Ana Pintado’s research while affiliated with Complutense University of Madrid and other places

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Publications (54)


Location of C. purpureus populations in Livingston Island (Maritime Antarctica, 62°39′ S, 60°23′ W), Granite Harbour (Continental Antarctica, 77°00′ S, 162°32′ E), and the Succulent Karoo Desert (South Africa, 32°21′ S, 22°34′ E). Each red dot represents one population for which macroclimatic conditions are summarized in the corresponding table. Letters indicate the references from which climate data were obtained: (a) Soebatsfontein weather station (http://www.biota-africa.org, accessed on 30 September 2018); (b) Granite Harbour soil climate station (https://www.nrcs.usda.gov/wps/portal/nrcs/site/national/home/, accessed on 30 September 2018); (c) Ascaso et al. [66]; and (d) AEMET [67].
Dependence of net photosynthesis on different PPFD at 0, 5, 10, 15, 20, 25 °C of C. purpureus in Livingston Island (Maritime Antarctica). The R²-adjust and standard error of each curve are detailed in Table S1.
Response of net photosynthesis measured at 1300 µmol photons m⁻² s⁻¹ PPFD (NP1300) and dark respiration (DRopt) to different temperatures in the Granite Harbour (Continental Antarctica), Livingston Island (Maritime Antarctica), and the Succulent Karoo Desert (South Africa).
Changes of dark respiration (DRopt) expressed as a proportion of gross photosynthesis for C. purpureus in Granite Harbour (Continental Antarctica), Livingston Island (Maritime Antarctica), and the Succulent Karoo Desert (South Africa). Data were measured at different temperatures (0, 5, 10, 15 and 20 °C) and at PPFD of 0 and 1300 µmol photons m⁻² s⁻¹ for DRopt and net photosynthesis (NP1300), respectively.
Principal Component Analysis (PCA) of the photosynthetic parameters calculated for C. purpureus in Granite Harbour (Continental Antarctica), Livingston Island (Maritime Antarctica), and the Succulent Karoo Desert (South Africa) at four different temperatures (5, 10, 15 and 20 °C). Abbreviations correspond to gross photosynthesis (GP), net photosynthesis at 1300 µmol photons m⁻² s⁻¹ (NP1300), dark respiration (DRopt), and photosynthetic efficiency (KF).
Physiological Plasticity as a Strategy to Cope with Harsh Climatic Conditions: Ecophysiological Meta-Analysis of the Cosmopolitan Moss Ceratodon purpureus in the Southern Hemisphere
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January 2023

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138 Reads

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1 Citation

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Ana Pintado

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Determining the physiological tolerance ranges of species is necessary to comprehend the limits of their responsiveness under strong abiotic pressures. For this purpose, the cosmopolitan moss Ceratodon purpureus (Hedw.) Brid. is a good model due to its wide geographical distribution throughout different biomes and habitats. In order to disentangle how this species copes with stresses such as extreme temperatures and high radiation, we designed a meta-analysis by including the main photosynthetic traits obtained by gas exchange measurements in three contrasting habitats from the Southern Hemisphere. Our findings highlight that traits such as respiration homeostasis, modulation of the photosynthetic efficiency, adjustment of the optimal temperature, and switching between shade and sun-adapted forms, which are crucial in determining the responsiveness of this species. In fact, these ecophysiological traits are in concordance with the climatic particularities of each habitat. Furthermore, the photosynthetic trends found in our study point out how different Livingston Island (Maritime Antarctica) and Granite Harbour (Continental Antarctica) are for plant life, while the population from the Succulent Karoo Desert (South Africa) shares traits with both Antarctic regions. Altogether, the study highlights the high resilience of C. purpureus under abrupt climate changes and opens new perspectives about the wide spectrum of physiological responses of cryptogams to cope with climate change scenarios.

