Hostname: page-component-5d59c44645-zlj4b Total loading time: 0 Render date: 2024-02-21T08:37:02.487Z Has data issue: false hasContentIssue false

The globally threatened epiphytic cyanolichen Erioderma pedicellatum depends on a rare combination of habitat factors

Published online by Cambridge University Press:  31 March 2022

Alexander R. Nilsson
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
Knut Asbjørn Solhaug
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
Yngvar Gauslaa*
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
*
Author for correspondence: Yngvar Gauslaa. E-mail: yngvar.gauslaa@nmbu.no

Abstract

Lichen extinction occurs at rapid rates as a result of human activity, although species could potentially be rescued by conservation management based on ecophysiological knowledge. The boreal old forest cyanolichen Erioderma pedicellatum currently occurs in few sites worldwide. To protect it from extinction, it is essential to learn more about it. The last remaining good European site is a canyon with a waterfall, in a low-rainfall region of Norway. Here, a spatially restricted population of 1500–2000 thalli dominates the epiphytic vegetation of a small number of Picea abies canopies. We were able to document that 1) E. pedicellatum grew on thin branches with higher bark pH than is normal for P. abies in a canyon that provided an unusual combination of very high light, high air humidity, and cool temperatures in the growing season. However, the species did not inhabit the main waterfall spray zone. 2) Erioderma pedicellatum had a high light saturation point, high CO2 uptake at high light (≥ 600 μmol m−2 s−1) and cool temperatures (5–20 °C), and experienced strong suprasaturation depression of photosynthesis when fully hydrated. 3) It showed good tolerance of desiccation and high light; it was slightly more tolerant than the morphologically similar, but more common cyanolichen Pectenia plumbea. 4) The European population in its sunny habitat had higher water holding capacity than previously recorded in slightly shaded rainforest populations in Newfoundland, consistent with acclimation to compensate for high evaporative demands. Understanding the ecological niche and responses to critical environmental factors is essential for action plans to avoid extinction of E. pedicellatum. Methods used in this study could also be applicable for ecological understanding of other threatened lichen species.

Type
Standard Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the British Lichen Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahlner, S (1948) Utbredningstyper bland Nordiska barrträdslavar. Acta Phytogeographica Suecica 22, 1257.Google Scholar
Ahlner, S (1954) Värmlands märkligaste lav. In Magnusson, NH and Curry-Lindahl, K (eds), Natur i Värmland. Stockholm: Bokförlaget Svensk Natur, pp. 99102.Google Scholar
Alam, MA, Gauslaa, Y and Solhaug, KA (2015) Soluble carbohydrates and relative growth rates in chloro-, cyano- and cephalolichens: effects of temperature and nocturnal hydration. New Phytologist 208, 750762.CrossRefGoogle ScholarPubMed
Asplund, J and Wardle, DA (2017) How lichens impact on terrestrial community and ecosystem properties. Biological Reviews 92, 17201738.CrossRefGoogle ScholarPubMed
Barkman, JJ (1958) Phytosociology and Ecology of Cryptogamic Epiphytes. Assen: van Gorcum.Google Scholar
Beckett, RP, Minibayeva, F, Solhaug, KA and Roach, T (2021) Photoprotection in lichens: adaptations of photobionts to high light. Lichenologist 53, 2133.CrossRefGoogle Scholar
Bidussi, M, Gauslaa, Y and Solhaug, KA (2013 a) Prolonging the hydration and active metabolism from light periods into nights substantially enhances lichen growth. Planta 237, 13591366.CrossRefGoogle ScholarPubMed
