Ecophysiology of Antarctic Vascular Plants: An Update on the Extreme Environment Resistance Mechanisms and Their Importance in Facing Climate Change.

Antarctic flowering plants have become enigmatic because of their unique capability to colonize Antarctica. It has been shown that there is not a single trait that makes Colobanthus quitensis and Deschampsia antarctica so special, but rather a set of morphophysiological traits that coordinately confer resistance to one of the harshest environments on the Earth. However, both their capacity to inhabit Antarctica and their uniqueness remain not fully explained from a biological point of view. These aspects have become more relevant due to the climatic changes already impacting Antarctica. This review aims to compile and update the recent advances in the ecophysiology of Antarctic vascular plants, deepen understanding of the mechanisms behind their notable resistance to abiotic stresses, and contribute to understanding their potential responses to environmental changes. The uniqueness of Antarctic plants has prompted research that emphasizes the role of leaf anatomical traits and cell wall properties in controlling water loss and CO2 exchange, the role of Rubisco kinetics traits in facilitating efficient carbon assimilation, and the relevance of metabolomic pathways in elucidating key processes such as gas exchange, nutrient uptake, and photoprotection. Climate change is anticipated to have significant and contrasting effects on the morphophysiological processes of Antarctic species. However, more studies in different locations outside Antarctica and using the latitudinal gradient as a natural laboratory to predict the effects of climate change are needed. Finally, we raise several questions that should be addressed, both to unravel the uniqueness of Antarctic vascular species and to understand their potential responses to climate change.

Leaf hydraulic properties of Antarctic plants: effects of growth temperature and its coordination with photosynthesis.

One of the well-documented effects of regional warming in Antarctica is the impact on flora. Warmer conditions modify several leaf anatomical traits of Antarctic vascular plants, increasing photosynthesis and growth. Given that CO2 and water vapor partially share their diffusion pathways through the leaf, changes in leaf anatomy could also affect the hydraulic traits of Antarctic plants. We evaluated the effects of growth temperature on several anatomical and hydraulic parameters of Antarctic plants and assessed the trait co-variation between these parameters and photosynthetic performance. Warmer conditions promoted an increase in leaf and whole plant hydraulic conductivity, correlating with adjustments in carbon assimilation. These adjustments were consistent with changes in leaf vasculature, where Antarctic species displayed different strategies. At higher temperature, Colobanthus quitensis decreased the number of leaf xylem vessels, but increased their diameter. In contrast, in Deschampsia antarctica the diameter did not change, but the number of vessels increased. Despite this contrasting behavior, some traits such as a small leaf diameter of vessels and a high cell wall rigidity were maintained in both species, suggesting a water-conservation response associated with the ability of Antarctic plants to cope with harsh environments.

Ecological and metabolic implications of the nurse effect of Maihueniopsis camachoi in the Atacama Desert.

Plant-plant positive interactions are key drivers of community structure. Yet, the underlying molecular mechanisms of facilitation processes remain unexplored. We investigated the 'nursing' effect of Maihueniopsis camachoi, a cactus that thrives in the Atacama Desert between c. 2800 and 3800 m above sea level. We hypothesised that an important protective factor is thermal amelioration of less cold-tolerant species with a corresponding impact on molecular phenotypes. To test this hypothesis, we compared plant cover and temperatures within the cactus foliage with open areas and modelled the effect of temperatures on plant distribution. We combined eco-metabolomics and machine learning to test the molecular consequences of this association. Multiple species benefited from the interaction with M. camachoi. A conspicuous example was the extended distribution of Atriplex imbricata to colder elevations in association with M. camachoi (400 m higher as compared to plants in open areas). Metabolomics identified 93 biochemical markers predicting the interaction status of A. imbricata with 79% accuracy, independently of year. These findings place M. camachoi as a key species in Atacama plant communities, driving local biodiversity with an impact on molecular phenotypes of nursed species. Our results support the stress-gradient hypothesis and provide pioneer insights into the metabolic consequences of facilitation.

Specialization patterns in symbiotic associations: A community perspective over spatial scales.

