The editor’s choice for our February issue is “Loss of nitrogen fixing capacity in a montane lichen is linked to increased nitrogen deposition” by Peter Crittenden et al., which is part of a Special Feature on ‘Leveraging Natural History Collections to Understand the Impacts of Global Change‘. Here, Associate Editor Frank Gilliam discusses the importance of this research:
Underseen, underappreciated components of terrestrial ecosystems
As denizens of some of the more stressful environments of the biosphere, lichens can easily be overlooked—both literally and figuratively—in terrestrial landscapes. Forming physically tight bonds with their substrates, usually bare rocks, their often mottled coloration and pattern can render them almost indistinguishable from those substrates (Allen and Lendemer 2022). By contrast, they represent an important biogeochemical flux of availably energy and nutrients to ecosystems sorely lacking in both (Palmqvist 2000). Paradoxically, then, they have an essential role in these environments that is notably disproportionate to their minimal stature. Although all lichens are important in this context, those whose symbionts are cyanobacteria represent a major flux of nitrogen (N) via N2-fixation.
Lichens as canaries in the coal mine
Because of their growth form as a mutualistic balance between a fungus and algal symbiont wherein they are exposed to the dynamic nature of the atmosphere (including gaseous chemistry and wet and dry deposition), lichens have been used as biological indicators of air pollution, especially N and sulfur (S)—the proverbial canaries in the coal mine (Geiser et al. 2019). Considerable experimental work has demonstrated that excess N inhibits N2-fixation in a variety of cyanobacteria, both free-living and lichenized strains (Kytöviita & Crittenden 1994). What has been missing among such studies is empirical evidence that this response (1) occurs at the landscape scale of gradients in N deposition and (2) has occurred historically in N-impacted regions.
An excellent combination of investigative techniques
This gap in our understanding of lichen ecology in the context of pollutant (especially N) effects has been bridged quite admirably by the Editor’s Choice in this issue of Journal of Ecology, “Loss of nitrogen fixing capacity in a montane lichen is linked to increased nitrogen deposition,” by Peter D. Crittenden, Christopher J. Ellis, Rognvald I. Smith, Wolfgang Wanek, and Barry Thornton. In their study, the authors deftly integrated several approaches to address this subject, including (1) direct sampling of lichen material from 12 sites spanning much of the eastern side of Great Britain that represents a gradient in virtually all chemical and physical forms of atmospheric N deposition, (2) analysis for concentrations of total N and δ15N and activity of nitrogenase (the enzyme involved in N2-fixation) in lichen biomass, and (3) direct examination of archived lichen specimens in five global herbaria for structural characteristics, in particular the presence/absence of cephalodia, the nodules produced in N2-fixing lichens wherein fixation takes place. Add to the mix that two contrasting lichen species—Stereocaulon vesuvianum (N2-fixing) and Parmelia saxatilis (non-N2-fixing)—co-occur at these sites and were sampled together, and you have a quasi-treatment/control design along the gradient in N deposition.
Brief sidebar—the intrinsic value of herbaria
As an aside, at a time when the very existence of herbaria has been under attack by university administrations who misguidedly question their intrinsic worth, Crittenden et al. (2022) is yet another example of why herbaria are essential. We have learned a great deal from the direct use of archived specimens of a wide variety of plant species, including changes in stomatal density to increased atmospheric CO2 (Woodward 1987), climate change-driven alterations of plant phenology (Miller et al. 2021), and long-term landscapes-scale changes in N availability (Tang et al. 2022), just to name a few.
The results are in—and quite clear
Crittenden et al. (2022) provide clear evidence that excess N diminishes N2-fixation in S. vesuvianum, based on strong negative correlations of cephalodia and 15N concentrations with rates of N deposition. They further found an apparent threshold of 8-9 kg N ha-1 yr-1 (especially as dry-deposited NHy), beyond which cephalodia were consistently absent. Similar negative correlations of 15N in P. saxatilis also suggest that lichens do, under these conditions, take up N from the atmosphere, wherein pollutant N is largely depleted in 15N. They further demonstrated, via herbarium evidence, this is a relatively recent phenomenon. That is, cephalodia were consistently present in herbarium specimens of S. vesuvianum in the 19th century, with absence not arising until the period of 1900—1940.
A look to the future
Appropriately, Crittenden et al. (2022) ends with a look to the future, one in which the problem they investigate—chronically elevated N deposition—is abating in many regions of the world, including Europe (Schmitz et al. 2019). Gilliam et al. (2019) suggested that recovery of impacted terrestrial ecosystems may follow a hysteretic model, wherein there may be considerable time lags in response to decreased N deposition. Crittenden et al. (2022) conclude that this may be the case for the recovery of N2-fixation in lichens.
References
Allen, J.L., & Lendemer, J.C. (2022). A call to reconceptualize lichen symbioses. Trends in Ecology & Evolution, 37, 582-589.
Geiser, L. H., Nelson, P. R., Jovan, S. E., Root, H. T., & Clark, C. M. (2019). Assessing ecological risks from atmospheric deposition of nitrogen and sulfur to US forests using epiphytic macrolichens. Diversity, 11, 87. https://doi.org/10.3390/d1106 0087
Gilliam, F. S., Burns, D. A., Driscoll, C. T., Frey, S. D., Lovett, G. M., & Watmough, S. A. (2019). Decreased atmospheric nitrogen deposition in eastern North America: Predicted responses of forest ecosystems. Environmental Pollution, 244, 560–574. https://doi.org/10.1016/j.envpol.2018.09.135
Kytöviita, M.-M., & Crittenden, P. D. (1994). Effects of simulated acid rain on nitrogenase activity (acetylene reduction) in the lichen Stereocaulon paschale (L.) Hoffm., with special reference to nutritional aspects. New Phytologist, 128, 263–271. https://doi.org/10.1111/j.1469-8137.1994.tb040 10.x
Miller, T.K., Gallinat, A.S., Smith, L.C., & Primack, R.B. (2021). Comparing fruiting phenology across two historical datasets: Thoreau’s observations and herbarium specimens. Annals of Botany, 128, 159-170.
Palmqvist, K. (2000). Carbon economy in lichens. New Phytologist, 148, 11-36.
Schmitz, A., Sanders, T., Bolte, A., Bussotti, F., Dirnböck, T., Johnson, J., Peñuelas, J., Pollastrini, M., Prescher, A.-K., Sardans, J., Verstraeten, A., de Vries, W. (2019). Responses of forest ecosystems in Europe to decreasing nitrogen deposition. Environmental Pollution, 244, 980–994.
Tang, S., Liu, J., Gilliam, F.S., Hietz, P., Wang, Z., Lu, X., Zeng, F., Wen, D., Hou E., Lai, Y., Fang, Y., Tu, Y., Xi, D., Huang, Z., Zhang, D., Wang, R, Kuang, Y. (2022). Drivers of foliar 15N trends in southern China over the last century. Global Change Biology, 28, 5441-5452.
Woodward, F. I. (1987). Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature, 327, 617–618.
