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Ascospore ontogeny and discharge in megalosporous Trypetheliaceae and Graphidaceae (Ascomycota: Dothideomycetes and Lecanoromycetes) suggest phylogenetic relationships and ecological constraints

Published online by Cambridge University Press:  08 February 2012

Garrett SWEETWOOD ,
Robert LÜCKING ,
Matthew P. NELSEN  and
André APTROOT
Garrett SWEETWOOD
Affiliation:
Roosevelt University, 430 S. Michigan Ave, Chicago, Illinois 60605, USA. Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496, USA. Email: rlucking@fieldmuseum.org
Robert LÜCKING
Affiliation:
Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496, USA. Email: rlucking@fieldmuseum.org
Matthew P. NELSEN
Affiliation:
Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496, USA. Email: rlucking@fieldmuseum.org Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th Street, Chicago, Illinois 60637, USA.
André APTROOT
Affiliation:
ABL Herbarium, G.v.d.Veenstraat 107, NL-3762 XK Soest, The Netherlands.
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Abstract

We studied ascospore dispersal and ontogeny in several species of Trypetheliaceae and one species of Graphidaceae with megalosporous (very large) ascospores, including Aptrootia terricola (Aptroot) Lücking, Umaña & Chaves, Architrypethelium nitens (Fée) Aptroot, A. seminudum (Mont.) Aptroot, Astrothelium diplocarpoides Müll. Arg., Laurera gigantospora (Müll. Arg.) Zahlbr., and Ocellularia subpraestans Hale. Although mature ascospores are very different among species of Trypetheliaceae, all species studied share plesiomorphic ontogenetic features such as the formation of a single central euseptum and subsequent development of a variable number of transverse distosepta with diamond-shaped lumina (astrothelioid ascospore type). Even the dark brown, richly muriform ascospores of Aptrootia terricola go through an astrothelioid stage. This suggests that ascospore types may be more closely related than suggested by their mature morphology, and could explain why related taxa can develop markedly different ascospore types. We discuss the implications for systematic classification of Trypetheliaceae in the light of recent molecular studies, and also speculate about the ecological importance of large ascospores, especially with muriform septation.

Keywords

Aptrootia robustaBathelium tuberculosumLaurera megaspermaLaurera phaeomelodeslichensTrypethelium eluteriae
Type
Research Article
Information
The Lichenologist , Volume 44 , Issue 2 , March 2012 , pp. 277 - 296
Copyright
Copyright © British Lichen Society 2012

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References

Abbayes, H. des (1951) Traité de Lichénologie. Paris: Paul Lechevalier.Google Scholar
Ahmadjian, V. & Hale, M. E. (eds) (1973) The Lichens. New York and London: Academic Press.Google Scholar
Aptroot, A. (1991) A monograph of the Pyrenulaceae (excluding Anthracothecium and Pyrenula) and the Requienellaceae, with notes on the Pleomassariaceae, the Trypetheliaceae and Mycomicrothelia (lichenized and non-lichenized Ascomycetes). Bibliotheca Lichenologica 44: 1–178.Google Scholar
Aptroot, A. (2009) Trypetheliaceae. Flora of Australia 57 (Lichens 5): 534–552.Google Scholar
Aptroot, A., Lücking, R., Sipman, H. J. M., Umaña, L. & Chaves, J. L. (2008) Pyrenocarpous lichens with bitunicate asci. A first assessment of the lichen biodiversity inventory in Costa Rica. Bibliotheca Lichenologica 97: 1–162.Google Scholar
