Abstract
Background and aims
We lack studies evaluating how the identity of plant, lichen and moss species relates to microbial abundance and soil functioning on Antarctica. If species identity is associated with soil functioning, distributional changes of key species, linked to climate change, could significantly affect Antarctic soil functioning.
Methods
We evaluated how the identity of six Antarctic plant, lichen and moss species relate to a range of soil attributes (C, N and P cycling), microbial abundance and structure in Livingston Island, Maritime Antarctica. We used an effect size metric to predict the association between species (vs. bare soil) and the measured soil attributes.
Results
We observed species-specific effects of the plant and biocrust species on soil attributes and microbial abundance. Phenols, phosphatase and β-D-cellobiosidase activities were the most important attributes characterizing the observed patterns. We found that the evaluated species positively correlated with soil nutrient availability and microbial abundance vs. bare soil.
Conclusions
We provide evidence, from a comparative study, that plant and biocrust identity is associated with different levels of soil functioning and microbial abundance in Maritime Antarctica. Our results suggest that changes in the spatial distribution of these species linked to climate change could potentially entail changes in the functioning of Antarctic terrestrial ecosystems.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Current exposed lands in Antarctica, mainly located at coastal regions or rock ridges, are the habitat for Antarctic plants and cryptogamic species –including the Antarctic flowering plants Deschampsia antarctica and Colobanthus quitensis, and multiple bryophyte and lichen species, some of them forming biocrust communities. In these areas, Antarctic vegetation shows a spatial patchy distribution as a consequence of multiple ecological conditions (Kappen et al. 1985; Melick and Seppelt 1997). The establishment and distribution of Antarctic vegetation is primarily conditioned by ice and snow melt at some point during the year, and thus is ultimately determined by microclimatic factors (Kennedy 1993; Hughes et al. 2006; Vieira et al. 2014). These factors (e.g. moisture or texture micro-gradients) also affect soil properties and may compromise successful propagule colonization (Bergstrom et al. 2006), but the irruption of vegetation can have direct consequences on soil functioning. For instance, we know that the presence of cryptogams is positively associated with fertility islands (sensu Schlesinger et al. 1996) leading to higher N and C concentration underneath them in continental Antarctic soils (Cannone et al. 2008) and elsewhere (Delgado-Baquerizo et al. 2016). However, the species-specific association of plant, lichen and moss species identity with multiple soil attributes, nutrient cycling and microbial abundance (Cornelissen et al. 2007; Mallen-Cooper and Eldridge 2016) remains largely unexplored in Antarctica.
The role of plant, lichen and moss species identity (at both functional and taxonomic levels) as a potential environmental predictor of soil functioning is well-known in terrestrial ecosystems (Hooper and Vitousek 1997; Chen and Stark 2000; Chapman et al. 2005; Fan et al. 2011). Primary productivity, nitrogen (N) fixation capacity or thallus/stem structure are known to be involved in litter quality and quantity production or dust capture, important factors involved in the formation of the so called fertility islands in patchy vegetated ecosystems (e.g. arid ecosystems; de Graaff et al. 2014; Ochoa-Hueso et al. 2018). Similarly, recent studies have stated that the identity of biocrusts has important implications for both microbial communities and soil functioning in drylands (Concostrina-Zubiri et al. 2013; Delgado-Baquerizo et al. 2015; Liu et al. 2016, 2017). Therefore, not only the presence but also the identity of plant and biocrust (i.e. lichens and bryophytes) species may differentially influence both microbial communities and soil functioning. However, studies providing evidence for a link between species identity and soil attributes are largely lacking, limiting our capacity to predict how ongoing changes in the coverage, relative abundance, and metabolic activity of these plant and biocrust species with climate change (e.g. Torres-Mellado et al. 2011; Cannone et al. 2016; Amesbury et al. 2017) may potentially impact the functioning of Antarctic terrestrial ecosystems.
Using a comparative approach, we evaluated how four lichen species (Leptogium puberulum, Stereocaulon alpinum, Sphaerophorus globosus, and Cladonia sp.), one moss (Sanionia uncinata), and the most common Antarctic flowering-plant (Deschampsia antarctica) (Sancho et al. 1999; Søchting et al. 2004) are associated with multiple soil attributes related to carbon, nitrogen and phosphorus cycling and the abundance of soil fungi and bacteria at Livingston Island (Antarctic Peninsula). The expected changes in the relative abundance of these species due to, for example climate change, could alter soil functioning in this continent (Kardol et al. 2010; van der Putten et al. 2016; Liu et al. 2017). Alternatively, if vegetation patterns do not relate to soil functioning, changes in their relative abundance in response to changing climatic conditions may not entail differentiated changes in soil functioning in the region. We hypothesized that the identity of plant and biocrust species will largely relate to different levels of multiple soil attributes (i.e. concentration and cycling of soil nutrients) and the abundance of soil fungi and bacteria. To test this, we first evaluated whether soil functioning and microbial abundance differed under monospecific patches of the plant and biocrust species evaluated. We then characterized which variations associated with the observed differences. Additionally, we determined which soil attributes were more sensitive to species identity. Finally, we evaluated the differences in soil functioning between the different species evaluated and areas devoid of vegetation. Our study is among the first exploring the species-specific connections of Antarctic vegetation (i.e. lichens, bryophyte and vascular species) with below-ground soil functioning. Advancing our knowledge on the relationships between the identity of vegetation components and soil biochemistry and microbial communities in Antarctica is critical to understand this ecosystem and to accurately predict potential impacts of changes in the relative abundance of these micro-habitats because of global change.
Materials and methods
Site description
The study was carried out in the vicinity of the Juan Carlos I Spanish Antarctic Base (62°39′46″S 60°23′20″W), which is located on Livingston Island (Fig. 1), 120 km north of the Antarctic Peninsula. Geology is primarily composed of acidic sedimentary, metamorphic, plutonic and volcanic rocks. The climate of Livingston Island is cold maritime, with mean summer temperature above freezing and minimum absolute temperature in winter not lower than −20 °C (Sancho et al. 2017). Annual precipitation is circa 445 mm, mainly concentrated in summer and autumn seasons (Bañón et al. 2013). Around 10% of the surface of Livingston Island is free of ice during the summer season (Fig. 1) –mainly coastal strips and rocky ridges– allowing the development of plant and cryptogamic species. Vegetation in these areas is dominated by terricolous or saxicolous lichens (species of the genera Buellia, Caloplaca, Cladonia, Leptogium, Pertusaria, Placopsis, Rhizocarpon, Stereocaulon and Usnea, among others), and bryophytes (species of the genera Andreaea, Brachythecium, Bryum, Polytrichum and Sanionia, among others), in combination with the native flowering plants Deschampsia antarctica and Colobanthus quitensis (Sancho et al. 1999; Søchting et al. 2004).
