Biocrust contribution to ecosystem carbon fluxes varies along an elevational gradient EVA DETTWEILER-ROBINSON, MICHELLE NUANEZ, AND MARCY E. LITVAK Department of Biology, MSC03 2020, 1, University of New Mexico, Albuquerque, New Mexico 87131 USA Citation: Dettweiler-Robinson, E., M. Nuanez, and M. E. Litvak. 2018. Biocrust contribution to ecosystem carbon fluxes varies along an elevational gradient. Ecosphere 9(6):e02315. 10.1002/ecs2.2315
Abstract. Understanding how each component of an ecosystem contributes to carbon fluxes across a range of abiotic conditions enables accurate forecasts for future emission scenarios. In drylands, biological soil crust (biocrust) contribution to ecosystem carbon fluxes may vary at a regional scale but is rarely quantified due to the difficulty of parameterizing process-based models or parsing biocrust (on the soil surface) from whole-soil flux measurements. We measured excised biocrust carbon fluxes across current and future predicted warmer summertime temperatures from dryland sites (grassland, shrubland, savanna, and woodland) and compared those to the ecosystem and soil fluxes from eddy flux towers. Overall, biocrust fluxes showed net carbon loss during the warm growing season temperatures, suggesting that cool-season photosynthesis is likely critical for maintaining positive biocrust carbon balance in these sites. Biocrust flux temperature responses differed by site: Grassland and shrubland biocrust gross photosynthesis was relatively invariant, while respiration increased with temperature; in the woodland and savanna, biocrust gross photosynthesis and respiration increased with temperature. Biocrust fluxes contributed 10% of observed soil respiration in grassland and shrubland at 19°C, reinforcing the need to separate biocrust activity from root and subsurface heterotroph activity to understand drivers of fluxes at different sites. Regional resolution of biocrust type and cover will improve predictions of biocrust contribution to global carbon flux with changing temperatures. Key words: biological soil crust; drylands; ecosystem carbon exchange; eddy flux covariance; soil respiration. Received 19 April 2018; accepted 20 April 2018. Corresponding Editor: Debra P. C. Peters. Copyright: © 2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail:
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INTRODUCTION
the growing season, and belowground resources (Raich and Schlesinger 1992, Friedlingstein et al. 2006). Additionally, species and functional group compositions affect the carbon flux responses to abiotic conditions (Chapin 2003, Lavorel 2013) because each taxon may have a different response to abiotic conditions. Quantifying magnitude of contribution of each species or functional group to the ecosystem carbon budget across a range of abiotic conditions will improve estimates of carbon budgets under future community composition or abiotic conditions. Biological soil crusts (biocrusts) are ubiquitous components of dryland biomes, but the
Dryland ecosystems play a dominant role in the global carbon cycle and, specifically, in regulating the inter-annual variability in atmospheric carbon dioxide (Poulter et al. 2014, Ahlstrom et al. 2015). Quantifying the carbon stocks and fluxes in these biomes and determining the processes that regulate them are crucial to understanding the productivity of these systems which cover 45% of the Earth’s terrestrial area (Prǎvǎlie 2016). Ecosystem carbon budgets integrate photosynthesis and respiration processes and are regulated by temperature, moisture, length of ❖ www.esajournals.org
