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).