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Bryology and Lichenology |
Departamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife, Brazil; and the University Herbarium, University of California at Berkeley, California 94720-2465 USA
Received for publication April 4, 2002. Accepted for publication June 4, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Atlantic forest • foliicolous lichens • isidia • lichen development • Phycopeltis • Phyllophiale • Porina
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Stocker-Wörgötter and Türk, 1994
; Stocker-Wörgötter, 2001
), this approach does have some significant limitations. Many lichens seem to resist laboratory cultivation. Those lichens that can be cultivated rarely complete their life cycle in culture; moreover, cultured thalli often do not exactly resemble their natural counterparts. Furthermore, combining lichen symbionts artificially or cultivating them from thallus fragments might not be representative of how lichen reproduction and ontogeny actually occur in nature. One alternative approach has been to study lichen development on natural substrates placed in situ, using scanning electron microscopy to elucidate surface features of symbiont behavior (Schuster, Ott, and Jahns, 1985
).
Recent experiments have shown that the foliicolous (leaf-dwelling) crustose lichens of the humid tropics will colonize transparent artificial substrates in situ, permitting developmental study with the light microscope (Sanders, 2001a
; Sanders and Lücking, 2002
). In the course of studies of reproductive strategies in foliicolous lichens over a period of 1 yr, all developmental stages of the lichen Phyllophiale were observed and documented from propagule germination to propagule production. Phyllophiale differs in thallus organization from lichens with unicellular or short-filamentous phycobionts (algal symbionts), which is the usual situation in taxa of temperate latitudes. In Phyllophiale, the phycobiont is Phycopeltis, a member of the Trentepohliaceae that has a multicellular thallus of closely appressed, tightly branched radial filaments forming a monostromatic disc. The term "thallus" is thus applicable to the body of this phycobiont as well as to the lichen as a whole. On plant surfaces in the humid tropics, Phycopeltis commonly occurs free-living as well as incorporated within lichens. Because of its larger size and more complex growth form compared to most other phycobionts, the alga Phycopeltis may more directly influence the growth, shape, and development of the lichen thallus it forms with the fungus Phyllophiale. This hypothesis is evaluated in the present work, and other distinctive developmental features of the Phyllophiale–Phycopeltis symbiosis are discussed.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Young lichens containing the alga Phycopeltis were recognized as Phyllophiale by the presence of a remnant of the central attachment stalk by which the original propagule was attached to the mother thallus (Sanders, 2001a
). Older thalli were recognized by their production of the characteristic propagules. Examination of the literature and foliicolous collections indicated that Phyllophiale thalli developing on the cover slips represented either Phyllophiale alba (Fig. 1), which is particularly abundant at the field site, or P. viridis, which is structurally rather similar, differing slightly in the mature size and coloring of the isidia and in the texture of the thallus surface (Cáceres, 1998
; Lücking and Cáceres, 1999
). A third species occurring in the area, P. fusca, has an irregular arrangement of phycobiont filaments, which distinguishes it more readily from the other two species. Examination of foliicolous collections showed that the phycobiont occupies a relatively small central area in the mature propagule of P. alba as compared to those of the other two Phyllophiale taxa; the predominance of fungal tissue gives P. alba isidia their whitish cast. In most cases the mature characters necessary to distinguish between P. alba and P. viridis were not clearly evident in the developmental stages observed on the plastic cover slips. Because of this uncertainty, no species epithet is applied to the stages observed in this study. Examination of foliicolous collections of these two taxa suggests that they share the same basic developmental features described below.