Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-26T15:06:35.089Z Has data issue: false hasContentIssue false

Lichen zonation on UK rocky seashores: a trait-based approach to delineating marine and maritime lichens

Published online by Cambridge University Press:  11 April 2023

Beth Tindall-Jones
Affiliation:
Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, UK School of Biological and Marine Sciences, University of Plymouth, Plymouth, UK
Michael Cunliffe
Affiliation:
Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, UK School of Biological and Marine Sciences, University of Plymouth, Plymouth, UK
Nathan Chrismas*
Affiliation:
Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, UK
*
Author for Correspondence: Nathan Chrismas. E-mail: natchr@mba.ac.uk

Abstract

Image of the first page of this content. For PDF version, please use the ‘Save PDF’ preceeding this image.'
Type
Short Communication
Copyright
Copyright © The Author(s), 2023. 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

Aptroot, A and Seaward, M (2003) Freshwater lichens. Fungal Diversity Research Series 10, 101110.Google Scholar
Boaventura, D, , P, da Fonseca L, Cancela and Hawkins, SJ (2002) Intertidal rocky shore communities of the continental Portuguese coast: analysis of distribution patterns. Marine Ecology 23, 6990.CrossRefGoogle Scholar
Brodo, IM and Sloan, NA (2004) Lichen zonation on coastal rocks in Gwaii Haanas National Park Reserve, Haida Gwaii (Queen Charlotte Islands), British Columbia. Canadian Field-Naturalist 118, 405424.CrossRefGoogle Scholar
Černajová, I, Schiefelbein, U and Škaloud, P (2022) Lichens from the littoral zone host diverse Ulvophycean photobionts. Journal of Phycology 58, 267280.10.1111/jpy.13234CrossRefGoogle ScholarPubMed
Chappuis, E, Terradas, M, Cefalì, ME, Mariani, S and Ballesteros, E (2014) Vertical zonation is the main distribution pattern of littoral assemblages on rocky shores at a regional scale. Estuarine, Coastal and Shelf Science 147, 113122.10.1016/j.ecss.2014.05.031CrossRefGoogle Scholar
Chrismas, NAM, Allen, R, Hollingsworth, AL, Taylor, JD and Cunliffe, M (2021) Complex photobiont diversity in the marine lichen Lichina pygmaea. Journal of the Marine Biological Association of the United Kingdom 101, 667674.CrossRefGoogle Scholar
Chu, FJ, Seaward, MRD and Hodgkiss, IJ (2000) Effects of wave exposure and aspect on Hong Kong supralittoral lichens. Lichenologist 32, 155170.CrossRefGoogle Scholar
Cordero, RJB and Casadevall, A (2017) Functions of fungal melanin beyond virulence. Fungal Biology Reviews 31, 99112.10.1016/j.fbr.2016.12.003CrossRefGoogle ScholarPubMed
Darienko, T and Pröschold, T (2017) Toward a monograph of non-marine Ulvophyceae using an integrative approach (molecular phylogeny and systematics of terrestrial Ulvophyceae II.). Phytotaxa 324, 141.CrossRefGoogle Scholar
Delmail, D, Grube, M, Parrot, D, Cook-Moreau, J, Boustie, J, Labrousse, P and Tomasi, S (2013) Halotolerance in lichens: symbiotic coalition against salt stress. In Ahmad, P, Azooz, MM and Prasad, MNV (eds), Ecophysiology and Responses of Plants under Salt Stress. New York: Springer, pp. 115148.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
Fletcher, A (1973 a) The ecology of marine (Littoral) lichens on some rocky shores of Anglesey. Lichenologist 5, 368400.CrossRefGoogle Scholar
Fletcher, A (1973 b) The ecology of maritime (Supralittoral) lichens on some rocky shores of Anglesey. Lichenologist 5, 401422.10.1017/S0024282973000460CrossRefGoogle Scholar
Françoise, LD, Holger, T, Marie-Laurence, A, David, D and Joël, B (2014) Oxidative stress regulation in lichens and its relevance for survival in coastal habitats. In Bourgougnon, N (ed.), Advances in Botanical Research: Sea Plants, Vol. 71. New York, London: Academic Press, pp. 467503.Google Scholar
Gasulla, F, Guéra, A, de los Ríos, A and Pérez-Ortega, S (2019) Differential responses to salt concentrations of lichen photobiont strains isolated from lichens occurring in different littoral zones. Plant and Fungal Systematics 64, 149162.10.2478/pfs-2019-0016CrossRefGoogle Scholar
Gostinčar, C, Muggia, L and Grube, M (2012) Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Frontiers in Microbiology 3, 390.CrossRefGoogle Scholar
Grube, M and Blaha, J (2005) Halotolerance and lichen symbioses. In Gunde-Cimerman, N, Oren, A and Plemenitaš, A (eds), Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya. Dordrecht: Springer Netherlands, pp. 471488.Google Scholar