Specialization, contextualized in a resource axis of an organism niche, is a core concept in ecology. In biotic interactions, specialization can be determined by the range of interacting partners. Evolutionary and ecological factors, in combination with the surveyed scale (spatial, temporal, biological, and/or taxonomic), influence the conception of specialization. This study aimed to assess the specialization patterns and drivers in the lichen symbiosis, considering the interaction between the principal fungus (mycobiont) and the associated Nostoc (cyanobiont), from a community perspective considering different spatial scales. Thus, we determined Nostoc phylogroup richness and composition of lichen communities in 11 Nothofagus pumilio forests across a wide latitudinal gradient in Chile. To measure specialization, cyanobiont richness, Simpson's and d' indices were estimated for 37 mycobiont species in these communities. Potential drivers that might shape Nostoc composition and specialization measures along the environmental gradient were analysed. Limitations in lichen distributional ranges due to the availability of their cyanobionts were studied. Turnover patterns of cyanobionts were identified at multiple spatial scales. The results showed that environmental factors shaped the Nostoc composition of these communities, thus limiting cyanobiont availability to establish the symbiotic association. Besides, specialization changed with the spatial scale and with the metric considered. Cyanolichens were more specialized than cephalolichens when considering partner richness and Simpson's index, whereas the d' index was mostly explained by mycobiont identity. Little evidence of lichen distributional ranges due to the distribution of their cyanobionts was found. Thus, lichens with broad distributional ranges either associated with several cyanobionts or with widely distributed cyanobionts. Comparisons between local and regional scales showed a decreasing degree of specialization at larger scales due to an increase in cyanobiont richness. The results support the context dependency of specialization and how its consideration changes with the metric and the spatial scale considered. Subsequently, we suggest considering the entire community and widening the spatial scale studied as it is crucial to understand factors determining specialization.

Trait evolution during a rapid global weed invasion despite little genetic differentiation.

Invasive species often possess a great capacity to adapt to novel environments in the form of spatial trait variation, as a result of varying selection regimes, genetic drift, or plasticity. We explored the geographic differentiation in several phenotypic traits related to plant growth, reproduction, and defense in the highly invasive Centaurea solstitialis by measuring neutral genetic differentiation (F ST), and comparing it with phenotypic differentiation (P ST), in a common garden experiment in individuals originating from regions representing the species distribution across five continents. Native plants were more fecund than non-native plants, but the latter displayed considerably larger seed mass. We found indication of divergent selection for these two reproductive traits but little overall genetic differentiation between native and non-native ranges. The native versus invasive P ST-F ST comparisons demonstrated that, in several invasive regions, seed mass had increased proportionally more than the genetic differentiation. Traits displayed different associations with climate variables in different regions. Both capitula numbers and seed mass were associated with winter temperature and precipitation and summer aridity in some regions. Overall, our study suggests that rapid evolution has accompanied invasive success of C. solstitialis and provides new insights into traits and their genetic bases that can contribute to fitness advantages in non-native populations.

Nutrient availability regulates Deschampsia antarctica photosynthetic and stress tolerance performance in Antarctica.

Deschampsia antarctica is one of the only two native vascular plants in Antarctica, mostly located in the ice-free areas of the Peninsula's coast and adjacent islands. This region is characterized by a short growing season, frequent extreme climatic events, and soils with reduced nutrient availability. However, it is unknown whether its photosynthetic and stress tolerance mechanisms are affected by the availability of nutrients to deal with this particular environment. We studied the photosynthetic, primary metabolic, and stress tolerance performance of D. antarctica plants growing on three close sites (<500 m) with contrasting soil nutrient conditions. Plants from all sites showed similar photosynthetic rates, but mesophyll conductance and photobiochemistry were more limiting (~25%) in plants growing on low-nutrient availability soils. Additionally, these plants showed higher stress levels and larger investments in photoprotection and carbon pools, most probably driven by the need to stabilize proteins and membranes, and remodel cell walls. In contrast, when nutrients were readily available, plants shifted their carbon investment towards amino acids related to osmoprotection, growth, antioxidants, and polyamines, leading to vigorous plants without appreciable levels of stress. Taken together, these findings demonstrate that D. antarctica displays differential physiological performances to cope with adverse conditions depending on resource availability, allowing it to maximize stress tolerance without jeopardizing photosynthetic capacity.

