Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-16T21:45:56.467Z Has data issue: false hasContentIssue false

The genus Lobariella (Ascomycota: Lobariaceae) in Hawaii: late colonization, high inferred endemism and three new species resulting from “micro-radiation”

Published online by Cambridge University Press:  14 November 2017

Robert LÜCKING
Affiliation:
Botanic Garden and Botanical Museum, Königin-Luise-Straße 6–8, 14195 Berlin, Germany. Email: r.luecking@bgbm.org
Bibiana MONCADA
Affiliation:
Licenciatura en Biología, Universidad Distrital Francisco José de Caldas, Cra. 4 No. 26B-54, Torre de Laboratorios, Herbario, Bogotá, Colombia; Research Associate, Integrative Science and Collections, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA
Clifford W. SMITH
Affiliation:
Oahu Army Natural Resources Program, 3190 Maile Way, St. John Hall Room #409, Honolulu, HI 96822, USA

Abstract

We assessed the taxonomy and phylogenetic relationships of Hawaiian species of the neotropical genus Lobariella. A single species was previously reported from the archipelago, the widespread neotropical L. crenulata. We targeted three loci of the mitochondrial and nuclear ribosomal rDNA gene cistron (mtSSU, nuLSU, ITS) and also performed a molecular clock analysis. Our results show that L. crenulata s. str. is seemingly present in the archipelago based on older herbarium collections. However, Hawaiian Lobariella includes three additional, presumably endemic, species unrelated to L. crenulata and new to science: L. flynniana Lücking, Moncada & C. W. Sm., with richly branched marginal phyllidia giving the thallus a fruticose appearance; L. robusta Lücking, Moncada & C. W. Sm., with a rather thick thallus and abundant, large, laminal phyllidia; and L. sandwicensis Lücking, Moncada & C. W. Sm., with a delicate thallus producing apothecia. Lobariella flynniana represents a novel morphotype within the genus, thus far known only from Hawaii. All three species are very closely related, forming a well-supported, monophyletic clade in spite of their morphological differences, suggesting local micro-radiation. Molecular clock analysis indicates that this clade colonized the islands between 1–8 mya and diverged between 0–2 mya. We interpret recent colonization as one of the main reasons why this clade has not diversified further.

Type
Articles
Copyright
© British Lichen Society, 2017 

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

Amo de Paz, G., Cubas, P., Divakar, P. K., Lumbsch, H. T. & Crespo, A. (2011) Origin and diversification of major clades in parmelioid lichens (Parmeliaceae, Ascomycota) during the Paleogene inferred by Bayesian analysis. PLoS ONE 6: e28161.CrossRefGoogle ScholarPubMed
Aptroot, A., Schumm, F. & Cáceres, M. E. S. (2012) Six new species of Pyrenula from the tropics. Lichenologist 44: 611618.Google Scholar
Asquith, A. (1995) Alien species and the extinction crisis of Hawaii’s invertebrates. Endangered Species Update 12: 611.Google Scholar
Baldwin, B. G. & Sanderson, M. J. (1998) Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences of the United States of America 95: 94029406.Google Scholar
Baldwin, B. G., Kyhos, D. W., Dvorak, J. & Carr, G. D. (1991) Chloroplast DNA evidence for a North American origin of the Hawaiian silversword alliance (Asteraceae). Proceedings of the National Academy of Sciences of the United States of America 88: 18401843.CrossRefGoogle ScholarPubMed
Barrier, M., Robichaux, R. H. & Purugganan, M. D. (2001) Accelerated regulatory gene evolution in an adaptive radiation. Proceedings of the National Academy of Sciences of the United States of America 98: 1020810213.Google Scholar
Beimforde, C., Feldberg, K., Nylinder, S., Rikkinen, J., Tuovila, H., Dörfelt, H., Grube, M., Jackson, D. J., Reitner, J., Seyfullah, L. J., et al. (2014) Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Molecular Phylogenetics and Evolution 77: 307319.Google Scholar
Brown, G. K., Murphy, D. J., Kidman, J. & Ladiges, P. Y. (2012) Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal. Australian Systematic Botany 25: 390403.Google Scholar
