Journal of Experimental Botany, Vol. 59, No. 5, pp. 1007–1011, 2008
doi:10.1093/jxb/ern004 Advance Access publication 3 March, 2008
SPECIAL ISSUE RESEARCH PAPER
A new species of Phyllopsora (Lecanorales, lichen-forming
Ascomycota) from Dominican amber, with remarks on the
fossil history of lichens
Jouko Rikkinen1,* and George O. Poinar Jr2
1
Department of Biological and Environmental Sciences, PO Box 65, University of Helsinki, FIN-00014 Helsinki,
Finland
2
Department of Zoology, Cordley Hall 3029, Oregon State University, Corvallis, OR 97331-2914, USA
Received 30 May 2007; Revised 30 November 2007; Accepted 21 December 2007
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 welldeveloped 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.
Key words: Amber,
symbiosis, Tertiary.
fossil,
fungi,
lichen,
Phyllopsora,
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
* To whom correspondence should be addressed. E-mail: jouko.rikkinen@helsinki.fi
ª The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1008 Rikkinen and Poinar
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 (4033633
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.
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
Photobionts of fossil lichen 1009
Fig. 1. Phyllopsora dominicanus (HOLOTYPE). (A) Squamiform to
subfoliose thallus fragments preserved together with bryophyte remains,
scale bar ¼ 10 mm. (B) Ascending thallus lobes of P. dominicanus,
scale bar ¼ 2 mm. (D) Photobiont layer under the upper cortex of
a cross-sectioned squamule, scale bar ¼ 10 lm. (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 ¼ 5 lm.
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 lm 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 ‘obscur-
ing 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
1010 Rikkinen and Poinar
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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