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A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens

A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with... Abstract Phyllopsora dominicanus sp. nov. (Bacidiaceae, Lecanorales, lichen-forming Ascomycota) is described and illustrated from Dominican amber. The diagnostic features of the lichen include a minute subfolious thallus of lacinulate, ascending squamules, a well-developed upper cortex, and a net-like pseudocortex on the lower surface. The algal symbionts are unicellular green algae, forming a distinct layer immediately below the upper cortex. The fossil demonstrates that distinguishing features of Phyllopsora have remained unchanged for tens of millions of years. The fossil also provides the first detailed views of mycobiont–photobiont contacts in Tertiary green algal lichens. The mycobiont hyphae formed apical and intercalary appressoria by pressing closely against the photobiont cells. This indicates that a conserved maintenance of structure is also seen in the fine details of the fungal–algal interface. Amber, fossil, fungi, lichen, Phyllopsora, symbiosis, Tertiary Introduction Lichen fossils are surprisingly rare. Green and Lange (1994) pointed out that problems of fossilization may be the most important reason for this overall scarcity. Fossil assemblages are indeed notorious for their many biases. For example, many ancient lichens may have lived in relatively dry habitats where they were not likely to become fossilized. Still, perhaps the best explanation for the apparent absence of fossil lichens is our relative inability to recognize them in the fossil record (Taylor and Osborne, 1996). Yuan et al. (2005) reported the discovery of lichen-like fossils, involving filamentous hyphae closely associated with coccoidal cyanobacteria or algae, preserved in marine phosphorite in South China. The oldest fossils were >600 million years old and indicated that filamentous fungi had already developed symbiotic partnerships with photoautotrophs before the evolution of vascular plants. Taylor et al. (1997) described a lichen-like fossil from the Early Devonian Rhynie chert. This 400 million-year-old specimen was described in a new genus Winfrenatia, and the authors proposed that its fungal component may have been an early zygomycete. The Rhynie chert paleoecosystem continues to provide invaluable information on many types of ancient fungal organisms and associations (Taylor et al., 2004a, 2005; Berbee and Taylor, 2007; Krings et al., 2007). A number of early enigmatic fossils such as the Paleozoic Prototaxites (Taylor and Osborn, 1996; Selosse, 2002; Boyce et al., 2007), the Lower to Middle Devonian Spongiophyton (Stein et al., 1993; Jahren et al., 2003; Flecher et al., 2004; Taylor et al., 2004b), and even some Ediacaran fossils (Retallack, 1994; Peterson et al., 2003; Butterfield, 2005) may have shared a lichen-like ecology. However, the hypothesis that some of these ancient organisms or associations were functionally similar to extant lichens does not necessarily imply that they were directly related to extant lichen-forming fungi. Amber fossils have shown that some modern lichen genera, and probably even species, were already present in the Tertiary. The first reports of lichen remains in Baltic amber were from the mid-19th century. The old literature records have been catalogued by Spahr (1993), but the original specimens remain to be located and reinvestigated. Mägdefran (1957) described a fertile alectorioid lichen from Baltic amber. Two fossil species of Parmelia s. lat. were described from Dominican amber by Poinar et al. (2000), and two specimens of Anzia have been found from European amber (Rikkinen and Poinar, 2002). Recently, an unidentified lichen was reported from Peruvian Miocene amber (Antoine et al., 2006). No inclusions of cyanolichens have yet been found from amber. However, a 12–24 million-year-old impression of a foliose macrolichen belonging to Lobariaceae was reported by Peterson (2000) from the Weaverville deposits of California. Apparently, only two amber fossils of crustose lichens have ever been found. These European fossils were basically identical to some modern Calicium and Chaenotheca species (Rikkinen, 2003). Also a non-lichenized, resinicolous Chaenothecopsis species was found from European amber (Rikkinen and Poinar, 2000). Extant species of this genus include not only resinicolous and saprophytic taxa, but also lichen parasites or parasymbionts. In addition, there is the impression of Pelicothallos villosus from Eocene deposits of Tennessee. This fossil has been interpreted as either a foliicolous green alga (Pirozynski, 1976) or a lichen (Sherwood-Pike, 1985). In addition to the fossils