• An international team analyzes for the first time how indirect interactions in mutualistic network shape species fitness and, therefore, their reproductive success and conservation,     
• The loss of species and their interactions, both directs and indirects, have ecological and evolutionary consequences.

An international scientific team has revealead in a new study that indirect interactions between species in a mutualistic network modulate, as well as the direct ones, the adaptation of species to the natural environment. Until now it was known that they could influence the ecological dynamics and the evolution of species characteristics, but there was no evidence of their immediate consequences on the biological fitness of these species, -that is, the ability to survive to reproductive age and produce offspringin- in mutualistic networks that include a high diversity of species. This finding, published in the journal Nature, is important, for example, for understanding why a population grows or declines and also how natural selection acts on individuals within a population.

"Species, in general, do not interact with each other individually, but within a network of much more complex interactions that include a multitude of species," says Pedro Jordano, CSIC researcher at the Doñana Biological Station. One of the most relevant interactions in the functioning of ecosystems are mutualistic interactions, those that are naturally beneficial for both interacting species, such as the pollination of plants by animals, generally insects, or the dispersal of seeds by animals that consume the fruits.

In recent decades, this holistic vision has been used to deepen our understanding of how ecosystems function. Under this approach, it is now known that in a given ecosystem there is a combination of both direct effects, mediated by interacting species, and indirect effects, between species that are not linked directly as interacting partners. However, until now, their relative importance in the biological fitness was unknown. "For example, the introduction of invasive species could also affect the magnitude of these effects and, ultimately, the reproductive capacity of the species and their conservation," adds the researcher.

Study co-authors include researchers of the Doñana Biological Station (EBD-CSIC), the University of Seville and the Institute of Natural Products and Agrobiology, as well as the University of São Paulo, the State University of Campinas – Unicamp, the University of California, Santa Cruz and the University of Zurich.

Indirect interactions also affect biological fitness

In this new study, researchers used novel analytical techniques in a total of 186 mutualistic networks and detected that both direct and indirect interactions affect biological fitness of species within a mutualistic network. "In this sense, results show that the increasing in the number of direct interactions leads to the increasing of the interacting species' fitness. However, there is a limit beyond which it tends to stabilize. This is marked by the effects of indirect interactions", points Alfredo Valido, CSIC researcher at the Institute of Natural Products and Agrobiology.

To a certain extent, indirect interactions would be "slowing down" the adaptation of species to their mutualistic agents. "This very novel result points to the importance of indirect interactions in the functioning of ecosystems. It becomes very evident when we analyze the impact of the introduction of invasive species in mutualistic networks, as in the case of domestic bees," says Pedro Jordano.

The average biological fitness of a species, essential for its evolution, depends not only on who it interacts with, but also on other species that do not interact directly with, creating a conflict of selective pressures. The researchers could also identify which positions within the network are favored and which suffer more negative effects. According to the results, species in peripheral positions within the network, the ones having less interactions, receive more indirect effects and have lower fitness than core species, that would benefit from many direct interactions.

The case of the honeybee

One of the examples studied was the impact of the presence of honeybees, encouraged by apicultural activity, on the diversity of native pollinators and their mutualistic interactions with plants. The honey bee (Apis mellifera, Apidae) is a species native to Eurasia and Africa, but has been introduced to practically the entire planet for honey production and pollination of certain crops. It is considered a super-generalist pollinator, visiting many plant species. It competes with other native pollinators for floral resources (nectar and pollen) and eventually displaces them, producing a homogenization of mutualistic networks. In addition, honeybees are known to increase pollen transfer within the individual plant itself, which ultimately affects fruit and seed production. "In the study published in Nature, we wondered how this anthropogenic activity could be reorganizing the direct and indirect interactions in the mutualistic networks and altering the fitness of the participating species," says Alfredo Valido.

To find this out, the researchers first analyzed, using analytical simulations, the absence of honeybees in a total of 73 mutualistic networks spread across the planet and characterized by the massive presence of honeybees. The idea was to compare the magnitude of direct and indirect interactions both in their presence and absence. "The results obtained are surprising," says Pedro Jordano. "Since honeybees integrate quite well in mutualistic networks, they increase the direct interactions in the network - in theory, there is one species more in the community - but significantly decrease the fitness of the species that interact indirectly with them."

This means that, with the introduction of honeybees, the magnitude of the indirect effects on the mutualistic networks increases, and as we have seen previously, the average fitness of the species is reduced. "This result is even more striking if we take into account that when honeybees invade a natural area, the resulting mutualistic network is characterized by a lower number of native pollinator species, as they are displaced, and also by a lower number of interactions, because the native species remaining reduce their interactions with the plants," says Alfredo Valido.

To understand in detail the implications of this fact, the team used data from an experimental field study conducted in the Teide National Park (Tenerife) where, each spring, up to 2700 hives are introduced. These experimental data have been used in analytical models that have compared the magnitude of change in direct and indirect interactions and their implications on biological fitness in a more realistic scenario, in the absence and presence of honeybees (before and after the installation of the hives). "The results obtained were even more solid and conclusive," Alfredo Valido points out. "The fitness of sixty-eight percent of the native species was reduced in the presence of honeybees. This effect was very clear, as honeybees not only increase indirect interactions, but actually decrease direct interactions as well."

The results of this work show new research lines in the coevolution process between species in high-diverse ecosystems and evidence the importance of indirect interactions. They also warn about the vulnerability of natural ecosystems to the loss of species and interactions due to the introduction of invasive species, with immediate measurable implications on biological fitness of species by rearranging direct and indirect interactions within the mutualistic network.

Reference:

Leandro G. Cosmo, Ana Paula A. Assis, Marcus A. Aguiar, Mathias M. Pires, Alfredo Valido, Pedro Jordano, John N. Thompson, Jordi Bascompte & Paulo R. Guimaraes Jr. (2023). Indirect effects shape species fitness in coevolved mutualistic networks. Nature. DOI: https://doi.org/10.1038/s41586-023-06319-7

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