Testing the stress gradient hypothesis in soil bacterial communities associated with vegetation belts in the Andean Atacama Desert.

BACKGROUND: Soil microorganisms are in constant interaction with plants, and these interactions shape the composition of soil bacterial communities by modifying their environment. However, little is known about the relationship between microorganisms and native plants present in extreme environments that are not affected by human intervention. Using high-throughput sequencing in combination with random forest and co-occurrence network analyses, we compared soil bacterial communities inhabiting the rhizosphere surrounding soil (RSS) and the corresponding bulk soil (BS) of 21 native plant species organized into three vegetation belts along the altitudinal gradient (2400-4500 m a.s.l.) of the Talabre-Lejía transect (TLT) in the slopes of the Andes in the Atacama Desert. We assessed how each plant community influenced the taxa, potential functions, and ecological interactions of the soil bacterial communities in this extreme natural ecosystem. We tested the ability of the stress gradient hypothesis, which predicts that positive species interactions become increasingly important as stressful conditions increase, to explain the interactions among members of TLT soil microbial communities. RESULTS: Our comparison of RSS and BS compartments along the TLT provided evidence of plant-specific microbial community composition in the RSS and showed that bacterial communities modify their ecological interactions, in particular, their positive:negative connection ratios in the presence of plant roots at each vegetation belt. We also identified the taxa driving the transition of the BS to the RSS, which appear to be indicators of key host-microbial relationships in the rhizosphere of plants in response to different abiotic conditions. Finally, the potential functions of the bacterial communities also diverge between the BS and the RSS compartments, particularly in the extreme and harshest belts of the TLT. CONCLUSIONS: In this study, we identified taxa of bacterial communities that establish species-specific relationships with native plants and showed that over a gradient of changing abiotic conditions, these relationships may also be plant community specific. These findings also reveal that the interactions among members of the soil microbial communities do not support the stress gradient hypothesis. However, through the RSS compartment, each plant community appears to moderate the abiotic stress gradient and increase the efficiency of the soil microbial community, suggesting that positive interactions may be context dependent.

Rapid upwards spread of non-native plants in mountains across continents.

High-elevation ecosystems are among the few ecosystems worldwide that are not yet heavily invaded by non-native plants. This is expected to change as species expand their range limits upwards to fill their climatic niches and respond to ongoing anthropogenic disturbances. Yet, whether and how quickly these changes are happening has only been assessed in a few isolated cases. Starting in 2007, we conducted repeated surveys of non-native plant distributions along mountain roads in 11 regions from 5 continents. We show that over a 5- to 10-year period, the number of non-native species increased on average by approximately 16% per decade across regions. The direction and magnitude of upper range limit shifts depended on elevation across all regions. Supported by a null-model approach accounting for range changes expected by chance alone, we found greater than expected upward shifts at lower/mid elevations in at least seven regions. After accounting for elevation dependence, significant average upward shifts were detected in a further three regions (revealing evidence for upward shifts in 10 of 11 regions). Together, our results show that mountain environments are becoming increasingly exposed to biological invasions, emphasizing the need to monitor and prevent potential biosecurity issues emerging in high-elevation ecosystems.

The Upper Range Limit of Alien Plants Is Not in Equilibrium with Climate in the Andes of Central Chile.

Alien plant species are colonizing high-elevation areas along roadsides. In this study, we evaluated whether the distributions of alien plants in the central Chilean mountains have reached climatic equilibrium (i.e., upper distribution limits consistent with their climatic requirements). First, we evaluated whether the upper elevational limits of alien plants changed between 2008 and 2018 based on the Mountain Invasion Research Network (MIREN) database. Second, we compared the observed upper elevational limits with the upper limits predicted by each species' global climatic niche. On average across species, the upper elevation limit did not change between 2008 and 2018. However, most species maintained the same limit or shifted downward, while only 23% of the species shifted upwards. This lack of change does not mean that the species' distributions are in equilibrium with the climate, because the observed upper limit was lower than the limit predicted by the global niche model for 87% of species. Our results suggest that alien species in this study region may not only be climate-limited, but could also be limited by other local-scale factors, such as seed dispersal, intermittent disturbance rates, soil type and biotic interactions.

