INTRODUCTION
In a seminal paper published in 2001, Dennis Gignac wrote: “Past climate changes have clearly shown that ecosystems and species will migrate when climatic conditions change (…) One of the expected effects of global warming is a migration of the different types of forest towards the poles (…) Although bryophytes have been successfully used to monitor deposition of heavy metals, acid rain, and radionuclides they have never been used to monitor climate change.” [001]
Ten years later, a truly comprehensive edited book titled Bryophyte Ecology and Climate Change (2011) offered a score of chapters to vindicate Gignac’s early idea that “an important utilization of bryophyte indicator species would be to predict the migration of climatically sensitive ecosystems.” A very recent paper (2022) describe how important bryophytes are in Northern ecosystems: “For instance, mosses cover between 50 and 100 % of the ground in subarctic tundra (…) and in boreal forests, feather mosses like Pleurozium schreberi (Brid.) Mitt. cover between 60 and 80 % of the ground, where the moss forms continuous carpets on the forest floor.” [020]
In her introduction to the above cited book, titled “The Ecological Value of Bryophytes as Indicators of Climate Change”, Nancy Slack insisted first on the importance of bryophytes in some environments: “especially in the Arctic, the Antarctic, in alpine habitats in mountains above treeline and in bogs, fens, and larger peatlands, bryophytes are often the dominant plants in terms of both biomass and productivity.” She then offered a useful image to stress their importance even more: “Although polar bears have recently been referred to, in relation to global warming, as the new ‘canaries in the coal mine,’ it is the bryophytes that deserve that title. They are sensitive not only to increasing global temperatures, but also to increasing carbon dioxide content of the atmosphere, to increasing UVB radiation, to decreasing precipitation in some regions, and to several factors affecting carbon storage, especially in peatlands.” [002] The following year, Aurélie Desamoré and her colleagues made the same point about temperate bryophytes: “Bryophytes are a group of early land plants, whose specific ecophysiological and biological features, including poikilohydry, sensitivity to moderately high temperature and high dispersal ability, make them ideal candidates for investigating the impact of climate changes.” [007]
In his own chapter, Zolta Tuba, one of Slack’s co-editors, also insisted that “Bryophytes are vulnerable to UV-B damage because of their relatively undifferentiated simple structure. The survival of Antarctic bryophytes under ozone depletion depends on their ability to acclimate to increasing UV-B radiation”. But most importantly, he stressed the following point: “The responses of bryophytes are thus likely to interact in quite complex ways with other climatic factors (Proctor 1990). No simple predictions can be made.” [003, my emphasis]. The same year, in conclusion of a paper focusing on the situation of Antarctic bryophytes, Peter Convey made another such warning, for methodological reasons:
One challenge yet to be fully addressed in relating climatic change predictions and terrestrial biological responses is in linking the range of scales that currently separate the two. At best, current macroclimatic predictions are based on models constructed on physical scales of tens and more commonly hundreds of kilometres and based on data derived from standard meteorological observations. However, most biological processes operate at the scale of the organism and its microhabitat, where environmental variability on the scale of millimetres to metres is more relevant. [006]
This year (2022), some of the most preeminent bryologists convened to provide “: a horizon scan of fundamental questions in bryology”. They also stressed the same point:
Species distribution modelling has become a common approach by which to forecast the potential responses of bryophyte distributions to climate change scenarios. The models often depend, however, on large-scale climatic predictors and rarely include small-scale variables accounting for microenvironmental differences such as the microclimatic ones (Zellweger et al. 2019). Indeed, because bryophytes are small organisms, the environment they experience may be strongly decoupled from macroclimatic conditions. Not accounting for small-scale ecological conditions that may lead to an overestimation of climate-warming effects, as has been shown for alpine (Scherrer and Körner 2011) and boreal plants (Greiser et al. 2020). [018]
Aurélie Desamoré and her colleagues agreed as early as 2012, but with an added “detail”:
The SDMs [species distribution modelling] predict a global net increase in range size owing to ongoing climate change, but substantial range reductions in southern areas. Presence of a significant phylogeographical signal at different spatial scales suggests, however, that dispersal limitations might constitute, as opposed to the traditional view of spore-producing plants as efficient dispersers, a constraint for migration. This casts doubts about the ability of the species to face the massive extinctions predicted in the southern areas, threatening their status of reservoir of genetic diversity. As a result, bryophyte distributions are expected to quickly vary depending on climate change.[007]
In 2020, this point was still debated, as Alain Vanderpoorten and his colleagues argued:
The extent to which species can balance out the loss of suitable habitats due to climate warming by shifting their ranges is an area of controversy (…) While climate change is making some current habitats unsuitable, it is also expected to create newly suitable areas for species to occupy. The extent to which species have the ability to balance the loss of suitable habitats by shifting their ranges and track areas of suitable climate has, however, been debated (…) Contrasting model predictions with actual distribution data revealed, however, that a substantial fraction of species are missing from areas projected as suitable. [015]
And in 2022, “the scan of the fundamental questions in bryology” confirmed that the debate is still open, although it also concluded with some indication of the same dire perspective:
The extent to which bryophyte species can compensate for climate warming–induced loss of suitable habitats by shifting their distribution ranges remains an area of debate. Projected rates of range loss derived from dispersal simulations under changing climate conditions in Europe significantly exceeded projected rates of range expansion, suggesting that even highly dispersive organisms such as bryophytes might not be fully equipped to cope with projected trends of climate change in the coming decades (Zanatta et al. 2020). [018]
So, the question of the fate of bipolar mosses in a time of climate warming is still the matter of debate among bryologists today, even if it seems that most of them envision a rather bad fate for them. It was expected from very early though, as this recent paper (2019) reminds us: “Because bryophyte species diversity does not decrease significantly with latitude, contrary to the situation for most other organisms (Shaw, Cox and Goffinet, 2005), climate warming will affect their diversity relatively more strongly than, for example, that of flowering plants. [014] At this point however, it is worth treating separately the Arctic and Antarctic bryophytes to examine their fate more closely.
NORTHERN BYROPHYTES
Focusing especially on the tundra bryophytes, Annika Jägerbrand and her colleagues first drew the most likely scenario for the circumpolar Arctic bryophytes:
In the 1990s global warming was envisioned scientifically as being highly influential and pronounced at high latitudes. Since then, impacts of climate change have been confirmed. The Arctic has had a rapid increase in mean temperatures over the past few decades, twice the rate of the rest of the world. Biomes already seem to be changing owing to climate differences. Continuing Arctic climate change will therefore have the effect of encouraging forest expansion into tundra biomes, and the tundra vegetation as we know it will greatly change, shifting in its extent, distribution, and species composition. These changes will probably be unprecedented compared with those of past millennia. As climate change is only one of several environmental changes occurring in the Arctic, such as increased UV-B radiation and transboundary contaminants, impacts on vegetation are expected to be compounded [004]
The order of magnitude of the increase of temperature they discussed, however, was still very conservative—albeit with dramatic effects on the tundra: “Even a moderate increase in global mean temperature of 2 oC (above the pre-industrial level)”, they wrote, “has been predicted to reduce the tundra area by 42%, with an additional 60% of the prostrate dwarf-shrub tundra habitats lost by 2100 (Kaplan & New 2006).” Moreover, they insisted, “since plants in tundra and high altitudinal areas are adapted to colder environments, for example by having relatively low reproductive output, slow and prolonged growth, and reduced competitive ability, their capacity to adapt to the new climate or to migrate is low.” [004]
Their premise was clearly ecological, and the resulting scenario centered on the Northern translation of the tundra and boreal forest ecosystems: “For non-Antarctic tundra bryophytes, impacts of a changed vegetation composition are probably most important in the longer term because many species in the tundra biome currently experience little or no competition from surrounding plants, particularly in the polar deserts and semi- deserts. When the tundra becomes shrub-like and forested, ecosystems that are now highly dominated by bryophytes will most likely relocate over a longer timescale; high Arctic ecosystems will colonize forefields of retreating glaciers, whereas tundra communities will spread into the polar deserts.” [004]
This could mean a relative advantage for the more Southern bryophytes: “Boreal and temperate bryophyte species with high growth rates, high temperature optima for photosynthesis and growth rates, and tolerance of shaded conditions, might benefit from climate change since both precipitation and temperature will increase in some parts of the tundra. If these bryophyte species are currently growing in Arctic and alpine areas, they might increase in dominance together with shrubs.” [004] However, this relative beneficial aspect for some bryophytes would necessarily translate into an overall loss of bryophytes biodiversity: “many tundra habitats in the non-Antarctic regions will decrease in extent or relocate due to climate-change-induced shrub and forest expansion, directly decreasing bryophyte cover, diversity and abundance of species and ecotypes that are adapted to the tundra environment or have low potential for acclimatization to the changing conditions. As the biodiversity of bryophytes in the Arctic is high, climate change will most probably have significant effects on the global diversity of bryophytes.” [004]