listed above, only unidentifiable lichen fragments have been reported from amber specimens (Garty et al., 1982; Rikkinen 2002). However, both public and private amber collections are likely to include many superficially studied or unidentified lichen fossils that still await detailed analysis (Pielinska, 1990). As phylogenetic hypotheses are constantly refined for different groups of lichens, even a very limited number of well-preserved fossils can be used to give minimum time estimates for major branching events. For example, Arup et al. (2007) found that Parmeliaceae seems to represent a well-supported group that also includes the sometimes recognized family segregates Alectoriaceae, Hypogymniaceae, Usneaceae, and Anziaceae. Baltic amber fossils give concrete evidence that species of several, if not all, of the family segregates were already present 40–60 million years ago. Hence, deep branching within the family, and particularly within the order Lecanorales, must have occurred very early, most probably during the Cretaceous. Here a fossil species of Phyllopsora Müll. Arg. (Bacidiaceae, Lecanorales, lichen-forming Ascomycota) from amber is described and the first detailed views of fungal–algal contacts in Tertiary green algal lichens are provided. The amber fossil originates from mines of the Dominican Republic in the Caribbean. The same deposits have produced tens of thousands of other fossils, together representing the largest assemblage of fossil invertebrates, bryophytes, lichens, and fungi in a terrestrial tropical environment (Poinar and Poinar, 1999; Arillo and Ortuno, 2005; Frahm and Newton, 2005). Materials and methods The fossilized lichen is preserved in a large fragment (40×36×3 mm) of Dominican amber (Poinar B 1–23, in the Poinar amber collection maintained at Oregon State University, USA). Dominican amber is fossilized exudate of the now extinct leguminous tree Hymenaea protera Poinar (Poinar, 1991). During fossilization, terpenoid materials of the exudate were progressively oxidized and polymerized to a point where they became resistant against chemical and biological degradation. The amber specimen originated from the amber mines in the Cordillera Septentrional of the Dominican Republic. These mines are in the El Mamey Formation (Upper Eocene), which is a shale–sandstone interspersed with a conglomerate of well-rounded pebbles (Eberle et al., 1980). The exact age of Dominican amber is unknown, with estimates ranging from 15–20 million years on the basis of foraminifera counts to 30–45 million years from studies with coccolith fossils (Schlee, 1990; Iturralde-Vincent and MacPhee, 1996; Poinar, 2002). The amber piece had been cut and polished to facilitate screening for inclusions. During polishing some squamules had been brought to the surface and sectioned. This provides the opportunity also to study some internal structures of the lichen, including the photobiont layer. In this study, no further destructive sampling was performed. All measurements and photographs were taken from the intact specimen under transmitted and/or incident light. Optical distortions were neutralized by coating the specimen in vegetable oil. Results Phyllopsora dominicanus Rikkinen, sp. nov. (Fig. 1) Lichen fossilis, in sucino asservatus. Thallus squamiformis vel subfoliaceus, laciniis elongatae, diameter 0.2–1.0 mm, ascendentes. Cortex crassus, typo 1–2. Fig. 1. View largeDownload slide Phyllopsora dominicanus (HOLOTYPE). (A) Squamiform to subfoliose thallus fragments preserved together with bryophyte remains, scale bar = 10 mm. (B) Ascending thallus lobes of P. dominicanus, scale bar = 2 mm. (D) Photobiont layer under the upper cortex of a cross-sectioned squamule, scale bar = 10 μm. (D) Fungal–algal interface of P. dominicanus. Note the dark, shrivelled chloroplast/protoplast inside the algal cell and a hyphal tip pressing against the algal surface (from below), scale bar = 5 μm. Fig. 1. View largeDownload slide Phyllopsora dominicanus (HOLOTYPE). (A) Squamiform to subfoliose thallus fragments preserved together with bryophyte remains, scale bar = 10 mm. (B) Ascending thallus lobes of P. dominicanus, scale bar = 2 mm. (D) Photobiont layer under the upper cortex of a cross-sectioned squamule, scale bar = 10 μm. (D) Fungal–algal interface of P. dominicanus. Note the dark, shrivelled chloroplast/protoplast inside the algal cell and a hyphal tip pressing against the algal surface (from below), scale bar = 5 μm. HOLOTYPUS: Poinar B 1–23, collection maintained at Oregon State University, USA. Fossil lichen, preserved in amber. Thallus squamiform to subfoliose, ascending, prothallus not seen. Squamules elongated, lachinulate, flat, or slightly convex, 0.2–1.0 mm wide. Upper surface with well-developed