Complete life cycle of the lichen fungus Calopadia puiggarii (Pilocarpaceae, Ascomycetes) documented in situ: Propagule dispersal, establishment of symbiosis, thallus development, and formation of sexual and asexual reproductive structures

American Journal of Botany

Volumn 101, Issue 11, 2014, Pages 1836-1848

  Sanders, William B ^a  

^a FLORIDA GULF COAST UNIVERSITY   (United States)

Author keywords

Calopadia puiggari; Campylidia; Conidia; Foliicolous lichens; Lichen development; Lichen life cycle; Lichenization; Photobiont; Prothallus; Pycnidia; Symbiont codispersal

Indexed keywords

ASCOMYCOTA; CALOPADIA; CALOPADIA PUIGGARII; FUNGI; PILOCARPACEAE;

ASCOMYCETES; CYTOLOGY; FUNGUS SPORE; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; LICHEN (ORGANISM); LIFE CYCLE STAGE; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

ASCOMYCOTA; GENOTYPE; LICHENS; LIFE CYCLE STAGES; SPORES, FUNGAL; SYMBIOSIS;

EID: 84908439318     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1400272     Document Type: Article

References (68)

1. AHMADJIAN, V. 2001. Trebouxia: Reflections on a perplexing and controversial lichen photobiont. In J. Sechbach [ed.], Symbiosis, 373–383. Kluwer, Dordrecht, Netherlands.
2. AHMADJIAN, V. 2002. Lingering lichen myths are hard to dispel. ISS Symbiosis International 2: 1-2.
3. AHMADJIAN, V., and J. B. JACOBS. 1983. Algal–fungal relationships in lichens: Recognition, synthesis, and development. In L. J. Goff [ed.], Algal symbiosis, 147–172. Cambridge University Press, Cambridge, UK.
4. ARMSTRONG, R., and T. BRADWELL. 2010. Growth of crustose lichens: A review. Geografiska Annaler 92 A(1): 3-17.
5. BUBRICK, P., M. GALUN, and A. FREMSDORFF. 1984. Observations on freeliving Trebouxia and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455-462.
6. CASANO, L. M., E. M. DEL CAMPO, F. J. García-Breijo, J. Reig-Armiñana, F. GASULLA, A. DEL HOYO, A. GUÉRA, and E. BARRENO. 2011. Two Trebouxia algae with different physiological performances are everpresent in lichen thalli of Ramalina farinacea. Coexistence versus competition? E nvironmental Microbiology 13: 806-818.
7. CLAYDEN, S. R. 1997. Intraspecific interactions and parasitism in an association of Rhizocarpon lecanorinum and R. geographicum. Lichenologist 29: 533-545.
8. CLAYDEN, S. R. 1998. Thallus initiation and development in the lichen Rhizocarpon lecanorinum. New Phytologist 139: 685-695.
9. DYER, P. S., G. J. MURTAGH, and P. D. CRITTENDEN. 2001. Use of RAPD-PCR DNA fingerprinting and vegetative incompatibility tests to investigate genetic variation within lichen forming fungi. Symbiosis 31: 213–229.
10. FARKAS, E., J. A. ELIX, and A. FLAKUS. 2012. Calopadia erythrocephala, a new foliicolous lichenized fungus from Brazil. Lichenologist 44: 395-399.
11. FRIEDL, T. 1987. Thallus development and phycobiont of the parasitic lichen Diploschistes muscorum. Lichenologist 19: 183-191.
12. GALLØE, O. 1927. Natural history of the Danish lichens. Part 1. H. Aschehoug & Co, Copenhagen, Denmark.
13. GALLØE, O. 1932. Natural history of the Danish lichens. Part 3. H. Aschehoug & Co, Copenhagen, Denmark.
14. GALLØE, O. 1954. Natural history of the Danish lichens. Part 9. Ejnar Munksgaard, Copenhagen, Denmark.
15. García-Breijo, F., J. Reig-Armiñana, G. SALV Á, V. M. VÁZQUEZ, and E. BARRENO. 2010. El liquen Ramalina farinacea (L.) Ach. en Asturias. Estructura de talos e identificación molecular de los ficobiontes de Trebouxia que coexisten. Boletín de Ciencias de la Naturaleza del Real Instituto de Estudios Asturianos 51: 325-336.
16. GARTY, J., and J. DELAREA. 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.
17. Gaßmann A, and S. OTT. 2000. Growth strategy and the gradual symbiotic interactions of the lichen Ochrolechia frigida. Plant Biology 2: 368-378.
18. HONEGGER, R. 1984. Ultrastructural studies of conidiomata, conidiophores, and conidiogenous cells in six lichen-forming ascomycetes. Canadian Journal of Botany 62: 2081-2093.
19. HONEGGER, R. 1985. Ascocarpontogenie, Askusstruktur und –funktion bei Vertretern der Gattung Rhizocarpon. Berichte der Deutschen Botanischen Gesellschaft 91: 579-594.