Sampling design
Soil sampling was conducted at the end of the Antarctic summer of 2015. We selected six of the most common species of vegetation growing on Livingston Island (Sancho et al. 1999; Søchting et al. 2004), including a flowering plant (Deschampsia antarctica,), four lichens (Stereocaulon alpinum, Sphaerophorus globosus, Leptogium puberulum, and Cladonia sp.), and one moss (Sanionia uncinata). We acknowledge that some selected species (i.e. S. alpinum and S. globosus) are not biocrusts per se but they grow forming dense and complex cryptogamic covers in combination with other biocrust forming species (e.g. Ceratodon purpureus, Cladonia chlorophaea, Psoroma hypnorum, Placopsis contortuplicata, Ochrolechia frigida). For simplicity, we use the term biocrust (sensu lato) throughout the manuscript to refer to these communities. Leptogium puberulum and S. alpinum are nitrogen fixing lichens including cyanobacteria (genus Nostoc) as a principal photobiont (L. puberulum) or as a secondary symbiont in cephalodia (S. alpinum). Sphaerophorus globosus and Cladonia sp. lack N-fixation capacity. The moss S. uncinata presents epiphytic cyanobacteria with lower fixation rates than that observed in abovementioned lichens (data not shown). Deschampsia antarctica was also included in our study because it has a significant presence in the studied area and coexists with the abovementioned biocrust species. From a total sampling area of 0.9 ha, we randomly selected single-species patches (having at least 10 cm diameter) for our soil sampling. A distance of at least 2 m was kept between patches to ensure spatial independency between samples (Delgado-Baquerizo et al. 2013). For each species, ten replicated soil samples from the top 5 cm mineral soil profile were collected with a 5 × 5 cm core, with the exception of Cladonia sp., which was more frequent on rocky substrates. This prevented us from obtaining more than six samples with soil profiles deeper than 5 cm for this species. Areas with no vegetation cover (bare soil) were used as controls (10 replicates). Thus, a total of 66 soil samples were collected, sieved with a 2 mm sieve and divided in two fractions. A fraction of soil was immediately frozen at −20 °C for molecular analysis. The other fraction was air dried for biogeochemical analyses. Both fractions were transported to the laboratory of Rey Juan Carlos University in Móstoles (Spain) for analyses.
Measurement of C, N and P variables in soil
We measured in the laboratory a total of 16 soil variables linked to the stocks and cycling of C, N and P: dissolved organic C (Corg), phenols, α-Glucosidase (AG, starch degradation), β-Glucosidase (BG, starch degradation), β-D-Cellobiosidase (CB, cellulose degradation), total N, available nitrogen (AN), proteins, potential net mineralization and nitrification rates, microbial biomass N, Xylosidase (XYL, hemicellulose degradation), L-Leucine-amidomethylcoumarin (LAP, protein degradation), N-acetyl-β-glucoasminidase (NAG, chitin degradation), dissolved inorganic P (DIP), and Phosphatase (PHOS, P mineralization). All these variables, referred as soil attributes hereafter (both including soil functions and properties), are either measurements of specific ecosystem processes (e.g. N mineralization rate) or key properties (e.g. organic C, total N, inorganic P and soil enzymes), which together constitute a good proxy of nutrient cycling, biological productivity and the build-up of nutrient pools (Reiss et al. 2009; Jax 2010; Maestre et al. 2012a, b).
The N of microbial biomass (MB-N) was determined using the fumigation-extraction method of Brookes et al. (1985). Soil pH was measured for all of the soil samples with a pH-meter in a 1:2.5 mass/volume soil and water suspension. Sand, clay, and silt contents were determined according to Kettler et al. (2001). Electrical conductivity was determined using a conductivity meter in the laboratory. Soil moisture content was measured by oven-drying the samples at 105 °C for 24 h, and soil water holding capacity was measured by gravimetry. Soil N was measured with a CN analyzer (Leco CHN628 Series; Leco Corporation, St Joseph, MI, USA). Organic C was determined following Anderson and Ingram (1993). Total available N (sum of ammonium, nitrate, and dissolved organic N) was colorimetrically analyzed from K2SO4 0.5 M soil extracts using a 1: 5 soil/extract ratio as described by Delgado-Baquerizo et al. (2011). Phosphate was determined by colorimetry from a 0.5 M NaHCO3 extraction (Bray and Kurtz 1945).
We measured the potential activity of seven hydrolytic soil enzymes involved in the degradation of common organic matter constituents: α-Glucosidase (starch degradation; AG), β-Glucosidase (starch degradation; BG), β-D-Cellobiosidase (cellulose degradation; CB), leucine aminopeptidase (protein degradation; LAP), N-acetyl-β-Glucosaminidase (chitin degradation; NAG), Phosphatase (P mineralization; PHOS) and β-Xylosidase (hemicellulose degradation; XYL). All the enzyme assays were set up in 96-well microplates following Bell et al. (2013). Fluorescence was measured using a microplate fluorometer (Synergy™ HTX Multi-Mode Microplate Reader, BioTek Instruments, Inc., USA). The activities were expressed as nmol h−1 g−1dry soil.
Quantification of fungi and bacteria
DNA was extracted from 0.5 g of defrosted soil fractions using the MoBio® PowerSoil DNA isolation kit (MoBio Laboratories, Carlsbad, CA) following manufacturer instructions. The quantity and quality of extracted DNA was checked using a NanoDrop® ND-2000c UV–Vis spectrophotometer (NanoDrop Technologies, Wilmington, DE, USA). The abundances of the bacterial (16 s rRNA) and fungal (ITS) genes were analyzed using quantitative PCR (qPCR) on a CFX-96 thermocycler (Biorad, USA). Total bacterial 16S and fungal 18 s rRNA genes were quantified using primer pairs Eub 338-Eub 518 and ITS1F-5.8 s respectively, following Evans and Wallenstein (2012). Efficiencies for all quantification reactions were higher than 90%, with R2 values above 0.90. The fungal: bacterial ratio was calculated using qPCR data. Results from qPCR were log-transformed for subsequent data analysis.
Statistical analyses
We first tested for significant differences in the 16 soil attributes measured across different plant and biocrust species by conducting a semiparametric MANOVA (PERMANOVA, Anderson 2001), with species as a fixed factor. Note that PERMANOVA allows unbalanced designs (i.e., different number of replicates), hence it is suitable for analyzing the data collected given our sampling design. Moreover, PERMANOVA do not require MANOVA assumptions (normality and homogeneity of variances), which were not met by our variables. We also conducted independent one-way PERMANOVA analyses for each soil and microbial variables evaluated, and tested for differences among plant and biocrust species for these variables using pairwise post hoc tests (Anderson 2001). To help visualize the differences among species, and to aid in the interpretation of PERMANOVA results, we conducted a principal component analysis (PCA) with the 16 soil attributes analyzed. We tested for differences in the soil variables analyzed including abundance of bacteria and fungi across different species by using one-way PERMANOVA. Before carrying out PERMANOVA and PCA analyses, the different variables measured were standardized by using the Z-score (Kreyszig 1978). PERMANOVA analyses were developed using 9999 permutations (permutation of raw data) and the Euclidean distance with the PERMANOVA+ for PRIMER statistical package (PRIMER-E Ltd., Plymouth Marine Laboratory, Ivybridge, UK). PCA analyses were also carried out using PRIMER.
We then assessed which soil variables, among the 16 measured related to C, N, and P cycling and storage, were the most important predictors of species identity (i.e. which variables differed the most across species). To do this, we conducted a classification random forests analysis (Breiman 2001) as described in Delgado-Baquerizo et al. (2015). The accuracy importance measure was computed for each tree, and was averaged over the forest (999 trees). These analyses were conducted using the rfpermute package (Archer 2013) of the R v3.3.2 software (http://cran.r-project.org/).