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Figure 1. Study area: a, view of Pico Veleta from Los Peñones de San Francisco; b, habitus of Umbilicaria virginis; c, lower surface of Umbilicaria virginis; d, lower surface of U. aprina. Bar = 1 cm.
Sierra Nevada (Spain), the southernmost European locality for the polar-alpine Umbilicaria aprina and U. virginis

April 2022

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96 Reads

Mediterranean Botany

Two strict polar-alpine Umbilicaria species (U. aprina and U. virginis) are reported growing together in Los Peñones de San Francisco. Other localities known on the highest summits of the Alps and Pyrenees are considered. We discussed the meaning of these isolated populations as glacial relicts.


Climate change leads to higher NPP at the end of the century in the Antarctic Tundra: Response patterns through the lens of lichens

April 2022

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197 Reads

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13 Citations

The Science of The Total Environment

Poikilohydric autotrophs are the main colonizers of the permanent ice-free areas in the Antarctic tundra biome. Global climate warming and the small human footprint in this ecosystem make it especially vulnerable to abrupt changes. Elucidating the effects of climate change on the Antarctic ecosystem is challenging because it mainly comprises poikilohydric species, which are greatly influenced by microtopographic factors. In the present study, we investigated the potential effects of climate change on the metabolic activity and net primary productivity (NPP) in the widespread lichen species Usnea aurantiaco-atra. Long-term monitoring of chlorophyll a fluorescence in the field was combined with photosynthetic performance measurements in laboratory experiments in order to establish the daily response patterns under biotic and abiotic factors at micro- and macro-scales. Our findings suggest that macroclimate is a poor predictor of NPP, thereby indicating that microclimate is the main driver due to the strong effects of microtopographic factors on cryptogams. Metabolic activity is also crucial for estimating the NPP, which is highly dependent on the type, distribution, and duration of the hydration sources available throughout the year. Under RCP 4.5 and RCP 8.5, metabolic activity will increase slightly compared with that at present due to the increased precipitation events predicted in MIROC5. Temperature is highlighted as the main driver for NPP projections, and thus climate warming will lead to an average increase in NPP of 167–171% at the end of the century. However, small changes in other drivers such as light and relative humidity may strongly modify the metabolic activity patterns of poikilohydric autotrophs, and thus their NPP. Species with similar physiological response ranges to the species investigated in the present study are expected to behave in a similar manner provided that liquid water is available.


Summer activity patterns for a moss and lichen in the maritime Antarctic with respect to altitude

October 2021

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146 Reads

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14 Citations

Polar Biology

There is considerable scientific interest as to how terrestrial biodiversity in Antarctica might respond, or be expected to respond, to climate change. The two species of vascular plant confined to the Antarctic Peninsula have shown clear gains in density and range extension. However, little information exists for the dominant components of the flora, lichens and bryophytes. One approach has been to look at change in biodiversity using altitude as a proxy for temperature change and previous results for Livingston Island suggested that temperature was the controlling factor. We have extended this study at the same site by using chlorophyll fluorometers to monitor activity and microclimate of the lichen, Usnea aurantiaco-atra , and the moss, Hymenoloma crispulum . We confirmed the same lapse rate in temperature but show that changes in water relations with altitude is probably the main driver. There were differences in water source with U. aurantiaco-atra benefitting from water droplet harvesting and the species performed substantially better at the summit. In contrast, activity duration, chlorophyll fluorescence and photosynthetic modelling all show desiccation to have a large negative impact on the species at the lowest site. We conclude that water relations are the main drivers of biodiversity change along the altitudinal gradient with nutrients, not measured here, as another possible contributor.