Vegetation drives the response of the active fraction of the rhizosphere microbial communities to soil warming in Antarctic vascular plants.

In the Antarctic Peninsula, increases in mean annual temperature are associated with the coverage and population density of the two Antarctic vascular plant species-Deschampsia antarctica and Colobanthus quitensis-potentially modifying critical soil processes. In this study, we characterized the diversity and community composition of active microorganisms inhabiting the vascular plant rhizosphere in two sites with contrasting vegetation cover in King George Island, Western Antarctic Peninsula. We assessed the interplay between soil physicochemical properties and microbial diversity and composition, evaluating the effect of an in situ experimental warming on the microbial communities of the rhizosphere from D. antarctica and C. quitensis. Bacteria and Eukarya showed different responses to warming in both sites, and the effect was more noticeable in microbial eukaryotes from the low vegetation site. Furthermore, important changes were found in the relative abundance of Tepidisphaerales (Bacteria) and Ciliophora (Eukarya) between warming and control treatments. Our results showed that rhizosphere eukaryal communities are more sensitive to in situ warming than bacterial communities. Overall, our results indicate that vegetation drives the response of the active fraction of the microbial communities from the rhizosphere of Antarctic vascular plants to soil warming.

Respiratory and Photosynthetic Responses of Antarctic Vascular Plants Are Differentially Affected by CO2 Enrichment and Nocturnal Warming.

Projected rises in atmospheric CO2 concentration and minimum night-time temperatures may have important effects on plant carbon metabolism altering the carbon balance of the only two vascular plant species in the Antarctic Peninsula. We assessed the effect of nocturnal warming (8/5 °C vs. 8/8 °C day/night) and CO2 concentrations (400 ppm and 750 ppm) on gas exchange, non-structural carbohydrates, two respiratory-related enzymes, and mitochondrial size and number in two species of vascular plants. In Colobanthus quitensis, light-saturated photosynthesis measured at 400 ppm was reduced when plants were grown in the elevated CO2 or in the nocturnal warming treatments. Growth in elevated CO2 reduced stomatal conductance but nocturnal warming did not. The short-term sensitivity of respiration, relative protein abundance, and mitochondrial traits were not responsive to either treatment in this species. Moreover, some acclimation to nocturnal warming at ambient CO2 was observed. Altogether, these responses in C. quitensis led to an increase in the respiration-assimilation ratio in plants grown in elevated CO2. The response of Deschampsia antarctica to the experimental treatments was quite distinct. Photosynthesis was not affected by either treatment; however, respiration acclimated to temperature in the elevated CO2 treatment. The observed short-term changes in thermal sensitivity indicate type I acclimation of respiration. Growth in elevated CO2 and nocturnal warming resulted in a reduction in mitochondrial numbers and an increase in mitochondrial size in D. antarctica. Overall, our results suggest that with climate change D. antarctica could be more successful than C. quitensis, due to its ability to make metabolic adjustments to maintain its carbon balance.

Anatomical and biochemical evolutionary ancient traits of Araucaria araucana (Molina) K. Koch and their effects on carbon assimilation.

The study of ancient species provides valuable information concerning the evolution of specific adaptations to past and current environmental conditions. Araucaria araucana (Molina) K. Koch belongs to one of the oldest families of conifers in the world, but despite this, there are few studies focused on its physiology and responses to changes in environmental conditions. We used an integrated approach aimed at comprehensively characterizing the ecophysiology of this poorly known species, focusing in its stomatal, mesophyll and biochemical traits, hypothesizing that these traits govern the carbon assimilation of A. araucana under past and present levels of atmospheric CO2. Results indicated that A. araucana presents the typical traits of an ancient species, such as large stomata and low stomatal density, which trigger low stomatal conductance and slow stomatal responsiveness to changing environmental conditions. Interestingly, the quantitative analysis showed that photosynthetic rates were equally limited by both diffusive and biochemical components. The Rubisco catalytic properties proved to have a low Rubisco affinity for CO2 and O2, similar to other ancient species. This affinity for CO2, together with the low carboxylation turnover rate, are responsible for the low Rubisco catalytic efficiency of carboxylation. These traits could be the result of the diverse environmental selective pressures that A. araucana was exposed during its diversification. The increase in measured temperatures induced an increase in stomatal and biochemical limitations, which together with a lower Rubisco affinity for CO2 could explain the low photosynthetic capacity of A. araucana in warmer conditions.

