral reward productivity and are qualitatively robust to variation in the prevalence of mutualism and pollinators feeding upon resources in addition to rewards. This work advances the ability of mechanistic network theory to synthesize different types of interactions and illustrates how mutualism can enhance the diversity, stability, and function of complex ecosystems.