Bidussi, M, Goward, T and Gauslaa, Y (2013 b) Growth and secondary compound investments in the epiphytic lichens Lobaria pulmonaria and Hypogymnia occidentalis transplanted along an altitudinal gradient in British Columbia. Botany 91, 621630.CrossRefGoogle Scholar
Björk, CR, Goward, T and Spribille, T (2009) New records and range extensions of rare lichens from waterfalls and sprayzones in inland British Columbia, Canada. Evansia 26, 219224.CrossRefGoogle Scholar
Büdel, B, Becker, U, Porembski, S and Barthlott, W (1997) Cyanobacteria and cyanobacterial lichens from inselbergs of the Ivory Coast, Africa. Botanica Acta 110, 458465.CrossRefGoogle Scholar
Cameron, R (2009) Are non-native gastropods a threat to endangered lichens? Canadian Field-Naturalist 123, 169171.CrossRefGoogle Scholar
Cameron, R, Goudie, I and Richardson, D (2013 a) Habitat loss exceeds habitat regeneration for an IUCN flagship lichen epiphyte: Erioderma pedicellatum. Canadian Journal of Forest Research (Revue Canadienne de Recherche Forestiere) 43, 10751080.CrossRefGoogle Scholar
Cameron, RP, Neily, T and Clapp, H (2013 b) Forest harvesting impacts on mortality of an endangered lichen at the landscape and stand scales. Canadian Journal of Forest Research (Revue Canadienne de Recherche Forestiere) 43, 507511.CrossRefGoogle Scholar
Colesie, C, Green, TGA, Raggio, J and Büdel, B (2016) Summer activity patterns of Antarctic and high alpine lichen-dominated biological soil crusts – similar but different? Arctic, Antarctic and Alpine Research 48, 449460.CrossRefGoogle Scholar
Cornejo, C, Nelson, PR, Stepanchikova, I, Himelbrant, D, Jørgensen, PM and Scheidegger, C (2016) Contrasting pattern of photobiont diversity in the Atlantic and Pacific populations of Erioderma pedicellatum (Pannariaceae). Lichenologist 48, 275291.CrossRefGoogle Scholar
Cornelissen, JHC, Callaghan, TV, Alatalo, JM, Michelsen, A, Graglia, E, Hartley, AE, Hik, DS, Hobbie, SE, Press, MC, Robinson, CH, et al. (2001) Global change and arctic ecosystems: is lichen decline a function of increases in vascular plant biomass? Journal of Ecology 89, 984994.CrossRefGoogle Scholar
Ellis, CJ, Asplund, J, Benesperi, R, Branquinho, C, Di Nuzzo, L, Hurtado, P, Martínez, I, Matos, P, Nascimbene, J, Pinho, P, et al. (2021) Functional traits in lichen ecology: a review of challenge and opportunity. Microorganisms 9, 766.CrossRefGoogle ScholarPubMed
Elmendorf, SC, Henry, GHR, Hollister, RD, Björk, RG, Bjorkman, AD, Callaghan, TV, Collier, LS, Cooper, EJ, Cornelissen, JHC, Day, TA, et al. (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecology Letters 15, 164175.CrossRefGoogle ScholarPubMed
Falkengren-Grerup, U (1986) Soil acidification and vegetational changes in deciduous forest in southern Sweden. Oecologia 70, 339347.CrossRefGoogle Scholar
Färber, L, Solhaug, KA, Esseen, P-A, Bilger, W and Gauslaa, Y (2014) Sunscreening fungal pigments influence the vertical gradient of pendulous lichens in boreal forest canopies. Ecology 95, 14641471.CrossRefGoogle ScholarPubMed
Gauslaa, Y (1985) The ecology of Lobarion pulmonariae and Parmelion caperatae in Quercus dominated forests in south-west Norway. Lichenologist 17, 117140.CrossRefGoogle Scholar
Gauslaa, Y (1995) The Lobarion, an epiphytic community of ancient forests threatened by acid rain. Lichenologist 27, 5976.CrossRefGoogle Scholar
Gauslaa, Y (2014) Rain, dew, and humid air as drivers of lichen morphology, function and spatial distribution in epiphytic lichens. Lichenologist 46, 116.CrossRefGoogle Scholar