Archer, A. W. (2004) Pertusariaceae. Flora of Australia 56A (Lichens 4): 116–172.Google Scholar
Archer, A. W. & Elix, J. A. (2011) A Preliminary World-wide Key to the Lichen Genus Pertusaria. http://www.rbgsyd.nsw.gov.au/science/Plant_Diversity_Research/Key_to_Pertusaria.Google Scholar
Bailey, R. H. (1976) Ecological aspects of dispersal and establishment in lichens. In Lichenology: Progress and Problems (Brown, D. H. Hawksworth, D. L. & Bailey, R. H., eds): 215–247. London: Academic Press.Google Scholar
Bailey, R. H. & Garrett, R. M. (1968) Studies on the discharge of ascospores from lichen apothecia. Lichenologist 4: 57–65.CrossRefGoogle Scholar
Bellemère, A. (1994) Asci and ascospores in ascomycete systematics. In Ascomycete Systematics. Problems and Perspectives in the Nineties (Hawksworth, D. L., ed.): 111–126. New York: Plenum Press.CrossRefGoogle Scholar
Bellemère, A. & Letrouit-Galinou, M. A. (1988) Asci, ascospores, and ascomata. In CRC Handbook of Lichenology. Volume I (Galun, M., ed.): 161–179. Boca Raton: CRC Press Inc.Google Scholar
Bragg, J. D. (1981) Inhibitory effects of light on ascospore germination of Pseudoarachniotus marginosporus. Mycologia 73: 681–688.CrossRefGoogle Scholar
Bungartz, F., Lücking, R. & Aptroot, A. (2010) The lichen family Graphidaceae in the Galapagos Islands. Nova Hedwigia 90: 1–44.CrossRefGoogle Scholar
Clayden, S. R. (1997) Seasonal variation in ascospore discharge by Rhizocarpon lecanorinum. Lichenologist 29: 495–499.CrossRefGoogle Scholar
Connell, J. H. (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In Dynamics of Populations (Den Boer, P. J. & Gradwell, G., eds): 298–312. Wageningen: Centre for Agricultural Publishing and Documentation (PUDOC).Google Scholar
Cuny, D., van Haluwyn, C. & Caron, B. (1997) Stimulation of ascospore germination by fumarprotocetraric acid in Diploschistes muscorum (Scop.) R. Sant. (lichenized Ascomycotina). Nova Hedwigia 64: 103–110.CrossRefGoogle Scholar
Deacon, J. (2005) Fungal Biology. Cambridge, MA: Blackwell Publishers.CrossRefGoogle Scholar
Del Prado, R., Schmitt, I., Kautz, S., Palice, Z. Lücking & Lumbsch, H. T. (2006) Molecular data place Trypetheliaceae in Dothideomycetes. Mycological Research 110: 511–520.CrossRefGoogle ScholarPubMed
Dibben, M. J. (1980) The chemosystematics of the lichen genus Pertusaria in North America north of Mexico. Publications in Biology and Geology 5: 1–162.Google Scholar
Durrell, L. W. (1964) The composition and structure of walls in dark fungus spores. Mycopathologia et Mycologia Applicata 23: 339–345.CrossRefGoogle ScholarPubMed
Dyer, L. A. & Letourneau, D. K. (2007) Determinants of lichen diversity in a rain forest understorey. Biotropica 39: 525–529.CrossRefGoogle Scholar
Elix, J. A., Aptroot, A. & Archer, A. W. (1997) The lichen genus Pertusaria (lichenised Ascomycotina) in Papua New Guinea and Australia: twelve new species and thirteen new reports. Mycotaxon 64: 17–35.Google Scholar
Eriksson, O. E. (1989) NaClO, sodium hypochlorite, a powerful agent in studies of ascospore morphology. Systema Ascomycetum 8: 29–57.Google Scholar
Eriksson, O. E. (2009) Ascomycota. In Encyclopedia of Life Sciences (ELS): 1–7. Chichester: John Wiley & Sons Ltd.Google Scholar
Eubanks, M. D., Nesci, K. A., Petersen, M. K., Liu, Z. & Sanchez, H. B. (1997). The exploitation of an ant-defended host plant by a shelter-building herbivore. Oecologia 109: 454–460.CrossRefGoogle ScholarPubMed
