High Resilience and Fast Acclimation Processes Allow the Antarctic Moss Bryum argenteum to Increase Its Carbon Gain in Warmer Growing Conditions.

Climate warming in Antarctica involves major shifts in plant distribution and productivity. This study aims to unravel the plasticity and acclimation potential of Bryum argenteum var. muticum, a cosmopolitan moss species found in Antarctica. By comparing short-term, closed-top chamber warming experiments which mimic heatwaves, with in situ seasonal physiological rates from Cape Hallett, Northern Victoria Land, we provide insights into the general inherent resilience of this important Antarctic moss and into its adaptability to longer-term threats and stressors associated with climate change. Our findings show that B. argenteum can thermally acclimate to mitigate the effects of increased temperature under both seasonal changes and short-term pulse warming events. Following pulse warming, this species dramatically increased its carbon uptake, measured as net photosynthesis, while reductions in carbon losses, measured as dark respiration, were not observed. Rapid growth of new shoots may have confounded the effects on respiration. These results demonstrate the high physiological plasticity of this species, with acclimation occurring within only 7 days. We show that this Antarctic moss species appears to have a high level of resilience and that fast acclimation processes allow it to potentially benefit from both short-term and long-term climatic changes.

Genetic diversity of soil invertebrates corroborates timing estimates for past collapses of the West Antarctic Ice Sheet.

During austral summer field seasons between 1999 and 2018, we sampled at 91 locations throughout southern Victoria Land and along the Transantarctic Mountains for six species of endemic microarthropods (Collembola), covering a latitudinal range from 76.0°S to 87.3°S. We assembled individual mitochondrial cytochrome c oxidase subunit 1 (COI) sequences (n = 866) and found high levels of sequence divergence at both small (<10 km) and large (>600 km) spatial scales for four of the six Collembola species. We applied molecular clock estimates and assessed genetic divergences relative to the timing of past glacial cycles, including collapses of the West Antarctic Ice Sheet (WAIS). We found that genetically distinct lineages within three species have likely been isolated for at least 5.54 My to 3.52 My, while the other three species diverged more recently (<2 My). We suggest that Collembola had greater dispersal opportunities under past warmer climates, via flotation along coastal margins. Similarly increased opportunities for dispersal may occur under contemporary climate warming scenarios, which could influence the genetic structure of extant populations. As Collembola are a living record of past landscape evolution within Antarctica, these findings provide biological evidence to support geological and glaciological estimates of historical WAIS dynamics over the last ca 5 My.

High nitrogen contribution by Gunnera magellanica and nitrogen transfer by mycorrhizas drive an extraordinarily fast primary succession in sub-Antarctic Chile.

Chronosequences at the forefront of retreating glaciers provide information about colonization rates of bare surfaces. In the northern hemisphere, forest development can take centuries, with rates often limited by low nutrient availability. By contrast, in front of the retreating Pia Glacier (Tierra del Fuego, Chile), a Nothofagus forest is in place after only 34 yr of development, while total soil nitrogen (N) increased from near zero to 1.5%, suggesting a strong input of this nutrient. We measured N-fixation rates, carbon fluxes, leaf N and phosphorus contents and leaf δ15 N in the dominant plants, including the herb Gunnera magellanica, which is endosymbiotically associated with a cyanobacterium, in order to investigate the role of N-fixing and mycorrhizal symbionts in N-budgets during successional transition. G. magellanica presented some of the highest nitrogenase activities yet reported (potential maximal contribution of 300 kg N ha-1  yr-1 ). Foliar δ15 N results support the framework of a highly efficient N-uptake and transfer system based on mycorrhizas, with c. 80% of N taken up by the mycorrhizas potentially transferred to the host plant. Our results suggest the symbiosis of G. magellanica with cyanobacteria, and trees and shrubs with mycorrhizas, to be the key processes driving this rapid succession.

Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals.