In a 2016 paper directly asking the central question of our own research—Will bryophytes survive in a warming world?—the Finnish bryologists Xiaolan He, Kate He and Jaakko Hyvönen insisted on the same point: “As a consequence of global warming, significant losses in bryophyte diversity can be expected, particularly in areas harbouring large number of species such as boreal forests of higher latitudes, alpine biomes and higher altitudes on tropical mountains.” [008] Referring to an earlier paper [009], they simply stated “Warming winters have been suggested to have negative effects on photosynthetic activities and growth rates of moss species of sub-arctic heathlands.”
Although he acknowledged the potential loss of bryophyte biodiversity, Lars Hedenäs also provided a rare glimpse of optimism: “Finally, the expected temperatures 50–100 years into the future under moderate climate warming scenarios are comparable to or slightly higher than those of the Scandinavian Holocene thermal maximum, at 1.0–3.5 °C above current temperatures (…) This gives us some hope that, unless we allow global warming to reach the high-end Representative Concentration Pathway (…), a large proportion of our northern and mountain species and NMGVs [northern and mountain genetic variants] will survive, or they would have gone extinct already during the Holocene thermal maximum.” [014] But this, of course, all depended on a “moderate scenario”… that is very unlikely (see Appendix 1: Update on Arctic Amplification).
This was not at all such an optimist scenario indeed that Alain Vanderpoorten and his colleagues anticipated, when they concluded that even if more northern regions would at first appear suitable for bryophytes to colonize because of their warming, the said bryophytes would most likely be unable to successfully colonize them: “our results suggest that, at best, ~30% of the species would be at equilibrium with their environment by 2050. This indicates that bryophytes are not equipped to track the very fast rates of ongoing climate change projected for the course of the next decades. (…) . In fact, a growing body of evidence supports the idea that plant species spread rates are consistently expected to be much lower than the velocity of climate change.” [015]
In a paper published this year (2022), Permin, Michelsen, and Rousk describe in detail the direct and indirect effects of warming on moss abundance, but also how it would impact several ecosystem processes, and most importantly, nitrogen fixation in soils:
The dense moss carpet affects the biogeochemistry of the underlying soil by buffering soil moisture and temperature, and by impacting organic matter turnover and nutrient mineralization processes (…) Moreover, mosses host a variety of microbiota (…) and the presence of epiphytic nitrogen (N2)-fixing cyanobacteria (diazotrophs) has been recognized in several moss species (…). These moss-cyanobacteria associations are particularly important in northern, N-limited ecosystems like arctic tundra and boreal forests, where biological N2 fixation (BNF) is a major N input pathway (…). BNF is controlled by abiotic factors like moisture and temperature (…) – factors that will change in future climate scenarios (…). Furthermore, the effects of climate change are expected to be particularly pronounced in northern ecosystems (…), where the impact on ecosystem processes (e.g. decomposition and N2 fixation) is controlled by the response in plant communities (…). This includes the response of mosses, in terms of abundance and function (e.g. moisture buffering) as well as in regard to associated N2 fixation. Higher temperatures in northern ecosystems are expected to stimulate microbial activity, leading to increased nutrient mineralization and -availability, which will promote plant growth and further alter plant community composition (…). Further, shrubs are expanding into the subarctic and arctic, and deciduous shrubs are responding more quickly to increased nutrient availability, because they have a shorter leaf lifespan and higher photosynthetic capacity as compared with mosses (…). With increased plant productivity, plant litter input will also increase, which can inhibit moss growth (…) and associated N2 fixation (…), but the effects depend on the type of litter (…). Further, increased N availability as a result of enhanced mineralization rates can also inhibit moss-associated N2 fixation. [020]
In conclusion, they stressed that their “study highlights the sensitivity of ground-covering mosses to a changing climate in arctic ecosystems by showing that experimental warming directly and indirectly led to a decrease in moss-associated N2 fixation.” Most importantly, they showed that “the negative, indirect effects of warming on moss associated N2 fixation activity were not due to the dominance of vascular plants, but rather due to reduced moss cover and soil water content.” [020]
In synthesis, this first part of our review of the literature, concerning specifically the Northern hemisphere circumpolar bryophytes (tundra and boreal forest), show that future scenarios seem especially grim, even if a warming climate could first mean a potential expansion for the aid mosses. Let us turn now to the Southern hemisphere.
