Introduction
Plant production, or the carbon fixed by primary producers, is the
energetic base of all food webs and also serves to regulate global
climate (Beer et al. 2010). In terrestrial systems, plant diversity and
plant-consumer interactions can have strong impacts on plant production
when measured as plant biomass (Gastine et al 2003; O’Connor et al.
2017; Seabloom et al. 2017). However, ecosystems with similar plant
biomass or the standing stock of carbon in plant tissue at the end of
season may differ in ecosystem carbon flux rates. Understanding the
effects of biotic interactions on changes in instantaneous carbon flux
rates will improve our understanding of the structure of ecosystems
(e.g., biomass distribution across trophic levels, energy fluxes between
organisms), help further integrate community ecology within ecosystem
ecology, and will lay the groundwork to incorporate biological
interactions in the next generation of global carbon models.
Human-mediated global changes are leading to an unprecedented decline in
biodiversity across the tree of life and a reorganization of foodwebs
that will likely have significant effects on ecosystem function (Naeem
et al. 1994; McGrady-Steed et al. 1997; Barnosky et al. 2011; Dirzo et
al. 2014; McCauley et al. 2015; Young et al. 2016; Seabloom et al. 2017;
Rosenberg et al. 2019). While the effects of changes in plant diversity
on plant biomass and production have been well documented (Gastine et al
2003; O’Connor et al. 2017), few studies have examined the direct
effects of plant diversity on instantaneous carbon flux rates (Stocker
et al. 1999; Wilsey & Polley 2004; Milcu et al. 2014). Fewer still have
examined the effects of plant-heterotroph interactions on ecosystem
carbon fluxes (e.g., Naeem et al. 1995; Strickland et al. 2013). Yet,
direct measurements of instantaneous carbon fluxes in response to
altered plant diversity and heterotroph community composition will
clarify the role of plant diversity and heterotroph groups in altering
carbon flux rates. The effects of plant-heterotroph interactions on
ecosystem fluxes can also reveal the role of plant diversity in
supporting consumer foodwebs, an important question given the growing
concern about changes in diversity and abundances of heterotrophs (Dirzo
et al. 2014; Ceballos et al. 2017) such as dramatic decline in
terrestrial arthropods (Hallmann et al. 2017; Loboda et al. 2018;
Seibold et al. 2019; van Klink et al. 2020) and the interactive effects
of reduced plant diversity, nutrient deposition and climatic changes on
the occurrence and spread of plant diseases (Mitchell et al. 2002;
Strengbom et al. 2002; Anderson et al. 2004; Garrett et al. 2006).
Plant diversity can influence instantaneous ecosystem carbon fluxes via
its effects on plant biomass (Stocker et al. 1999; O’Connor et al. 2017)
or on mass specific flux rates (Fig. 1). For example, plant nitrogen (N)
content, which strongly predicts mass-specific, leaf-scale
photosynthesis and respiration rates (Reich et al. 1997; Reich et al.
2006), can change in response to plant diversity (Guiz et al. 2016,
2018). These changes can arise both at the species scale due to an
intraspecific change in nitrogen content (Borer et al. 2015; Guiz et al.
2018), and community-wide due to changes in the relative abundance of
plant species that differ in their photosynthetic or respiration rates,
because of their photosynthetic pathway (e.g., C3 vs. C4) or tissue
nutrient concentration (e.g., %N difference between leguminous forbs
and grasses) (Guiz et al. 2016).
Plants exist in a milieu of heterotrophs including consumers, mutualists
and pathogens, all of which can rely on and can influence ecosystem
carbon fluxes via their effects on plant biomass or on mass-specific
flux rates (Fig. 1). Consumption by herbivores or infection fungal
pathogens can reduce both aboveground and belowground plant biomass
(Mitchell 2002; Seabloom et al. 2017) and alter the plant
diversity-productivity relationship (Eisenhauer et al. 2012; Seabloom et
al. 2017; Wang et al. 2019), directly affecting the amount of carbon
fixed and respired. Further, heterotrophs affect the nutrient and water
availability to and acquisition by plants, which can affect the
instantaneous rates of photosynthesis and respiration. For example,
mycorrhizal fungi can increase acquisition of phosphorous and water
(Bolan 1991; Smith & Read 2008), and herbivores and detritivores can
impact nitrogen mineralization in soil (Hobbie and Villéger 2015) and
water transport in plant tissue (Nabity et al. 2009). Finally, plants
also respond to disease and defoliation by a direct down-regulation of
photosynthesis (Mitchell 2003; Bilgin et al. 2010). Like plant-plant
interactions, plant-herbivore and plant-fungal interactions also
influence plant nitrogen content at the species and community scale
(Pastor et al. 1993; Pastor & Cohen 1997; Ritchie et al. 1998; Borer et
al. 2015), potentially driving changes in ecosystem carbon fluxes (Reich
et al. 1997).
Here, we report changes in the instantaneous fluxes of
CO2 in experimental prairie communities with varying
plant species richness (1, 4 or 16 plant species, Tilman et al. 1996)
from which heterotroph groups (arthropods, foliar fungi and soil fungi)
were experimentally removed either singly or all together (Borer et al.
2015). We partitioned CO2 flux into uptake via gross
primary production (GPP), respiration at the whole-plot scale, or
ecosystem respiration (Re), and their difference, the
net ecosystem exchange (NEE) (Lasslop et al. 2010). We examined the
effects of plant diversity and foodweb manipulation on total plot scale
fluxes and fluxes per unit plant biomass to tease apart biomass driven
effects from effects on mass-specific flux rates. To further understand
how ecosystem carbon fluxes are affected by biotic interactions, we
examined mass specific flux rates in relation to the composition and
foliar nitrogen content of the plant community.
We generated a priori hypotheses based on existing literature
where possible:
(H1) Total GPP and Re will increase with plant
diversity; the overall effect of NEE will depend on the relative changes
in GPP and Re . Previous research suggests that high
diversity plots accumulate more biomass (O’Connor et al. 2017) which
results in increased soil carbon (e.g., Yang et al. 2019), we expected
GPP to increase more than Re with increasing plant
diversity.
(H2) Heterotroph removal will lead to an increase in total GPP and
Re . As plant communities accumulate more above and
belowground biomass when heterotrophs are removed (Maron et al. 2011;
Seabloom et al. 2017), we expected an overall increase in NEE.
(H3) Removal of foliar fungi and arthropods will lead to an
increase in mass-specific GPP and reduction in Re . Both
pathogens and herbivores have been shown to increase plant respiration
rate and suppress photosynthetic rate (Mitchell 2003; Lambers et al.
2008; Nabity et al. 2009; Bilgin et al. 2010; Strickland et al. 2013).
(H4) The effects of heterotroph removal on carbon fluxes will
depend on the plant community (e.g., species richness, foliar
chemistry) . Previous research has shown that the intensity of herbivory
and pathogen infection vary with host community (e.g., species richness,
relative abundance of host, Mitchell et al. 2002). Further, previous
studies have also shown that the plant and heterotroph communities
interactively influence plant chemistry (Borer et al. 2015).