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). They resemble a shallow bowl or funnel attached to the thallus by a short central stalk, like a short-stemmed cocktail glass. The dispersed propagules observed on the substrate surface usually settled in an inverted position, with the remnant of the central attachment stalk facing upward. They subsequently became more flattened and disc-like, appearing as circular patches. The elongate fungal cells comprising the surface of the propagule were radially arranged and nearly uniform in length and thickness. Within the center of the propagule was a single young discoid thallus of the algal symbiont, Phycopeltis, with radial, dichotomously branched filaments (Fig. 2). Germination of colonizing propagules was observed within 3 wk of placement of the cover slips in the field; this occurred by outgrowth of the fungal cells at the propagule margin. The germination hyphae were distinguishable by their often slightly narrower diameter, more irregular growth trajectory, and branching and anastomosing behavior, as compared to the very straight and uniformly radial cells from which they first arose (Fig. 2). Thus, as the young lichen thalli developed, the radially oriented fungal cells of the original propagule gave way to a reticulum of anastomosing hyphae covering the growing Phycopeltis within (Fig. 3). These stages were also observed in preliminary experiments using glass slides as a substrate (Sanders, 2001a
). Conditions favorable for thallus establishment and development appeared to vary substantially within the microhabitat: degeneration of germinated Phyllophiale isidia was observed on some cover slips. The fungal structure deteriorated, their cells becoming devoid of cytoplasm. Sectors of the phycobiont disc died back, isolating peripheral lobes of growth (Fig. 4). The cells of the phycobiont in large portions of the propagule also became discolored and died; however, the outermost extremities of the algal filaments often gave rise to new, apparently unlichenized thalli of Phycopeltis near the margins of the degenerated propagule (Fig. 5).
The developing lichen maintained a prothallus of fungal hyphae advancing over the substrate beyond the radius of the phycobiont. The prothallic hyphae contacted free-living algal cells upon the substrate and often associated with them (Fig. 6). Only Phycopeltis appeared to be incorporated into the lichen thallus as a stable component (Fig. 7). The algal filament system maintained its monostromatic, laterally coherent radial organization within the lichen, although with increasing size the discoid shape often gave way to more lobate forms as growth became more heterogeneous along the algal thallus perimeter. Algal filament growth was generally restricted to a single plane, without filament overlapping or overgrowth. Lateral extension ceased at points of contact between adjacent Phycopeltis thalli within the lichen. As a result, individual phycobiont thalli were easily distinguished within the Phyllophiale lichen. Older thalli of Phyllophiale contained a mosaic of several to many abutting thalli of Phycopeltis (Fig. 8). The unbounded margins of the Phycopeltis thalli continued their growth, giving the lichen a lobed appearance. Gametangia were often observed on the lichenized algal thalli (Fig. 9). The stalked sporangia produced by aposymbiotic Phycopeltis at the field site (Sanders, 2001a
) were not observed on thalli lichenized by Phyllophiale. Where coalescence of the growing phycobionts was less rapid or less complete, the lichen appeared to consist of separated patches or areolae, each often bearing isidia at its periphery.
Scutelliform isidia began to appear on thalli of Phyllophiale 5–6 mo after placement of the substrate in the field. Production of an isidium was initiated by one to several algal filaments and associated fungal hyphae at the margin of the lichenized Phycopeltis thallus (Fig. 10). These algal filaments first extended slightly beyond their neighbors, rebranched, and initiated upward growth (Fig. 11). Branching of algal filaments was always observed to be apical and dichotomous. The isidial primordium comprised a stub-like bundle of fungal and algal filaments projecting vertically from the lichen surface. These rebranching filaments diverged radially thereafter to produce the goblet-shaped propagule directly above the margin of the Phycopeltis within the mother thallus. A transverse view of the base of the isidial stalk near the point of confluence with the thallus showed a filament or filaments of the phycobiont surrounded by a bundle of fungal cells (Fig. 12). The isidium always contained a single, central, radially symmetrical Phycopeltis thallus (Fig. 13). Although isidia were frequently observed in interior (nonmarginal) positions upon the lichen (Fig. 1), they arose in marginal position with respect to the phycobiont mother thalli within the lichen (Figs. 8, 10–12). Algal filaments giving rise to isidia by upward growth terminated their radial extension upon the substrate. However, continued growth and branching of horizontal filaments adjacent to those giving rise to the isidium typically converged to close the discontinuity left by isidial filaments growing upward (Fig. 14). This subsequent space-filling growth left the marginally produced isidium in an apparently submarginal or interior position. Isidium formation on larger thalli of Phyllophiale was particularly frequent at contacting margins of adjacent phycobiont thalli within the lichen (Fig. 8).