Invasive Stages within Alien Species and Hutchinson's Duality: An Example Using Invasive Plants of the Family Fabaceae in Central Chile.

To understand the factors that limit invasive expansion in alien species, it is critical to predict potential zones of colonization. Climatic niche can be an important way to predict the potential distribution of alien species. This correlation between niche and geographic distribution is called Hutchinson's duality. A combination of global and regional niches allows four invasive stages to be identified: quasi-equilibrium, local adaptation, colonization and sink stage. We studied the invasive stages of six alien leguminous species either in the niche or the geographical space. In five of the six species, a higher proportion of populations were in the quasi-equilibrium stage. Notably, Acacia species had the highest proportion of populations in local adaptation. This picture changed dramatically when we projected the climatic niche in the geographic space: in all species the colonization stage had the highest proportional projected area, ranging from 50 to 90%. Our results are consistent with Hutchinson's duality, which predicts that small areas in the niche space can be translated onto large areas of the geographic space. Although the colonization stage accounted for a low proportion of occurrences, in all species, the models predicted the largest areas for this stage. This study complements invasive stages, projecting them in geographic space.

Net plant interactions are highly variable and weakly dependent on climate at the global scale.

Although plant-plant interactions (i.e. competition and facilitation) have long been recognised as key drivers of plant community composition and dynamics, their global patterns and relationships with climate have remained unclear. Here, we assembled a global database of 10,502 pairs of empirical data from the literature to address the patterns of and climatic effects on the net outcome of plant interactions in natural communities. We found that plant interactions varied among plant performance indicators, interaction types and biomes, yet competition occurred more frequently than facilitation in plant communities worldwide. Unexpectedly, plant interactions showed weak latitudinal pattern and were weakly related to climate. Our study provides a global comprehensive overview of plant interactions, highlighting competition as a fundamental mechanism structuring plant communities worldwide. We suggest that further investigations should focus more on local factors (e.g. microclimate, soil and disturbance) than on macroclimate to identify key environmental determinants of interactions in plant communities.

Think globally, measure locally: The MIREN standardized protocol for monitoring plant species distributions along elevation gradients.

Climate change and other global change drivers threaten plant diversity in mountains worldwide. A widely documented response to such environmental modifications is for plant species to change their elevational ranges. Range shifts are often idiosyncratic and difficult to generalize, partly due to variation in sampling methods. There is thus a need for a standardized monitoring strategy that can be applied across mountain regions to assess distribution changes and community turnover of native and non-native plant species over space and time. Here, we present a conceptually intuitive and standardized protocol developed by the Mountain Invasion Research Network (MIREN) to systematically quantify global patterns of native and non-native species distributions along elevation gradients and shifts arising from interactive effects of climate change and human disturbance. Usually repeated every five years, surveys consist of 20 sample sites located at equal elevation increments along three replicate roads per sampling region. At each site, three plots extend from the side of a mountain road into surrounding natural vegetation. The protocol has been successfully used in 18 regions worldwide from 2007 to present. Analyses of one point in time already generated some salient results, and revealed region-specific elevational patterns of native plant species richness, but a globally consistent elevational decline in non-native species richness. Non-native plants were also more abundant directly adjacent to road edges, suggesting that disturbed roadsides serve as a vector for invasions into mountains. From the upcoming analyses of time series, even more exciting results can be expected, especially about range shifts. Implementing the protocol in more mountain regions globally would help to generate a more complete picture of how global change alters species distributions. This would inform conservation policy in mountain ecosystems, where some conservation policies remain poorly implemented.

Network motifs involving both competition and facilitation predict biodiversity in alpine plant communities.