Burkhardt, F. & Smith, S. (1984) The Correspondence of Charles Darwin. Cambridge: Cambridge University Press.Google Scholar
Carlquist, S., Baldwin, B. G. & Carr, G. D. (eds) (2003) Tarweeds & Silverswords: Evolution of the Madiinae (Asteraceae). St. Louis, Missouri: Missouri Botanical Garden Press.Google Scholar
Castro, S., Daehler, C. C., Silva, L., Torres-Santana, C. W., Reyes-Betancort, J. A., Atkinson, R., Jaramillo, P., Guezou, A. & Jaksic, F. M. (2010) Floristic homogenization as a teleconnected trend in oceanic islands. Diversity and Distributions 16: 902910.Google Scholar
Dal Forno, M., Bungartz, F., Yánez-Ayabaca, A., Lücking, R. & Lawrey, J. D. (2017) High levels of endemism among Galapagos basidiolichens. Fungal Diversity (in press). doi: 10.1007/s13225-017-0380-6 Google Scholar
Dal Grande, F., Beck, A., Cornejo, C., Singh, G., Cheenacharoen, S., Nelsen, M. P. & Scheidegger, C. (2014) Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont‐mediated guilds in the lichen family Lobariaceae . New Phytologist 202: 455470.Google Scholar
Department of Land and Natural Resources (2007) Hawaii’s Most Invasive Horticultural Plants – Kahili Ginger. State of Hawaii, Department of Land and Natural Resources. Available at: www.hear.org/hortweeds/species/hedgar.htm Google Scholar
Drummond, A. J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.Google Scholar
Edwards, D. & Feehan, J. (1980) Records of Cooksonia-type sporangia from late Wenlock strata in Ireland. Nature 287: 4142.Google Scholar
Eldredge, L. G. & Evenhuis, N. L. (2002) Numbers of Hawaiian species for 2000. Bishop Museum Occasional Papers 68: 7178.Google Scholar
Eldredge, L. G. & Miller, S. E. (1995) How many species are there in Hawaii? Bishop Museum Occasional Papers 41: 318.Google Scholar
Esslinger, T. L. (1978) Studies in the lichen family Physciaceae. III. A new species of Phaeophyscia from Hawaii. Mycologia 70: 12471249.Google Scholar
Evenhuis, N. L. & Eldredge, L. G. (eds) (2002 a) Records of the Hawaii Biological Survey. Part 1: Articles. Bishop Museum Occasional Papers 68: 178.Google Scholar
Evenhuis, N. L. & Eldredge, L. G. (eds) (2002 b) Records of the Hawaii Biological Survey. Part 2: Notes. Bishop Museum Occasional Papers 69: 152.Google Scholar
Fleischer, R. C., McIntosh, C. E. & Tarr, C. L. (1998) Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K–Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Molecular Ecology 7: 533545.CrossRefGoogle ScholarPubMed
Follmann, G. (1974) Zur Nomenclatur der Lichenen. I. Ergänzungen und Neukombinationen. Philippia 2: 7374.Google Scholar
Fosberg, E. R. (1936) The Hawaiian geraniums. Occasional Papers of the Bernice P. Bishop Museum 12: 119.Google Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113118.CrossRefGoogle Scholar
Geiger, J. M. O., Ranker, T. A., Neale, J. M. R. & Klimas, S. T. (2007) Molecular biogeography and origins of the Hawaiian fern flora. Brittonia 59: 142158.Google Scholar
Givnish, T. J., Millam, K. C., Theim, T. T., Mast, A. R., Patterson, T. B., Hipp, A. L., Henss, J. M., Smith, J. F., Wood, K. R. & Sytsma, K. J. (2009) Origin, adaptive radiation, and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society of London, Series B 276: 407416.Google Scholar
Grant, K. T. & Estes, G. B. (2009) Darwin in Galápagos: Footsteps to a New World. Princeton, New York: Princeton University Press.Google Scholar
Hall, T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 9598.Google Scholar
Imada, C. T. (ed.) (2012) Hawaiian native and naturalized vascular plants checklist (December 2012 update). Bishop Museum Technical Report 60: 1–29, 7 appendices.Google Scholar
Inoue, M. (2002) Four Arctic-alpine or bipolar species of Lecidea (Lichenes) new to the Hawaii Islands. Bulletin of the National Science Museum (Tokyo), Series B (Botany) 28: 710.Google Scholar
Kalb, K. & Vězda, A. (1980) Tres lichenes novi Hawaiienses. Folia Geobotanica et Phytotaxonomica 15: 309311.Google Scholar
