Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts

Abstract

1. Species interactions may couple the resource dynamics of different primary producers and may enhance productivity by reducing loss from the system. In low-resource systems, this biotic control may be especially important for maintaining productivity. In drylands, the activities of vascular plants and biological soil crusts can be decoupled in space because biocrusts grow on the soil surface but plant roots are underground, and decoupled in time due to biocrusts activating with smaller precipitation events than plants. Soil fungi are hypothesized to functionally couple the plants and biocrusts by transporting nutrients. We studied whether disrupting fungi between biocrusts and plants reduces nitrogen transfer and retention and decreases primary production as predicted by the fungal loop hypothesis. Additionally, we compared varying precipitation regimes that can drive different timing and depth of biological activities.2. We used field mesocosms in which the potential for fungal connections between biocrusts and roots remained intact or were impeded by mesh. We imposed a precipitation regime of small, frequent or large, infrequent rain events. We used 15 N to track fungal-mediated nitrogen (N) transfer. We quantified microbial carbon use efficiency and plant and biocrust production and N content. Fungal connections with biocrusts benefitted plant biomass and nutrient retentionunder favourable (large, infrequent) precipitation regimes but not under stressful (small, frequent) regimes, demonstrating context dependency in the fungal loop.Translocation of a 15 N tracer from biocrusts to roots was marginally lower when fungal connections were impeded than intact. Under large, infrequent rains, when fungal connections were intact, the C:N of leaves converged towards the C:N of biocrusts, suggesting higher N retention in the plant, and plant above-ground biomass was greater relative to the fungal connections-impeded treatment. Carbon use efficiency in both biocrust and rooting zone soil was less C-limited when connections were intact than impeded, again only in the large, infrequent precipitation regime. Synthesis.Although we did not find evidence of a reciprocal transfer of C and N between plants and biocrusts, plant production was benefited by fungal connections with biocrusts under favourable conditions. | 895 Journal of Ecology DETTWEILER-ROBINSON ET aL. | 901 Journal of Ecology DETTWEILER-ROBINSON ET aL. | 907 Journal of Ecology DETTWEILER-ROBINSON ET aL. and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Applied and Environmental Microbiology, 70(2), 973-983. https ://doi.Additional supporting information may be found online in the Supporting Information section. How to cite this article: Dettweiler-Robinson E, Sinsabaugh RL, Rudgers JA. Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts. J Ecol. 2020;108:894-907. https ://doi.

Evidence for a fungal loop in shrublands

“…Similar to the lack of translocation from plants to biocrusts observed in our study, Dettweiler‐Robinson et al. (2020) found that some North American grasses benefitted from a fungal loop connection to cyanobacterial biocrusts, while this relationship had neutral to negative effects on the biocrust communities depending on precipitation regime. Considering that C movement from grasses to cyanobacterial biocrusts has been shown to occur (Green et al., 2008), our results suggest that the drivers for or mechanisms involving C exchange in previous studies were not present in this shrubland system or under these moisture conditions.…”

“…Given that our study limited precipitation to 2.5 mm to simulate a common rain event for the season, it is likely that this rainfall event was not suitable to fully reinstate metabolic activity in the L. tridentata found in our study plots and therefore led to the lack of bidirectional nutrient exchange in this system. Similar to the lack of translocation from plants to biocrusts observed in our study, Dettweiler-Robinson et al (2020) found that some North American grasses benefitted from a fungal loop connection to cyanobacterial biocrusts, while this relationship had neutral to negative effects on the biocrust communities depending on precipitation regime. Considering that C movement from grasses to cyanobacterial biocrusts has been shown to occur (Green et al, 2008), our results suggest that the drivers for or mechanisms involving C exchange in previous studies were not present in this shrubland system or under these moisture conditions.…”

“…Dryland vascular plants are primarily limited by water (and secondarily N), and in contrast to biocrusts, usually require rainfall events >5 mm to activate metabolism (Collins et al., 2014; Lauenroth & Bradford, 2012). The spatial separation between dryland vascular plant rooting depth and biocrusts, along with the decoupled nature of their metabolic activities in response to rainfall thresholds, suggests that these communities may operate using relatively isolated nutrient pools (Collins et al, 2014; Dettweiler‐Robinson et al., 2020). If present, a fungal loop between biocrusts and vascular plants would enable the retention and exchange of limiting nutrients (such as N and C) that would otherwise be isolated or lost from the system through processes such as volatilization and photodegradation (Adair et al., 2017; Austin & Vivanco, 2006), as well as leaching and erosion (Peterjohn & Schlesinger, 1990; Throop & Archer, 2009).…”

“…Evidence for the existence and functional role of fungal loops in dryland systems derives primarily from studies conducted in grasslands in North America and Asia (Aanderud et al., 2018; Dettweiler‐Robinson et al., 2018, 2019; Green et al., 2008; Hawkes, 2003; Lingfei et al, 2005; Lutgen et al, 2003; Rudgers et al., 2018; Zhuang et al., 2015). These studies have documented the biologically mediated (Collins et al., 2014) movement of the stable isotope 15 N from cyanobacterial biocrusts to nearby grasses and forbs (with one study showing the reciprocal movement of 13 C from grasses to biocrusts; Green et al., 2008), and have found that dark septate fungal endophytes in orders such as Pleosporales and Pezizales routinely dominate the microbial communities in both biocrust and plant tissues (Allen, 2007; Apple, 2010; Barrow, 2003; Bates et al., 2012; Maier et al, 2016; Massimo et al., 2015), as well as the rhizosphere soils and soil interspaces in these experiments (Aanderud et al., 2018; de Mesquita et al, 2018; Green et al., 2008; Porras‐Alfaro & Bayman, 2011; She et al., 2018).…”

“…Considering current literature relating N translocation through dark septate fungal bodies (Collins et al, 2014; de Mesquita et al, 2018; Green et al., 2008; Rudgers et al., 2018; She et al., 2018; Zhuang et al., 2015), the direct role of DSEs in the exchange of nutrients across drylands is likely. In grasslands, the direct or indirect severing of fungal connections has resulted in decreased primary production in vascular plant communities (Dettweiler‐Robinson et al., 2018, 2020), and even changes in plant community composition (reviewed by Zhang et al, 2016), indicating that the presence of fungal networks directly impacted these two phenomena. Evidence suggests the presence of fungal nutrient exchange networks between biocrust and plant communities in grasslands.…”