Biological diversity depends on multiple, cooccurring ecological interactions. However, most studies focus on one interaction type at a time, leaving community ecologists unsure of how positive and negative associations among species combine to influence biodiversity patterns. Using surveys of plant populations in alpine communities worldwide, we explore patterns of positive and negative associations among triads of species (modules) and their relationship to local biodiversity. Three modules, each incorporating both positive and negative associations, were overrepresented, thus acting as "network motifs." Furthermore, the overrepresentation of these network motifs is positively linked to species diversity globally. A theoretical model illustrates that these network motifs, based on competition between facilitated species or facilitation between inferior competitors, increase local persistence. Our findings suggest that the interplay of competition and facilitation is crucial for maintaining biodiversity.

Carbon allocation to growth and storage depends on elevation provenance in an herbaceous alpine plant of Mediterranean climate.

It is unclear whether the frequently observed increase in non-structural carbohydrates (NSC) in plants exposed to low temperatures or drought reflects a higher sensitivity of growth than photosynthesis in such conditions (i.e. sink limitation), or a prioritization of carbon (C) allocation to storage. Alpine areas in Mediterranean-type climate regions are characterized by precipitation increases and temperature decreases with elevation. Thus, alpine plants with wide elevational ranges in Mediterranean regions may be good models to examine these alternative hypotheses. We evaluated storage and growth during experimental darkness and re-illumination in individuals of the alpine plant Phacelia secunda from three elevations in the Andes of central Chile. We hypothesized that storage is prioritized regarding growth in plants of both low- and high elevations where drought and cold stress are greatest, respectively. We expected that decreases in NSC concentrations during darkness should be minimal and, more importantly, increases in NSC after re-illumination should be higher than increases in biomass. We found that darkness caused a significant decrease in NSC concentrations of both low- and high-elevation plants, but the magnitude of the decrease was lower in the latter. Re-illumination caused higher increase in NSC concentration than in biomass in both low- and high-elevation plants (1.5- and 1.9-fold, respectively). Our study shows that C allocation in Phacelia secunda reflects ecotypic differences among elevation provenances and suggests that low temperature, but not drought, favours C allocation to storage over growth after severe C limitation.

The seed germination spectrum of alpine plants: a global meta-analysis.

Assumptions about the germination ecology of alpine plants are presently based on individual species and local studies. A current challenge is to synthesise, at the global level, the alpine seed ecological spectrum. We performed a meta-analysis of primary data from laboratory experiments conducted across four continents (excluding the tropics) and 661 species, to estimate the influence of six environmental cues on germination proportion, mean germination time and germination synchrony; accounting for seed morphology (mass, embryo : seed ratio) and phylogeny. Most alpine plants show physiological seed dormancy, a strong need for cold stratification, warm-cued germination and positive germination responses to light and alternating temperatures. Species restricted to the alpine belt have a higher preference for warm temperatures and a stronger response to cold stratification than species whose distribution extends also below the treeline. Seed mass, embryo size and phylogeny have strong constraining effects on germination responses to the environment. Globally, overwintering and warm temperatures are key drivers of germination in alpine habitats. The interplay between germination physiology and seed morphological traits further reflects pressures to avoid frost or drought stress. Our results indicate the convergence, at the global level, of the seed germination patterns of alpine species.

Going off trails: How dispersed visitor use affects alpine vegetation.

Mountain protected areas provide a range of ecosystem services including conserving biodiversity, while often providing recreation and tourism opportunities. Unfortunately, tourists and pack animals used to transport equipment can damage sensitive alpine vegetation particularly when they leave trails. This study assessed the impacts of disturbance from off trail use on alpine vegetation in a popular park in the Andes. The effect of different levels of disturbance as well as abiotic factors on alpine steppe vegetation was assessed using generalized linear models and ordinations in 91 plots (20 m2) in the popular Horcones Valley that is used to access remote areas in Aconcagua Provincial Park in Argentina. Disturbance off trails resulted in declines in the cover of native plants, including the endemic shrub Adesmia aegiceras but increases in the cover of herbs including the non-native Convolvulus arvensis. Increased disturbance was associated with shifts from stress tolerant species to ruderal plants characterized by more acquisitive traits, including shorter plants with greater Specific Leaf Area. The research demonstrates the severity of impacts from off trail trampling including how trampling favours some species with specific traits over others and why it is important to limit off track use in areas of high conservation value.