Abiotic factors are major determinants of soil animal distributions and their dominant role is pronounced in extreme ecosystems, with biotic interactions seemingly playing a minor role. We modelled co-occurrence and distribution of the three nematode species that dominate the soil food web of the McMurdo Dry Valleys (Antarctica). Abiotic factors, other biotic groups, and autocorrelation all contributed to structuring nematode species distributions. However, after removing their effects, we found that the presence of the most abundant nematode species greatly, and negatively, affected the probability of detecting one of the other two species. We observed similar patterns in relative abundances for two out of three pairs of species. Harsh abiotic conditions alone are insufficient to explain contemporary nematode distributions whereas the role of negative biotic interactions has been largely underestimated in soil. The future challenge is to understand how the effects of global change on biotic interactions will alter species coexistence.

Functional ecology of soil microbial communities along a glacier forefield in Tierra del Fuego (Chile).

A previously established chronosequence from Pia Glacier forefield in Tierra del Fuego (Chile) containing soils of different ages (from bare soils to forest ones) is analyzed. We used this chronosequence as framework to postulate that microbial successional development would be accompanied by changes in functionality. To test this, the GeoChip functional microarray was used to identify diversity of genes involved in microbial carbon and nitrogen metabolism, as well as other genes related to microbial stress response and biotic interactions. Changes in putative functionality generally reflected succession-related taxonomic composition of soil microbiota. Major shifts in carbon fixation and catabolism were observed, as well as major changes in nitrogen metabolism. At initial microbial dominated succession stages, microorganisms could be mainly involved in pathways that help to increase nutrient availability, while more complex microbial transformations such as denitrification and methanogenesis, and later degradation of complex organic substrates, could be more prevalent at vegetated successional states. Shifts in virus populations broadly reflected changes in microbial diversity. Conversely, stress response pathways appeared relatively well conserved for communities along the entire chronosequence. We conclude that nutrient utilization is likely the major driver of microbial succession in these soils. [Int Microbiol 19(3):161-173 (2016)].

Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN).

Here we report details of the European research initiative "Soil Crust International" (SCIN) focusing on the biodiversity of biological soil crusts (BSC, composed of bacteria, algae, lichens, and bryophytes) and on functional aspects in their specific environment. Known as the so-called "colored soil lichen community" (Bunte Erdflechtengesellschaft), these BSCs occur all over Europe, extending into subtropical and arid regions. Our goal is to study the uniqueness of these BSCs on the regional scale and investigate how this community can cope with large macroclimatic differences. One of the major aims of this project is to develop biodiversity conservation and sustainable management strategies for European BSCs. To achieve this, we established a latitudinal transect from the Great Alvar of Öland, Sweden in the north over Gössenheim, Central Germany and Hochtor in the Hohe Tauern National Park, Austria down to the badlands of Tabernas, Spain in the south. The transect stretches over 20° latitude and 2,300 m in altitude, including natural (Hochtor, Tabernas) and semi-natural sites that require maintenance such as by grazing activities (Öland, Gössenheim). At all four sites BSC coverage exceeded 30 % of the referring landscape, with the alpine site (Hochtor) reaching the highest cyanobacterial cover and the two semi-natural sites (Öland, Gössenheim) the highest bryophyte cover. Although BSCs of the four European sites share a common set of bacteria, algae (including cyanobacteria) lichens and bryophytes, first results indicate not only climate specific additions of species, but also genetic/phenotypic uniqueness of species between the four sites. While macroclimatic conditions are rather different, microclimatic conditions and partly soil properties seem fairly homogeneous between the four sites, with the exception of water availability. Continuous activity monitoring of photosystem II revealed the BSCs of the Spanish site as the least active in terms of photosynthetic active periods.

Bryophyte-cyanobacteria associations during primary succession in recently Deglaciated areas of Tierra del Fuego (Chile).

