An international scientific team with the participation of the Higher Council for Scientific Research (CSIC) has revealed in a study that the indirect interactions that occur between species in a mutualistic network between species modulate, just like 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 on their immediate consequences on the biological fitness of these species, that is, on their ability to leave more offspring, in networks that include a high diversity of species. The finding, published in the journal Nature, it is important, for example, to understand why a population grows or shrinks and also how natural selection acts on individuals within a population.
“Species, in general, do not interact with each other individually, but rather within a much more complex network of interactions that includes a multitude of species,” he comments. Peter Jordan, CSIC researcher at the Doñana Biological Station (EBD). One of the most relevant interactions in the functioning of ecosystems are mutualistic interactions, those in which both participants mutually benefit from the interaction, such as the cases of plant pollination 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 the knowledge of how ecosystems work. Under this approach, it is now known that in a given ecosystem both direct effects, mediated by the interacting species, and indirect effects, between species that do not interact, are combined. However, until now its relative importance in the biological effectiveness of individuals, which is technically known as fitness, was unknown. “Thus, 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.
The study has included the participation of researchers from the Doñana Biological Station, the University of Seville and the Institute of Natural Products and Agrobiology (IPNA – CSIC), as well as the University of São Paulo and the State University of Campinas in Brazil, as well as the University of Santa Cruz in California and the University of Zurich in Switzerland.
Indirect interactions also affect biological efficacy
In this new study, novel analytical techniques have been applied to a total of 186 mutualistic networks and it has been detected that both direct and indirect interactions affect the biological efficacy of the species that make up the network of interactions. “In this sense, moreover, it is shown that as the number of direct interactions increases, the fitness of the interacting species increases, but surprisingly there is a limit beyond which it stabilizes. This is marked by the magnitude of the indirect interactions”, points out Alfredo ValidoCSIC researcher at the IPNA.
To a certain extent, indirect interactions would be “slowing down” the adaptation of species to their mutual agents. “This very novel result points to the importance of indirect interactions in the functioning of ecosystems and, furthermore, it becomes very evident when we analyze the impact of the introduction of invasive species in mutualistic networks, as is the case of domestic bees”, Jordano points out.
The average biological fitness of a certain species, essential in its evolution, not only depends on who it interacts with, but also depends on other species that do not directly interact with it, creating a conflict of selective pressures. The scientific team was also able to identify which positions in these interaction networks are favored and which are more negatively influenced. According to the results obtained, the species that are on the periphery of the network, those that have few interactions, would be harmed by the indirect effects, which propagate through the network. Species in the middle, with many direct interactions, would generally benefit.
The case of the domestic bee
One of the examples studied was the impact generated by the presence of domestic bees, fostered by agricultural activity, on the diversity of native pollinators and on their mutualistic interactions with plants. The domestic or honey bee (Apis mellifera, Apidae) is a species native to Eurasia and Africa, but it has been introduced to practically the entire planet to obtain honey and pollinate certain crops. It is considered a super-generalist pollinator, that is, it visits many plant species. It competes with the rest of the native pollinators for floral resources (nectar and pollen) and ends up displacing them, producing a homogenization of mutualistic networks. In addition, it is known that domestic bees increase pollen transfer within the individual plant itself, which ultimately affects fruit and seed production. “In the study we considered to what extent this anthropic activity could be reorganizing the direct and indirect interactions in the mutualistic networks and altering the fitness of the participating species”, says Valido.
To do this, the researchers firstly analysed, using analytical simulations, the absence of domestic bees in a total of 73 mutualistic networks spread all over the planet and characterized by the massive presence of honey bees. The idea was to compare the magnitude of direct and indirect interactions both in their presence and in their absence. “The results obtained are surprising,” says Pedro Jordano. “Since honey bees integrate quite well into mutualistic networks, they increase direct interactions in the network—in theory, there is one more species in the community—but significantly decrease the fitness of species that interact indirectly with them.”
This means that, with the introduction of honey bees, the magnitude of indirect effects in mutualistic networks increases, and as we have seen previously, it would reduce the average fitness of the species. “This result is even more impressive if we take into account that when honey bees invade a natural area, the resulting mutualistic network is characterized by presenting a lower number of native pollinator species, since they are displaced, and also of interactions, because the species still present reduce their interactions with the plants,” says Alfredo Valido.
To find out in detail the implications of this last aspect, the team has used data from an experimental field study carried out in the Teide National Park (Tenerife) where, each spring, up to 2,700 beehives are introduced. These experimental data have been used in the analytical models that have compared the magnitude of the change in the direct and indirect interactions and their implications in the biological efficiency in a more real scenario, in the absence and presence of domestic bees (before and after the installation of the hives). “The results obtained were even more solid and conclusive”, indicates the IPNA researcher. “68% of native species see their fitness reduced in the presence of domestic bees. This effect was very apparent, as honey bees not only increase indirect interactions, but actually decrease direct interactions as well.”
The results of this work show new lines of analysis of the coevolution process between species in ecosystems of high diversity, and show 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 repercussions on the biological efficiency, the fitness of the species by reorganizing both direct and indirect interactions.
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