Kashiwadani, H., Smith, C. W. & Moon, K. H. (2002) New species of Ramalina (Ascomycotina, Ramalinaceae) from the Hawaiian Islands. Journal of Japanese Botany 77: 351355.Google Scholar
Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 30593066.CrossRefGoogle ScholarPubMed
Katoh, K., Asimenos, G. & Toh, H. (2009) Multiple alignment of DNA sequences with MAFFT. Methods in Molecular Biology 537: 3964.Google Scholar
Kauff, F. & Lutzoni, F. (2002) Phylogeny of Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Molecular Phylogenetics and Evolution 25: 138156.Google Scholar
Kay, E. A. (1997) Missionary contributions to Hawaiian natural history: what Darwin didn’t know. Hawaiian Journal of History 31: 2752.Google Scholar
Kidd, S. E. (2005) Molecular phylogenetics of the Hawaiian geraniums. MSc thesis, Bowling Green State University, Ohio.Google Scholar
Kirch, P. V. (1982) The impact of the prehistoric Polynesians on the Hawaiian ecosystem. Pacific Science 36: 114.Google Scholar
Lücking, R., Huhndorf, S., Pfister, D. H., Rivas Plata, E. & Lumbsch, H. T. (2009) Fungi evolved right on track. Mycologia 101: 810822.CrossRefGoogle ScholarPubMed
Lücking, R., Hodkinson, B. P. & Leavitt, S. D. (2017 ‘2016’) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – Approaching one thousand genera. Bryologist 119: 361416.CrossRefGoogle Scholar
Lumbsch, H. T., Ahti, T., Altermann, S., Amo de Paz, G., Aptroot, A., Arup, U., Bárcenas Peña, A., Bawingan, P. A., Benatti, M. N., Betancourt, L. et al. (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18: 1127.Google Scholar
Magnusson, A. H. & Zahlbruckner, A. (1943) Hawaiian lichens I. The families Verrucariaceae to Peltigeraceae . Arkiv för Botanik 31A (1): 196.Google Scholar
Mangold, A., Martín, M. A., Lücking, R. & Lumbsch, H. T. (2008) Molecular phylogeny suggests synonymy of Thelotremataceae within Graphidaceae (Ascomycota: Ostropales). Taxon 57: 476486.Google Scholar
Marbach, B. (2000) Corticole und lignicole Arten der Flechtengattung Buellia sensu lato in den Subtropen und Tropen. Bibliotheca Lichenologica 74: 1384.Google Scholar
Mason-Gamer, R. J. & Kellogg, E. A. (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology 45: 524545.Google Scholar
McCarthy, P. M. (1993) New saxicolous species of Ditremis Clements (lichenized Ascomycotina, Monoblastiaceae) from New Zealand and Hawaii. Muelleria 8: 14.Google Scholar
Miadlikowska, J. & Lutzoni, F. (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical and large subunit nuclear ribosomal DNA data. International Journal of Plant Science 161: 925968.Google Scholar
Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, Louisiana, pp. 1–8.Google Scholar
Mitchell, A. A., Li, R., Brown, J. W., Schönberger, I. & Wen, J. (2012) Ancient divergence and biogeography of Raukaua (Araliaceae) and close relatives in the southern hemisphere. Australian Systematic Botany 25: 432446.Google Scholar
Moncada, B., Lücking, R. & Betancourt, L. (2013) Phylogeny of the Lobariaceae (lichenized Ascomycota: Peltigerales), and a reappraisal of the genus Lobariella . Lichenologist 45: 203263.CrossRefGoogle Scholar
Moncada, B., Reidy, B. & Lücking, R. (2014) A phylogenetic revision of Hawaiian Pseudocyphellaria (lichenized Ascomycota: Lobariaceae) reveals eight new species and a high degree of inferred endemism. Bryologist 117: 119160.Google Scholar
Moon, K. H., Kurokawa, S. & Kashiwadani, H. (2001) The genus Rimelia (lichens) from the Hawaiian Islands. Journal of Japanese Botany 76: 321328.Google Scholar
Morden, C. W. & Loeffler, W. (1999) Fragmentation and genetic differentiation among subpopulations of the endangered Hawaiian mint Haplostachys haplostachya (Lamiaceae). Molecular Ecology 8: 617625.Google Scholar
Morden, C. W., Weniger, D. & Gardner, D. E. (2003) Phylogeny and biogeography of Pacific Rubus subg. Idaeobatus (Rosaceae) species: investigating the origin of the endemic Hawaiian raspberry R. macraei . Pacific Science 57: 181197.Google Scholar
Mueller-Dombois, D. (1987) Forest dynamics in Hawaii. Trends in Ecology and Evolution 2: 216220.Google Scholar
