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.