How plant communities change when conquering uninhabited ground

Some plants are able to take over uninhabited spaces like sand dunes, volcanic substrates and rockfall areas. The first colonizers have specific traits that allow them to grow in such hostile environments. Other plants lack such traits but will soon follow these pioneers. Ricardo Martínez-García from the Center for Advanced Systems Understanding (CASUS), an institute of the Helmholtz-Zentrum Dresden-Rossendorf (HZDR), and collaborators from Spain and Brazil investigated the type of interaction between different species on these newly conquered grounds with the help of a mathematical model based on existing root physiology knowledge. Their new model connects the type of species interaction with the general availability of a scarce soil resource. It also reveals the best strategy for the pioneer who can harness a resource that is not freely available.

Plants interact in many different ways and very often we see that one individual is supporting another from a different species. The term experts use for that is facilitation. With symbiotic facilitation, both plants support each other. With commensalistic facilitation, the nurtured plant neither affects its benefactor positively nor negatively. The third type of facilitation is called antagonistic facilitation. Here, the nurtured partner benefits at the expense of the benefactor. The latter, for example, leaves a self-produced resource to the partner, even though he could actually use it himself. The benefactor appears to “accept” this situation: Neither a kind of defensive reaction against the removal of resources nor a complete halt to production can be observed.

“There is an ongoing debate about whether antagonistic facilitation actually exists. Our study provides a clear result: this type of interaction between plant species could occur in nature,” says Dr. Ricardo Martínez-García, CASUS Young Investigator and corresponding author of the study that will be published in the second October issue of the journal New Phytologist. “To prove antagonistic facilitation experimentally, requires a big effort. To begin with, it must be ruled out that this type of interaction is neither symbiotic nor commensalistic facilitation. In addition, it has to be shown that it is not a classic competition where both plants are harming each other in the fight for resources.”

Plants as miners

Martínez-García as well as Ciro Cabal (King Juan Carlos University, Madrid, Spain) and Gabriel A. Maciel (South American Institute for Fundamental Research, São Paulo, Brazil), the two lead authors of the study, focused with their modelling efforts on an example from nature where the existence of antagonistic facilitation had been suspected for a long time: pioneering plants starting to grow on uninhabited ground and other plants soon following track. Such pioneer plants can engineer their environment to increase the availability of certain scarce soil resources like nitrogen and phosphorus. Their abilities certainly help them thrive and they do not seem to be bothered by appearing opportunistic plants helping themselves at the buffet. The bottom line is that the pioneer still benefits from its special traits. From an experimental point of view, the pioneer plant example appears to be a manageable system. Nevertheless, practitioners have not yet been able to determine the type of interaction for this example with certainty. The results of the model presented here are now a strong argument for the existence of antagonistic facilitation in these pioneer areas. Of course, it stands to reason that this type of interaction probably exists not only here, but also elsewhere in nature.

“Our model also shows that plant interactions are an emergent property of resource availability,” adds Cabal. “It turned out that in environments with low and intermediate resource availability antagonistic facilitation is the best strategy. This too was suggested some time ago but it was so far not backed by either experimental data or theoretical models.” Consequently, the research team was not only able to provide reliable results for the general existence of this type of interaction. In fact, antagonistic facilitation is even the optimal interaction between two plant communities under some environmental conditions.

As over time the soil changes and more and more plant species flourish, the interaction between the species changes. Although the pioneer species continue to increase the availability of resources, this no longer affects the other plants due to the generally good resource situation. The phase of antagonistic facilitation is over and all plants compete against each other. Further into the future, the mining capability of the pioneer will even become a burden in this competition. The pioneers are at a disadvantage. In the end, other plant species prevail in the competition and pioneer plants are no longer to be found on the site.

How root modeling helps to explain ecological patterns

Modeling is an important tool in ecology, because it allows to test hypotheses and explore ideas that are hard to investigate in field or laboratory experiments. In these cases, computational simulations can help understanding ecological dynamics and patterns and even guide the design of field and lab experiments. In a 2020 Science paper Cabal, Martínez-García and others presented a mathematical model that predicts the density and spatial distribution of roots of interacting plants. A comparison with greenhouse experiments showed great overlap with the model’s prediction.

For the New Phytologist study, the 2020 root model has been extended and refined to represent the interaction of pioneer plants with their environment as well as with other plants. Among others, the model takes into account the dynamics of an in-demand soil resource (input, decay, availability for the plants, mining trait of the pioneer plants), the size and shape of the plants’ root systems and the costs of growing and maintaining roots, mining the resource as well as transporting it within the plants.

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