Bryophyte establishment represents a positive feedback process that enhances soil development in newly exposed terrain. Further, biological nitrogen (N) fixation by cyanobacteria in association with mosses can be an important supply of N to terrestrial ecosystems, however the role of these associations during post-glacial primary succession is not yet fully understood. Here, we analyzed chronosequences in front of two receding glaciers with contrasting climatic conditions (wetter vs drier) at Cordillera Darwin (Tierra del Fuego) and found that most mosses had the capacity to support an epiphytic flora of cyanobacteria and exhibited high rates of N2 fixation. Pioneer moss-cyanobacteria associations showed the highest N2 fixation rates (4.60 and 4.96 µg N g-1 bryo. d-1) very early after glacier retreat (4 and 7 years) which may help accelerate soil development under wetter conditions. In drier climate, N2 fixation on bryophyte-cyanobacteria associations was also high (0.94 and 1.42 µg N g-1 bryo. d-1) but peaked at intermediate-aged sites (26 and 66 years). N2 fixation capacity on bryophytes was primarily driven by epiphytic cyanobacteria abundance rather than community composition. Most liverworts showed low colonization and N2 fixation rates, and mosses did not exhibit consistent differences across life forms and habitat (saxicolous vs terricolous). We also found a clear relationship between cyanobacteria genera and the stages of ecological succession, but no relationship was found with host species identity. Glacier forelands in Tierra del Fuego show fast rates of soil transformation which imply large quantities of N inputs. Our results highlight the potential contribution of bryophyte-cyanobacteria associations to N accumulation during post-glacial primary succession and further describe the factors that drive N2-fixation rates in post-glacial areas with very low N deposition.

Habitat stress initiates changes in composition, CO2 gas exchange and C-allocation as life traits in biological soil crusts.

Biological soil crusts (BSC) are the dominant functional vegetation unit in some of the harshest habitats in the world. We assessed BSC response to stress through changes in biotic composition, CO2 gas exchange and carbon allocation in three lichen-dominated BSC from habitats with different stress levels, two more extreme sites in Antarctica and one moderate site in Germany. Maximal net photosynthesis (NP) was identical, whereas the water content to achieve maximal NP was substantially lower in the Antarctic sites, this apparently being achieved by changes in biomass allocation. Optimal NP temperatures reflected local climate. The Antarctic BSC allocated fixed carbon (tracked using (14)CO2) mostly to the alcohol soluble pool (low-molecular weight sugars, sugar alcohols), which has an important role in desiccation and freezing resistance and antioxidant protection. In contrast, BSC at the moderate site showed greater carbon allocation into the polysaccharide pool, indicating a tendency towards growth. The results indicate that the BSC of the more stressed Antarctic sites emphasise survival rather than growth. Changes in BSC are adaptive and at multiple levels and we identify benefits and risks attached to changing life traits, as well as describing the ecophysiological mechanisms that underlie them.

Life form and water source interact to determine active time and environment in cryptogams: an example from the maritime Antarctic.

Antarctica, with its almost pristine conditions and relatively simple vegetation, offers excellent opportunities to investigate the influence of environmental factors on species performance, such information being crucial if the effects of possible climate change are to be understood. Antarctic vegetation is mainly cryptogamic. Cryptogams are poikilohydric and are only metabolically and photosynthetically active when hydrated. Activity patterns of the main life forms present, bryophytes (10 species, ecto- and endohydric), lichens (5 species) and phanerogams (2 species), were monitored for 21 days using chlorophyll a fluorescence as an indicator of metabolic activity and, therefore, of water regime at a mesic (hydration by meltwater) and a xeric (hydration by precipitation) site on Léonie Island/West Antarctic Peninsula (67°36'S). Length of activity depended mainly on site and form of hydration. Plants at the mesic site that were hydrated by meltwater were active for long periods, up to 100 % of the measurement period, whilst activity was much shorter at the xeric site where hydration was entirely by precipitation. There were also differences due to life form, with phanerogams and mesic bryophytes being most active and lichens generally much less so. The length of the active period for lichens was longer than in continental Antarctica but shorter than in the more northern Antarctic Peninsula. Light intensity when hydrated was positively related to the length of the active period. High activity species were strongly coupled to the incident light whilst low activity species were active under lower light levels and essentially uncoupled from incident light. Temperatures were little different between sites and also almost identical to temperatures, when active, for lichens in continental and peninsular Antarctica. Gradients in vegetation cover and growth rates across Antarctica are, therefore, not likely to be due to differences in temperature but more likely to the length of the hydrated (active) period. The strong effect on activity of the mode of hydration and the life form, plus the uncoupling from incident light for less active species, all make modelling of vegetation change with climate a more difficult exercise.

Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis.

BACKGROUND AND AIMS: Cyanolichens are usually stated to be bipartite (mycobiont plus cyanobacterial photobiont). Analyses revealed green algal carbohydrates in supposedly cyanobacterial lichens (in the genera Pseudocyphellaria, Sticta and Peltigera). Investigations were carried out to determine if both cyanobacteria and green algae were present in these lichens and, if so, what were their roles. METHODS: The types of photobiont present were determined by light and fluorescence microscopy. Small carbohydrates were analysed to detect the presence of green algal metabolites. Thalli were treated with selected strengths of Zn(2+) solutions that stop cyanobacterial but not green algal photosynthesis. CO(2) exchange was measured before and after treatment to determine the contribution of each photobiont to total thallus photosynthesis. Heterocyst frequencies were determined to clarify whether the cyanobacteria were modified for increased nitrogen fixation (high heterocyst frequencies) or were normal, vegetative cells. KEY RESULTS: Several cyanobacterial lichens had green algae present in the photosynthetic layer of the thallus. The presence of the green algal transfer carbohydrate (ribitol) and the incomplete inhibition of thallus photosynthesis upon treatment with Zn(2+) solutions showed that both photobionts contributed to the photosynthesis of the lichen thallus. Low heterocyst frequencies showed that, despite the presence of adjacent green algae, the cyanobacteria were not altered to increase nitrogen fixation. CONCLUSIONS: These cyanobacterial lichens are a tripartite lichen symbiont combination in which the mycobiont has two primarily photosynthetic photobionts, 'co-primary photobionts', a cyanobacterium (dominant) and a green alga. This demonstrates high flexibility in photobiont choice by the mycobiont in the Peltigerales. Overall thallus appearance does not change whether one or two photobionts are present in the cyanobacterial thallus. This suggests that, if there is a photobiont effect on thallus structure, it is not specific to one or the other photobiont.

The advantage of growing on moss: facilitative effects on photosynthetic performance and growth in the cyanobacterial lichen Peltigera rufescens.

Facilitative effects and plant-plant interactions are well known for higher plants, but there is a lack of information about their relevance in cryptogams. Additional information about facilitative effects between bryophytes and lichens would be an important contribution to recent research on positive plant-plant interactions, as these can have striking influences not only on the organisation of early successional terrestrial communities but also on succession dynamics by kick-starting ecosystem development through the import of key nutrients. We investigated and quantified these mechanisms between Peltigera rufescens and its associated mosses. Moss-associated thalli had a different morphology that led to several benefits from the association. They had 66% higher net photosynthetic rate and, because the majority of the gas exchange of lichen thalli took place through the lower surface, there was a further increase as the CO(2) concentration was >25% higher beneath moss-associated thalli. Microclimatic measurements showed that mean light levels were substantially lower and temperature extremes slightly ameliorated for moss-associated thalli. As a consequence, desiccation was slower which is, together with an increase in thallus thickness and water storage, the reason for extended periods of optimal net photosynthesis for the moss-associated thalli. All these benefits combined to produce a growth rate of the moss-associated thalli which was significantly higher, twice that of non-associated thalli [0.75 ± 0.4 vs. 0.30 ± 0.1 mm/month (mean ± SD)]. This appears to be the first demonstration of a strong mechanistic basis for facilitative effects between lichens and bryophytes.

Nocturnal respiration of lichens in their natural habitat is not affected by preceding diurnal net photosynthesis.