cortex, 20–60 mm thick, of type 1–2 (Swinscow and Krog, 1981). Lower surface with net-like pseudocortex. Medulla composed of loosely interwoven hyphae. Photobionts unicellular green algae, diameter 8–12 mm, forming a layer immediately below the upper cortex. Soralia, isidia, and rhizines absent. Ascomata and pycnidia not seen. Phyllopsora dominicanus is characterized by its minute thallus of ascending, partly overlapping squamules, which by repeated proliferations have become more or less lacinulate (Fig. 1B). The upper surface of the thallus has a well-developed cortex, which may at the lobe tips extend slightly over the thallus margins. The surface of the cortex varies from smooth to irregular. In places, the cortex hyphae are highly gelatinized with narrow hyphal lumina forming a network of thread-like channels. The lower surface of the lichen thallus is delimited by a very loose, net-like pseudocortex. The photobionts, representing unicellular green algae, form a distinct layer immediately below the upper cortex (Fig. 1C). The photobiont cells average ∼10 μm in diameter and contain dark amorphous bodies representing shrivelled protoplasts and/or chloroplasts. The photobiont cells are intimately associated with mycobiont hyphae. Fungal hyphae often follow the contours of algae and form appressoria against their cell walls (Fig. 1D). The contacts may be apical or intercalary, and some hyphae had formed several successive contact points. No intracellular haustoria are seen. However, peg-like haustoria are often difficult to detect even in fresh lichen specimens. Discussion The overall scarcity of lichen fossils in amber is undoubtedly partly explained by the morphological characteristics of lichen thalli. Most crustose epiphytes grow tightly attached to bark and are likely only to be preserved together with their substrate. While amber prospectors and entomologists search for amber inclusions, such ‘obscuring debris’ is often polished away, and, even if preserved, tightly attached fragments of crustose lichens are extremely difficult to recognize as such, especially if deeply imbedded in amber. Some lichens produce soredia or other vegetative diaspores, but such tiny fragments are very unlikely to be recognized as lichen remains. The structural features of foliose and fruticose macrolichens may also hinder their preservation in amber. During initial contact with fresh resin, the relatively thick and three-dimensional thalli will usually be only partly enclosed in resin: almost invariably some thallus lobe is left protruding. This provides a perfect starting point for the decay of the immersed lichen fragment, and the subsequent weathering of the hardened or fossilized resin. One may presume that obvious differences in preservation potentials partly account for the apparent proportional imbalance of leafy bryophytes and lichens in European and Neotropical ambers, for example (Frahm et al., 2007). The thallus morphology and anatomy of modern Phyllopsora species have been described in detail by Swinscow and Krog (1981) and Brako (1991). Slightly different views of species delimitation have been expressed in recent treatments of the genus. However, the growth form, presence, and nature of symbiotic propagules, the pruinosity and pubescence of the thallus, features of the upper cortex, ascus, and spore characteristics, thallus chemistry, and to some degree also the structure of the prothallus have been used in the circumscription of modern species (Swinscow and Krog, 1981; Brako, 1989, 1991; Timdal and Krog, 2001). All structural features of P. dominicanus have close parallels in modern species: a more or less identical combination of features is found in several extant taxa, including P. chlorophaea (Müll. Arg.) Zahlbr. However, as many Phyllopsora species are morphologically quite plastic and reliable identification typically requires close examination of spores and/or thallus chemistry, the fossil cannot be safely assigned to any extant species. The fossilized lichen does not have apothecia nor isidia. However, it did produce small dorsiventral thallus sections deeply constricted at the base. Similar apical and/or marginal lachinules are characteristic of several modern, non-isidiate Phyllopsora species (Timdal and Krog, 2001). Lacinules are easily shed and they probably play a role in the vegetative reproduction of the lichens. The fossil specimen does not have an obvious filamentous prothallus, typical of all extant Phyllopsora species. However, even if P. dominicanus did produce a prothallus, this may not have been preserved, as the preserved fragments of the thallus only consist of ascending squamules. In addition to the Phyllopsora thallus, the amber specimen also contains a variety of