Finally, we evaluated the “fertility effect” of selected species on soil attributes using the relative interaction index (RII) of Armas et al. (2004). By “fertility effect” we mean the increase or decrease of a soil attribute under a given plant/lichen/moss species regarding the value of this attribute obtained in bare ground areas. RII was calculated as (Sli − Sbg)/(Sli + Sbg), where Sli and Sbg are the values of a given soil attribute under the lichen thalli/plant canopy and in bare ground areas, respectively (Armas et al. 2004). The RII index was calculated separately for each attribute and species studied, using as replicates for Sli the values obtained under each species sampled (n = 10, except for Cladonia sp. with n = 6), which were compared in all cases with the average of the ten replicates obtained from bare ground areas. Values of RII range from −1 to +1, with positive values indicating increases in the variable studied under the canopy of species compared to bare ground areas and negative values the opposite. To test whether RII values differed significantly from zero, we assessed their 95% bootstrap confidence interval by using the bootes R package (Kirby and Gerlanc 2013). Differences among species in the RII values were also evaluated by using one-way PERMANOVA, with species as a fixed factor. These analyses were carried out using 9999 permutations (permutation of raw data) and the Euclidean distance with the PERMANOVA+ for PRIMER statistical package.
Results
Soil functioning and microbial abundance levels under different plant and biocrust species
We found significant differences in soil functioning across different species (PERMANOVA P < 0.001; Pseudo-F = 3.97; d.f. = 6). In addition, we found the strongest differences in soil attribute for biocrusts vs. bare soil; and for Leptogium puberulum vs. all other studied species (P < 0.001; Table 1; Fig. 2). Similarly, Sanionia uncinata significantly differed to all other studied species except Cladonia sp. These observed differences were driven by species-associated variations of particular soil attributes and microbial abundances. However, we did not detect differences for Cladonia sp., D. Antarctica, Stereocaulon alpinum, and Sphaerophorus globosus when analyzed together (Fig. 2, Table 1).
The values of the soil functioning variables measured differed under each studied species. The differences between L. puberulum and the rest of studied species were driven mostly by the lowest values of soil nutrients (organic C, total N and phenols; P < 0.05; Table 2), the highest potential nitrification rate, and the values of soil enzyme activities (highest AG activity, lowest BG and CB, and lowest PHOS) found under this species (P < 0.05; Table 2). In the case of S. uncinata, its differences with the rest of species were related to the highest PHOS activity and bacterial abundance (see below), and to the intermediate values of total N and organic C found under this species (Table 2).
We found large differences in the abundance and structure (fungal:bacterial ratio) of soil bacteria and fungi across the studied species. Soils under most plant and biocrust species studied showed higher microbial abundance compared to bare ground areas, with the exception of S. globosus and S. alpinum, which had the lowest fungal and bacterial abundances, respectively (Fig. 3ab). In the case of S. globosus, soil fungal abundance was even lower than in soils devoid of vegetation. Soil fungal abundance under S. alpinum, S. uncinata, and D. antarctica was ~10 fold higher compared to bare ground areas. The highest soil bacterial abundances were reported under S. uncinata and L. puberulum, while soils under S. alpinum showed similar bacterial abundance than soils devoid of vegetation. The highest value of the fungal:bacterial ratio was observed under D. antarctica (P < 0.05, Fig. 3c). Soils under L. puberulum and S. alpinum showed intermediate values, which were different to those observed under D. antarctica and S. globosus (P < 0.05, Fig. 3c). Sphaerophorus globosus also showed similar fungal:bacterial ratio compared to soils devoid of vegetation.
Soil attributes and microbial abundance predicting observed differences across species
Our Random Forest analysis revealed that phosphatase activity, phenols, and β-D-cellobiosidase activity were the most important variables characterizing observed differences across soils under the studied species (Fig. 4), followed by other soil attributes related to nutrient availability, enzyme activities and abundance of soil microbes. However, some of the studied variables (e.g. NAG, proteins, available nitrogen, NIP, and phosphate) did not predict the differences observed across the plant and biocrust studied species.
RII index results
We observed differences in the “fertility effect” (as calculated by the RII index) of the plant, moss and lichen species studied (Fig. 5). Most of the RII values obtained were positive, i.e. the concentration and rates of the analyzed soil attributes were higher under plant and biocrust species when compared to soils devoid of vegetation. The fruticose lichen S. globosus had the highest positive RII value for soil total N and organic C content, potential mineralization rate and microbial biomass N. Deschampsia antarctica showed the highest RII value for all the soil nutrients evaluated, being the only species that had positive RII value for inorganic P. Similar results were observed under the moss S. uncinata, except for inorganic P, which decreased under this species compared to bare ground soils. Soil nutrient content under S. uncinata remained at intermediate levels. However, we also detected some negative relationships between RII and particular species (e.g., L. puberulum and Cladonia sp.). Leptogium puberulum showed the lowest RII values for soil total N, organic C, inorganic P, phenols and potential mineralization rates. However, this species showed the highest RII values for potential nitrification. Species-specific fertility effects were also observed when evaluating the RII values of soil enzymes (Fig. 3b). Deschampsia antarctica and S. uncinata had positive RII values for soil enzymatic activities, while enzymes such as BG, CB and PHOS showed very low RII values under L. puberulum. Similarly, we found very low levels of RII for AG and XYL under Cladonia sp.
Discussion
We provide solid evidence from a comparative study that the identity of plant, moss and lichen species is associated with different levels of soil functioning and microbial abundance in maritime Antarctica. More specifically, we observed that selected plant and biocrust species were related to very different values for soil variables linked to C, N and P cycling and storage (nutrient availability and enzyme activities) and microbial abundance (total fungi, bacteria and their ratio). Our observations are supported by previous observational and experimental studies conducted in drylands (Delgado-Baquerizo et al. 2015; Liu et al. 2016, 2017). Among measured soil attributes, the activity of phosphatase and β-D-cellobiosidase, and the concentration of phenols, were the most important variables characterizing the differences in soil functioning across the studied plant and cryptogamic species. Different concentrations of soil phenols and surrogates of soil P cycling (phosphatase and dissolved inorganic P) have been previously reported to be associated with different biocrust species (Delgado-Baquerizo et al. 2015), suggesting that these variables may consistently characterize soil-biocrust identity associations across the globe.
Soil functioning and microbial abundance levels under different plant and biocrust species
Most of the studied species were positively, but differentially, associated with soil attributes and microbial abundances when compared to bare ground areas devoid of vegetation. This positive association of vegetation patches with greater soil nutrient availability and cycling is similar to patterns previously observed in other regions (e.g. fertility islands in drylands or alpine tundra; Schlesinger et al. 1996; Cross and Schlesinger 1999; Escudero et al. 2004; Allington and Valone 2014). Here, we found that soils under particular species such as L. puberulum showed lower values of total and available N, organic C and inorganic P availability, which was also reduced under Cladonia sp. Although an explicit link with climate change is always difficult to establish using observational data, our results could provide some insights to help predict the responses of soil functioning and microbial abundance to climate change in Antarctica. Such predictions are linked to the expected changes in the community composition of plant and biocrust communities in response to warming in this region (e.g., Amesbury et al. 2017; Lee et al. 2017; Sancho et al. 2017). For example, D. antarctica has experienced an expansion in some regions of the Antarctic Peninsula and associated archipelagoes (Torres-Mellado et al. 2011; Cannone et al. 2016). According to our results, the expansion of this species due to warmer conditions and increased growing season length, could promote an increase in the availability of N and inorganic P in Antarctic soils, positively impacting local primary productivity (Wasley et al. 2006). Furthermore, it could promote an increment in soil phenolics, which may directly impact on soil microbial community composition (Qu and Wang 2008). On the contrary, an opposite situation migth be expected with the expansion of the Antarctic endemic cyanolichen L. puberulum. This species predominantly occurs on temporarily wet snow beds and melt water channels (Sancho et al. 1999). Thus, increased ice melt and runoff due to warming may promote its expansion, negatively influencing soil fertility (lower soil N, organic C and inorganic P concentration). However, the absence of species-specific studies dealing with species acclimation to altered climatic conditions makes it impossible to accurately predict which trend (expansion or recession) is expected for the studied species (Colesie et al. 2017), which is an important topic for future research.