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). They were the only lichens for which all stages of the (vegetative) life cycle could be observed upon the experimental substrate within the study period. The relatively large isidial propagule germinated and developed directly into a thallus, without any apparent reorganizational phase. These results contrast with assertions that lichen isidia cannot develop directly into a thallus but instead must first degenerate into a more loosely organized association of fungal and algal symbionts, from which a new thallus is eventually reorganized (Jahns, 1988
). This apparent discrepancy merely indicates that the variety of thallus outgrowths treated under the term "isidia" represent a very diverse and heterogeneous group of structures, with different developmental possibilities. Some isidia may serve mainly as incrementations of the thallus surface area (Henssen and Jahns, 1974
), acting facultatively as propagules when incidentally detached from the thallus. As fragments of differentiated tissue, such propagules may be more likely to require dedifferentiation and reorganization before giving rise to a young thallus. Other types of isidia seem to be more specialized for rapid development into new thalli soon after detachment and dispersal, with apparent pre-organization of growth zones. The isidia of Parmelia pastillifera, for example, are substantially differentiated, like miniature thalli, and develop directly when detached (Honegger, 1987
). The isidia of Lobaria pulmonaria also appear to germinate directly into young thalli without dedifferentiation (Scheidegger, 1995
). Clearly, the traditional categorization of so many lichen vegetative propagules as either soredia or isidia does not reflect their substantial heterogeneity in structure and ontogeny; a number of additional categories have been proposed in recognition of this diversity (Poelt, 1980
, 1995
). Further field studies are needed to determine the extent to which germination and establishment might vary among propagule types.
Phycobiont capability of sexual reproduction and dispersal
The production of sporangia or gametangia by phycobionts in the lichenized state is rarely reported. It is known in the trentepohliaceous phycobionts of Microtheliopsis (Santesson, 1952
; Lücking, 1994
). In the present study, the lichenized Phycopeltis thalli were capable of producing sessile intercalary gametangia that released flagellated cells through a distinct pore in the upper surface wall. Printz (1939)
referred to these structures as sporangia ("Kugelsporangien"), although he reported that the flagellated cells released were capable of sexual fusion. He further noted that the flagellated cells could also settle and germinate directly into new thalli. Thus, the functional presence of these structures on lichenized Phycopeltis thalli indicates that the alga is reproducing and dispersing independently, probably by both sexual and asexual means. This situation seems to contrast with that of the common lichen phycobiont Trebouxia, whose reproductive and dispersive possibilities appear to be much reduced in the lichenized state. Although culture studies show that Trebouxia species are capable of producing flagellated cells in the absence of the lichen fungus (Archibald, 1975
; Hildreth and Ahmadjian, 1981
), this process appears to be generally arrested in the lichenized state. The arrested zoospores do show evidence of flagellar initiation, which has led some researchers to suggest that zoospores might be liberated in a functional state from hydrated thalli (Slocum, Ahmadjian, and Hildreth, 1980
); however, this interpretation has been questioned (Tschermak-Woess, 1989
). Detailed studies of lichen phycobiont occurrence and behavior in the free-living state are much needed to evaluate the effects of symbiosis on phycobiont reproductive patterns and capacities. It is noteworthy that species of Phycopeltis are believed to have diplohaplontic (diplobiontic) life histories, with alternation of more or less isomorphic generations (Thompson and Wujek, 1997
). This raises the intriguing question of whether gametophyte and sporophyte are equally suitable as phycobionts, or whether a more specific and complex relationship exists between the life history of the alga and that of Phyllophiale and/or other fungi that lichenize it (see discussion of Porina below).