20. JAHNS, H. M. 1970. Untersuchungen zur Entwicklungsgeschichte der Cladoniaceen unter besonderer Berücksichtingung der Podetien- Problems. N ova Hedwigia 20: 1-177.
21. JAHNS, H. M., D. MOLLENHAUER, M. JENNIGER, and D. SCHÖNBORN. 1979. Die Neubesiedlung von Baumrinde durch Flechten. I. Natur und Museum 109: 40-51.
22. JAHNS, H. M., and S. OTT. 1997. Life strategies in lichens-Some general considerations. In L. Kappen [ed.], New species and novel aspects in ecology and physiology of lichens. Bibliotheca Lichenologica 67: 49–67.
23. JONESON, S., and F. LUTZONI. 2009. Compatibiliy and thigmotropism in the lichen symbiosis: A reappraisal. Symbiosis 47: 109-115.
24. KALB, K., and A. Vězda. 1987. Einige nicht-foliicole Arten der Familie Ectolechiaceae (Lichenes) aus Brasilien. Folia Geobotanica et Phytotaxonomica 22: 287-312.
25. KIRK, P. M., P. F. CANNON, J. C. DAVID, and J. A. STALPERS. 2001. Ainsworth and Bisby’s Dictionary of the Fungi, 9th ed. CAB International, Wallingford, UK.
26. LAMB, I. M. 1959. Lichens. Scientific American 201: 144-156.
27. LARSEN, E. 2010. Progress in culturing foliicolous lichens on coverslips. In T. H. Nash III, L. Geiser, B. McCune, D. Triebel, A. M. F. Tomescu and W. B. Sanders [eds.], Biology of lichens—Symbiosis, ecology, environmental monitoring, systematics and cyber applications. Bibliotheca Lichenologica 105: 17–23.
28. LAUNDON, J. R. 1978. Haematomma chemotypes form fused thalli. Lichenologist 10: 221-225.
29. LESLIE, J. F. 1993. Fungal vegetative incompatibility. Annual Review of Phytopathology 31: 127-150.
30. Létrouit-Galinou, M.-A., and J. ASTA. 1994. Thallus morphogenesis in some lichens. Cryptogamic Botany 4: 274-282.
31. LÜCKING, R. 1997. Additions and corrections to the knowledge of the foliicolous lichen flora of Costa Rica. The genus Fellhanera, wih notes on Bacidia paucisepta. Tropical Bryology 13: 141-173.
32. LÜCKING, R. 1998. “Plasticolous” lichens in a tropical rain forest at La Selva Biological Station, Costa Rica. Lichenologist 30: 287-291.
33. LÜCKING, R. 1999. Ergänzungen und Verbesserungen zur Kenntnis der foliikolen Flechtenflora Costa Ricas. Die Familie Ectolechiaceae. Phyton (Horn, Austria) 39: 131-165.
34. LÜCKING, R. 2001. Lichens on leaves in tropical rainforests: Life in a permanently ephemerous environment. In G. Gottsberger and S. Liede [eds.], Life forms and dynamics in tropical forests. Dissertationes Botanicae 346: 41–77.
35. LÜCKING, R. 2008. Foliicolous lichenized fungi. Flora Neotropica Monograph 103. New York Botanical Garden Press, Bronx, New York, USA.
36. LÜCKING, R., and A. Bernecker-Lücking. 2002. Distance, dynamics, and diversity in tropical rainforests: An experimental approach using foliicolous lichens on artificial leaves. I. Growth performance and succession. Ecotropica 8: 1-13.
37. LÜCKING, R., H. T. LUMBSCH, and J. ELIX. 1994. Chemistry, anatomy and morphology of foliicolous species of Fellhanera and Badimia (Lichenized Ascomycotina: Lecanorales). Botanica Acta 107: 393–401.
38. LÜCKING, R., and R. SANTESSON, R. 2001. New species or interesting records of foliicolous lichens. VIII. Two new taxa from tropical Africa, with a key to sorediate Fellhanera species. Lichenologist 33: 111-116.
39. MALME, G. O. A. 1935. Das Kampylidium. Ein verkanntes Fortpflanzungsorgan der Flechten. Svensk Botanisk Tidskrift 29: 302-305.
40. MANSOURNIA, M. R., B. WU, N. MATSUSHITA, and T. HOGETSU. 2012. Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: Association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44: 419-440.
41. Monge-Najera, J., and M. A. BLANCO. 1995. The influence of leaf characteristics on epiphyll cover: A test of hypotheses with artificial leaves. Tropical Bryology 11: 5-9.
42. MUGGIA, L., E. BALOCH, E. STABENTHEINER, M. GRUBE, and M. WEDIN. 2011. Photobiont association and genetic diversity of the optionally lichenized fungus Schizoxylon albescens. FEMS Microbiology Ecology 75: 255-272.