Olson, S. L. & James, H. F. (1982) Fossil birds from the Hawaiian Islands: evidence for wholesale extinction by man before western contact. Science 217: 633635.Google Scholar
Orange, A., James, P. W. & White, F. J. (2010) Microchemical Methods for the Identification of Lichens, 2nd edn. London: British Lichen Society.Google Scholar
Pax, D. L., Price, R. A. & Michaels, H. L. (1997) Phylogenetic position of the Hawaiian geraniums based on rbcL sequences. American Journal of Botany 84: 7278.CrossRefGoogle Scholar
Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D. & Pupko, T. (2010 a) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38: W23W28.Google Scholar
Penn, O., Privman, E., Landan, G., Graur, D. & Pupko, T. (2010 b) An alignment confidence score capturing robustness to guide-tree uncertainty. Molecular Biology and Evolution 27: 17591767.Google Scholar
Percy, D. M., Garver, A. M., Wagner, W. L., James, H. F., Cunningham, C. W., Miller, S. E. & Fleischer, R. C. (2008) Progressive island colonization and ancient origin of Hawaiian Metrosideros (Myrtaceae). Proceedings of the Royal Society of London Series B-Biological Sciences 275: 14791490.Google ScholarPubMed
Pérez-Ortega, S., Garrido-Benavent, I., Grube, M., Olmo, R. & de los Ríos, A. (2016) Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Diversity 80: 285300.Google Scholar
Peterson, E. B. (2000) An overlooked fossil lichen (Lobariaceae). Lichenologist 32: 298300.Google Scholar
Pratt, T. K., Atkinson, C. T., Banko, P. C., Jacobi, J. D. & Woodworth, B. L. (eds) (2009) Conservation Biology of Hawaiian Forest Birds: Implications for Island Avifauna. New Haven: Yale University Press.Google Scholar
Prieto, M. & Wedin, M. (2013) Dating the diversification of the major lineages of Ascomycota (fungi). PLoS ONE 8: e65576.CrossRefGoogle ScholarPubMed
Rivas Plata, E. (2011) Historical biogeography, ecology, and systematics of the family Graphidaceae (Ascomycota: Ostropales). Ph.D. thesis, University of Illinois at Chicago.Google Scholar
Roskov, Y., Abucay, L., Orrell, T., Nicolson, D., Flann, C., Bailly, N., Kirk, P., Bourgoin, T., DeWalt, R. E., Decock, W. et al. (eds) (2016) Species 2000 & ITIS Catalogue of Life, 2016 Annual Checklist. Digital resource at www.catalogueoflife.org/annual-checklist/2016. Species 2000: Naturalis, Leiden, the Netherlands.Google Scholar
Sakai, A. K., Wagner, W. L. & Mehrhoff, L. A. (2002) Patterns of endangerment in the Hawaiian flora. Systematic Biology 51: 276302.Google Scholar
Sérusiaux, E. & Lücking, R. (2007) Gallaicolichen, a new genus of foliicolous lichen with unique diaspores. Bibliotheca Lichenologica 95: 509516.Google Scholar
Silvestro, D., Cascales‐Miñana, B., Bacon, C. D. & Antonelli, A. (2015) Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytologist 207: 425436.Google Scholar
Simon, A., Magain, N., Goffinet, B. & Sérusiaux, E. (2016) Recent and rapid radiation of the lichen genus Sticta in the Western Indian Ocean islands. In Abstracts of the 8th International Association for Lichenology Symposium, 1–5 August, 2016, Helsinki, Finland, p. 41.Google Scholar
Smith, C. W. (1977) Notes on Hawaiian lichens I. Obligately foliicolous species. Bryologist 80: 342343.Google Scholar
Smith, C. W. (1984) Hawaii’s alectorioid lichens. Pacific Science 38: 249252.Google Scholar
Smith, C. W. (1991) Lichen conservation in Hawaii. In Tropical Lichens: Their Systematics, Conservation, and Ecology (The Systematics Association Special Volume No 43) (D. J. Galloway, ed.): 35–45. Oxford: Clarendon Press.Google Scholar
Smith, C. W. (1993) Notes on Hawaiian parmelioid lichens. Bryologist 96: 326332.Google Scholar
Smith, C. W. (1995) Notes on long-distance dispersal in Hawaiian lichens: ascospore characters. Cryptogamic Botany 5: 209213.Google Scholar
Smith, C. W. (2001) The lichen genus Umbilicaria in the Hawaiian Islands. Bibliotheca Lichenologica 78: 389394.Google Scholar
Smith, C. W. (2013) Checklist of lichens and lichenicolous fungi of Hawaii (USA). Available at: http://www.biologie.uni-hamburg.de/checklists/oceania/usa_hawaii_l.htm.Google Scholar