Hawksworth, D (2000) Freshwater and marine lichen-forming fungi. Fungal Diversity 5, 17.Google Scholar
Hervé, M (2021) RVAideMemoire: Testing and Plotting Procedures for Biostatistics. R package [WWW resource] URL https://CRANR-projectorg/package=RVAideMemoireGoogle Scholar
Higgins, NF, Connan, S and Stengel, DB (2015) Factors influencing the distribution of coastal lichens Hydropunctaria maura and Wahlenbergiella mucosa. Marine Ecology 36, 14001414.10.1111/maec.12239CrossRefGoogle Scholar
Käffer, MI, Port, RK, Brito, JBG and Schmitt, JL (2021) Lichen functional traits and light influx in the analysis of environmental quality of subtropical riparian ecosystems. Ecological Indicators 125, 107510.CrossRefGoogle Scholar
Knowles, MC (1913) The maritime and marine lichens of Howth. Scientific Proceedings of the Royal Dublin Society 14, 79143.Google Scholar
Koch, NM, Matos, P, Branquinho, C, Pinho, P, Lucheta, F, de Azevedo Martins, SM and Vargas, VMF (2019) Selecting lichen functional traits as ecological indicators of the effects of urban environment. Science of The Total Environment 654, 705713.10.1016/j.scitotenv.2018.11.107CrossRefGoogle ScholarPubMed
Kogej, T, Stein, M, Volkmann, M, Gorbushina, AA, Galinski, EA and Gunde-Cimerman, N (2007) Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization. Microbiology 153, 42614273.CrossRefGoogle ScholarPubMed
Kosanić, M and Ranković, B (2019) Studies on antioxidant properties of lichen secondary metabolites. In Ranković, B (ed.), Lichen Secondary Metabolites: Bioactive Properties and Pharmaceutical Potential. Cham: Springer International Publishing, pp. 129153.CrossRefGoogle Scholar
Kranner, I, Beckett, R, Hochman, A and Nash, TH III (2008) Desiccation-tolerance in lichens: a review. Bryologist 111, 576593.CrossRefGoogle Scholar
Lange, OL, Büdel, B, Meyer, A and Kilian, E (1993) Further evidence that activation of net photosynthesis by dry cyanobacterial lichens requires liquid water. Lichenologist 25, 175189.10.1006/lich.1993.1025CrossRefGoogle Scholar
Lange, OL, Green, TGA, Reichenberger, H and Meyer, A (1996) Photosynthetic depression at high thallus water contents in lichens: concurrent use of gas exchange and fluorescence techniques with a cyanobacterial and a green algal Peltigera species. Botanica Acta 109, 4350.10.1111/j.1438-8677.1996.tb00868.xCrossRefGoogle Scholar
Lud, D, Huiskes, AHL and Ott, S (2001) Morphological evidence for the symbiotic character of Turgidosculum complicatulum Kohlm. & Kohlm. (= Mastodia tesselata Hook.f. & Harvey). Symbiosis 31, 141151.Google Scholar
Mafole, TC, Solhaug, KA, Minibayeva, FV and Beckett, RP (2019) Occurrence and possible roles of melanic pigments in lichenized ascomycetes. Fungal Biology Reviews 33, 159165.CrossRefGoogle Scholar
Máguas, C, Griffiths, H and Broadmeadow, MSJ (1995) Gas exchange and carbon isotope discrimination in lichens: evidence for interactions between CO2 -concentrating mechanisms and diffusion limitation. Planta 196, 95102.CrossRefGoogle Scholar
Martinez, Arbizu P (2020) pairwiseAdonis: Pairwise multilevel comparison using adonis. R package version 0.4. [WWW resource] URL https://github.com/pmartinezarbizu/pairwiseAdonisGoogle Scholar
Matos, P, Pinho, P, Aragón, G, Martínez, I, Nunes, A, Soares, AMVM and Branquinho, C (2015) Lichen traits responding to aridity. Journal of Ecology 103, 451458.CrossRefGoogle Scholar
McEvoy, M, Nybakken, L, Solhaug, KA and Gauslaa, Y (2006) UV triggers the synthesis of the widely distributed secondary lichen compound usnic acid. Mycological Progress 5, 221229.10.1007/s11557-006-0514-9CrossRefGoogle Scholar
McEvoy, M, Gauslaa, Y and Solhaug, KA (2007) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytologist 175, 271282.CrossRefGoogle ScholarPubMed
Mohr, F, Ekman, S and Heegaard, E (2004) Evolution and taxonomy of the marine Collemopsidium species (lichenized Ascomycota) in north-west Europe. Mycological Research 108, 515532.10.1017/S095375620400992XCrossRefGoogle ScholarPubMed
Money, NP, Caesar-TonThat, TC, Frederick, B and Henson, JM (1998) Melanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis. Fungal Genetics and Biology 24, 240251.CrossRefGoogle ScholarPubMed
Muggia, L, Gueidan, C, Knudsen, K, Perlmutter, G and Grube, M (2013) The lichen connections of black fungi. Mycopathologia 175, 523535.CrossRefGoogle ScholarPubMed