Gauslaa, Y and Arsenault, A (2020) The cyanolichens Erioderma pedicellatum and Coccocarpia palmicola need much more than a dewfall to fill their water holding capacity. Flora 269, 151648.CrossRefGoogle Scholar
Gauslaa, Y and Coxson, D (2011) Interspecific and intraspecific variations in water storage in epiphytic old forest foliose lichens. Botany 89, 787798.CrossRefGoogle Scholar
Gauslaa, Y and Goward, T (2012) Relative growth rates of two epiphytic lichens, Lobaria pulmonaria and Hypogymnia occidentalis, transplanted within and outside of Populus dripzones. Botany 90, 954965.CrossRefGoogle Scholar
Gauslaa, Y and Goward, T (2020) Melanic pigments and canopy-specific elemental concentration shape growth rates of the lichen Lobaria pulmonaria in unmanaged mixed forest. Fungal Ecology 47, 100984.CrossRefGoogle Scholar
Gauslaa, Y and Holien, H (1998) Acidity of boreal Picea abies-canopy lichens and their substratum, modified by local soils and airborne acidic depositions. Flora 193, 249257.CrossRefGoogle Scholar
Gauslaa, Y and Solhaug, KA (1996) Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stands. Functional Ecology 10, 344354.CrossRefGoogle Scholar
Gauslaa, Y and Solhaug, KA (1998) The significance of thallus size for the water economy of the cyanobacterial old-forest lichen Degelia plumbea. Oecologia 116, 7684.CrossRefGoogle ScholarPubMed
Gauslaa, Y, Coxson, DS and Solhaug, KA (2012) The paradox of higher light tolerance during desiccation in rare old forest cyanolichens than in more widespread co-occurring chloro- and cephalolichens. New Phytologist 195, 812822.CrossRefGoogle ScholarPubMed
Gauslaa, Y, Solhaug, KA and Longinotti, S (2017) Functional traits prolonging photosynthetically active periods in epiphytic cephalolichens during desiccation. Environmental and Experimental Botany 141, 8391.CrossRefGoogle Scholar
Gauslaa, Y, Goward, T and Pypker, T (2020) Canopy settings shape elemental composition of the epiphytic lichen Lobaria pulmonaria in unmanaged conifer forests. Ecological Indicators 113, 106294.CrossRefGoogle Scholar
Gauslaa, Y, Goward, T and Asplund, J (2021) Canopy throughfall links canopy epiphytes to terrestrial vegetation in pristine conifer forests. Fungal Ecology 52, 101075.CrossRefGoogle Scholar
Goward, T and Arsenault, A (2000) Cyanolichen distribution in young unmanaged forests: a dripzone effect? Bryologist 103, 2837.CrossRefGoogle Scholar
Greenspan, L (1977) Humidity fixed points of binary saturated aqueous solutions. Journal of Research of the National Bureau of Standards – A, Physics and Chemistry 81, 8996.CrossRefGoogle Scholar
Hauck, M and Spribille, T (2002) The Mn/Ca and Mn/Mg ratios in bark as possible causes for the occurrence of Lobarion lichens on conifers in the dripzone of Populus in western North America. Lichenologist 34, 527532.CrossRefGoogle Scholar
Holien, H (2015) Faggrunnlag til handlingsplan for fire lavarter i boreal regnskog. Høgskolen i Nord-Trøndelag Utredning 177, 159.Google Scholar
Holien, H and Tønsberg, T (1996) Boreal regnskog i Norge - habitater for trøndelagselementets lavarter. Blyttia 54, 157177.Google Scholar
Honegger, R (2003) The impact of different long-term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biology 5, 324330.CrossRefGoogle Scholar
IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-1. [WWW resource] URL https://www.iucnredlist.org/ [Accessed 8 April 2021].Google Scholar
Jørgensen, PM (1990) Trønderlav (Erioderma pedicellatum) – Norges mest gåtefulle plante? Blyttia 48, 119123.Google Scholar
Jørgensen, PM (2000) Survey of the lichen family Pannariaceae on the American continent, north of Mexico. Bryologist 103, 670704.CrossRefGoogle Scholar
Kranner, I, Beckett, RP, Hochman, A and Nash, TH III (2008) Desiccation-tolerance in lichens: a review. Bryologist 111, 576593.CrossRefGoogle Scholar