Functional performance of biocrusts across Europe and its implications for drylands

March 2021

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126 Reads

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22 Citations

Journal of Arid Environments

The Soil Crust International (SCIN) project was a multidisciplinary attempt to obtain a complete understanding of biocrusts communities across Europe, including among the monitored locations the Tabernas badlands in Spain, the driest habitat in the whole continent. Here we provide an overview in a Mini-Review format of our research about the functional performance of the more relevant biocrust forming organisms involved, looking for similarities and differences in the behavior of these communities in regions with contrasting environmental conditions, allowing a deeper understanding of habitat over biocrusts functioning. New unpublished results linked to SCIN are also included in order to reinforce or clarify some general ideas proposed within the text. The general perspective provided to the data through this unique multi-site comparison, will allow in depth studies of relevant functional traits that can shed some light over the possibility of biocrusts behaving as functional types under some circumstances. Poikilohydry is proposed as an essential driving force involved, at different extents, in all key traits ruling biocrusts ecophysiology.


Himantormia lugubris, an Antarctic endemic on the edge of the lichen symbiosis

November 2020

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600 Reads

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18 Citations

Himantormia lugubris is an Antarctic endemic with a distribution restricted to the northwest tip of Antarctic Peninsula, adjacent islands and South Georgia Island. In this region H. lugubris is an important component of the epilithic lichen community. The species has a fruticose thallus with usually simple and flattened branches whose grey surface is often disrupted exposing the black and dominant chondroid axis. Because the photobiont cells are mainly restricted to the patchy grey areas, positive carbon balance seems to be rather difficult for this species. Therefore, the aim of this paper is to elucidate which functional strategy, possibly linked with thallus anatomy, is used by H. lugubris that enables it to be a successful species in the maritime Antarctic. To achieve this goal, we constructed a picture of the lichen’s physiological, anatomical and morphological characteristics by using a broad range of technologies, such as chlorophyll fluorescence, CO2 exchange and electron microscopy. We found that H. lugubris has a very low net photosynthesis, apparently restricted to the grey areas, but high respiratory rates. Therefore, positive net photosynthesis is only possible at low temperatures. Chlorophyll content is also low but is present in both gray and black areas. Our conclusion is that the only possibility for this species to achieve a positive carbon balance is to be active for long periods under optimal conditions, that means, wet, cold and with enough light, a common combination in this region of Antarctica. Given these constrains, we suggest that H. lugubris is likely to be especially sensitive species to predicted climate warming in the maritime Antarctic.


Symbiosis at its limits: ecophysiological consequences of lichenization to the genus Prasiola in Antarctica

September 2019

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100 Reads

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7 Citations

Annals of Botany

Background and Aims Lichens represent a symbiotic relationship between at least one fungal and one photosynthetic partner. The association between the lichen-forming fungus Mastodia tessellata (Verrucariaceae) and different species of Prasiola (Trebouxiophyceae) has an amphipolar distribution and represents a unique case study for the understanding of lichen symbiosis because of the macroalgal nature of the photobiont, the flexibility of the symbiotic interaction and the coexistence of free-living and lichenized forms in the same microenvironment. In this context, we aimed to (1) characterise the photosynthetic performance of co-occurring populations of free-living and lichenized Prasiola and (2) assess the effect of the symbiosis on the water relations in Prasiola, including its tolerance to desiccation and its survival and performance under sub-zero temperatures.  Methods Photochemical responses to irradiance, desiccation, and freezing temperature and pressure-volume curves of co-existing free-living and lichenized Prasiola thalli were measured in situ in Livingston Island (Maritime Antarctica). Analyses of photosynthetic pigment, glass transition and ice nucleation temperatures, surface hydrophobicity extent and molecular analyses were conducted in the lab.  Key Results Free-living and lichenized forms of Prasiola were identified as two different species: P. crispa and Prasiola sp., respectively. While the lichenization appears to have no effect on the photochemical performance of the alga, or in its tolerance to desiccation (at short-term), the symbiotic lifestyle involves (1) changes in water relations, (2) a considerable decrease in the net carbon balance and (3) an enhanced freezing tolerance.  Conclusions Our results support an improved tolerance to subzero temperature as main benefit of lichenization for the photobiont, but highlight that lichenization represents a delicate equilibrium between a mutualistic and a less reciprocal relationship. In a warmer climate scenario, the spread of the free-living Prasiola in detriment of the lichen form would be likely, with unknown consequences for the Maritime Antarctic ecosystems.