other biological inclusions, including insect fragments, a small fungal mycelium (Rikkinen and Poinar, 2001), yeast-like fungal cells (Rikkinen and Poinar, 2002), and remains of several bryophyte species (JRikkinen et al., unpublished results). The bryophytes include two mosses (Octoblepharum sp. and Syrrhopodon sp.) and at least two hepatics (Aphanolejeunea sp. and Cololejeunea sp.). All these bryophytes belong to extant genera that are widely distributed in the Tropics (Gradstein, 1993; Frahm and Newton, 2005). Extant Phyllopsora species are predominantly tropical and subtropical, with few extensions into the temperate zone (Swinscow and Krog, 1981; Brako, 1991; Timdal and Krog, 2001; Upreti et al., 2003). Several species are pantropical, and both widespread and common in the Neotropics, including the Caribbean region. For example, Brako (1991) listed 11 species and varieties from the Dominican Republic in her monograph of the Neotropical taxa. Printzen and Lumbsch (2000) used paleoclimatic data and evidence of forest history to calibrate a molecular clock based on fungal ITS sequences of Phyllopsora and Biatora. Structural differences between the two genera are small and they also share a similar habitat ecology. However, despite being closely related, the genera are almost strictly allopatric, with Phyllopsora being tropical and Biatora restricted to temperate and cool regions of the Northern hemisphere. The authors concluded that the two genera were first separated 170–140 million years BP, when the expanding Tethys ocean started to separate Laurasia completely from Gondwana. Later diversification within Biatora was linked to periods of climate cooling, when new forest vegetation types evolved and spread in the Northern hemisphere. Thus, while anatomical, morphological, and chemical differences between Biatora and Phyllopsora are relatively small, the genera appear to be phylogenetically old (Printzen and Lumbsch, 2000). This general conclusion is supported by the current findings. Most extant Phyllopsora species are corticolous or lignicolous, but some species also grow on rocks and bryophytes. Phyllospora dominicanus seems to have had a similar ecology. All organisms preserved in the amber specimen indicate an epiphytic or epixylic microhabitat in a tropical forest. The ancient community seems to have been entrapped in place, possibly by viscous exudate running down a tree trunk or dripping from the forest canopy. The preservation of actively reproducing filamentous fungi and yeasts may indicate a sudden preservation event during moist conditions (Rikkinen and Poinar, 2001, 2002). The photobionts of most extant lichens are coccoid green algae. Some 40% of all lichen-forming fungi associate with Trebouxia or related green algae (Trebouxiophyceae). These photobionts are particularly dominant in lichen species of cool and temperate regions, but also occur in many tropical lichen genera. The photobionts of modern Phyllopsora species have not been studied in any detail but, when analysed, they have been identified as belonging to Pseudochlorella (Chlorellales, Trebouxiophyceae) (Brako, 1991). The exchange of metabolites requires intricate connections between lichen symbionts, and several types of fungal–algal contacts are known from green algal lichens. While some lichen mycobionts penetrate deeply into photobiont cells, most produce specialized haustoria in which the surface layers of the fungal hyphae spread to cover the algal cells. Water, minerals, and metabolites are then translocated between this fungal-derived surface layer and the symbiotic algal cell (Ahmadjian, 1993; Honegger, 2001). Also, in the fossil, the mycobiont hyphae follow the contours of algae and press closely against their cell walls. No intracellular haustoria are seen. However, tiny peg-like haustoria are very difficult to detect even in fresh lichen specimens. Amber fossils have shown that several lineages among epiphytic lichens and fungi have conserved their morphological adaptations to successful ecological niches. Subsequently, many genera and possibly even species have remained more or less unchanged for tens of millions of years (Rikkinen and Poinar, 2000, 2002; Rikkinen, 2003; Rikkinen et al., 2003; Dörfelt and Schmidt, 2005). The present new findings show that this phenomenon is also seen in the epiphytic lichen genus Phyllopsora. A conserved maintenance of structural features seems also to apply to fine details of the fungal–algal interface. 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A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens

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Publisher
Oxford University Press
Copyright
© The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org