Frisch, A., Kalb, K. & Grube, M. (2006) Contributions towards a new systematics of the lichen family Thelotremataceae III. Molecular phylogeny of the Thelotremataceae. Bibliotheca Lichenologica 92: 517–539.Google Scholar
Galloway, D. J. (1985) Flora of New Zealand Lichens. Wellington, New Zealand: Hasselberg Government Printer.Google Scholar
Galloway, D. J. (2007) Flora of New Zealand – Lichens. Revised Second Edition. Lincoln, New Zealand: Manaaki Whenua Press.Google Scholar
Garrett, R. M. (1971) Studies on some aspects of ascospore liberation and dispersal in lichens. Lichenologist 5: 33–44.Google Scholar
Garty, J. & Delarea, J. (1988) Evidence of liberation of lichen ascospores in clusters and reports on contact between free-living algal cells and germinating lichen ascospores under natural conditions. Canadian Journal of Botany 66: 2171–2177.Google Scholar
Gerson, U. (1973) Lichen-arthropod associations. Lichenologist 5: 434–443.CrossRefGoogle Scholar
Hale, M. E. Jr. (1973) Studies on the lichen family Thelotremataceae. 1. Phytologia 26: 413–420.Google Scholar
Hale, M. E. Jr. (1978a) A revision of the lichen family Thelotremataceae in Panama. Smithsonian Contributions to Botany 38: 1–60.CrossRefGoogle Scholar
Hale, M. E. Jr. (1978b) Studies on the lichen family Thelotremataceae. 4. Mycotaxon 7: 377–385.Google Scholar
Harris, R. C. (1986) The family Trypetheliaceae (Loculoascomycetes: lichenized Melanommatales) in Amazonian Brazil. Supplement Acta Amazonica 14: 55–80.CrossRefGoogle Scholar
Harris, R. C. (1995) More Florida Lichens. Including the 10ø Tour of the Pyrenolichens. Bronx, New York: Published by the author.Google Scholar
Herrera, C. M. & Pellmyr, O. (2002) Plant-Animal Interactions: An Evolutionary Approach. Oxford: Blackwell Scientific Publications.Google Scholar
Ingold, C. T. (2001) Range in size and form of basidiospores and ascospores. Mycologist 15: 165–166.CrossRefGoogle Scholar
Janzen, D. H. (1970) Herbivores and the number of tree species in tropical forests. The American Naturalist 104: 501–528.CrossRefGoogle Scholar
Jennings, D. H. & Lysek, G. (1996) Fungal Biology: Understanding the Fungal Lifestyle. Guildford, UK: Bios Scientific Publishers Ltd.Google Scholar
Kirk, P. M., Cannon, P. F., Minter, D. W. & Stalpers, J. A. (2008) Dictionary of the Fungi. 10th edn. Wallingford, UK: CAB International.Google Scholar
Kohn, L. M. & Korf, R. P. (1975) Variation in ascomycete iodine reactions: KOH pretreatment explored. Mycotaxon 3: 165–172.Google Scholar
Komposch, H. & Hafellner, J. (2002) Life form diversity of lichenized fungi in an Amazon lowland rainforest. Bibliotheca Lichenologica 82: 311–326.Google Scholar
Leal, I. R. & Oliveira, P. S. (2000) Foraging ecology of attine ants in a Neotropical savanna: seasonal use of fungal substrate in the cerrado vegetation of Brazil. Insectes Sociaux 47: 376–382.CrossRefGoogle Scholar
Lorentsson, S. & Mattsson, J.-E. (1999) New reports of soredia dispersed by ants, Formica cunicularia. Lichenologist 31: 204–207.Google Scholar
Lücking, R. & Bernecker-Lücking, A. (2000) Lichen feeders and lichenicolous fungi: do they affect dispersal and diversity in tropical foliicolous lichen communities? Ecotropica 6: 23–41.Google Scholar
Lücking, R., Sipman, H. J. M., Umaña, L., Chaves, J. L. & Lumbsch, H. T. (2007) Aptrootia (Dothideomycetes: Trypetheliaceae), a new genus of pyrenocarpous lichens for Thelenella terricola. Lichenologist 39: 187–193.CrossRefGoogle Scholar