43. MUGGIA, L., L. VANCUROVA, P. ŠKALOUD, O. PEKSA, M. WEDIN, and M. GRUBE. 2013. The symbiotic playground of lichen thalli-A highly flexible photobiont association in rock-inhabiting lichens. FEMS Microbiology Ecology 85: 313-323.
44. MURTAGH, G. J., P. S. DYER, and P. D. CRITTENDEN. 2000. Reproductive systems: Sex and the single lichen. Nature 404: 564.
45. NAKANO, T. 1996. Diversity of lichen photobionts in Cladia aggregata [abstract]. In book of abstracts [page number unknown] for Third Symposium of the International Association for Lichenology (IAL3), Salzburg, Austria.
46. NELSEN, M., and A. GARGAS. 2008. Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytologist 177: 264-275.
47. NELSEN, M., and A. GARGAS. 2009. Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112: 404-417.
48. NYATI, S., S. WERTH, and R. HONEGGER. 2013. Genetic diversity of sterile cultured Trebouxia photobionts associated with the lichen-forming fungus Xanthoria parietina visualized with RAPD-PCR techniques. Lichenologist 45: 825-840.
49. OHMURA, Y., I. M. KAWACHI, F. KASAI, M. M. WATANABE, and S. TAKESHITA. 2006. Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmelia tinctorum, based on rDNA sequences. Bryologist 109: 43-59.
50. OTT, S. 1987. Sexual reproduction and developmental adaptations in Xanthoria parietina. Nordic Journal of Botany 7: 219-228.
51. Piercey-Normore, M. D. 2006. The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytologist 169: 331-344.
52. Piercey-Normore, M. D. 2009. Vegetatively reproducing fungi in three genera of the Parmeliaceae show divergent algal partners. Bryologist 112: 773-785.
53. POELT, J. 1986. Morphologie der Flechten; Fortschritte und Probleme. Berichte der Deutschen Botanischen Gesellschaft 99: 3-29.
54. SANDERS, W. B. 2001. Preliminary light microscope observations of fungal and algal colonization and lichen thallus initiation on glass slides placed near foliicolous lichen communities within a lowland forest. Symbiosis 31: 85-94.
55. SANDERS, W. B. 2002. In situ development of the foliicolous lichen Phyllophiale (Trichotheliaceae) from propagule germination to propagule production. American Journal of Botany 89: 1741-1746.
56. SANDERS, W. B. 2005. Observing microscopic phases of lichen life cycles on transparent substrata placed in situ. Lichenologist 37: 373-382.
57. SANDERS, W. B., and R. LÜCKING. 2002. Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425-435.
58. SANTESSON, R. 1952. Foliicolous lichens I. Symbolae Botanicae Upsalienses 12: 1-590.
59. SCHEIDEGGER, C. 1995. Reproductive strategies in Vezdaea (Lecanorales, lichenized ascomycetes): A low-temperature scanning electron microscopy study of a ruderal species. Cryptogamic Botany 5: 161-171.
60. SCHUSTER, G., S. OTT, and H. M. JAHNS. 1985. Artificial cultures of lichens in the natural environment. Lichenologist 17: 247-253.
61. SÉrusiaux, E. 1986. The nature and origin of campylidia in lichenized fungi. Lichenologist 18: 1-35.
62. SÉRUSIAUX, E. 1995. Further new lichen species producing campylidia or complex conidiomata. In E. E. Farkas, R. Lücking, and V. Wirth [eds], Scripta lichenologica—Lichenological papers dedicated to Antonin Vězda. Bibliotheca Lichenologica 58: 411–431.
63. SIPMAN, H. J. M. 1994. Foliicolous lichens on plastic tape. Lichenologist 26: 311-312.
64. VOBIS, G. 1977. Studies on the germination of lichen conidia. Lichenologist 9: 131-136.
65. WARD, H. M. 1884. On the structure, development and life history of a tropical epiphyllous lichen (Strigula complanata Fée). Transactions of the Linnean Society of London, Botany 2: 87-119.
66. WEDIN, M., H. DÖRING, and G. GILENSTAM. 2004. Saprotrophy and lichenization as options for the same fungal species on different substrata: Environmental plasticity and fungal life styles in the Stictis- Conotrema complex. New Phytologist 164: 459-465.
67. WERNER, R.-G. 1931. Histoire de la synthèse lichénique. Mémoires de la Société des Sciences Naturelles du Maroc 27: 7-45.
68. WORNIK, S., and M. GRUBE. 2010. Joint dispersal does not imply maintenance of partnerships in lichen symbiosis. Microbial Ecology 59: 150-157.