Smith, C. W., Gardner, D. E. & Hoe, W. J. (1997) Foliicolous Hawaiian cryptogams. Abstracta Botanica 21 (1): 163167.Google Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.Google Scholar
Staples, G. W. & Imada, C. T. (2006) Checklist of Hawaiian Anthocerotes and Hepatics. Tropical Bryology 28: 1547.Google Scholar
Staples, G. W., Imada, C. T., Hoe, W. J. & Smith, C. W. (2004) A revised checklist of Hawaiian mosses. Tropical Bryology 25: 3569.Google Scholar
Stenroos, S. & Smith, C. W. (1993) Notes on the amphipacific relations of Hawaiian Cladoniaceae . Tropical Bryology 8: 275280.Google Scholar
Stone, C. P. & Scott, J. M. (eds) (1985) Hawaii’s Terrestrial Ecosystems: Preservation and Management. Honolulu: Cooperative Parks Studies Unit, University of Hawaii Press.Google Scholar
Stone, C. P., Smith, C. W. & Tunison, J. T. (eds) (1992) Alien Plant Invasions in Native Ecosystems of Hawaii: Management and Research. Honolulu: Cooperative Parks Studies Unit, University of Hawaii Press.Google Scholar
Sulloway, F. (1982) Darwin and his finches: the evolution of a legend. Journal of the History of Biology 15: 153.Google Scholar
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 46734680.Google Scholar
US Fish and Wildlife Service (2010) Endangered and threatened wildlife and plants; determination of endangered status for 48 species on Kauai and designation of critical habitat. Final rule. Federal Register 75: 1896019165.Google Scholar
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 42384246.Google Scholar
Wagner, W. L. & Funk, V. A. (eds) (1995) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press.Google Scholar
Wagner, W. L. & Herbst, D. R. (2002) Electronic Supplement to the Manual of the Flowering Plants of Hawai’i. Available at: http://rathbun.si.edu/botany/pacificislandbiodiversity/hawaiianflora/supplement.htm Google Scholar
Wagner, W. L., Herbst, D. R. & Sohmer, S. H. (1999) Manual of the Flowering Plants of Hawai’i: Revised Edition. Honolulu: University of Hawai’i Press and Bishop Museum Press.Google Scholar
Weiner, J. (1994) The Beak of the Finch: A Story of Evolution in Our Time. New York: Knopf Doubleday Publishing Group.Google Scholar
White, T. J., Bruns, T. D., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315322. San Diego: Academic Press.Google Scholar
Willis, K. & McElwain, J. (2014) The Evolution of Plants. Oxford: Oxford University Press.Google Scholar
Wirth, V. (1997) Additional lichen records from Oceania 3. Trapeliopsis flexuosa. Australasian Lichenological Newsletter 40: 11.Google Scholar
Wood, K. R. (2007) New plant records, rediscoveries, range extensions, and possible extinctions within the Hawaiian Islands. Bishop Museum Occasional Papers 96: 1317.Google Scholar
Wood, K. R. (2012) Possible extinctions, rediscoveries, and new plant records within the Hawaiian Islands. Bishop Museum Occasional Papers 113: 91102.Google Scholar
Wright, S. D., Yong, C. G., Wichman, S. R., Dawson, J. W. & Gardner, R. C. (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS+ETS). Journal of Biogeography 28: 769774.Google Scholar
Yoshimura, I. (1984) Taxonomic studies on Lobaria crenulata and its allies. Journal of the Hattori Botanical Laboratory 57: 97126.Google Scholar
Yoshimura, I. (1998) Lobaria in Latin America: taxonomic, geographic and evolutionary aspects. In Lichenology in Latin America: History, Current Knowledge and Applications (M. P. Marcelli & M. R. D. Seaward, eds): 129134. São Paulo, Brazil: CETESB – Companhia de Tecnologia de Saneamento Ambiental.Google Scholar
Yoshimura, I. & Arvidsson, L. (1994) Taxonomy and chemistry of the Lobaria crenulata group in Ecuador. Acta Botanica Fennica 150: 223333.Google Scholar
Zhou, S. & Stanosz, G. R. (2001) Primers for amplification of mt SSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. Mycological Research 105: 10331044.Google Scholar
Zoller, S., Scheidegger, C. & Sperisen, C. (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31: 511516.Google Scholar