Lücking, R., Chaves, J. L., Sipman, H. J. M., Umaña, L. & Aptroot, A. (2008) A first assessment of the Ticolichen Biodiversity Inventory in Costa Rica: the genus Graphis, with notes on the genus Hemithecium (Ascomycota: Ostropales: Graphidaceae). Fieldiana Botany, New Series 46: 1–126.CrossRefGoogle Scholar
Lücking, R., Rivas Plata, E., Chaves, J. L., Umaña, L. & Sipman, H. J. M. (2009) How many tropical lichens are there… really? Bibliotheca Lichenologica 100: 399–418.Google Scholar
Lundqvist, N. (1972) Nordic Sordariaceae s. lat. Symbolae Botanicae Upsalienses 20: 1–374.Google Scholar
Makhija, U. & Patwardhan, P. G. (1988) The lichen genus Laurera (family Trypetheliaceae) in India. Mycotaxon 31: 565–590.Google Scholar
Makhija, U. & Patwardhan, P. G. (1993) A contribution to our knowledge of the lichen genus Trypethelium (family Trypetheliaceae). Journal of the Hattori Botanical Laboratory 73: 183–219.Google Scholar
Mangold, A., Elix, J. A. & Lumbsch, H. T. (2009) Thelotremataceae. Flora of Australia 57 (Lichens 5): 195–420.Google Scholar
Meehan, C. J., Olson, E. J., Reudink, M. W., Kurt, T. & Curry, R. L. (2009) Herbivory in a spider through exploitation of an ant-plant mutualism. Current Biology 19: 1591–1682.CrossRefGoogle Scholar
Meier, F. A., Scherrer, S. & Honegger, R. (2002) Faecal pellets of lichenivorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola. Biological Journal of the Linnean Society 76: 259–268.Google Scholar
Müller Argoviensis, J. (1887) Graphideae Féeanae inclus. trib. affinibus nec non Graphidaea exoticae Acharii, El. Friesii et Zenkeri e novo studio speciminum originalium expositae et in novam dispositionem ordinatae. Mémoires de la Societé de Physique et d'Histoire Naturelle de Gèneve 29: 1–80.Google Scholar
Müller Argoviensis, J. (1891) Lichenes Brisbanenses a cl. F. M. Bailey, Gouvernment Botanist, prope Brisbane (Queensland) in Australia orientali lecti. Nuovo Giornale Botanico Italiano 23: 385–404.Google Scholar
Nagarkar, M. B., Sethy, P. K. & Patwardhan, P. G. (1985) A contribution to our knowledge of the lichen family Thelotremataceae from South India II. Kavaka 13: 57–62.Google Scholar
Nelsen, M. P., Lücking, R., Grube, M., Mbatchou, J. S., Muggia, L., Rivas Plata, E. & Lumbsch, H. T. (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Studies in Mycology 64: 135–144.CrossRefGoogle ScholarPubMed
Ostrofsky, A. & Denison, W. C. (1980) Ascospore discharge and germination in Xanthoria polycarpa. Mycologia 72: 1171–1179.CrossRefGoogle Scholar
Pentecost, A. (1981) Some observations on the size and shape of lichen ascospores in relation to ecology and taxonomy. New Phytologist 89: 667–678.CrossRefGoogle Scholar
Pyatt, F. B. (1968a) An investigation into conditions influencing ascospore discharge and germination in lichens. Revue Bryologique et Lichenologique 36: 323–329.Google Scholar
Pyatt, F. B. (1968b) Ascospore germination in Pertusaria pertusa (L.) Tuck. Revue Bryologique et Lichenologique 36: 316–320.Google Scholar
Pyatt, F. B. (1968c) The occurrence of a rotifer on the surfaces of apothecia of Xanthoria parietina. Lichenologist 4: 74–75.CrossRefGoogle Scholar
Pyatt, F. B. (1968d) The ultrastructure of the ascospore wall of the lichen Pertusaria pertusa. Transactions of the British Mycological Society 52: 167–170.Google Scholar
Pyatt, F. B. (1969) Studies on the periodicity of spore discharge and germination in lichens. Bryologist 72: 48–53.Google Scholar
Raja, H. A. & Shearer, C. A. (2006) Arnium gigantosporum, a new ascomycete species from fresh water in Florida. Fungal Diversity 22: 219–225.Google Scholar