Soil attributes and microbial abundance drive observed differences across species
We found that phosphatase activity was the most important attribute distinguishing soil functioning across the studied species. For example, soils under S. uncinata, Cladonia sp. and D. antarctica had the highest phosphatase activities, while the opposite occurred under L. puberulum and S. alpinum. The capacity to obtain P is an essential functional trait for biocrust species. While C and N can be directly or indirectly obtained from the atmosphere (via collaboration with microbes; Barger et al. 2016; Sancho et al. 2016), P is mainly obtained from the bedrock (Belnap 2011; Jones and Oburger 2011), and therefore, the ability to obtain P will be an advantageous functional trait in these environments (i.e. bare rock left after ice retreat). Plants and biocrusts are known to influence soil P availability (Belnap et al. 2003; Delgado-Baquerizo et al. 2015; Mihoč et al. 2016). They secrete a wide range of organic acids and powerful metal chelators, and produce phosphatases in their cell walls and mucilaginous sheaths (Jones and Wilson 1985; Belnap 2011). These chemical or enzymatic compounds, which are highly genus-specific in many cases, promote rock weathering and increase the concentration of available P in the soil (Whitton et al. 2005; Belnap 2011; Jones and Oburger 2011). Thus, differences in P acquisition traits may explain the observed differences in both P concentration and phosphatase activities in soil under selected species, reinforcing the idea that species identity has a large influence on P availability.
After phosphatase activity, the concentration of phenols was the second most important variable characterizing the observed differences in soil functioning under the studied species. Thus, we found species promoting high (e.g., D. antarctica) and low (e.g. L. puberulum) levels of phenols underneath them. We would like to highlight the case of L. puberulum, as soils under its thalli had low levels of soil phenols. Interestingly, this genus is known to lack typical lichen secondary metabolites (Otálora et al. 2014). Similarly, the concentration of soil phenols was also a major factor charactering the differences observed among the lichen species studied by Delgado-Baquerizo et al. (2015) in a dryland ecosystem from central Spain. Phenolic substances are common UV protection compounds (Dixon and Paiva 1995; Agati and Tattini 2010), and are highly important for photosynthetic organisms in stratospheric ozone depleted territories such as Antarctica (Solomon 1999, 2004). The two native Antarctic vascular plants (D. antarctica and C. quitensis) are known to synthesize and store phenolic-type molecules against UV radiation (Xiong and Day 2001; Köhler et al. 2017). For example, Ruhland et al. (2005) observed the influence of ultraviolet-B radiation on the phenylpropanoid concentrations of D. antarctica during the springtime ozone depletion season, observing up to 60% increase in the concentration of some phenolic substances. We observed that soils under D. antarctica showed the highest concentration of phenols, which may be explained by the accumulation of phenolic substances in the soil released by decaying plant material. Furthermore, phenolic compounds are also common plant root exudates with different functions (e.g. micronutrient mobility; Cesco et al. 2010), which can also act as microbial allelopathic substances. Conversely, despite its high phenolic content, soils under D. antarctica showed high fungal and bacterial abundances, suggesting a lack of allelopathic effects from the phenolic substances produced by this species on soil microorganisms. Similarly, phenolic derivatives are an important feature of the biochemistry of lichens, which show a great diversity of compounds that are also highly species-specific (Crittenden 1999). Contrary to D. antarctica, soils under S. globosus thalli showed low microbial abundance (lowest fungal abundance and second lowest values for bacteria). Interestingly, soils under S. globosus showed the second highest concentration of phenols. This suggests that synthesized phenolic substances by S. globosus may be involved, among other functions, in the chemical defense of this species against fungal activity (i.e. antimicrobial action; Lawrey 1986, 1989).
β-D-Cellobiosidase was the third most important variable characterizing the observed differences in soil functioning across the species studied. This enzyme, a cellulase, catalyzes the degradation of polysaccharides such as cellulose. This polymer is synthesized by higher plants, but also by bryophytes and, to a lesser extent, by algae and fungi (both constituents of lichen symbiosis; Haigler and Weimer 1991). Exoglucanases such as β-D-cellobiosidase are known to hydrolyze other polysaccharides (e.g. Lichenin, a storage polysaccharide found in lichens; Kanda et al. 1989; Iakiviak et al. 2011). Thus, the registered differences in soil CB activity may reflect different species-specific functional traits related to the polysaccharide content of their tissues and on their decomposability.
Microbial abundance, and fungi in particular, played a secondary but still important role in distinguishing soil functioning across species. In general, the studied species increased fungal and bacterial abundances and the fungi:bacteria ratio, in the soils under them. In addition, here we observed that plant and biocrust species patterns were related to spatial differences in soil microbial abundance. Similar results have been reported from other ecosystems (Delgado-Baquerizo et al. 2016). This is not surprising, as soil microbes are predominantly involved in soil nutrient cycling (Heritage et al. 1999), and vegetation traits (e.g. SLA in plants) indirectly condition soil microbial abundance and community composition by quantity and quality of litter production (Cleveland et al. 2014; Ochoa-Hueso et al. 2018). Thus, differences in vegetation traits may differentially condition the observed soil microbial abundance in vegetation patches in Livingston Island. Moreover, our results match with generally reported bacterial dominance over fungi under biocrusts (Bates et al. 2010; Delgado-Baquerizo et al. 2015). The fungi:bacteria ratio was generally higher under studied species compared to bare soil, indicating an enhanced soil capacity to sequester C (Malik et al. 2016). Interestingly, S. globosus was related to a lower fungal abundance, even lower than bare soil and differing up to two orders of magnitude with values registered under S. uncinata. As previously mentioned, this lower fungal abundance under S. globosus may reflect an antimicrobial effect of some synthetized phenolic substances (e.g. the depside sphaerophorin and the depsidone pannarin; Celenza et al. 2012, 2013).
Soil functioning under plant and biocrust species compared to bare ground areas
The values of the soil attributes evaluated were, in most cases, higher under the canopy of the studied species compared to bare ground areas. The positive relation between vegetation, including cryptogamic organisms, and soil nutrient availability compared to non-vegetated areas is largely referred to in literature (Schlesinger et al. 1990, 1996; Cross and Schlesinger 1999; Perroni-Ventura et al. 2010; Concostrina-Zubiri et al. 2013; Delgado-Baquerizo et al. 2015). Such connection has also been reported in Antarctica for single soil attributes. For example, Beyer et al. (2000) found that soil colonization by mosses in this region coincided with higher soil organic C and N. Here we have observed similar associations, but their magnitude varied with the species and soil variable considered.
All the species except the lichen L. puberulum were associated with greater soil nitrogen availability. As a cyanolichen with Nostoc as a unique photobiont, L. puberulum was expected to promote higher soil N concentrations due to its N fixation capacity. Lichens (both N-fixers and non-N fixers) are susceptible to N leaching during rewetting processes (Millbank 1978, 1982), but specifically N fixers have been proposed as important N sources in areas with low N availability (Vitousek et al. 2002). Thus, the low N concentration found under L. puberulum may respond to biotic or abiotic factors. For instance, habitat preference (wet snow beds and melt water channels; Sancho et al. 1999) may deplete soil N availability by washing soluble compounds leached from L. puberulum. Conversely, lower N availability may indicate the presence of a higher rate of N transformation and cycling under this species. Supporting this idea, soils under this species showed also the highest potential nitrification rate, lowest ammonium concentration, highest nitrate concentration and highest abundance of ammonia oxidizing bacteria (unpublished data). Conversely, soils under S. alpinum –also a N-fixing species– did not follow the same pattern (i.e. higher values of total and available N and lower nitrification rate than L. puberulum). This may be a consequence of its lower N-fixation rate (compared to L. puberulum, data not shown) or better retention capacity of fixed N in its cephalodia (Rai 2002). Although our study was not designed to specifically assess the influence of functional traits on soil attributes, the relationship between both N-fixing lichens and soil N attributes strengthens the statement that species-specific functional traits may play an important role influencing soil biogeochemical cycles.