SOUTHERN BRYOPHYTES
Providing a specifically Antarctic perspective on bryophytes and lichens in a changing climate in the afore mentioned 2011 book edited by Nancy Slack and her colleagues [002], the Australian bryologist Rodney Seppelt first remind us of two important facts about this part of the world: (1) “the Antarctic continent having less than 1% of the land ice-free and with a not surprisingly depauperate flora and fauna. By contrast, the Arctic has a rich and diverse flora and fauna”, and (2) “Relatively rapid ecological changes are occurring in the sub-Antarctic region, but the changes are far less understood for the terrestrial ecosystem of continental Antarctica”. [005] Peter Convey, a terrestrial ecologist with the British Antarctic Survey concurred: “The Antarctic Peninsula is one of the three most rapidly warming regions on the planet, and Antarctica is central to research into regional and global environmental change”. [006] Another paper stresses this point for the Southern tip of South America, where our study will lead us: “At the present rate of ice recession, most, if not all of the cirque glaciers in Patagonia and Tierra del Fuego will disappear during the next two decades, and both valley glaciers and the Patagonian ice sheets will be severely reduced as well.” [005b]
In this perspective, Seppelt, like Slack (after Gignac), insists that “Bryophytes appear to be the key ecological markers, with vitality of the moss being indicative of soil moisture.” But he also notices that “Healthy, lichen-free bryophyte communities make up only a small proportion of the vegetation and are confined almost entirely to the wettest habitats.” [005] Convey confirms this statement: “This unique [Antarctic terrestrial] biota now faces the twin challenges of responding to the complex processes of climate change facing some parts of the continent, and the direct impacts associated with human occupation and activity.” [006] Like in the Northern scenario, he also stresses that “in many instances, this biota is likely to benefit, initially at least, from the current environmental changes, and there is an expectation of increased production, biomass, population size, community complexity, and colonisation.” But like in the Northern scenario again, these early benefits might be negated by further evolution: “However, the impacts of climate change may themselves be outweighed by other, direct, impacts of human activities, and in particular, the introduction of non-indigenous organisms from which until recently the terrestrial ecosystems of the continent have been protected.”