Dark respiration (DR) of lichens is reported to be higher in species with a high photosynthetic potential (suggesting a metabolic maintenance cost effect) and also, often in laboratory studies, transiently after photosynthesis (suggesting a substrate-driven effect). We investigated the occurrence of the latter, the effect of diurnal net photosynthesis (NP) on subsequent nocturnal DR, under natural temperate climate conditions in the chlorolichens Lecanora muralis and Cladonia convoluta and the cyanolichen Collema cristatum. Data sets totalling 15 months, 106 and 113 days, respectively, were obtained from automatic cuvettes that continually measured CO2 exchange and ambient conditions at 30 min intervals. For each 24 h period (sunrise to following sunrise), several measures of NP and DR were extracted, including maximal and mean rates and daily sums. No statistically significant correlations between the various measures of DR and preceding NP were found for L. muralis, only one weak correlation for Co. cristatum (the means of DR and NP) and three for Cl. convoluta (sums and means of DR and NP). It is proposed that even these significant correlations are actually a result of embedded codependencies between NP, DR and thallus water content. Overall it is concluded that no substrate-driven dependency of DR on preceding NP under natural conditions could be recognised. The periods of desiccation that often occur between the NP and following DR as well as the wide range of combinations of conditions would certainly contribute to this lack of relationship.

Lichens show that fungi can acclimate their respiration to seasonal changes in temperature.

Five species of lichens, the majority members of a soil-crust community ( Cladonia convoluta, Diploschistes muscorum, Fulgensia fulgens, Lecanora muralis, Squamarina lentigera) showed seasonal changes of temperature sensitivity of their dark respiration (DR) to such an extent that several substantially met the definition of full acclimation, i.e. near identical DR under different nocturnal temperature conditions during the course of the year. C. convoluta, for example, had maximal DR at 5 degrees C of -0.42, -1.11 and -0.09 nmol CO(2) g(-1) s(-1) in autumn, winter, and summer, respectively, a tenfold range. However, at the mean night temperatures for the same three seasons, 9.7 degrees C, 4.2 degrees C and 13.6 degrees C, maximal DR were almost identical at -1.11, -0.93, and -1.45 nmol CO(2) g(-1) s(-1). The information was extracted from measurements using automatic cuvettes that continuously recorded a sample lichen's gas exchange every 30 min under near-natural conditions. The longest period (for L. muralis) covered 15 months and 22,000 data sets whilst, for the other species studied, data blocks were available throughout the calendar year. The acclimation of DR means that maximal net carbon fixation rates remain substantially similar throughout the year and are not depressed by increased carbon loss by respiration in warmer seasons. This is especially important for lichens because of their normally high rate of DR compared to net photosynthesis. We suggest that lichens, especially soil-crust species, could be a suitable model for fungi generally, a group of organisms for which little is known about temperature acclimation because of the great difficulty in separating the organism from its growth medium. Fungi, whether saprophytic, symbiotic or parasitic, including soil lichens, are important components of soil ecosystems and contribute much of the respired CO(2) from these systems. Temperature acclimation by fungi would mean that expected increases in carbon losses caused by global climate warming from soil ecosystems might not be as extensive as first thought. This would ameliorate this positive feedback loop present in some climate models and might substantially lower the predicted warming.

Are lichens active under snow in continental Antarctica?

Photosynthetic activity, detected as chlorophyll a fluorescence, was measured for lichens under undisturbed snow in continental Antarctica using fibre optics. The fibre optics had been buried by winter snowfall after being put in place the previous year under snow-free conditions. The fibre optics were fixed in place using specially designed holding devices so that the fibre ends were in close proximity to selected lichens. Several temperature and PPFD (photosynthetic photon flux density) sensors were also installed in or close to the lichens. By attaching a chlorophyll a fluorometer to the previously placed fibre optics it proved possible to measure in vivo potential photosynthetic activity of continental Antarctic lichens under undisturbed snow. The snow cover proved to be a very good insulator for the mosses and lichens but, in contrast to the situation reported for the maritime Antarctic, it retained the severe cold of the winter and prevented early warming. Therefore, the lichens and mosses under snow were kept inactive at subzero temperatures for a prolonged time, even though the external ambient air temperatures would have allowed metabolic activity. The results suggest that the major activity period of the lichens was at the time of final disappearance of the snow and lasted about 10-14 days. The activation of lichens under snow by high air humidity appeared to be very variable and species specific. Xanthoria mawsonii was activated at temperatures below -10 degrees C through absorption of water from high air humidity. Physcia dubia showed some activation at temperatures around -5 degrees C but only became fully activated at thallus temperatures of 0 degrees C through liquid water. Candelariella flava stayed inactive until thallus temperatures close to zero indicated that liquid water had become available. Although the snow cover represented the major water supply for the lichens, lichens only became active for a brief time at or close to the time the snow disappeared. The snow did not provide a protected environment, as reported for alpine habitats, but appeared to limit lichen activity. This provides at least one explanation for the observed negative effect of extended snow cover on lichen growth.