Phosphorus availability was mostly negatively associated with biocrust presence, as all cryptogamic species studied had lower P values in soils under their thalli (compared to bare ground areas), while the opposite occurred under the vascular plant D. antarctica. This may result from a high input of organic matter deposited around this species due to sea bird nesting preferences. Some studies have reported that Antarctic sea birds (Catharacta spp. and Larus dominicanus) use D. antarctica communities for breeding (Albuquerque et al. 2012; Parnikoza et al. 2012). However, this should increase N availability as well by guano addition, and the highest levels of N were not found under this species. Although always negative, the magnitude of changes in P availability under biocrusts compared to bare ground areas differed across species. Delgado-Baquerizo et al. (2015) also observed that variables related to soil P availability showed the highest contrast among different biocrust-forming lichens in a dryland ecosystem from Spain. This again supports the idea that species identity may potentially exert a large influence on the P availability in the soil surface.
Finally, we found that the occurrence of most of the studied species was associated with greater enzyme activities under their canopy/thalli. However, differences were also observed depending on the enzyme considered. Similar species-specific associations of plant (Bell et al. 2014a) and biocrust (Liu et al. 2014) species with soil enzymes have been previously reported. Soil enzymes are fundamental drivers of organic matter degradation (Bell et al. 2014b), and the presence of vegetation is considered a factor enhancing enzyme activity in comparison with bare ground areas (Gianfreda 2015). Some studies conducted in drylands (Miralles et al. 2012; Zhang et al. 2012; Liu et al. 2014) have found that the activity of several enzymes is positively associated with biocrust-forming species (when compared to bare ground areas), a relationship that depend on the species considered. Enzyme activities are highly dependent on soil temperature and moisture (Burns et al. 2013; Arnosti et al. 2014; Baker and Allison 2017), and both factors are directly associated with vegetation traits. The functional diversity of cryptogams is known to influence these soil properties by, for instance, increasing substrate temperature because of dark pigment concentration and increasing soil aggregation via the exudation of carbon compounds (Belnap et al. 2003; Belnap 2006; Almeida et al. 2014). The thalli of Sphaerophorus globosus (unpublished data) and the lichen Umbilicaria aprina (Schroeter et al. 2011) are known to reach temperatures above 10 °C compared to air temperature in Antarctica. Similarly, Schlensog et al. (2013) observed differences in the temperature of thalli among Antarctic moss and lichen species. This increased temperature may enhance soil nutrient cycling under lichen thalli, naturally constrained by low soil temperature in Antarctica. Besides temperature, there are multiple other pathways for biocrust control on soil enzymes (i.e. soil pH, nutrient release or microbial activity conditioned by secondary metabolites synthesis; Hauck et al. 2009; Bowker et al. 2011). Similarly, other microhabitat features associated with spatial patterns of species distribution may also influence enzymatic activity in soil (e.g. liquid water availability or debris accumulation by cryoturbation; Cannone et al. 2008; Cannone and Guglielmin 2010). Our data highlight the enzymes phosphatase and β-D-cellobiosidase as being greatly associated with species identity. As mentioned above, the enzyme phosphatase has previously been found highly connected to biocrust identity (Delgado-Baquerizo et al. 2015) and may be a crucial variable to characterize biocrust identity effects globally. However, more efforts are needed to clarify the magnitude and pathways and explain the mechanisms by which biocrust identity regulates soil attributes such as nutrient mineralization and, consequently, to accurately predict consequences of changing species distribution for soil and ecosystem functioning in Antarctica.
Conclusions
Using a comparative approach, we provide evidence that the identity of plant, lichen and moss species was largely associated with different concentrations of soil C, N and P cycling variables and the abundance and structure (fungal:bacterial ratio) of soil microbes in maritime Antarctica. Soil phenolic content and enzymatic activity (phosphatase and β-D-cellobiosidase) were the most important variables predicting the observed differences in soil functioning across the studied species. Most evaluated species were positively associated (as measured using the RII index) to higher availability of C, N and P in soil compared to bare ground areas, which may be explained by higher soil enzymatic activities and microbial abundance. However, the magnitude of these differences was species-specific, and negative associations with some soil attributes were also observed. Our results suggest that any changes in the distribution and composition of plant and cryptogamic communities, linked to ongoing climate change or seasonal patterns, might lead to changes in the functioning and microbial abundances of Antarctic soils. They also highlight that the links between Antarctic vegetation and soil functioning are species-specific; consequently black-box approaches –considering vegetation or biocrusts as a unique entity– must be avoided to accurately characterize the role of plant and biocrust species in the functioning of Antarctic ecosystems.
References
Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytol 186:786–793. https://doi.org/10.1111/j.1469-8137.2010.03269.x
Allington GRH, Valone TJ (2014) Islands of fertility: a byproduct of grazing? Ecosystems 17:127–141. https://doi.org/10.1007/s10021-013-9711-y
Almeida ICC, Schaefer CEGR, Fernandes RBA, Pereira TTC, Nieuwendam A, Pereira AB (2014) Active layer thermal regime at different vegetation covers at lions rump, king George Island, maritime Antarctica. Geomorphology 225:36–46. https://doi.org/10.1016/j.geomorph.2014.03.048
Amesbury MJ, Roland TP, Royles J, Hodgson DA, Convey P, Griffiths H, Charman DJ (2017) Widespread biological response to rapid warming on the Antarctic peninsula. Curr Biol 27:1616–1622.e2. https://doi.org/10.1016/j.cub.2017.04.034
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility: a handbook of methods. Wallingford:CABI
Archer E (2013) Estimate permutation p-values for importance metrics. R package version 1.5.2
Armas C, Ordiales R, Pugnaire FICN (2004) Measuring plant interactions: a new comarative index. Ecology 85(10):2682–2686. https://doi.org/10.1890/03-0650
Arnosti C, Bell C, Moorhead DL, Sinsabaugh RL, Steen AD, Stromberger M, Wallenstein M, Weintraub MN (2014) Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs. Biogeochemistry 117:5–21. https://doi.org/10.1007/s10533-013-9906-5
Baker NR, Allison SD (2017) Extracellular enzyme kinetics and thermodynamics along a climate gradient in southern California. Soil Biol Biochem 114:82–92. https://doi.org/10.1016/j.soilbio.2017.07.005