Again, like in the Northern scenario, the issues of biodiversity are key:
Antarctic terrestrial ecosystems are thought to be sensitive to environmental change. In the short- to mid-term, their responses to the types of environmental change trends being experienced in parts of the Antarctic may be positive, in the sense that relaxation of current environmental limits (particularly from low temperature and desiccation) will lead to greater biological productivity, population growth and local distribution expansion. However, a further widely accepted predicted consequence is for changes to distributions of indigenous species and of colonisation and invasion by non-indigenous species. [006]
However, in their afore cited synthesis, the Finnish bryologists mention that “reduction of bryophyte cover has also been reported in extreme environments of continental Antarctica where there is no resource competition between bryophytes and vascular plants (…) However, the authors suggest that the observed decline of bryophytes can be related to the active layer thickening, increase of solar radiation and decrease of ground- water availability.” But they also mention a key difference with the Northern scenario: “Even though no air warming has been observed in continental Antarctica, its ecosystem changes have occurred rapidly.” [008]
Both the thickening of the active layer and the absence of air warming were in fact addressed by a 2104 paper published by Italian scholars: “In continental Antarctica, in northern Victoria Land, the active layer thickened by 1 cm y−1 from 1996 to 2009 (…) Our data confirm on a longer time span (until 2012/13) the trend of stability of the mean annual air temperature (MAAT) already outlined by Chapman and Walsh (2007) for the period 1958–2002 (…) Despite the lack of air warming in continental Antarctica our data emphasize that ecosystem changes occurred rapidly, as they are already detectable in only 10 years.” [010]
Based on their study of Antarctic moss bank archives, Jessica Royles and Harrold Griffiths agreed: “Many of the eight factors identified by Fenton & Smith (1982) as being important for moss establishment in Antarctica, are sensitive to a changing climate, including length of growing season, reduction in permanent snow cover, substrate stability (extent of permafrost), wind speed, nutrient availability and water supply.” [011]
Again, like in the Northern scenario, “increasing temperature and precipitation in polar regions due to climate change (Chen et al. 2009) were predicted to result in increased bryophyte growth rates through increases in water availability and length of the growing season (Robinson et al. 2003).” [012] But these earlier predictions were then corrected to take into account that air temperature might not have been increasing in the Antarctic region (yet?): “Even though temperature patterns in this region remain unclear, a shift to either warmer or cooler conditions could have serious consequences for Antarctic vegetation. The majority of bryophyte species respond positively to warmer temperatures, suggesting that a rise in temperatures would generate more productivity and vice versa (…) On the other hand, too high a rise in temperature has been demonstrated to reduce bryophyte productivity.” [012]
The Finnish bryologists did include all these results into their conclusion: “Increase of temperature enhances nutrient turnover and will lead to dominance of fast-growing species over those with slower growth rate such as bryophytes (…) Climate-change induced decrease of bryophyte cover will undoubtedly threaten bryophyte diversity, as well as function of the whole ecosystems.” [008]
In other words, with the marked difference of a lack of observed increase of air temperature in the Southern regions so far, the scenario of evolution for the Antarctic bryophytes seems as grim there as it is for the Northern regions, reminding us that there is more than warming in climate change.
REFERENCES
[001] Gignac, L. Dennis (2001). Bryophytes as Indicators of Climate Change The Bryologist, 104(3) : 410-420
[002] Nancy G. Slack (2011). The Ecological Value of Bryophytes as Indicators of Climate Change. In Z. Tuba, N. Slack, & L. Stark (Eds.), Bryophyte Ecology and Climate Change (pp. 3-12). Cambridge: Cambridge University Press. doi:10.1017/CBO9780511779701.002
[003] Zolta N. Tuba (2011). Bryophyte Physiological Processes in a Changing Climate: An Overview. In Z. Tuba, N. Slack, & L. Stark (Eds.), Bryophyte Ecology and Climate Change (pp. 13-32). Cambridge: Cambridge University Press. doi:10.1017/CBO9780511779701.003
[004] Annika k. Jägerbrand, Robert G. Björk, Terry Callaghan, and Rodney D. Seppelt (2011). Effects of Climate Change on Tundra Bryophytes. In Z. Tuba, N. Slack, & L. Stark (Eds.), Bryophyte Ecology and Climate Change (pp. 211-236). Cambridge: Cambridge University Press. doi:10.1017/CBO9780511779701.003
[005] Rodney D. Seppelt (2011). Bryophytes and Lichens in a Changing Climate: An Antarctic Perspective. In Z. Tuba, N. Slack, & L. Stark (Eds.), Bryophyte Ecology and Climate Change (pp. 251-273). Cambridge: Cambridge University Press. doi:10.1017/CBO9780511779701.003
[005b] Reni Jorge (2010). The global climatic change in Patagonia and tierra del fuego since voyage of Charles Darwin until present times, Revista de la Asociacion Geologica Argentina 67(1):139-156.
[006] Convey, Peter (2011). Antarctic terrestrial biodiversity in a changing world. Polar Biology 34 : 1629 (2011).