ISSN
0022-0957
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1460-2431
DOI
10.1093/jxb/ern004
pmid
18319239
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Abstract

Abstract Phyllopsora dominicanus sp. nov. (Bacidiaceae, Lecanorales, lichen-forming Ascomycota) is described and illustrated from Dominican amber. The diagnostic features of the lichen include a minute subfolious thallus of lacinulate, ascending squamules, a well-developed upper cortex, and a net-like pseudocortex on the lower surface. The algal symbionts are unicellular green algae, forming a distinct layer immediately below the upper cortex. The fossil demonstrates that distinguishing features of Phyllopsora have remained unchanged for tens of millions of years. The fossil also provides the first detailed views of mycobiont–photobiont contacts in Tertiary green algal lichens. The mycobiont hyphae formed apical and intercalary appressoria by pressing closely against the photobiont cells. This indicates that a conserved maintenance of structure is also seen in the fine details of the fungal–algal interface. Amber, fossil, fungi, lichen, Phyllopsora, symbiosis, Tertiary Introduction Lichen fossils are surprisingly rare. Green and Lange (1994) pointed out that problems of fossilization may be the most important reason for this overall scarcity. Fossil assemblages are indeed notorious for their many biases. For example, many ancient lichens may have lived in relatively dry habitats where they were not likely to become fossilized. Still, perhaps the best explanation for the apparent absence of fossil lichens is our relative inability to recognize them in the fossil record (Taylor and Osborne, 1996). Yuan et al. (2005) reported the discovery of lichen-like fossils, involving filamentous hyphae closely associated with coccoidal cyanobacteria or algae, preserved in marine phosphorite in South China. The oldest fossils were >600 million years old and indicated that filamentous fungi had already developed symbiotic partnerships with photoautotrophs before the evolution of vascular plants. Taylor et al. (1997) described a lichen-like fossil from the Early Devonian Rhynie chert. This 400 million-year-old specimen was described in a new genus Winfrenatia, and the authors proposed that its fungal component may have been an early zygomycete. The Rhynie chert paleoecosystem continues to provide invaluable information on many types of ancient fungal organisms and associations (Taylor et al., 2004a, 2005; Berbee and Taylor, 2007; Krings et al., 2007). A number of early enigmatic fossils such as the Paleozoic Prototaxites (Taylor and Osborn, 1996; Selosse, 2002; Boyce et al., 2007), the Lower to Middle Devonian Spongiophyton (Stein et al., 1993; Jahren et al., 2003; Flecher et al., 2004; Taylor et al., 2004b), and even some Ediacaran fossils (Retallack, 1994; Peterson et al., 2003; Butterfield, 2005) may have shared a lichen-like ecology. However, the hypothesis that some of these ancient organisms or associations were functionally similar to extant lichens does not necessarily imply that they were directly related to extant lichen-forming fungi. Amber fossils have shown that some modern lichen genera, and probably even species, were already present in the Tertiary. The first reports of lichen remains in Baltic amber were from the mid-19th century. The old literature records have been catalogued by Spahr (1993), but the original specimens remain to be located and reinvestigated. Mägdefran (1957) described a fertile alectorioid lichen from Baltic amber. Two fossil species of Parmelia s. lat. were described from Dominican amber by Poinar et al. (2000), and two specimens of Anzia have been found from European amber (Rikkinen and Poinar, 2002). Recently, an unidentified lichen was reported from Peruvian Miocene amber (Antoine et al., 2006). No inclusions of cyanolichens have yet been found from amber. However, a 12–24 million-year-old impression of a foliose macrolichen belonging to Lobariaceae was reported by Peterson (2000) from the Weaverville deposits of California. Apparently, only two amber fossils of crustose lichens have ever been found. These European fossils were basically identical to some modern Calicium and Chaenotheca species (Rikkinen, 2003). Also a non-lichenized, resinicolous Chaenothecopsis species was found from European amber (Rikkinen and Poinar, 2000). Extant species of this genus include not only resinicolous and saprophytic taxa, but also lichen parasites or parasymbionts. In addition, there is the impression of Pelicothallos villosus from Eocene deposits of Tennessee. This fossil has been interpreted as either a foliicolous green alga (Pirozynski, 1976) or a lichen (Sherwood-Pike, 1985). In addition to the