Bañón M, Justel A, Velázquez D, Quesada A (2013) Regional weather survey on byers peninsula, Livingston Island, south Shetland Islands, Antarctica. Antarct Sci 25:146–156. https://doi.org/10.1017/S0954102012001046
Barger NN, Weber B, Garcia-Pichel F, et al (2016) Patterns and Controls on Nitrogen Cycling of Biological Soil Crusts. In: Weber B, Büdel B, Belnap J (eds) Biological Soil Crusts: An Organizing Principle in Drylands. Springer International Publishing, Cham, pp 257–285
Bates ST, Nash TH, Sweat KG, Garcia-Pichel F (2010) Fungal communities of lichen-dominated biological soil crusts: diversity, relative microbial biomass, and their relationship to disturbance and crust cover. J Arid Environ 74:1192–1199. https://doi.org/10.1016/j.jaridenv.2010.05.033
Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput Fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp:1–16. https://doi.org/10.3791/50961
Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014a) Rhizosphere stoichiometry: are C : N : P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytol 201:505–517. https://doi.org/10.1111/nph.12531
Bell C, Stromberger M, Wallenstein M (2014b) New insights into enzymes in the environment. Biogeochemistry 117:1–4. https://doi.org/10.1007/s10533-013-9935-0
Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178. https://doi.org/10.1002/hyp.6325
Belnap J (2011) Biological phosphorus cycling in Dryland regions. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action. Springer Berlin Heidelberg, pp 371–406
Belnap J, Prasse R, Harper KT (2003) Influence of biological soil crusts on soil environments and vascular plants. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 281–300
Bergstrom DM, Convey P, Huiskes AHL (2006) Trends in Antarctic Terrestrial and Limnetic Trends in Antarctic Terrestrial and Limnetic
Beyer L, Pingpank K, Wriedt G, Bölter M (2000) Soil formation in coastal continental Antarctica (Wilkes land). Geoderma 95:283–304. https://doi.org/10.1016/S0016-7061(99)00095-6
Bowker MA, Mau RL, Maestre FT, Escolar C, Castillo-Monroy AP (2011) Functional profiles reveal unique ecological roles of various biological soil crust organisms. Funct Ecol 25:787–795. https://doi.org/10.1111/j.1365-2435.2011.01835.x
Bray RH, Kurtz LT (1945) Determination of Total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46
Breiman L (2001) Random forests. Mach Learn 45:5–32. https://doi.org/10.1186/1478-7954-9-29
Brookes P, Landman A, Pruden G (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol 17:837–842
Burns RG, DeForest JL, Marxsen J et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Cannone N, Guglielmin M (2010) Relationships between periglacial features and vegetation development in Victoria Land, continental Antarctica. 22:703–713. doi: https://doi.org/10.1017/S0954102010000751
Cannone N, Wagner D, Hubberten HW, Guglielmin M (2008) Biotic and abiotic factors influencing soil properties across a latitudinal gradient in Victoria land, Antarctica. Geoderma 144:50–65. https://doi.org/10.1016/j.geoderma.2007.10.008
Cannone N, Guglielmin M, Convey P, Worland MR, Favero Longo SE (2016) Vascular plant changes in extreme environments: effects of multiple drivers. Clim Chang 134:651–665. https://doi.org/10.1007/s10584-015-1551-7
Celenza G, Segatore B, Setacci D, Bellio P, Brisdelli F, Piovano M, Garbarino JA, Nicoletti M, Perilli M, Amicosante G (2012) In vitro antimicrobial activity of pannarin alone and in combination with antibiotics against methicillin-resistant Staphylococcus aureus clinical isolates. Phytomedicine 19:596–602. https://doi.org/10.1016/j.phymed.2012.02.010
Celenza G, Segatore B, Setacci D, Perilli M, Brisdelli F, Bellio P, Piovano M, Garbarino JA, Amicosante G, Nicoletti M (2013) Antibacterial activity of selected metabolites from Chilean lichen species against methicillin-resistant staphylococci. Nat Prod Res 27:1528–1531. https://doi.org/10.1080/14786419.2012.730043
Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25. https://doi.org/10.1007/s11104-009-0266-9
Chapman SK, J a L, Hart SC, Koch GW (2005) Plants actively control nitrogen cycling: uncorking the microbail bottleneck. New Phytol 169:27–34. https://doi.org/10.1111/j.1469-8137.2005.01571.x
Chen J, Stark JM (2000) Plant species e € ects and carbon and nitrogen cycling in a sagebrush ± crested wheatgrass soil. 32:47–57
Cleveland CC, Reed SC, Keller AB, Nemergut DR, O’Neill SP, Ostertag R, Vitousek PM (2014) Litter quality versus soil microbial community controls over decomposition: a quantitative analysis. Oecologia 174:283–294. https://doi.org/10.1007/s00442-013-2758-9
Colesie C, Büdel B, Hurry V, Green TGA (2017) Can Antarctic lichens acclimatize to changes in temperature? Glob Chang Biol 24:1123–1135. https://doi.org/10.1111/gcb.13984
Concostrina-Zubiri L, Huber-Sannwald E, Martínez I, Flores Flores JL, Escudero A (2013) Biological soil crusts greatly contribute to small-scale soil heterogeneity along a grazing gradient. Soil Biol Biochem 64:28–36. https://doi.org/10.1016/j.soilbio.2013.03.029
Cornelissen JHC, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001. https://doi.org/10.1093/aob/mcm030
Crittenden PD (1999) Aspects of the ecology of mat-forming lichens. Rangifer 20:127–139
Cross AF, Schlesinger WH (1999) Plant regulation of soil nutrient distribution in the northern Chihuahuan Desert. Plant Ecol 145:11–25
De Albuquerque MP, de Victoria FC, Schünemann AL et al (2012) Plant composition of Skuas nests at Hennequin point, king George Island, Antarctica. Am J Plant Sci 3:688–692. https://doi.org/10.4236/ajps.2012.35082
de Graaff MA, Throop HL, Verburg PSJ, Arnone JA, Campos X (2014) A synthesis of climate and vegetation cover effects on biogeochemical cycling in shrub-dominated Drylands. Ecosystems 17:931–945. https://doi.org/10.1007/s10021-014-9764-6
Delgado-Baquerizo M, Covelo F, Gallardo A (2011) Dissolved organic nitrogen in Mediterranean ecosystems ∗ 1. Pedosph an. Int J 21:309–318. https://doi.org/10.1016/S1002-0160(11)60131-8
Delgado-Baquerizo M, Covelo F, Maestre FT, Gallardo A (2013) Biological soil crusts affect small-scale spatial patterns of inorganic N in a semiarid Mediterranean grassland. J Arid Environ 91:147–150. https://doi.org/10.1016/j.jaridenv.2013.01.005
Delgado-Baquerizo M, Gallardo A, Covelo F, Prado-Comesaña A, Ochoa V, Maestre FT (2015) Differences in thallus chemistry are related to species-specific effects of biocrust-forming lichens on soil nutrients and microbial communities. Funct Ecol 29:1087–1098. https://doi.org/10.1111/1365-2435.12403
Delgado-Baquerizo M, Maestre FT, Eldridge DJ, Bowker MA, Ochoa V, Gozalo B, Berdugo M, Val J, Singh BK (2016) Biocrust-forming mosses mitigate the negative impacts of increasing aridity on ecosystem multifunctionality in drylands. New Phytol 209:1540–1552. https://doi.org/10.1111/nph.13688
Dixon RA, Paiva NL (1995) Stress-induced Phenylpropanoid metabolism. Plant Cell 7:1085–1097. https://doi.org/10.2307/3870059
Escudero A, Giménez-Benavides L, Iriondo JM, Rubio A (2004) Patch dynamics and islands of fertility in a high mountain Mediterranean community. Arct Antarct Alp Res 36:518–527. https://doi.org/10.1657/1523-0430(2004)036[0518:PDAIOF]2.0.CO;2