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contribution to ecosystem carbon fluxes across a range of biomes is poorly resolved. Biocrusts are an important group of organisms for understanding carbon fluxes because they consist of primary producers (cyanobacteria, mosses, lichens, algae) and heterotrophs (fungi, bacteria) living in the top ~5 cm of the soil surface, at the intersection of soil processes and the atmosphere. Current estimates suggest that biocrusts are important to resource cycling of drylands (Belnap et al. 2016) and can contribute 1–10 gCm 2yr 1 (Porada et al. 2013) or 1% of the global terrestrial NPP (Elbert et al. 2012: supplement). However, biocrust composition varies among biomes, generally driven by climate (Belnap et al. 2016), and these compositional differences contribute to functional differences in carbon cycling at both local and regional scales. For example, gross photosynthesis by light cyanobacterial biocrust is lower than by dark, complex moss/lichen/cyanobacterial biocrusts (Housman et al. 2006, Grote et al. 2010). Thus, direct measurements across a range of biocrust communities and dryland biomes will improve our ability to estimate local-to-global biocrust contribution to carbon fluxes. Biocrust communities include organisms with different sensitivities to abiotic conditions. Biocrusts have organism-specific optimum temperature ranges for performance (Lange et al. 1998, Su et al. 2012, Tamm et al. 2018), and their respiration generally increases with temperature (Brostoff et al. 2005, Housman et al. 2006, Grote et al. 2010). Given that temperatures are rising in the western United States (Gutzler and Robbins 2010) and globally, with associated effects on evaporative demand and soil moisture (Cook et al. 2014), understanding biocrust carbon flux responses to temperature (Grote et al. 2010, Maestre et al. 2013) will enable more accurate predictions of dryland carbon dynamics under future climate conditions. In this study, we quantified (1) mixed autotrophic and heterotrophic biocrust communities flux sensitivity to current and predicted future warmer summer temperatures across four dryland sites across an elevation gradient in central New Mexico, in order to (2) predict the magnitude of biocrust contribution to ecosystem and shallow soil respiration flux in each site. We focused on the summer months when the sites ❖ www.esajournals.org
are consistent carbon sinks (Petrie et al. 2016) indicating the highest net overall uptake. We hypothesized that net carbon fluxes from biocrusts in all of our sites would increase with temperature as respiration increases (Brostoff et al. 2005, Housman et al. 2006, Grote et al. 2010). We also expected higher contribution of biocrusts to ecosystem and soil flux in sparsely vegetated grasslands compared to ecosystems with larger woody shrubs or trees. Quantifying biocrust fluxes is limited by the difficulty of disentangling surface-dwelling organisms’ fluxes from fluxes that originate in deeper soil layers using in situ measurements alone (Darrouzet-Nardi et al. 2015, but see use of biocrust-free collars in Wilske et al. 2008). In addition, process-based modeling with multiple domains of organisms is extremely complex (Porada et al. 2013). Here, we use ex situ measurements of biocrust fluxes and relate these to the ecosystem-scale fluxes with regression-based modeling to predict biocrust contributions to ecosystem fluxes across multiple sites.
METHODS Study sites
We measured biocrust fluxes from four sites in the New Mexico Elevation Gradient network (Table 1). The pi~ non–juniper woodland is dominated by pi~ non pine (Pinus edulis [Engelm.]) and one-seed juniper (Juniperus monosperma [(Engelm.) Sarg.]) trees with the C4 bunchgrass blue grama (Bouteloua gracilis [(Willd. ex Kunth) Lag. ex Griffiths]). Biocrusts at the woodland include lichens (Collema spp., Placidium sp.), patches of mosses (Pterygoneurum sp., Bryum sp.), and dark cyanobacterial biocrusts (Nostoc sp., Microcoleus sp.). The juniper savanna consists of open J. monosperma tree canopy with the C4 bunchgrass black grama (Bouteloua eriopoda [(Torr.) Torr.]) dominating the understory. The shrubland is dominated by the shrub creosote (Larrea tridentata [(DC.) Coville]) and B. eriopoda. Both the savanna and shrubland sites have patches of cyanobacterial lichens (Collema spp.) with cyanobacterial biocrusts, generally light biocrusts (Microcoleus sp.) but with patches of visible dark cyanobacterial crusts (Scytonema sp., Nostoc sp.). Vegetation in the grassland is dominated by the C4 bunchgrasses B. eriopoda, B. gracilis, 2
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DETTWEILER-ROBINSON ET AL. Table 1. Geographic data and average abiotic conditions of sites in the New Mexico Elevation Gradient 2007– 2012 (Woodland missing 2007).
Site
Location, County, Lat./Lon.