Symbiosis at its limits: ecophysiological consequences of lichenization to the genus Prasiola in Antarctica

September 2019

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151 Reads

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21 Citations

Annals of Botany

Background and aims: Lichens represent a symbiotic relationship between at least one fungal and one photosynthetic partner. The association between the lichen-forming fungus Mastodia tessellata (Verrucariaceae) and different species of Prasiola (Trebouxiophyceae) has an amphipolar distribution and represents a unique case study for the understanding of lichen symbiosis because of the macroalgal nature of the photobiont, the flexibility of the symbiotic interaction and the co-existence of free-living and lichenized forms in the same microenvironment. In this context, we aimed to (1) characterise the photosynthetic performance of co-occurring populations of free-living and lichenized Prasiola and (2) assess the effect of the symbiosis on the water relations in Prasiola, including its tolerance to desiccation and its survival and performance under sub-zero temperatures. Methods: Photochemical responses to irradiance, desiccation, and freezing temperature and pressure-volume curves of co-existing free-living and lichenized Prasiola thalli were measured in situ in Livingston Island (Maritime Antarctica). Analyses of photosynthetic pigment, glass transition and ice nucleation temperatures, surface hydrophobicity extent and molecular analyses were conducted in the lab. Key results: Free-living and lichenized forms of Prasiola were identified as two different species: P. crispa and Prasiola sp., respectively. While the lichenization appears to have no effect on the photochemical performance of the alga, or in its tolerance to desiccation (at short-term), the symbiotic lifestyle involves (1) changes in water relations, (2) a considerable decrease in the net carbon balance and (3) an enhanced freezing tolerance. Conclusions: Our results support an improved tolerance to subzero temperature as main benefit of lichenization for the photobiont, but highlight that lichenization represents a delicate equilibrium between a mutualistic and a less reciprocal relationship. In a warmer climate scenario, the spread of the free-living Prasiola in detriment of the lichen form would be likely, with unknown consequences for the Maritime Antarctic ecosystems.


(a) Schematic description of the glacier foreland in front of Pia Glacier (Tierra del Fuego, Chile). Areas 1 and 2 are the sampling locations (moraine and forest areas, respectively) and the arrow indicates the location of the field camp. (b) Nothofagus spp. forest (area 2) with dense cover of Gunnera magellanica at the herbaceous layer. (c) Pia Glacier front (area 1) and the initial colonization stages of G. magellanica.
Nitrogen fixation rates under field natural conditions for the different species considered: Gunnera magellanica (a, b, d) and N‐fixing lichens (Stereocaulon alpinum, Petigera patagonica, Placopsis perrugosa; c and e). Values are mean (n = 5) ± standard error for all cases. Note that S. alpinum (c, e) and P. perrugosa (e) refer to the secondary axis on the right.
Gas exchange (respiration, negative values; net photosynthesis, positive) under field natural conditions of light (a–c) and temperature (d–f) for different species considered: Gunnera magellanica (a, d), Nothofagus antarctica (b, e) and N‐fixing lichens (c and f: Peltigera patagonica, Placopsis perrugosa). n = 5 for all cases except for Nothofagus tree, where five leaves of the same individual were used. PAR, photosynthetically active radiation; T, temperature.
Leaf elemental and isotopic analysis in selected plant species (see Table 1) along the chronosequence in front of the Pia Glacier, Tierra del Fuego (Chile). (a) Leaf N content (% DW); (b) leaf P content (ppm); (c) δ¹⁵N patterns; (d) estimated values for Tr (transfer ratio for N from fungus to host) calculated for each species along the chronosequence. Estimations followed these assumptions (see Supporting Information data for a more detailed explanation of assumptions): F is set to 0.7 for all plants except Gunnera magellanica which receives its N from the air and has been set at 0.1. Non‐N‐fixing plants receive N from their mycorrhizas calculated as 90% sourced from G. magellanica at 7 yr, 70% at 10 yr, 50% at 19 yr and 30% at 34 yr (mean δ¹⁵N = −0.74, −0.96, −1.92 and −4.39‰, respectively). δ¹⁵N available to G. magellanica has been adjusted in the early years to reflect that it is coming mainly from meltwater from the glacier. The values used are estimates only. Values are mean (n = 5) ± standard error.
Nitrogen fixation rates (averaged) for evaluated species from both sampling locations obtained from daily cycles of nitrogenase activity measured by acetylene reduction assay.
High nitrogen contribution by Gunnera magellanica and nitrogen transfer by mycorrhizas drive an extraordinarily fast primary succession in sub‐Antarctic Chile