Lambers, H, Oliveira, RS (2019) Photosynthesis, respiration, and long-distance transport: respiration. In Plant Physiological Ecology. Cham, Switzerland: Springer International, pp. 115-172.CrossRefGoogle Scholar
Lang, SI, Cornelissen, JHC, Shaver, GR, Ahrens, M, Callaghan, TV, Molau, U, ter Braak, CJF, Hölzer, A and Aerts, R (2012) Arctic warming on two continents has consistent negative effects on lichen diversity and mixed effects on bryophyte diversity. Global Change Biology 18, 10961107.CrossRefGoogle Scholar
Lange, OL (1969) Die funktionellen Anpassungen der Flechten an die ökologischen Bedingungen arider Gebiete. Berichte der Deutschen Botanischen Gesellschaft 82, 322.Google Scholar
Lange, OL (2003) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation: III. Diel, seasonal, and annual carbon budgets. Flora 198, 277292.Google Scholar
Lange, OL and Kilian, E (1985) Reaktiverung der Photosynthese trockener Flechten durch Wasserdampfaufnahme aus dem Luftraum: Artsspezifisch unterschiedliches Verhalten. Flora 176, 723.CrossRefGoogle Scholar
Lange, OL, Kilian, E and Ziegler, H (1986) Water vapor uptake and photosynthesis in lichens: performance differences in species with green and blue-green algae as phycobionts. Oecologia 71, 104110.CrossRefGoogle ScholarPubMed
Lange, OL, Büdel, B, Heber, U, Meyer, A, Zellner, H and Green, TGA (1993) Temperate rainforest lichens in New Zealand: high thallus water content can severely limit photosynthetic CO2 exchange. Oecologia 95, 303313.CrossRefGoogle ScholarPubMed
Lange, OL, Green, TGA, Reichenberger, H and Meyer, A (1996) Photosynthetic depression at high thallus water content in lichens: concurrent use of gas exchange and fluorescence techniques with a cyanobacterial and a green algal Peltigera species. Botanica Acta 109, 4350.CrossRefGoogle Scholar
Lange, OL, Belnap, J and Reichenberger, H (1998) Photosynthesis of the cyanobacterial soil-crust lichen Collema tenax from arid lands in southern Utah, USA: role of water content on light and temperature responses of CO2 exchange. Functional Ecology 12, 195202.CrossRefGoogle Scholar
Lange, OL, Büdel, B, Meyer, A, Zellner, H and Zotz, G (2000) Lichen carbon gain under tropical conditions: water relations and CO2 exchange of three Leptogium species of a lower montane rainforest in Panama. Flora 195, 172190.CrossRefGoogle Scholar
Larsen, HME and Rasmussen, HN (2021) Bark extract influence on spore germination in corticolous lichen Xanthoria parietina in vitro. Mycological Progress 20, 313323.CrossRefGoogle Scholar
Merinero, S, Hilmo, O and Gauslaa, Y (2014) Size is a main driver for hydration traits in cyano- and cephalolichens of boreal rainforest canopies. Fungal Ecology 7, 5966.CrossRefGoogle Scholar
Moen, A (1999) National Atlas of Norway: Vegetation. Hønefoss: Norwegian Mapping Authority.Google Scholar
Nilsson, SI and Tyler, G (1995) Acidification-induced chemical changes of forest soils during recent decades – a review. Ecological Bulletins 44, 5464.Google Scholar
Odland, A, Birks, HH, Botnen, A, Tønsberg, T and Vevle, O (1991) Vegetation change in the spray zone of a waterfall following river regulation in Aurland, Western Norway. Regulated Rivers: Research and Management 6, 147162.CrossRefGoogle Scholar
Palmqvist, K (2000) Carbon economy in lichens. New Phytologist 148, 1136.CrossRefGoogle ScholarPubMed
Penn, CJ and Camberato, JJ (2019) A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 9, 120.CrossRefGoogle Scholar
Phinney, NH, Solhaug, KA and Gauslaa, Y (2018) Rapid resurrection of chlorolichens in humid air: specific thallus mass drives rehydration and reactivation kinetics. Environmental and Experimental Botany 148, 184191.CrossRefGoogle Scholar