Rickson, F. R. (1969) Developmental aspects of the shoot apex, leaf, and beltian bodies of Acacia cornigera. American Journal of Botany 56: 195–200.CrossRefGoogle Scholar
Rickson, F. R. (1976) Anatomical development of the leaf trichilium and Müllerian bodies of Cecropia peltata L. American Journal of Botany 63: 1266–1271.Google Scholar
Rivas Plata, E. & Lumbsch, H. T. (2011) Parallel evolution and phenotypic divergence in lichenized fungi: a case study in the lichen-forming fungal family Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales). Molecular Phylogenetics and Evolution 61: 45–63.Google Scholar
Rivas Plata, E. T., Lücking, R. & Lumbsch, H. T. (2008) When family matters: an analysis of Thelotremataceae (lichenized Ascomycota: Ostropales) as bioindicators of ecological continuity in tropical forests. Biodiversity and Conservation 17: 1319–1351.Google Scholar
Roper, M., Pepper, R. E., Brenner, M. & Pringle, A. (2008) Explosively launched spores of ascomycete fungi have drag minimizing shapes. Proceedings of the National Academy of Sciences 105: 20583.Google Scholar
Sanders, W. B. & Lücking, R. (2002) Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425–435.CrossRefGoogle ScholarPubMed
Santesson, R. (1952) Foliicolous lichens I. A revision of the taxonomy of the obligately foliicolous, lichenized fungi. Symbolae Botanicae Upsalienses 12(1): 1–590.Google Scholar
Shields, L. M., Durrell, L. W. & Sparrow, A. H. (1961) Preliminary observations on radiosensitivity of algae and fungi from soils of the Nevada test site. Ecology 42: 440–441.Google Scholar
Sipman, H. J. M. (1983) A monograph of the lichen family Megalosporaceae. Bibliotheca Lichenologica 18: 1–241.Google Scholar
Sipman, H. J. M. & Harris, R. C. (1989) Lichens. In Tropical Rain Forest Ecosystems (Lieth, H. & Werger, M. J. A., eds): 303–309. Amsterdam: Elsevier Science.Google Scholar
Skorepa, A. C. & Sharp, A. J. (1971) Lichens in “packets” of lacewing larvae (Chrysopidae). Bryologist 74: 363–364.Google Scholar
Smith, C. W. (1995) Notes on long-distance dispersal in Hawaiian lichens: ascospore characters. Cryptogamic Botany 5: 209–213.Google Scholar
Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A. (eds) (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Staiger, B. (2002) Die Flechtenfamilie Graphidaceae. Studien in Richtung einer natürlicheren Gliederung. Bibliotheca Lichenologica 85: 1–526.Google Scholar
Tibell, L. (1971) The genus Cyphelium in Europe. Svensk Botanisk Tidskrift 65: 138–164.Google Scholar
Wilson, P. J. & Methven, A. S. (1997) Lichen use by larval Leucochrysa pavida (Neuroptera: Chrysopidae). Bryologist 100: 448–453.CrossRefGoogle Scholar
Yamamoto, Y. (2002) Discharge and germination of lichen ascospores in the laboratory. Lichenology 1: 11–22.Google Scholar
Yamamoto, Y., Kinoshita, Y., Takahagi, T., Kroken, S., Kurokawa, T. & Yoshimura, I. (1998) Factors affecting discharge and germination of lichen ascospores. Journal of the Hattori Botanical Laboratory 85: 267–278.Google Scholar
Zahlbruckner, A. (1905) Flechten. In Die Natürliche Pflanzenfamilien (Engler, A. & Prantl, K., eds) T. 1, Abt. 1. Leipzig: Engelmann.Google Scholar
Zhao, Z.-T., Ren, Q. & Aptroot, A. (2004) An annotated key to the lichen genus Pertusaria in China. Bryologist 107: 531–541.CrossRefGoogle Scholar
Zopf, W. (1905a) Vielkernigkeit grosser Flechtensporen. Berichte der Deutschen Botanischen Gesellschaft 23: 121–122.Google Scholar
Zopf, W. (1905b) Zur Vielkernigkeit grosser Flechtensporen. Berichte der Deutschen Botanischen Gesellschaft 23: 206.Google Scholar