Decadal legacies in community assembly in response to single seed and soil biota introductions
Earth’s ecosystems are not in equilibrium. Not only because of the continuous stream of human-induced disturbances, but importantly also due to the dynamic nature of ecological processes. Both human interventions and natural events can have long-lasting effects on the composition of plant and soil communities: i.e. historical legacies. There are several well-documented examples (e.g. Terra preta de Índio, Sami reindeer herding grounds) where prolonged human management has led to centuries-old legacy effects on the composition and productivity of natural vegetation through altered soil abiotic and biotic conditions. This suggests that if we can create the right legacies this can be a powerful tool for the long-term management of ecosystems.
Plants and their soil biota constantly interact in myriad ways. We know from greenhouse and field experiments that plants not only shape the composition of their soil communities, but that soil communities in turn determine plant fitness and community composition – i.e. plant-soil feedbacks. The interplay between plants and soil biota drives succession within a given abiotic context. In addition, the soil community can determine the direction in which the plant community develops. Nevertheless, our understanding so far is based on short-term experiments and mathematical models are used to project the long-term consequences.
So the big open question is how long do biotic legacies persist in real ecosystems?
Field experiment showing in front a row of 2x2 m plots used in the experiment.
Wim van der Putten (rightmost person) explaining the concepts behind the field experiment back in the good old days.
Field experiment
Way back when I had not yet started high school, my future PhD-adviser Wim van der Putten and colleagues, Simon Mortimer, Gerard Korthals and others, sat in a room in Heteren, the Netherlands, and decided it was time for a field experiment. A real test of above- and belowground community assembly and how altered biotic composition can reshape succession.
On an arable field that had just been taken out of agricultural production and reserved for nature they laid out plots. On the plots they either sowed fifteen species of mid-succession plant species, or they introduced small amounts of topsoil from a nearby ex-arable field in a mid-successional stage. The design was completed with a treatment where sowing and soil inoculation were combined and a ‘do-nothing’ control. This all happened in 1996, and since then every year researchers went back to the experiment. Every year they inventoried all vascular plants and took soil cores to determine nematode community composition. Nematodes form a central component of the soil food web and as such reflect changes in overall soil community composition.
Decadal legacies
After twenty years of data collection we sat down to rigorously analyse the data from this long-term experiment. We found that seed sowing had the strongest effect on plants, while soil inoculation had the strongest effect on nematode community composition. Both nematode and plant communities were undergoing ongoing successional changes, but due to the biotic introductions, the successional trajectories remained distinct over two decades. This was most pronounced for the treatment where sowing and soil inoculation were combined compared to the ‘do nothing’ control.
The plant species composition changed immediately in response to sowing, while the belowground nematode community took seven years to show the largest separation in terms of taxonomic composition. Such a belowground time lag has been consistently observed in previous field experiments and indicates this may be a general phenomenon. This suggests that competitive and predator-prey interactions belowground take several years to lead to consistent species sorting in response to new environmental conditions. The smaller body sizes, dispersal rates, heterogeneous soil environment and the long lasting resting stages of many soil-borne organisms may all play a role in the different response rates we found above- and belowground respectively.
Finally, we found that over the twenty years the plant and soil nematode community composition became increasingly tightly correlated. While the evidence is indirect, together with experimental evidence of plant-soil feedbacks driving succession, this suggests that the initial differences in biotic composition induced by our one-time introductions put the coupled plant-nematode communities on alternative successional trajectories. Over time, the reciprocal plant-soil feedbacks lead to consistent species sorting in the different treatments.
The future of legacies
In conclusion, our study shows for the first time that even a single introduction of plants and soil biota can lead to long-term legacies in above-belowground community assembly. This suggests that if we can find the right mix of species to introduce we can restore natural species composition long-term with limited effort, if the abiotic conditions are in order.
Open questions are now how long these legacies will still persist and to what extent the community assembly trajectories can be altered by outside influences. Interestingly the field experiment was always open to colonisations from outside for both plants and soil biota. The fact that we found consistent treatment effects over such a prolonged time period suggests that their influence is minimal. In addition, the reciprocal feedbacks among plants and soil biota can in theory prolong the existence of the historical legacies for much beyond the two decades that we document so far.
E. R. Jasper Wubs, Wim H. van der Putten, Simon R. Mortimer, Gerard W. Korthals, Henk Duyts, Roel Wagenaar and T. Martijn Bezemer. 2019. Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly. Ecology Letters doi: 10.1111/ele.13271