Phinney, NH, Solhaug, KA and Gauslaa, Y (2019) Photobiont-dependent humidity threshold for chlorolichen photosystem II activation. Planta 250, 20232031.CrossRefGoogle ScholarPubMed
Pintado, A, Valladares, F and Sancho, LG (1997) Exploring phenotypic plasticity in the lichen Ramalina capitata: morphology, water relations and chlorophyll content in north- and south-facing populations. Annals of Botany 80, 345353.CrossRefGoogle Scholar
Rasband, WS (2014) ImageJ. US National Institutes of Health. [WWW resource] URL http://imagej.nih.gov/ij/Google Scholar
Reiso, S and Hofton, TH (2006) Trønderlav Erioderma pedicellatum og fossefiltlav Fuscopannaria confusa funnet i Hedmark. Blyttia 64, 8388.Google Scholar
Richardson, DHS and Cameron, RP (2004) Cyanolichens: their response to pollution and possible management strategies for their conservation in northeastern North America. Northeastern Naturalist 11, 122.CrossRefGoogle Scholar
Richardson, SJ, Peltzer, DA, Allen, RB, McGlone, MS and Parfitt, RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139, 267276.CrossRefGoogle ScholarPubMed
Rose, F (1988) Phytogeographical and ecological aspects of Lobarion communities in Europe. Botanical Journal of the Linnean Society 96, 6979.CrossRefGoogle Scholar
Sancho, LG, de la Torre, R, Horneck, G, Ascaso, C, de los Rios, A, Pintado, A, Wierzchos, J and Schuster, M (2007) Lichens survive in space: results from the 2005 LICHENS experiment. Astrobiology 7, 443454.CrossRefGoogle ScholarPubMed
Scheidegger, C (Lichen Specialist Group) (2003) Erioderma pedicellatum. The IUCN Red List of Threatened Species. eT43995A10839336 [WWW resource] URL http://dx.doi.org/10.2305/IUCN.UK.2003.RLTS.T43995A10839336.enCrossRefGoogle Scholar
Schlensog, M, Schroeter, B and Green, TGA (2000) Water dependent photosynthetic activity of lichens from New Zealand: differences in the green algal and the cyanobacterial thallus parts of photosymbiodemes. Bibliotheca Lichenologica 75, 149160.Google Scholar
Solhaug, KA, Asplund, J and Gauslaa, Y (2021) Apparent electron transport rate – a non-invasive proxy of photosynthetic CO2 uptake in lichens. Planta 253, 14.CrossRefGoogle Scholar
Spribille, T (2018) Relative symbiont input and the lichen symbiotic outcome. Current Opinion in Plant Biology 44, 5763.CrossRefGoogle ScholarPubMed
Stehn, SE, Nelson, PR, Roland, CA and Jones, JR (2013) Patterns in the occupancy and abundance of the globally rare lichen Erioderma pedicellatum in Denali National Park and Preserve, Alaska. Bryologist 116, 214.CrossRefGoogle Scholar
Stofer, S, Bergamini, A, Aragón, G, Carvalho, P, Coppins, BJ, Davey, S, Dietrich, M, Farkas, E, Kärkkäinen, K, Keller, C, et al. (2006) Species richness of lichen functional groups in relation to land use intensity. Lichenologist 38, 331353.CrossRefGoogle Scholar
Tagirdzhanova, G, Stepanchikova, IS, Himelbrant, DE, Vyatkina, MP, Dyomina, AV, Dirksen, VG and Scheidegger, C (2019) Distribution and assessment of the conservation status of Erioderma pedicellatum in Asia. Lichenologist 51, 575585.CrossRefGoogle Scholar
Tønsberg, T, Gauslaa, Y, Haugan, R, Holien, H and Timdal, E (1996) The threatened macrolichens of Norway – 1995. Sommerfeltia 23, 1283.CrossRefGoogle Scholar
Tørseth, K and Manø, S (1996) Overvåkning av langtransportert forurenset luft og nedbør. Atmosfærisk tilførsel, 1996. NILU OR 33/97. Kjeller: Norwegian Institute of Air Research.Google Scholar
Ås Hovind, AB, Phinney, NH and Gauslaa, Y (2020) Functional trade-off of hydration strategies in old forest epiphytic cephalolichens. Fungal Biology 124, 903913.CrossRefGoogle ScholarPubMed