June 2019

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308 Reads

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18 Citations

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 δ¹⁵N 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 δ¹⁵N 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.


Citations (48)


... How such limitations may play out across contrasting environments and species is also unclear. The global distribution of the cosmopolitan moss species Ceratodon purpureus, for instance, appears to be tightly linked with its ability to adjust its physiology to match its habitat, allowing it to thrive in the sunny desert and maritime Antarctic and increasing the likelihood that it will also be better able to adjust alongside changing climate scenarios (Beltrán-Sanz et al., 2023). High levels of plasticity are also reported for other broadly distributed moss species (e.g., Funaria hygrometrica: Shaw and Bartow, 1992;Calliergonella cuspidata: Bergamini and Peintinger, 2002) but poorly resolved in species with more limited distributions. ...

Reference:

Moss functional trait ecology: Trends, gaps, and biases in the current literature
Physiological Plasticity as a Strategy to Cope with Harsh Climatic Conditions: Ecophysiological Meta-Analysis of the Cosmopolitan Moss Ceratodon purpureus in the Southern Hemisphere

... As an important part of terrestrial ecosystem, vegetation plays an important role in climate regulation and maifntenance of terrestrial carbon balance Bai et al., 2023;Beltrán-Sanz et al., 2022). Net primary productivity (NPP) of vegetation refers to the portion of the total organic matter produced by plants through photosynthesis in a given unit of time and area, after subtracting the amount lost through autotrophic respiration (Field et al., 1995). ...

Climate change leads to higher NPP at the end of the century in the Antarctic Tundra: Response patterns through the lens of lichens

The Science of The Total Environment

... Polytrichum juniperinum Hedw., widely distributed in Antarctica, is one of the most studied species due to its resistance to adverse climatic conditions. It plays a vital role in structuring biological communities in exposed soils and contributes to carbon retention (Casanova-Katny et al. 2016;Carvalho et al. 2020;Schroeter et al. 2021). These mosses are not only essential for Antarctic ecology but also hold biotechnological potential, as their extreme adaptations can be applied in environmental biotechnology, such as the discovery of novel bioactive compounds. ...

Summer activity patterns for a moss and lichen in the maritime Antarctic with respect to altitude

Polar Biology

... The restoration of biocrusts has demonstrated encouraging outcomes in several applications, as scientists and environmentalists are employing inventive methods to promote the resuscitation of biocrusts in arid environments [25,106]. An ongoing groundbreaking project from the USA aims to cultivate whole biocrust communities on a large scale, with the possibility that this initiative could lead to significant advancements in restoring biocrusts in the face of climate change, aiding in ecological restoration and protecting dryland ecosystems globally [107]. A study conducted by Bowker et al. [108] documented a remarkable success story in the restoration of biocrust in a degraded ecosystem. ...