Muggia, L, Quan, Y, Gueidan, C, Al-Hatmi, AMS, Grube, M and de Hoog, S (2021) Sequence data from isolated lichen-associated melanized fungi enhance delimitation of two new lineages within Chaetothyriomycetidae. Mycological Progress 20, 911927.10.1007/s11557-021-01706-8CrossRefGoogle Scholar
Nascimbene, J and Nimis, PL (2006) Freshwater lichens of the Italian Alps: a review. Annales de Limnologie – International Journal of Limnology 42, 2732.10.1051/limn/2006003CrossRefGoogle Scholar
Nimis, PL, Martellos, S, Chiarucci, A, Ongaro, S, Peplis, M, Pittao, E and Nascimbene, J (2020) Exploring the relationships between ecology and species traits in cyanolichens: a case study on Italy. Fungal Ecology 47, 100950.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL and Solymos, P (2018) vegan: Community Ecology Package. R package version 2.5-2. [WWW resource] URL http://CRAN.R-project.org/package=veganGoogle Scholar
Orange, A (2012) Semi-cryptic marine species of Hydropunctaria (Verrucariaceae, lichenized Ascomycota) from north-west Europe. Lichenologist 44, 299320.CrossRefGoogle Scholar
Ortiz-Álvarez, R, de los Ríos, A, Fernández-Mendoza, F, Torralba-Burrial, A and Pérez-Ortega, S (2015) Ecological specialization of two photobiont-specific maritime cyanolichen species of the genus Lichina. PLoS ONE 10, e0132718.CrossRefGoogle ScholarPubMed
Palmqvist, K (1993) Photosynthetic CO2-use efficiency in lichens and their isolated photobionts: the possible role of a CO2-concentrating mechanism. Planta 191, 4856.CrossRefGoogle Scholar
Pentecost, A (1987) The lichen flora of Gwynedd. Lichenologist 19, 97166.CrossRefGoogle Scholar
Prieto, M, Martínez, I, Aragón, G and Verdú, M (2017) Phylogenetic and functional structure of lichen communities under contrasting environmental conditions. Journal of Vegetation Science 28, 871881.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [WWW resource] URL https://www.R-project.org/Google Scholar
Raven, JA, Johnston, AM, Handley, LL and McInroy, SG (1990) Transport and assimilation of inorganic carbon by Lichina pygmaea under emersed and submersed conditions. New Phytologist 114, 407417.10.1111/j.1469-8137.1990.tb00408.xCrossRefGoogle ScholarPubMed
Ravishankar, JP, Muruganandam, V and Suryanarayanan, TS (1995) Isolation and characterization of melanin from a marine fungus. Botanica Marina 38, 413416.CrossRefGoogle Scholar
Ryan, BD (1988) Zonation of lichens on a rocky seashore on Fidalgo Island, Washington. Bryologist 91, 167180.CrossRefGoogle Scholar
Sheard, JW (1968) The zonation of lichens on three rocky shores of Inishowen, Co. Donegal. Proceedings of the Royal Irish Academy, Section B: Biological, Geological and Chemical Science 66, 101112.Google Scholar
Sheard, JW and Ferry, BW (1967) The lichen flora of the Isle of May. Transactions of the Botanical Society of Edinburgh 40, 268282.CrossRefGoogle Scholar
Smith, CW, Aptroot, A, Coppins, BJ, Fletcher, A, Gilbert, OL, James, PW and Wolseley, PA (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Smith, JMB and Simpson, RD (1985) Biotic zonation on rocky shores of Heard Island. Polar Biology 4, 8994.CrossRefGoogle Scholar
Søchting, U and Gjelstrup, P (1985) Lichen communities and the associated fauna on a rocky sea shore on Bornholm in the Baltic. Ecography 8, 6675.CrossRefGoogle Scholar
Sonina, AV (2012) Epilithic lichens and their morphological adaptations to the conditions of the White and Barents Seas coast (Russian Arctic). Czech Polar Reports 2: 109116.CrossRefGoogle Scholar
Sonina, AV and Androsova, VI (2020) Coastal lichens. In Grigore, MN (ed.), Handbook of Halophytes. Cham: Springer International Publishing, pp. 122.Google Scholar
Thüs, H, Muggia, L, Pérez-Ortega, S, Favero-Longo, SE, Joneson, S, O'Brien, H, Nelsen, MP, Duque-Thüs, R, Grube, M, Friedl, T, et al. (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). European Journal of Phycology 46, 399415.CrossRefGoogle Scholar
Vail, CA and Walker, AK (2021) Vertical zonation of some crustose lichens (Verrucariaceae) in Bay of Fundy littoral zones of Nova Scotia. Northeastern Naturalist 28, 311326.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.CrossRefGoogle Scholar
Wolseley, PA, James, PW, Coppins, BJ and Purvis, OW (1996) Lichens of Skomer Island, West Wales. Lichenologist 28, 543570.CrossRefGoogle Scholar
Supplementary material: PDF

Tindall-Jones et al. supplementary material

Figure S1

Download Tindall-Jones et al. supplementary material(PDF)
PDF 1.8 MB