Nematodes driving the fate of carbon under climate change

Fig. 1. Multiple experimental microcosms with blue grama seedlings.

I was among a group of soil ecologists from Colorado State University who collaborated with plant ecologists from Arizona State University to investigate belowground controls on plant responses to drought. Droughts are becoming more frequent, severe, and longer lasting than in recent decades in many places. Ecological theory suggests that certain plant species may respond to drought by producing fewer leaves because leaves lose water through transpiration, and instead allocate more production to roots, which capture water. These patterns are important in the context of ecosystem responses to climate change because they set limits on ecosystem carbon assimilation and biomass production.

Plants interact with many other organisms in ecosystems, and the response of those to drought may also affect plant responses. Our previous multi-site grassland field study revealed that more frequent extreme droughts can increase populations of root-feeding soil nematodes (roundworms) in sub-humid grasslands by suppressing their predators. These root parasites limit plant biomass production in grasslands, and their increased abundance under drought led us to ask whether high levels of root herbivory by nematodes would prevent the high biomass allocation to roots by grasses expected in response to drought.

In order to find out, we set up a greenhouse experiment in which we exposed a dominant shortgrass steppe species, blue grama (Bouteloua gracilis), to extreme low and high amounts of water under a variable amount of root feeders (Fig. 1). We added root-feeding nematodes to increase their abundance in soil microcosms from 35% (that found in native shortgrass communities) to ≈ 50% (that found in field plots under extreme drought) relative to the total nematode abundance. We tested whether high levels of root herbivory by nematodes would prevent the high grass biomass allocation to roots normally expected in response to drought. After 12 weeks, the results showed that the effects of dry conditions on grass biomass allocation depends on the abundance of root-feeding nematodes. High abundance of those nematodes impeded grass responses that otherwise allocated relatively more biomass to roots than leaves under drought conditions to benefit water uptake (Fig. 2). This indicated that when the root-feeding nematodes thrive, they undermine an important plant mechanism that buffers grasses and ecosystems against the effects of drought.

The findings presented in our paper challenge current predictions of increasing plant biomass allocation belowground in water-stressed grasslands, and can be of special interest to ecosystem modelers. Terrestrial biosphere models still have a low capacity in reproducing the magnitude of vegetation responses to temporal changes in annual rainfall at a given ecosystem. Our findings support the idea that including soil biota parameters (specifically those related to belowground primary consumers) will enhance the predictive capacity when modelling vegetation responses to drought. Accurately modelling vegetation responses to changes in rainfall is crucial to predicting water and carbon cycling rates into the future, and to providing solid scientific guidance to grassland land managers.

Fig. 2.Response of the fraction of total plant biomass allocated below- ground (fBNPP) to water treatments and soil-fauna manipulations (Franco et al., 2020).

It should be noted that the hypotheses presented in this study were tested using a single grass species (B. gracilis) and under controlled greenhouse conditions. While these controlled conditions allowed us to test mechanistic hypotheses and evaluate cause-effect relationships by manipulating only a few variables, they obviously miss the complexity existing in the field. Therefore, we call for caution in extrapolating our results to grassland ecosystems, as field experiments are likely to reveal scale- and ecosystem-dependent patterns that are not testable in a greenhouse setting. This being said, B. gracilis accounts for most of the net primary productivity in the shortgrass steppe of the central and southern Great Plains, and our use of native nematode species (and quantities) and soils from that ecosystem provide a certain degree of ecological realism.

Our next step is to investigate this nematode control on plant responses to drought in field plots in different grassland sites (arid to mesic). We have already completed field experiments in this regard, and are currently processing the dataset. We expect that the importance of nematode control of biomass allocation will be greater in mesic compared to arid environments where root-feeder populations seem to be primarily regulated by resource availability rather than predation pressure. Another emergent question is how this phenomenon affects carbon fixation in grassland soils, given that root inputs contribute more to soil organic matter than aboveground litter.

Publication: Franco, ALC; Gherardi, LA; de Tomasel, CM; Andriuzzi, WS; Ankrom, KE; Bach, EM; Guan, P; Sala, OE; Wall, DH (2020) Root herbivory controls the effects of precipitation on the partitioning between above-belowground grass biomass. Functional Ecology. In Press. doi: 10.1111/1365-2435.13661

dr. andre franco