Plant attributes interact with fungal pathogens and nitrogen addition to drive soil enzymatic activities and their temporal variation

Nwe, Thu Zar; Maaroufi, Nadia I.; Allan, Eric; Soliveres, Santiago; Kempel, Anne (2023). Plant attributes interact with fungal pathogens and nitrogen addition to drive soil enzymatic activities and their temporal variation. Functional ecology, 37(3), pp. 564-575. Wiley 10.1111/1365-2435.14280

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Nitrogen enrichment can alter soil communities and their functioning directly, via changes in nutrient availability and stoichiometry, or indirectly, by changing plant communities or the abundance of consumers. However, most studies have only focused on one of these potential drivers and we know little about the relative importance of the different mechanisms (changes in nutrient availability, in plant diversity or functional composition or in consumer abundance) by which nitrogen enrichment affects soil functioning. In addition, soil functions could vary dramatically between seasons; however, they are typically measured only once during the peak growing season. We therefore know little about the drivers of intra-annual stability in soil functioning.
In this study, we measured activities of β-glucosidase and acid phosphatase, two extracellular enzymes that indicate soil functioning. We did so in a large grassland experiment which tested the effects, and relative importance, of nitrogen enrichment, plant functional composition and diversity, and foliar pathogen presence (controlled by fungicide) on soil functioning. We measured the activity of the two enzymes across seasons and years to assess the stability and temporal dynamics of soil functioning.
Overall β-glucosidase activity was slightly increased by nitrogen enrichment over time but did not respond to the other experimental treatments. Conversely, plant functional diversity and interactions between plant attributes and fungicide application were important drivers of mean acid phosphatase activity. The temporal stability of both soil enzymes was differently affected by two facets of plant diversity: species richness increased temporal stability and functional diversity decreased it; however, these effects were dampened when nitrogen and fungicide were added.
The fungicide effects on soil enzyme activities suggest that foliar pathogens can also affect below-ground processes and the interacting effect of fungicide and plant diversity suggests that these plant enemies can modulate the relationship between plant diversity and ecosystem functioning. The contrasting effects of our treatments on the mean versus stability of soil enzyme activities clearly show the need to consider temporal dynamics in below-ground processes, to better understand the responses of soil microbes to environmental changes such as nutrient enrichment.
Since the 1960s, nitrogen pollution has increased due to widespread fertilizer use and nitrogen deposition from polluted air. Nitrogen can affect soil health directly because soil organisms respond to the increased nutrient levels. Or nitrogen can indirectly alter soils, via changes in plant communities or in the abundance of plant enemies, such as fungi that attack plant leaves. However, most studies have only focused on one of these factors and we do not know much about their relative importance in determining soil health. Further, although the activity of soil organisms could vary dramatically between seasons, it is typically measured only once, during the peak plant growing season.

We conducted a large grassland experiment where we manipulated plant species richness (1 to 20 species), and plant functional composition (fast- and slow-growing species) together with nitrogen and fungicide application. We investigated the effects of these treatments on the annual average levels of two soil enzyme activities and on their variation over time. The two soil enzymes are proteins produced by soil microbes or plant roots, and are able to decompose and recycle soil nutrients, in this case carbon and phosphorus. We therefore used these two enzymes as a measure of organic matter decomposition and soil functioning.

The soil community and its functioning was driven by multiple factors in the PaNDiv grassland experiment, Münchenbuchsee, near Bern, Switzerland (credit: Dr. Hugo Vincent)
Our results show that the ability of the soil to recycle carbon slightly increased with nitrogen enrichment over time but did not respond to the other treatments. Conversely, interactions between plant communities and fungicide application were the main drivers of the release of phosphorus in the soil.

Our unique experiment was able to i) show the importance of foliar fungal pathogens for soil functioning, ii) highlight the role these plant enemies can play in modulating the relationship between plant diversity and ecosystem functioning, and iii) show extensive seasonal variation in soil processes. Our study is a step towards better understanding the myriad ways in which nitrogen pollution alters soil health, which is crucial to predict the responses of ecosystems to ongoing global change.

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