Effects on mass specific fluxes via changes in plant community
Our results reveal the complex nature of the relationship between the plant community, heterotroph foodweb and ecosystem carbon fluxes. Plant community compositional change in response to heterotroph removal treatments influenced grassland carbon fluxes via changes in community-wide plant nitrogen content. In concordance with and previously reported patterns at organ and plant scale (Reich et al. 1997; Reich et al. 2006; Reich et al. 2008), we found a positive correlation between community wide mass-specific plant nitrogen and ecosystem carbon flux rates. In the presence of heterotrophs, C4 grasses, which have traits characterizing ‘slow’ plant economics (Wright et al. 2004) e.g., low tissue N content and greater root biomass, dominated plant mixtures. As a result, community belowground biomass increased and community wide foliar N content decreased as relative abundance of C4 plants increased. In turn, these led to lower mass-specific rates of ecosystem CO2 uptake and respiration (Tjoelker et al. 2005). However, in the absence of foliar or soil fungi, the relative cover of C4 grasses declined while that of leguminous forbs increased, supporting previous observations that pathogens suppress legumes (Allan et al. 2010; Borer et al. 2015; Seabloom et al. 2018) and promote slow growing species (Cappelli et al. 2020). The increase in legumes and decrease in C4 abundance increased community N content and thus mass specific flux rates. Thus, the effects of foliar and soil fungi on plant community composition scaled up to influence ecosystem carbon fluxes.
Changes in the composition of the plant community and community wide foliar N content were not sufficient to explain patterns observed here. For example, removal of foliar fungi caused the greatest increase in leguminous forbs and decrease in C4 grasses in the high diversity plots (Seabloom et al. 2018), yet increased mass specific carbon fluxes most strongly in low diversity communities. Further, although bivariate analyses showed that mass-specific flux rates increased as community N content increased, path analysis suggested that this is not an important mechanism underlying the effects of plant diversity and heterotrophs on carbon fluxes. This is supported by our findings that the relationship between N content and flux rates, and the decline in N content with belowground biomass were both weakened by the removal of heterotrophs. Together, these results suggest that heterotrophs may alter the scaling of carbon exchange rates with plant nitrogen content (Reich et al. 1997; Wright et al. 2004; Reich et al. 2006). Some of this divergence might be reconciled by previously reported intraspecific responses to treatments. Specifically, foliar N content of four abundant species decreased and increased in response to removal of foliar fungi and arthropods, respectively, from low diversity plots (Borer et al. 2015), likely counteracting some of the effects of changes in plant community composition on community-wide foliar N content. It is also possible that in the absence of heterotrophs, more N became available for plant (rather than heterotroph) function (Strengbom et al. 2002; El-Hajj et al. 2004), leading to an increase in carbon flux despite a decline in foliar N. These findings pave the way for further research into how consumers alter fundamental relationships between plant traits and functioning. Our findings emphasize the importance of incorporating plant-consumer interactions to link organ- and individual-scale patterns (such as flux-N content relationship) to whole communities and ecosystems (Schmitz 2010).
Manipulating multiple heterotrophs independently and simultaneously in the same study allowed us to compare their relative and joint effects on carbon fluxes. Firstly, we found that foliar fungi had large direct and indirect effects on ecosystem carbon fluxes, while soil fungi indirectly influenced mass-specific fluxes by reducing legumes and increasing C4 grasses, whereas arthropods had no direct or indirect effects on carbon fluxes. Neither soil fungi nor arthropods influenced plant biomass in our study, unlike previous studies that have shown significant effects of these heterotrophs on plant biomass, and diversity-production relationship (e.g., Schnitzer et al. 2010; Maron et al. 2011; Seabloom et al. 2017), partly explaining the lack of any effect on carbon fluxes. Our results highlight a potential critical role of foliar fungi in driving ecosystem functions compared with the well-studied effects of herbivores and soil fungi. In addition, our findings demonstrate that foodweb and plant community context mediate the response of carbon fluxes to removal of foliar fungi. Foliar fungi influenced carbon fluxes only when arthropods and soil fungi were present; when all three heterotroph groups were removed together, there was no significant effect on carbon fluxes even though arthropods or soil fungi did not independently alter carbon flux. The divergent effects of heterotrophs on plant community, and on intraspecific foliar N content can partly explain this finding. Specifically, while foliar fungi suppressed legumes and favored C4 grasses, arthropods had the opposite (although statistically insignificant) effect. Further, independent removal of foliar fungi and arthropods induces opposite effects on intraspecific foliar N content, which balance out when these are removed together (Borer et al. 2015). The presence of herbivores can also influence the severity of fungal infection in plants (Clay, Holah & Rudgers 2005), potentially explaining why foliar fungi affected carbon fluxes only in the presence of other heterotrophs.
To reemphasize, we found that the effects of foliar fungi on carbon fluxes varied with the plant community and heterotroph foodweb context. Together, these findings demonstrate that the effects of biotic interactions, especially plant-pathogen interactions, on ecosystem processes such as carbon flux, are not easily predicted by species-specific and leaf-scale studies. Thus, long-term experiments such as the one in this study, that manipulate multiple biotic variables, are invaluable for revealing the complexity of ecosystems.