Evans SE, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116. https://doi.org/10.1007/s10533-011-9638-3
Fan F, Zhang F, Lu Y (2011) Linking plant identity and interspecific competition to soil nitrogen cycling through ammonia oxidizer communities. Soil Biol Biochem 43:46–54. https://doi.org/10.1016/j.soilbio.2010.09.009
Gianfreda L (2015) Enzymes of importance to rhizosphere processes. J Soil Sci Plant Nutr 15(2):283–306
Haigler CH, Weimer PJ (eds) (1991) Biosynthesis and biodegradation of cellulose. Marcel Dekker, New York, p 694. https://doi.org/10.1016/0307-4412(92)90135-9
Hauck M, Jürgens SR, Willenbruch K, Huneck S, Leuschner C (2009) Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens. Ann Bot 103:13–22. https://doi.org/10.1093/aob/mcn202
Heritage J, Evans EGV, Killington RA (1999) The microbiology of soil and nutrient cycling. Microbiol Action:2–13
Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science (80-) 277:1302–1305
Hughes KA, Ott S, Bölter M, Convey P (2006) Colonisation processes. In: Trends in Antarctic terrestrial and limnetic ecosystems: Antarctica as a global indicator, pp 35–54
Iakiviak M, Mackie RI, Cann IKO (2011) Functional analyses of multiple lichenin-degrading enzymes from the rumen bacterium Ruminococcus albus 8. Appl Environ Microbiol 77:7541–7550. https://doi.org/10.1128/AEM.06088-11
Jax K (2010) Ecosystem functioning. Cambridge University Press, Cambridge
Jones DL, Oburger E (2011) Solubilization of phosphorus by soil microorganisms. In: Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling pp 169–198
Jones D, Wilson M (1985) Chemical activity of lichens on mineral surfaces. A Rev Int Biodeterior 21:99–104
Kanda T, Yatomi H, Makishima S, Amano Y, Nisizawa K (1989) Substrate specificities of exo- and endo-type cellulases in the hydrolysis of β-(1→3)- and β-(1→4)-mixed D-glucans. J Biochem 105:127–132
Kappen L, Polarkologie I, Kiel U et al (1985) Vegetation and ecology of ice, free areas of northern Victoria land, Antarctica 2. Ecological conditions in typical microhabitats of lichens at birthday ridge. Polar Biol 4:213–225
Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781. https://doi.org/10.1890/09-0135.1
Kennedy AD (1993) Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arct Alp Res 25:308–315. https://doi.org/10.2307/1551914
Kettler TA, Doran JW, Gilbert TL (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Am J 65:849–852. https://doi.org/10.2136/sssaj2001.653849x
Kirby KN, Gerlanc D (2013) BootES: an R package for bootstrap confidence intervals on effect sizes. Behav Res Methods 45:905–927. https://doi.org/10.3758/s13428-013-0330-5
Köhler H, Contreras RA, Pizarro M, Cortés-Antíquera R, Zúñiga GE (2017) Antioxidant responses induced by UVB radiation in Deschampsia antarctica Desv. Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.00921
Kreyszig E (1978) Introductory Functional Analysis with Applications
Lawrey JD (1986) Biological role of lichen substances. Bryologist 89:111–122. https://doi.org/10.2307/3242751
Lawrey JD (1989) Lichen secondary compounds: evidence for a correspondence between Antiherbivore and antimicrobial function. Bryologist 92:326–328
Lee JR, Raymond B, Bracegirdle TJ, Chadès I, Fuller RA, Shaw JD, Terauds A (2017) Climate change drives expansion of Antarctic ice-free habitat. Nature 547:49–54. https://doi.org/10.1038/nature22996
Liu Y, Yang H, Li X, Xing Z (2014) Effects of biological soil crusts on soil enzyme activities in revegetated areas of the Tengger Desert, China. Appl Soil Ecol 80:6–14. https://doi.org/10.1016/j.apsoil.2014.03.015
Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Singh BK (2016) Species identity of biocrust-forming lichens drives the response of soil nitrogen cycle to altered precipitation frequency and nitrogen amendment. Soil Biol Biochem 96:128–136. https://doi.org/10.1016/j.soilbio.2016.01.021
Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Wang JT, Singh BK (2017) Identity of biocrust species and microbial communities drive the response of soil multifunctionality to simulated global change. Soil Biol Biochem 107:208–217. https://doi.org/10.1016/j.soilbio.2016.12.003
Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R (2012a) Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–330. https://doi.org/10.1111/j.1365-2745.2011.01918.x
Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, Delgado-Baquerizo M, Garcia-Gomez M, Bowker MA, Soliveres S, Escolar C, Garcia-Palacios P, Berdugo M, Valencia E, Gozalo B, Gallardo A, Aguilera L, Arredondo T, Blones J, Boeken B, Bran D, Conceicao AA, Cabrera O, Chaieb M, Derak M, Eldridge DJ, Espinosa CI, Florentino A, Gaitan J, Gatica MG, Ghiloufi W, Gomez-Gonzalez S, Gutierrez JR, Hernandez RM, Huang X, Huber-Sannwald E, Jankju M, Miriti M, Monerris J, Mau RL, Morici E, Naseri K, Ospina A, Polo V, Prina A, Pucheta E, Ramirez-Collantes DA, Romao R, Tighe M, Torres-Diaz C, Val J, Veiga JP, Wang D, Zaady E (2012b) Plant species richness and ecosystem multifunctionality in global Drylands. Science (80- ) 335:214–218. https://doi.org/10.1126/science.1215442
Malik AA, Chowdhury S, Schlager V, Oliver A, Puissant J, Vazquez PGM, Jehmlich N, von Bergen M, Griffiths RI, Gleixner G (2016) Soil fungal: bacterial ratios are linked to altered carbon cycling. Front Microbiol 7:1–11. https://doi.org/10.3389/fmicb.2016.01247
Mallen-Cooper M, Eldridge DJ (2016) Laboratory-based techniques for assessing the functional traits of biocrusts. Plant Soil 406:131–143. https://doi.org/10.1007/s11104-016-2870-9
Melick ADR, Seppelt RD (1997) Vegetation patterns in relation to climatic and endogenous changes in Wilkes land, continental Antarctica Source: The Journal of Ecology, Vol. 85, No. 1, ( Feb ., 1997 ), pp. 43–56 Published by : British Ecological Society Stable URL: http://www. J Ecol 85:43–56
Mihoč MAK, Giménez-Benavides L, Pescador DS, Sánchez AM, Cavieres LA, Escudero A (2016) Soil under nurse plants is always better than outside: a survey on soil amelioration by a complete guild of nurse plants across a long environmental gradient. Plant Soil 408:31–41. https://doi.org/10.1007/s11104-016-2908-z
Millbank JW (1978) The Contribution of nitrogen-fixing lichens to the nitrogen status of their environment. In: Environmental Role of Nitrogen-fixing Blue-green Algae and Asymbiotic Bacteria. p 260–?? (incomplete pages)
Millbank JW (1982) The assessment of nitrogen fixation and throughput by lichens: III. Losses of nitrogenous compounds by Peltigera Membranacea, P. Polydactyla and Lobaria Pulmonaria in simulated rainfall episodes. New Phytol 92:229–234. https://doi.org/10.1111/j.1469-8137.1982.tb03380.x
Miralles I, Domingo F, Cantón Y, Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2012) Hydrolase enzyme activities in a successional gradient of biological soil crusts in arid and semi-arid zones. Soil Biol Biochem 53:124–132. https://doi.org/10.1016/j.soilbio.2012.05.016