fossils listed above, only unidentifiable lichen fragments have been reported from amber specimens (Garty et al., 1982; Rikkinen 2002). However, both public and private amber collections are likely to include many superficially studied or unidentified lichen fossils that still await detailed analysis (Pielinska, 1990). As phylogenetic hypotheses are constantly refined for different groups of lichens, even a very limited number of well-preserved fossils can be used to give minimum time estimates for major branching events. For example, Arup et al. (2007) found that Parmeliaceae seems to represent a well-supported group that also includes the sometimes recognized family segregates Alectoriaceae, Hypogymniaceae, Usneaceae, and Anziaceae. Baltic amber fossils give concrete evidence that species of several, if not all, of the family segregates were already present 40–60 million years ago. Hence, deep branching within the family, and particularly within the order Lecanorales, must have occurred very early, most probably during the Cretaceous. Here a fossil species of Phyllopsora Müll. Arg. (Bacidiaceae, Lecanorales, lichen-forming Ascomycota) from amber is described and the first detailed views of fungal–algal contacts in Tertiary green algal lichens are provided. The amber fossil originates from mines of the Dominican Republic in the Caribbean. The same deposits have produced tens of thousands of other fossils, together representing the largest assemblage of fossil invertebrates, bryophytes, lichens, and fungi in a terrestrial tropical environment (Poinar and Poinar, 1999; Arillo and Ortuno, 2005; Frahm and Newton, 2005). Materials and methods The fossilized lichen is preserved in a large fragment (40×36×3 mm) of Dominican amber (Poinar B 1–23, in the Poinar amber collection maintained at Oregon State University, USA). Dominican amber is fossilized exudate of the now extinct leguminous tree Hymenaea protera Poinar (Poinar, 1991). During fossilization, terpenoid materials of the exudate were progressively oxidized and polymerized to a point where they became resistant against chemical and biological degradation. The amber specimen originated from the amber mines in the Cordillera Septentrional of the Dominican Republic. These mines are in the El Mamey Formation (Upper Eocene), which is a shale–sandstone interspersed with a conglomerate of well-rounded pebbles (Eberle et al., 1980). The exact age of Dominican amber is unknown, with estimates ranging from 15–20 million years on the basis of foraminifera counts to 30–45 million years from studies with coccolith fossils (Schlee, 1990; Iturralde-Vincent and MacPhee, 1996; Poinar, 2002). The amber piece had been cut and polished to facilitate screening for inclusions. During polishing some squamules had been brought to the surface and sectioned. This provides the opportunity also to study some internal structures of the lichen, including the photobiont layer. In this study, no further destructive sampling was performed. All measurements and photographs were taken from the intact specimen under transmitted and/or incident light. Optical distortions were neutralized by coating the specimen in vegetable oil. Results Phyllopsora dominicanus Rikkinen, sp. nov. (Fig. 1) Lichen fossilis, in sucino asservatus. Thallus squamiformis vel subfoliaceus, laciniis elongatae, diameter 0.2–1.0 mm, ascendentes. Cortex crassus, typo 1–2. Fig. 1. View largeDownload slide Phyllopsora dominicanus (HOLOTYPE). (A) Squamiform to subfoliose thallus fragments preserved together with bryophyte remains, scale bar = 10 mm. (B) Ascending thallus lobes of P. dominicanus, scale bar = 2 mm. (D) Photobiont layer under the upper cortex of a cross-sectioned squamule, scale bar = 10 μm. (D) Fungal–algal interface of P. dominicanus. Note the dark, shrivelled chloroplast/protoplast inside the algal cell and a hyphal tip pressing against the algal surface (from below), scale bar = 5 μm. Fig. 1. View largeDownload slide Phyllopsora dominicanus (HOLOTYPE). (A) Squamiform to subfoliose thallus fragments preserved together with bryophyte remains, scale bar = 10 mm. (B) Ascending thallus lobes of P. dominicanus, scale bar = 2 mm. (D) Photobiont layer under the upper cortex of a cross-sectioned squamule, scale bar = 10 μm. (D) Fungal–algal interface of P. dominicanus. Note the dark, shrivelled chloroplast/protoplast inside the algal cell and a hyphal tip pressing against the algal surface (from below), scale bar = 5 μm. HOLOTYPUS: Poinar B 1–23, collection maintained at Oregon State University, USA. Fossil lichen, preserved in amber. Thallus squamiform to subfoliose, ascending, prothallus not seen. Squamules elongated, lachinulate, flat, or slightly convex, 0.2–1.0 mm wide. Upper surface with well-developed