Prothallic growth and incorporation of additional phycobiont thalli
In many crustose lichens, the mycobiont forms a marginal fringe of hyphae, a prothallus or hypothallus, which grows out beyond the alga-containing portion of the thallus. Compatible phycobiont cells encountered externally on the substrate surface may be incorporated into the lichen at the growing margin. In Phyllophiale, a record of this incorporative process is strikingly apparent, since the young lichen initially contains a single phycobiont thallus, to which others are eventually added. In intermediate stages, the position of the algal thallus of the original propagule is sometimes recognizable when the propagule's attachment stalk can still be distinguished. Reproduction of the phycobiont occurs by flagellated cells (gametes and/or zoospores) that swim free of the lichen, as the fungal covering is not extensive enough to retain them. Depending on where the flagellated cells settle, however, the germling thalli might be subsequently incorporated into the same or another lichen by contact with the fungal prothallus. Although many other crustose lichens probably incorporate external algal cells by prothallic capture during growth, their internal phycobiont population usually also increases in number by abundant aplanospore or autospore formation entirely within the lichen thallus. In Phyllophiale and perhaps other lichens of similar construction, there does not appear to be any mechanism for maintaining the products of phycobiont sporogenesis within the confines of the lichen thallus; the progeny of its phycobiont are therefore always free-living, at least initially. Correspondingly, free-living Phycopeltis thalli are often observed abundantly in the vicinity of the lichenized form, in contrast to the situation with phycobionts such as Trebouxia. These observations suggest a lower degree of specialization of Phycopeltis for symbiosis with lichen fungi than that evident in Trebouxia lichen associations.
In the case of the phycobiont Trebouxia, some controversy exists concerning the status of aposymbiotic populations reported. Ahmadjian (1988)
suggested that such reports did not represent truly free-living Trebouxia populations but rather phycobiont cells liberated from degenerated propagules or thallus fragments. Whether such an origin should disqualify them as "free-living" will depend on their subsequent capacity to survive and reproduce, which cannot be evaluated here. Nonetheless, the present study does provide evidence that phycobionts can indeed be liberated from degenerating lichen propagules (Figs. 4–5). The importance of this process for free-living populations of Phycopeltis, however, may be of somewhat lesser significance than for those of Trebouxia, since Phycopeltis appears fully capable of producing free-living progeny even while lichenized by Phyllophiale. In view of the genetic diversity demonstrated in phycobiont genera examined so far, it is likely that dynamic interrelationships and genetic exchange exist between lichenized and free-living populations, even in the most highly coevolved lichen algae.
Morphological influences of phycobiont and mycobiont
Because so many lichens resemble plants quite dissimilar morphologically from either the fungal or the algal component (Sanders, 2001b
), the question of relative influence of the fungus vs. the alga on lichen thallus form has often been discussed. This relative influence appears to vary according to the lichen considered (Goebel, 1928
, pp. 66–67; Henssen and Jahns, 1974
, p. 18). In most lichens the fungus is the dominant structural component and has consequently been interpreted as most directly responsible for lichen thallus form. However, a conspicuous influence of the alga is evident in some lichens where a reduced structural presence of the fungus leaves the shape of the alga apparent or in other lichens where very different thallus forms are correlated with presence of a green vs. a blue-green phycobiont (e.g., Jordan, 1972
). In Phyllophiale, the multicellular discoid thalli of the phycobiont predominate, and the fungal contribution to the lichen structure is limited to a simple covering network and prothallus of hyphae. The radial form of the algal thallus is thus expressed in the discoid shape of the isidium and young thallus developing from it. Larger Phyllophiale thalli have a lobed or discontinuous appearance corresponding to the incorporation of additional thalli of Phycopeltis, as well as to the increasingly lobate growth of individual algal thalli with age. Similar correspondence of lichen thallus morphology to that of the phycobiont occurs in some lichenized forms of Trentepohlia, a close relative of Phycopeltis. When associated with lichen fungi such as Cystocoleus or Coenogonium, the filamentous form of the alga is relatively unaltered and is apparent in the overall form of the lichen thallus (Skuje and Ore, 1933