Functional performance of biocrusts across Europe and its implications for drylands
  • Citing Article
  • March 2021

Journal of Arid Environments

... Vertically-arranged young thalli are regularly smooth and grey-cream coloured. In old thalli that have a complex 3-D structure showing a great variety of branching patterns the greyish surface is often disrupted and showing the black chondroid axis (Sancho et al. 2020). Some thalli have brown apothecia, sometimes very numerous in complex thalli, located on the top of the branches. ...

Himantormia lugubris, an Antarctic endemic on the edge of the lichen symbiosis

... DMTA enables the measurement of molecular mobility directly and accurately by applying a small oscillating force (stress) to a sample and then measuring the resulting change in dimension (deformation or strain) and its recovery when the force is removed (Ballesteros and Walters, 2011). This technique has been used successfully to study molecular mobility in the DT moss Syntrichia ruralis (Fernández-Marín et al., 2013), the DT angiosperm Ramonda myconi, and the lichen Mastodia tesselata , 2019. In S. ruralis, molecular mobility was studied in relation to WC in combination with an assessment of the activity of the xanthophyll cycle, which is enzyme dependent, and it was concluded that it is possible to demonstrate the absence of enzymatic activity in vitrified photosynthetic tissue (Fernández-Marín et al., 2013). ...

Symbiosis at its limits: ecophysiological consequences of lichenization to the genus Prasiola in Antarctica
  • Citing Article
  • September 2019

Annals of Botany

... Prasiola species show a remarkable ecological plasticity and stress tolerance and comprise freshwater, supralitoral and aeroterrestrial species (Holzinger et al., 2017;Huiskes et al., 1997;Kang et al., 2013;Moniz et al., 2012;Ram ırez et al., 2007;Ze z bek et al., 2021). Thus, physiological and/or structural responses to desiccation tolerance have been examined from urban environments (Holzinger et al., 2017), from Arctic supralittoral sites (Kang et al., 2013) and from Antarctica (Bacior et al., 2017;Fern andez-Mar ın, L opez-Pozo, et al., 2019;Huiskes et al., 1997;. Several species show high physiological plasticity to acclimate to wide ranges of salinity (Jacob et al., 1991;. ...

Symbiosis at its limits: ecophysiological consequences of lichenization to the genus Prasiola in Antarctica
  • Citing Article
  • September 2019

Annals of Botany

... Core taxa in the bacterial network, such as fast-growing Proteobacteria, Actinobacteria, and Bacteroidetes, can expand rapidly (Fierer et al., 2007;Zhou et al., 2019), initially promoting P i solubilization and P O accumulation, as evidenced by shifts in soil P fractions and P-cycling gene abundances (Figures 1 and 4). Additionally, the dominance of N 2fixing bacteria and their symbiotic relationships with plants at the early stage can stimulate soil P cycling along with increasing N contents (Benavent-González et al., 2019;Bergkemper et al., 2016). This is confirmed by the significant increase in available soil P concentration and the decrease in P i concentration at the early stage ( Figure 1). ...

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

... Lichens are the main type of terrestrial vegetation in Antarctica [88]. In this study, Acidipila, Bryocella, and Endobacter were found to be more abundant in the two species of Antarctic lichens tested (U. aurantiacoatra and U. antarctica) (Fig. S1b). ...

Antarctic Studies Show Lichens to be Excellent Biomonitors of Climate Change

... While other lichens may differ, but Rhizocarpon behaves like the annual rings of a regularly growing tree (e.g., holm oak). There is no evidence that Rh. geographicum's growth curve is exponential, but rather the opposite (Armstrong, 2013) and in the species there is no significant relationship between photosynthetic rates and stem size (Raggio et al., 2018). Team members who participated in the field surveys, data processing and interpretation of the results have also participated in studies that applied lichenometric dating to several exposed surfaces of known age (Sancho et al., 2011) that confirmed the linear relationship between age and diameter. ...

Photosynthetic rate and thallus size are not related in alpine yellow-green Rhizocarpon crustose lichens: Implications for lichenometry and growth
  • Citing Article
  • July 2018

Geomorphology