[007] Désamoré, Aurélie et al. (2012). How do temperate bryophytes face the challenge of a changing environment? Lessons from the past and predictions for the future. Global Change Biology 18(9): 2915-2924.
[008] Xiaolan He, Kate S. He, Jaakko Hyvönen (2016). Will bryophytes survive in a warming world? Perspectives in Plant Ecology, Evolution and Systematics 19: 49–60.
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[010] Mauro Guglielmin, Michele Dalle Fratte and Nicoletta Cannone (2014). Permafrost Warming and Vegetation Changes in Continental Antarctica. Environmental Research Letters 9.
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[011] Jessica Royles, Harold Griffiths (2015). Invited review: climate change impacts in polar regions: lessons from Antarctic moss bank archives. Global Change Biology 21(3) : 1041-1057. http:// dx.doi.org/10.1111/gcb.12774 .
[012] Jessica Bramley-Alves, Diana H. King, Sharon A. Robinson, Rebecca E. Miller (2014). Dominating the Antarctic environment: bryophytes in a time of change. In: Hanson, D.T., Rice, S.K. (Eds.), Photosynthesis in Bryophytes and Early Land Plants, Advances in Photosynthesis and Respiration, 37: 309–324.
[013] Lily R. Lewis, Stefanie M. Ickert-Bond, Elisabeth M. Biersma, Peter Convey, Bernard Goffinet, Kristian Hassel, Hans (J.D.) Kruijer, Catherine La Farge, Jordan Metzgar, Michael Stech, Juan Carlos Villarreal, and Stuart F. McDaniel (2017). Future directions and priorities for Arctic bryophyte research. Arctic Science 3:475-497.
[014] Hedenäs, Lars (2019). On the frequency of northern and mountain genetic variants of widespread species: essential biodiversity information in a warmer world, Botanical Journal of the Linnean Society 191(4): 440–474.
[015] Vanderpoorten, Alain et al. (2020). Bryophytes are predicted to lag behind futureclimate change despite their high dispersal capacities. Nature Communications. 2020, 11:5601 | https://doi.org/10.1038/s41467-020-19410-8
[016] Paulo E. A. S. Câmara, Daiane Valente and Leopolodo G. Sancho (2020). Changes in the moss (Bryophyta) flora in the vicinity of the Spanish Juan Carlos I Station (Livingston island, Antarctica) over three decades, Polar Biology 43: 1745-1752.
[017] Mundim, Júlia V. et al. (2021). Small areas and small plants: Updates on Antarctic bryophytes. Acta Botanica Brasilica [online]. 35(4): 532-539 https://doi.org/10.1590/0102-33062020abb0431
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[018] Jairo Patiño, Irene Bisang, Bernard Goffinet, Lars Hedenäs, Stuart McDaniel, Silvia Pressel, Michael Stech, Claudine Ah-Peng, Ariel Bergamini, Richard T. Caners, D. Christine Cargill, Nils Cronberg, Jeffrey Duckett, Sarah Eppley, Nicole J. Fenton, Kirsten Fisher, Juana González-Mancebo, Mitsuyasu Hasebe, Jochen Heinrichs, Kristoffer Hylander, Michael S. Ignatov, Javier Martínez-Abaigar, Nagore G. Medina, Rafael Medina, Dietmar Quandt, Stefan A. Rensing, Karen Renzaglia, Matthew Renner, Rosa M. Ros, Alfons Schäfer-Verwimp, Juan Carlos Villarreal & Alain Vanderpoorten (2022). Unveiling the nature of a miniature world: a horizon scan of fundamental questions in bryology, Journal of Bryology, 44:1, 1-34, DOI:
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[019] H. Hespanhol, K. Cezón, J. Muñoz, R.G. Mateo, J. Gonçalves (2022). How vulnerable are bryophytes to climate change? Developing new species and community vulnerability indices, Ecological Indicators 136, 108643, https://doi.org/10.1016/j.ecolind.2022.108643 .
[020] Permin, A., Michelsen, A. & Rousk, K. (2022). Direct and indirect effects of warming on moss abundance and associated nitrogen fixation in subarctic ecosystems. Plant Soil 471: 343–358 https://doi.org/10.1007/s11104-021-05245-9