; Karling, 1934
; Meier and Chapman, 1983
). In crustose lichens of the Trichotheliaceae, Aptroot and Sipman (1993)
noted in general that when the phycobiont is the filamentous Trentepohlia, the lichen thallus tends to be continuous; when the phycobiont is Phycopeltis, the lichen thallus shows dispersed and rounded parts corresponding to the thallus form of that algal symbiont. In many other trentepohliaceous lichens, however, the structure of the alga may be greatly altered in symbiosis, showing no apparent correspondence to the overall form of the lichen thallus. Indeed, it is often the case that Phycopeltis and Trentepohlia cannot be readily distinguished from each other in the lichenized state. Matthews, Tucker, and Chapman (1989)
and Tucker, Matthews, and Chapman (1991)
relied on ultrastructural differences in filament crosswalls to distinguish these phycobiont genera within a number of epiphytic crustose lichens. However, the diagnostic character, a thickened ring of wall tissue surrounding the plasmodesmata, has been observed in but a single identified species of Phycopeltis, P. epiphyton (Chapman and Good, 1978
). Species-level identifications of Phycopeltis phycobionts appear to be lacking in the literature (Tschermak-Woess, 1988
), although the recent publication of a well-illustrated treatment of the genus (Thompson and Wujek, 1997
) may facilitate future work. Although differences in cell arrangement in trentepohliaceous phycobionts have been noted as useful characters in distinguishing some foliicolous lichen taxa (e.g., Sérusiaux, 1984
; Lücking, 1995
, 1996
), it remains unclear to what extent these distinctions may correspond to genetic/biosystematic differences in the phycobiont or to differences in the degree to which different lichen fungi may alter the growth form of their phycobiont. Culture studies of trentepohliaceous phycobionts are much needed to resolve these questions.
In Phyllophiale, isidial position is dependent on phycobiont position, since these propagules arise at points corresponding to the margins of the Phycopeltis thalli within the lichen. There is some tendency for isidia to be more frequent where adjacent phycobiont thalli abut within the thallus, suggesting that upward growth of the algal filaments might be to some extent stimulated where their continued lateral expansion is impeded. The morphogenetic influence of the lichenizing fungus in isidial production cannot be ignored, however. The vertical reorientation of algal filament growth in primordium initiation, followed by horizontal radiation and rebranching above the thallus to form the isidium, are key developmental features that are not observed in the unlichenized alga. Free-living Phycopeltis thalli commonly produce erect short-stalked sporangia (Chapman and Good, 1983
; Sanders, 2001a
), and some species have limited development of sterile erect filaments, structures that have not been observed on the lichenized algal thalli. Although developmental studies are lacking, illustrations from previous works treating Phycopeltis (Karsten, 1891
; Printz, 1939
) suggest that these specialized vertical outgrowths arise as lateral branches initiated by cell division on the upper surface of the horizontal filament system. By contrast, the isidial primordia of lichenized forms are produced marginally by upturning and dichotomous rebranching of filament tips. They appear to be vertical continuations of the horizontal vegetative filament system under the influence of the lichen fungus, rather than a modification of any of the specialized types of erect filaments known in Phycopeltis.
Relationship of Phyllophiale to Porina (Trichotheliaceae)
The genus Phyllophiale was proposed to include lichen fungi that reproduce asexually by scutelliform isidia; these fungi were believed to be independent of any known taxa of sexual fungi (Santesson, 1952
). More recent reports, however, described lichen thalli bearing scutelliform isidia exactly like those of Phyllophiale as well as fruiting bodies referable to the genus Porina in the Trichotheliaceae, suggesting that Phyllophiale should be considered as an asexual stage of Porina (Lücking, 1991
; Aptroot and Sipman, 1993
). A one-to-one correspondence between the three known species of Phyllophiale and three distinct species of Porina has been recently proposed (Lücking and Cáceres, 1999
). Those authors noted that, quite surprisingly, the three species of Porina with "Phyllophiale" stages are not considered to be closely related to each other within the large genus Porina. Until definitive evidence can be provided from molecular studies, they recommend retention of Phyllophiale for asexual isidiate thalli. The full cycle of development from propagule to propagule observed in the present study is therefore likely to be a portion of the lichen's complete life history, which may include a sexual Porina phase under certain, as yet undetermined, conditions.