Woodland
Heritage Land Conservancy, Torrance, 34.4384, 106.2377 Private, Torrance, 34.4255, 105.8615 Sevilleta NWR, Socorro, 34.3349, 106.7442 Sevilleta NWR, Socorro, 34.3623, 106.7019
Savanna Shrubland Grassland
Extent in SW U.S. (9106 ha)
Elevation (m)
MAT (°C)
MST (°C)
TAP (mm)
SP (%)
Texture (NRCS)
pH (NRCS)
16
2126
10.8
18.3
287
60
39% sand, 37% silt
7.4–8.4
2
1926
12.8
20.1
251
67
69% sand, 16% silt
6.6–8.4
85
1605
14.3
22.4
194
61
66% sand, 23% silt
7.9–8.4
39
1596
13.6
22.7
214
63
66% sand, 23% silt
7.9–8.4
Notes: Summer is considered 25 April–2 October. Projection system is WGS84 Web Mercator. Abbreviations are as follows: MAT, mean annual air temperature; MST, mean summer air temperature; TAP, total annual precipitation; SP, percent of precipitation arriving in summer. Texture and pH are from U.S. Natural Resources Conservation Service, USA (Soil Survey Staff, 2017).
for the ~2 weeks prior to measurement; one-third of the samples were stored dry in the dark at room temperature up to ~4 months, while our equipment was under repair; these samples were stored in the window as the ones above for ~2 weeks prior to measurement. Although these less harsh conditions (reduced UV, higher soil moisture availability) may have promoted a shift in species composition (Ayuso et al. 2017), we did not observe visible algal/bacterial films. Chlorophyll content was quantified as a proxy of potential photosynthetic capacity in a subset of the samples (9 samples each from grassland and shrubland, 10 from woodland, and 11 from savanna; one tray of samples was dropped prior to analysis, so sample size differs from total collected). Each sample was ground and passed through a 2-mm mesh, and then, 1 g of each sample was dissolved in 1 mL dimethyl sulfoxide; thus, we were unable to standardize to a per-area basis. Samples were incubated for 72 h in the dark at room temperature (so we captured ~75% of the chlorophyll content; Castle et al. 2011); then, absorbance of 280 lL of supernatant at 665 and 750 nm was recorded on a Synergy H1 Hybrid Multi-Mode Microplate Reader (BioTek U.S., Winooski, Vermont, USA) and chlorophyll a concentration (lg/g soil) was calculated according to Castle et al. (2011). To understand the temperature response of individual photosynthetic taxa, isolated cultures would need to be used. However, this method would overlook the community structure and abiotic context of the soil biocrust system. Future
dropseed (Sporobolus spp. [R. Br.]), James’ galleta (Pleuraphis jamesii [Torr.]), and muhly (Muhlenbergia spp. [Schreb]) with light cyanobacterial biocrusts (Microcoleus sp.). The standing vegetation biomass is highest in the woodland (~50 Mg/ha2) and decreases to the grassland and shrubland (1 h after water addition). To compare biocrust flux and ecosystem flux, we subset eddy flux and soil respiration data to match conditions measured ex situ. We subset data to summer of 2012 (25 April–2 October; day ❖ www.esajournals.org
of year = 115–175) surrounding the times when we collected the biocrust samples. We selected data within the temperature range 18°–30°C and that had soil moisture gravimetric water content >0.095 m/m (the minimum value for field capacity for ex situ samples). We averaged across the 30-min intervals between noon and 16:00 hours when PAR >1000 (NEE and GPP) and midnight and 4:00 hours when PAR = 0 (RE and SR) so that light and temperature were fairly stable.