cortex, 20–60 mm thick, of type 1–2 (Swinscow and Krog, 1981). Lower surface with net-like pseudocortex. Medulla composed of loosely interwoven hyphae. Photobionts unicellular green algae, diameter 8–12 mm, forming a layer immediately below the upper cortex. Soralia, isidia, and rhizines absent. Ascomata and pycnidia not seen. Phyllopsora dominicanus is characterized by its minute thallus of ascending, partly overlapping squamules, which by repeated proliferations have become more or less lacinulate (Fig. 1B). The upper surface of the thallus has a well-developed cortex, which may at the lobe tips extend slightly over the thallus margins. The surface of the cortex varies from smooth to irregular. In places, the cortex hyphae are highly gelatinized with narrow hyphal lumina forming a network of thread-like channels. The lower surface of the lichen thallus is delimited by a very loose, net-like pseudocortex. The photobionts, representing unicellular green algae, form a distinct layer immediately below the upper cortex (Fig. 1C). The photobiont cells average ∼10 μm in diameter and contain dark amorphous bodies representing shrivelled protoplasts and/or chloroplasts. The photobiont cells are intimately associated with mycobiont hyphae. Fungal hyphae often follow the contours of algae and form appressoria against their cell walls (Fig. 1D). The contacts may be apical or intercalary, and some hyphae had formed several successive contact points. No intracellular haustoria are seen. However, peg-like haustoria are often difficult to detect even in fresh lichen specimens. Discussion The overall scarcity of lichen fossils in amber is undoubtedly partly explained by the morphological characteristics of lichen thalli. Most crustose epiphytes grow tightly attached to bark and are likely only to be preserved together with their substrate. While amber prospectors and entomologists search for amber inclusions, such ‘obscuring debris’ is often polished away, and, even if preserved, tightly attached fragments of crustose lichens are extremely difficult to recognize as such, especially if deeply imbedded in amber. Some lichens produce soredia or other vegetative diaspores, but such tiny fragments are very unlikely to be recognized as lichen remains. The structural features of foliose and fruticose macrolichens may also hinder their preservation in amber. During initial contact with fresh resin, the relatively thick and three-dimensional thalli will usually be only partly enclosed in resin: almost invariably some thallus lobe is left protruding. This provides a perfect starting point for the decay of the immersed lichen fragment, and the subsequent weathering of the hardened or fossilized resin. One may presume that obvious differences in preservation potentials partly account for the apparent proportional imbalance of leafy bryophytes and lichens in European and Neotropical ambers, for example (Frahm et al., 2007). The thallus morphology and anatomy of modern Phyllopsora species have been described in detail by Swinscow and Krog (1981) and Brako (1991). Slightly different views of species delimitation have been expressed in recent treatments of the genus. However, the growth form, presence, and nature of symbiotic propagules, the pruinosity and pubescence of the thallus, features of the upper cortex, ascus, and spore characteristics, thallus chemistry, and to some degree also the structure of the prothallus have been used in the circumscription of modern species (Swinscow and Krog, 1981; Brako, 1989, 1991; Timdal and Krog, 2001). All structural features of P. dominicanus have close parallels in modern species: a more or less identical combination of features is found in several extant taxa, including P. chlorophaea (Müll. Arg.) Zahlbr. However, as many Phyllopsora species are morphologically quite plastic and reliable identification typically requires close examination of spores and/or thallus chemistry, the fossil cannot be safely assigned to any extant species. The fossilized lichen does not have apothecia nor isidia. However, it did produce small dorsiventral thallus sections deeply constricted at the base. Similar apical and/or marginal lachinules are characteristic of several modern, non-isidiate Phyllopsora species (Timdal and Krog, 2001). Lacinules are easily shed and they probably play a role in the vegetative reproduction of the lichens. The fossil specimen does not have an obvious filamentous prothallus, typical of all extant Phyllopsora species. However, even if P. dominicanus did produce a prothallus, this may not have been preserved, as the preserved fragments of the thallus only consist of ascending squamules. In addition to the Phyllopsora thallus, the amber specimen also contains a variety