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FOOTNOTES |
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2 Current address: Centro de Ciencias Medioambientales, C.S.I.C., Calle Serrano 115 bis, 28006 Madrid, Spain (william{at}ccma.csic.es
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ahmadjian V. L. A. Russell K. C. Hildreth 1980 Artificial reestablishment of lichens. I. Morphological interactions between the phycobiont of different lichens and the mycobionts of Cladonia cristatella and Lecanora chrysoleuca. Mycologia 72: 73-89[CrossRef][ISI]
Aptroot A. H. J. M. Sipman 1993 Trichotheliaceae. In A. R. A. Görts-van Rijn [ed.], Flora of the Guianas, Series E, Fascicle 2. Koeltz Scientific Books, Konigstein, Germany
Archibald P. A. 1975 Trebouxia de Pulmaly (Chlorophyceae, Chlorococcales) and Pseudotrebouxia gen. nov. (Chlorophyceae, Chlorosarcinales). Phycologia 14: 125-137
Cáceres M. E. S. 1998 Liquens Foliícolas da Mata Atlântica de Pernambuco (Brasil): Diversidade, Ecogeografia, e Conservação. Master's thesis, Universidade Federal de Pernambuco, Recife, Brazil
Chapman R. L. B. H. Good 1978 Ultrastructure of plasmodesmata and cross walls in Cephaleuros, Phycopeltis, and Trentepohlia (Chroolepidaceae, Chlorophyta). British Phycological Journal 13: 241-246[CrossRef][ISI]
Chapman R. L. B. H. Good 1983 Subaerial symbiotic green algae: interactions with vascular plant hosts. In L. J. Goff [ed.], Algal symbiosis. Cambridge University Press, Cambridge, UK
Goebel K. 1928 Organographie der Pflanzen. Dritte Auflage. I. Allgemeine Organographie. Gustav Fischer, Jena, Germany
Henssen A. H. M. Jahns 1974 Lichenes: Eine Einführung in die Flechtenkunde. Georg Thieme, Stuttgart, Germany
Hildreth K. C. V. Ahmadjian 1981 A study of Trebouxia and Pseudotrebouxia isolates from different lichens. Lichenologist 13: 65-86
Honegger R. 1987 Isidium formation and the development of juvenile thalli in Parmelia pastillifera. Botanica Helvetica 97: 147-152[ISI]
Jahns H. M. 1988 The lichen thallus. In M. Galun [ed.], CRC handbook of lichenology, vol. I. CRC Press, Boca Raton, Florida, USA
Jordan W. P. 1972 Erumpent cephalodia, an apparent case of phycobial influence on lichen morphology. Journal of Phycology 8: 112-117[ISI]
Karling J. S. 1934 A preliminary contribution to the structure and development of Coenogonium linkii. Annals of Botany 48: 823-855
Karsten G. 1891 Untersuchungen über die Familie der Chroolepideen. Annales du Jardin Botanique de Buitenzorg 10: 1-66
Lücking R. 1991 Neue Arten foliikoler Flechten aus Costa Rica, Zentralamerika. Nova Hedwigia 52: 267-304[ISI]
Lücking R. 1994 A new foliicolous species of Microtheliopsis (Lichens, Microtheliopsidaceae) from Costa Rica. Mycotaxon 51: 69-73[ISI]
Lücking R. 1995 Additions and corrections to the foliicolous lichen flora of Costa Rica: the family Arthoniaceae, with notes on the genus Stirtonia. Lichenologist 27: 127-153[ISI]
Lücking R. 1996 Taxonomic studies in foliicolous species of the lichen genus Porina. I. The Porina rufula aggregate. Botanica Acta 109: 248-260[ISI]
Lücking R. M. Cáceres 1999 New species or interesting records of foliicolous lichens. IV. Porina pseudoapplanata (lichenized ascomycetes: Trichotheliaceae), a remarkable new species with Phyllophiale-type isidia. Lichenologist 31: 349-358[ISI]