Lichen fungi have low cyanobiont selectivity in maritime Antarctica.

• The cyanobionts of lichens and free-living Nostoc strains from Livingston Island (maritime Antarctica) were examined to determine both the cyanobiont specificity of lichens and the spatial distribution of Nostoc strains under extreme environmental conditions. • We collected five different lichen species with cyanobacteria as primary or secondary photobiont (Massalongia carnosa, Leptogium puberulum, Psoroma cinnamomeum, Placopsis parellina and Placopsis contortuplicata) and free-living cyanobacteria from different sample sites and analysed them using the tRNALeu (UAA) intron as a genetic marker to identify the cyanobacterial strains. • Our results showed that the same Nostoc strain was shared by all five lichen species and that an additional strain was present in two of the lichens. Both Nostoc strains associated with lichen fungi also occurred free-living in their surrounding. Bi- and tri-partite lichens were not different in their cyanobiont selectivity. • Contrary to studies on different lichen species in temperate regions, the Antarctic lichen species here did not use species-specific cyanobionts; this could be because of a selection pressure in this extreme environment. Limiting factors under these ecological conditions favor more versatile mycobionts. This results in selection against photobiont specificity, a selection pressure that may be more important for lichen distribution than the effect of cold temperatures on metabolism.

High thallus water content severely limits photosynthetic carbon gain of central European epilithic lichens under natural conditions.

Experiments under controlled conditions have shown that net photosynthesis (NP) of many lichens is depressed when their thalli are highly hydrated. In this study we characterise the light and water content (WC) dependency of CO2 exchange for selected epilithic lichens in the laboratory and match this against samples monitored in their natural habitat by a novel, fully automatic cuvette. Laboratory measurements showed that, at a photosynthetic photon flux density (PPFD) of 1500 µmol m-2 s-1, NP of the epilithic foliose lichen Xanthoria calcicola was reduced by about 85% (compared to NP at optimal water content) when the thallus was suprasaturated (maximal hydration was defined as WC after spraying, submerging and subsequent removal of adhering water droplets by shaking). Only after loss of about 80% of its maximal WC were the highest rates of NP possible. This depression was still substantial at 50 µmol m-2 s-1 PPFD. Responses were similar for the crustose epilithic species Lecanora muralis. CO2 exchange of both lichens was monitored under natural conditions by means of the cuvette built into a man-made wall-a common habitat of the species-in the Botanical Garden, Würzburg. For both species, rates of NP were low during and after heavy rain even if incident PPFD and temperature were favourable. This situation occurred frequently and could last through all daylight hours, resulting in a negative carbon balance when nocturnal rates of respiration were high. Often, after rainfall, there was a brief, high peak of NP when optimal WC was transiently attained before metabolic activity finally ceased through desiccation. Other periods with profitable rates of NP occurred after moderate moistening of the lichens by dew, fog or light rain. The lichens were found to perform identically in the field and laboratory. When the two data sets were compared it was clear that the full range of WC produced in the laboratory also occurred in nature and that the productivity of the epilithic lichens was regularly and severely limited by high WC. It is concluded that blockage of diffusive pathways for CO2 in the thallus through high water contents is an important ecological factor for productivity of these central European epilithic lichens.