of other biological inclusions, including insect fragments, a small fungal mycelium (Rikkinen and Poinar, 2001), yeast-like fungal cells (Rikkinen and Poinar, 2002), and remains of several bryophyte species (JRikkinen et al., unpublished results). The bryophytes include two mosses (Octoblepharum sp. and Syrrhopodon sp.) and at least two hepatics (Aphanolejeunea sp. and Cololejeunea sp.). All these bryophytes belong to extant genera that are widely distributed in the Tropics (Gradstein, 1993; Frahm and Newton, 2005). Extant Phyllopsora species are predominantly tropical and subtropical, with few extensions into the temperate zone (Swinscow and Krog, 1981; Brako, 1991; Timdal and Krog, 2001; Upreti et al., 2003). Several species are pantropical, and both widespread and common in the Neotropics, including the Caribbean region. For example, Brako (1991) listed 11 species and varieties from the Dominican Republic in her monograph of the Neotropical taxa. Printzen and Lumbsch (2000) used paleoclimatic data and evidence of forest history to calibrate a molecular clock based on fungal ITS sequences of Phyllopsora and Biatora. Structural differences between the two genera are small and they also share a similar habitat ecology. However, despite being closely related, the genera are almost strictly allopatric, with Phyllopsora being tropical and Biatora restricted to temperate and cool regions of the Northern hemisphere. The authors concluded that the two genera were first separated 170–140 million years BP, when the expanding Tethys ocean started to separate Laurasia completely from Gondwana. Later diversification within Biatora was linked to periods of climate cooling, when new forest vegetation types evolved and spread in the Northern hemisphere. Thus, while anatomical, morphological, and chemical differences between Biatora and Phyllopsora are relatively small, the genera appear to be phylogenetically old (Printzen and Lumbsch, 2000). This general conclusion is supported by the current findings. Most extant Phyllopsora species are corticolous or lignicolous, but some species also grow on rocks and bryophytes. Phyllospora dominicanus seems to have had a similar ecology. All organisms preserved in the amber specimen indicate an epiphytic or epixylic microhabitat in a tropical forest. The ancient community seems to have been entrapped in place, possibly by viscous exudate running down a tree trunk or dripping from the forest canopy. The preservation of actively reproducing filamentous fungi and yeasts may indicate a sudden preservation event during moist conditions (Rikkinen and Poinar, 2001, 2002). The photobionts of most extant lichens are coccoid green algae. Some 40% of all lichen-forming fungi associate with Trebouxia or related green algae (Trebouxiophyceae). These photobionts are particularly dominant in lichen species of cool and temperate regions, but also occur in many tropical lichen genera. The photobionts of modern Phyllopsora species have not been studied in any detail but, when analysed, they have been identified as belonging to Pseudochlorella (Chlorellales, Trebouxiophyceae) (Brako, 1991). The exchange of metabolites requires intricate connections between lichen symbionts, and several types of fungal–algal contacts are known from green algal lichens. While some lichen mycobionts penetrate deeply into photobiont cells, most produce specialized haustoria in which the surface layers of the fungal hyphae spread to cover the algal cells. Water, minerals, and metabolites are then translocated between this fungal-derived surface layer and the symbiotic algal cell (Ahmadjian, 1993; Honegger, 2001). Also, in the fossil, the mycobiont hyphae follow the contours of algae and press closely against their cell walls. No intracellular haustoria are seen. However, tiny peg-like haustoria are very difficult to detect even in fresh lichen specimens. Amber fossils have shown that several lineages among epiphytic lichens and fungi have conserved their morphological adaptations to successful ecological niches. Subsequently, many genera and possibly even species have remained more or less unchanged for tens of millions of years (Rikkinen and Poinar, 2000, 2002; Rikkinen, 2003; Rikkinen et al., 2003; Dörfelt and Schmidt, 2005). The present new findings show that this phenomenon is also seen in the epiphytic lichen genus Phyllopsora. A conserved maintenance of structural features seems also to apply to fine details of the fungal–algal interface. 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Journal

Journal of Experimental BotanyOxford University Press

Published: Mar 3, 2008

Keywords: Amber fossil fungi lichen Phyllopsora symbiosis Tertiary

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