Ochoa-Hueso R, Eldridge DJ, Delgado-Baquerizo M, Soliveres S, Bowker MA, Gross N, le Bagousse-Pinguet Y, Quero JL, García-Gómez M, Valencia E, Arredondo T, Beinticinco L, Bran D, Cea A, Coaguila D, Dougill AJ, Espinosa CI, Gaitán J, Guuroh RT, Guzman E, Gutiérrez JR, Hernández RM, Huber-Sannwald E, Jeffries T, Linstädter A, Mau RL, Monerris J, Prina A, Pucheta E, Stavi I, Thomas AD, Zaady E, Singh BK, Maestre FT (2018) Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J Ecol 106:242–253. https://doi.org/10.1111/1365-2745.12871
Otálora MAG, Jørgensen PM, Wedin M (2014) A revised generic classification of the jelly lichens, Collemataceae. Fungal Divers 64:275–293. https://doi.org/10.1007/s13225-013-0266-1
Parnikoza I, Dykyy I, Ivanets V, Kozeretska I, Kunakh V, Rozhok A, Ochyra R, Convey P (2012) Use of Deschampsia antarctica for nest building by the kelp gull in the argentine islands area (maritime Antarctica) and its possible role in plant dispersal. Polar Biol 35:1753–1758. https://doi.org/10.1007/s00300-012-1212-5
Perroni-Ventura Y, Montaña C, García-Oliva F (2010) Carbon-nitrogen interactions in fertility island soil from a tropical semi-arid ecosystem. Funct Ecol 24:233–242. https://doi.org/10.1111/j.1365-2435.2009.01610.x
Qu XH, Wang JG (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179. https://doi.org/10.1016/j.apsoil.2007.12.007
Rai AN, Bergman B, Rasmussen U (eds) (2002) Cyanobacteria in Symbiosis. Springer Netherlands, Dordrecht. https://doi.org/10.1007/0-306-48005-0
Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514. https://doi.org/10.1016/j.tree.2009.03.018
Ruhland CT, Xiong FS, Clark WD, Day TA (2005) The influence of ultraviolet-B radiation on growth, Hydroxycinnamic acids and flavonoids of Deschampsia antarcfica during springtime ozone depletion in Antarctica. Photochem Photobiol 81:1086–1093. https://doi.org/10.1562/2004-09-18-RA-321
Sancho LG, Schulz F, Schroeter B, Kappen L (1999) Bryophyte and lichen flora of South Bay (Livingston Island: south Shetland Islands, Antarctica). Nova Hedwigia 68:301–337
Sancho LG, Belnap J, Colesie C, et al (2016) Carbon Budgets of Biological Soil Crusts at Micro-, Meso-, and Global Scales. In: Weber B, Büdel B, Belnap J (eds) Biological Soil Crusts: An Organizing Principle in Drylands. Springer International Publishing, Cham, pp 287–304
Sancho LG, Pintado A, Navarro F, Ramos M, de Pablo MA, Blanquer JM, Raggio J, Valladares F, Green TGA (2017) Recent warming and cooling in the Antarctic peninsula region has rapid and large effects on lichen vegetation. Sci Rep 7:5689. https://doi.org/10.1038/s41598-017-05989-4
Schlensog M, Green TGA, Schroeter B (2013) Life form and water source interact to determine active time and environment in cryptogams: an example from the maritime Antarctic. Oecologia 173:59–72. https://doi.org/10.1007/s00442-013-2608-9
Schlesinger WH, Reynolds JF, Cunningham GL, Huenneke LF, Jarrell WM, Virginia RA, Whitford WG (1990) Biological feedbacks in global desertification. Science (80-) 247:1043–1048. https://doi.org/10.1126/science.247.4946.1043
Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77:364–374
Schroeter B, Green TGA, Pannewitz S, Schlensog M, Sancho LG (2011) Summer variability, winter dormancy: lichen activity over 3 years at Botany Bay, 77°S latitude, continental Antarctica. Polar Biol 34:13–22. https://doi.org/10.1007/s00300-010-0851-7
Søchting U, Øvstedal D, Sancho LG (2004) The lichens of Hurd peninsula, Livingston Island, south Shetlands. Antarctica Biblioth Lichenol:607–658
Solomon S (1999) Stratospheric ozone depletion: A review of concepts and history. 275–316
Solomon S (2004) The hole truth. Nature 427:289–291. https://doi.org/10.1038/427289a
Torres-Mellado GA, Jaña R, Casanova-Katny MA (2011) Antarctic hairgrass expansion in the south Shetland archipelago and Antarctic peninsula revisited. Polar Biol 34:1679–1688. https://doi.org/10.1007/s00300-011-1099-6
van der Putten WH, Bradford MA, Pernilla Brinkman E, van de Voorde TFJ, Veen GF (2016) Where, when and how plant–soil feedback matters in a changing world. Funct Ecol 30:1109–1121. https://doi.org/10.1111/1365-2435.12657
Vieira G, Mora C, Pina P, Schaefer CER (2014) A proxy for snow cover and winter ground surface cooling: mapping Usnea sp. communities using high resolution remote sensing imagery (maritime Antarctica). Geomorphology 225:69–75. doi: https://doi.org/10.1016/j.geomorph.2014.03.049
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
Wasley J, Robinson SA, Lovelock CE, Popp M (2006) Climate change manipulations show Antarctic flora is more strongly affected by elevated nutrients than water. Glob Chang Biol 12:1800–1812. https://doi.org/10.1111/j.1365-2486.2006.01209.x
Whitton B, Al-Shehri AM, Ellwood NTW, Turner BL (2005) Ecological aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. Org Phosphorus Environ:1–43
Xiong FS, Day TA (2001) Effect of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of Antarctic vascular plants. Plant Physiol 125:738–751. https://doi.org/10.1104/pp.125.2.738
Zhang W, Zhang G, Liu G, Dong Z, Chen T, Zhang M, Dyson PJ, An L (2012) Bacterial diversity and distribution in the southeast edge of the Tengger Desert and their correlation with soil enzyme activities. J Environ Sci (China) 24:2004–2011. https://doi.org/10.1016/S1001-0742(11)61037-1
Acknowledgements
We thank the reviewers and editor of this article for their constructive and precise comments. We also thank Victoria Ochoa, Beatriz Gozalo and Chanda Trivedi for their kind assistance through laboratory work and Jasmine Grinyer for revising the English of this manuscript. We thank José Manuel Blanquer, the B.I.O. Hesperides crew and the Spanish Antarctic Base JCI team for their support during the field campaign. This research was supported by grants from the Spanish Ministerio de Economía y Competitividad (CTM2015-64728-C2-1-R, CTM2012-38222-CO2-01 and CGL2013-44661-R) and the European Research Council (BIODESERT project, ERC Grant agreement n° 647038). ABG was supported by FPI (BES-2013-062945) and short stay (EEBB-I-15-09187) grants from Spanish Ministerio de Economía y Competitividad. MDB is supported from the Marie Sklodowska-Curie Actions of the Horizon 2020 Framework Program H2020-MSCA-IF-2016 under REA grant agreement n° 702057 and from the BES (MUSGONET) grant agreement n° LRA17\1193. BKS work is supported by the Australian Research Council (DP170104634).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Sasha Reed.
Electronic supplementary material
Figure S1
Fertility effect of the species studied (vs. bare ground areas), as measured with the relative interaction index (RII), on soil variables that did not show statistical differences between species (n = 10, except Cladonia sp. with n = 6). CL: Cladonia sp.; DA: Deschampsia antarctica; LP: Leptogium puberulum; SA: Stereocaulon alpinum; SG: Sphaerophorus globosus; SU: Sanionia uncinata. (PNG 120 kb)
Rights and permissions
About this article
Cite this article
Benavent-González, A., Delgado-Baquerizo, M., Fernández-Brun, L. et al. Identity of plant, lichen and moss species connects with microbial abundance and soil functioning in maritime Antarctica. Plant Soil 429, 35–52 (2018). https://doi.org/10.1007/s11104-018-3721-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3721-7