Analysis All analyses were conducted in R (version 3.3.1; 2016-06-21; R Core Team 2016). Models are described in each section below. Effect of temperature on biocrust carbon fluxes.— We investigated the effect of temperature on observed biocrust flux data. The general linear model included interactions of site and temperature, and for the subset with chlorophyll data, chlorophyll a content was included as a covariate. Quantile–quantile plots and histograms of the standardized residuals were visually inspected to assess that the models adequately met assumptions of homogeneity of variance and normality of residuals. Controls on biocrust contribution to ecosystem and soil carbon fluxes.—To compare mature biocrust fluxes to the ecosystem scale, we scaled the fluxes by the cover of the subjectively selected biocrust types from each site (Sancho et al. 2016). We investigated the effect of temperature on ecosystem fluxes and soil respiration using general linear models with site and temperature, as above. We estimated the contribution of biocrust fluxes to ecosystem fluxes in the observed range of temperatures. High-soil-moisture periods were rare because the region experienced severe drought in 2012, and thus, not all sites have days observed across the entire range of possible temperatures. There were so few days of high soil moisture at the savanna site (n < 7) that we excluded it from analyses. We thus chose temperatures in common across all sites (26°C for gross primary production and 19°C for soil and ecosystem respiration) and then qualitatively compared changes across the available ranges in temperature. Comparing shallow soil respiration data to the magnitude of predicted biocrust respiration also served as a check for the estimates; the 5
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predicted magnitude of flux from ex situ biocrust-only measurements should not exceed the magnitude of fluxes observed in situ in the shallow soil column.
accounted for 1.7% 0.68 SE relative surface cover. The mature biocrusts from the shrubland were dark cyanobacteria with few cyanolichens and accounted for 2.6% 1.3 SE relative cover. Grassland biocrusts were light cyanobacterial biocrusts and accounted for 10.9% 0.93 SE relative cover. We had limited sample size of ecosystem fluxes and soil respiration after subsetting the ecosystem-scale data to match set conditions in the chamber, specifically the high soil moisture requirement >0.095 m/m. The resulting data did not span the entire range of temperatures at all sites because there were seldom daytime conditions with both high soil moisture and low temperatures in the shrubland or grassland sites, or nighttime conditions with high temperatures (Fig. 2). Over the range of conditions observed at the grassland, shrubland, and woodland, only ecosystem respiration significantly responded to temperature (Table 3) where respiration decreased over the narrow temperature range in the woodland, and was relatively independent of temperature over the ranges in shrubland and grassland (Fig. 2). Model-predicted means provided estimates of both the biocrust contribution to ecosystem flux (measured by the eddy flux towers) and soil respiration (measured by soil sensors) under periods of high soil moisture. Biocrust respiration flux rates at 19°C in the woodland and shrubland were small compared to ecosystem respiration rates measured in these sites, with 0.5% and 0.8% contribution, respectively. The contribution of biocrust to ecosystem respiration rates at grassland at 19°C (1.5%) was higher than
RESULTS Abiotic controls on biocrust carbon flux We measured net carbon release (defined as positive numbers) from biocrusts under nearly all of the tested temperatures, and dark respiration increased with temperature across all sites (Table 2, Fig. 1). Calculated biocrust gross photosynthesis from different sites responded divergently to air temperature (Table 2, Fig. 1), with woodland uptake rates strongly increasing (aka, more negative) in warmer conditions while grassland, shrubland, and savanna uptake did not change across the range of experimental temperatures. Chlorophyll content was positively related to the magnitude of gross photosynthesis (slope estimate 0.10 [ 0.15 to 0.05 95% CI]) in the subset of the samples, but did not affect dark respiration or net biocrust exchange (Table 2).
Biocrusts fluxes relative to ecosystem and soil fluxes We used the relative surface cover of the selected biocrust types in the ex situ experiment to scale the biocrust fluxes to ecosystem scale based on surface area. Mixed lichen biocrusts at the pi~ non–juniper woodland accounted for 1.1% 0.36 SE relative surface cover. The mature biocrusts from the savanna included cyanolichens with dark cyanobacteria and
Table 2. Analysis of variance table with type 3 sum of squares for net biocrust exchange (NBE), NBE per unit chlorophyll a, respiration (DR), DR per unit chlorophyll a, calculated gross photosynthesis (GP), and GP per unit chlorophyll a for each site.
Term Intercept Site Temperature Site 9 temperature Chlorophyll
NBE (0.41) F; df; P
NBE with Chla (0.34) F; df; P
DR (0.58) F; df; P
DR with Chla (0.60) F; df; P
GP (0.46) F; df; P
GP with Chla (0.76) F; df; P
13.6; 1,55; 0.001 0.9; 3,55; 0.437 29.2; 1,55;