Matthews S. S. C. Tucker R. L. Chapman 1989 Ultrastructural features of mycobionts and trentepohliaceous phycobionts in selected subtropical crustose lichens. Botanical Gazette 150: 417-438
Meier J. L. R. L. Chapman 1983 Ultrastructure of the lichen Coenogonium interplexum Nyl. American Journal of Botany 70: 400-407[CrossRef][ISI]
Poelt J. 1980 Physcia opuntiella s.n. und die Lebensform der sprossende Flechten. Flora 169: 23-31[ISI]
Poelt J. 1995 On lichenized asexual diaspores in foliose lichens—a contribution towards a more differentiated nomenclature (Lichens, Lecanorales). Cryptogamic Botany 5: 159-162
Printz H. 1939 Vorarbeiten zu einer Monographie der Trentepohliaceen. Nytt Magasin for Naturvidenskapene 80: 137-210
Sanders W. B. 2001a Preliminary light microscope observations of fungal and algal colonization and lichen thallus initiation on glass slides placed near foliicolous lichen communities within a lowland tropical forest. Symbiosis 31: 85-94
Sanders W. B. 2001b Lichens: the interface between mycology and plant morphology. BioScience 51: 1025-1035[CrossRef][ISI]
Sanders W. B. R. Lücking 2002 Reproductive strategies, relichenization, and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425-435[CrossRef][ISI]
Santesson R. 1952 Foliicolous Lichens. I. Symbolae Botanicae Upsaliensis 12: 1-590
Scheidegger C. 1995 Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27: 361-374[ISI]
Schuster G. S. Ott H. M. Jahns 1985 Artificial cultures of lichens in the natural environment. Lichenologist 17: 247-253[CrossRef][ISI]
Sérusiaux E. 1984 New species or interesting records of foliicolous lichens. Mycotaxon 20: 283-306[ISI]
Skuja H. M. Ore 1933 Die Flechte Coenogonium nigrum (Huds.) Zahlbr. und ihre Gonidie. Acta Horti Botanici Universitatis Latviensis 8: 21-44
Slocum R. D. V. Ahmadjian K. C. Hildreth 1980 Zoosporogenesis in Trebouxia gelatinosa: ultrastructural potential for zoospore release and implications for the lichen association. Lichenologist 12: 173-187[CrossRef][ISI]
Stocker-Wörgötter E. 2001 Experimental lichenology and microbiology of lichens: culture experiments, secondary chemistry of cultured mycobionts, resynthesis, and thallus morphogenesis. Bryologist 104: 576-581[CrossRef][ISI]
Stocker-Wörgötter E. R. Türk 1994 Artificial resynthesis of the photosymbiodeme Peltigera leucophlebia under laboratory conditions. Cryptogamic Botany 4: 300-308
Thompson R. H. D. E. Wujek 1997 Trentepohliales: Cephaleuros, Phycopeltis, and Stomatochroon. Morphology, taxonomy, and ecology. Science Publishers, Enfield, New Hampshire, USA
Tschermak-Woess E. 1988 The algal partner. In M. Galun [ed.], CRC handbook of lichenology, vol. I, 39–92. CRC Press, Boca Raton, Florida, USA
Tschermak-Woess E. 1989 Developmental studies in trebouxioid algae and taxonomical consequences. Plant Systematics and Evolution 164: 161-195[CrossRef][ISI]
Tucker S. C. S. W. Matthews R. L. Chapman 1991 Ultrastructure of subtropical crustose lichens. In D. J. Galloway [ed.], Tropical lichens: their systematics, conservation, and ecology, 171–191. Clarendon Press, Oxford, UK
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