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0 Division of Science and Mathematics, College of General Studies, Boston University, 871 Commonwealth Avenue, Boston, Massachusetts 02215 USA
Received for publication December 11, 1998. Accepted for publication May 6, 1999.
ABSTRACT
Branching patterns in the lichen family Cladoniaceae are varied and taxonomically important. Branching occurs on the podetium, the erect secondary thallus that characterizes most species in the Cladoniaceae, and is influenced by growth dynamics of the fungal meristem tissue at the apex of the podetium. Branching is primarily the result of meristem divisions, and branching patterns are modified by meristem enlargement, deformation, and torsion. Branching processes are conserved, and early branch ontogeny provides information from which to determine relationships in the Cladoniaceae. Branching is characterized by two major patterns. In one pattern, branches arise from the relatively late divisions of a large meristem (
100 µm in diameter), whose shape changes during ontogeny. In a second pattern, branches arise from small meristems (<100 µm in diameter), which split early in ontogeny but whose shape does not change. The trend toward reduced meristems that split early in ontogeny is seen as an evolutionary advance in the Cladoniaceae. Some "small meristem" species retain aspects of the "large meristem" habit in early ontogeny, and this provides a clue to their relationships. Patterns of meristem growth dynamics provide a basis for interpreting phylogeny in mycobionts of the Cladoniaceae. Meristem activities in four genera of the Cladoniaceae were compared in order to determine trends in growth dynamics within the family.
Key Words: branching patterns • Cladoniaceae • lichen architecture • lichen evolution • morphogenesis
Among ~11 genera in the Cladoniaceae (Ahti, 1993
), branching is conspicuous in the genera Cladia Nyl., Cladina Nyl., and Cladonia Browne. In the genera Pycnothelia Dufour and Neophyllis F. Wilson, branching is less pronounced. The genus Cladonia is the most diverse in the family, with ~500 species worldwide. It is also the most intensively studied of the genera. Historically, Cladia, Cladina, and Pycnothelia were included within it (Vainio, 1887, 1894, 1897
). The genus Cladonia is polythetic (see Stevens, 1984a, b
), possessing a wide range of morphologies that are poorly characterized (Ahti, 1982a
). The taxonomy of Cladonia and its allied genera is based primarily on the morphology and secondary chemistry of the macroscopic podetium, the erect thallus verticalis (see Thomson, 1968
). The photosynthetic podetium, which is perennial, can grow to several centimetres in length. Podetia arise from the surface of the thallus horizontalis (primary thallus), which is composed of leaf-like squamules. In some species, particularly in the genus Cladina, the primary thallus is crustose. In many species, podetia persist after the primary thallus has disappeared. Podetia may be hollow, tubular structures, or they may be solid. As the name Cladonia implies, podetia of many of the species are branched. Mature podetia are composed of strata of fungal and algal cells. They generally bear apothecia, and some authors (see Hammer, 1993
; Jahns, Sensen, and Ott, 1995
) consider the entire podetium to be composed of ascomal tissue. The gross morphology of the mature lichenized podetium is highly variable, which tends to obfuscate the inherited morphological features of the fungus. Thus, characters that represent the named organism (the fungus) have not been adequately studied within a morphogenetic framework. Most authors have not considered the ontogeny of the Cladoniaceae to be phylogenetically informative. This may be attributable to a perception of the morphology of these species as "variable" or "polymorphic" (Jahns, Pfeifer, and Schuster, 1981
; Krabbe, 1891
), a concept that may reflect historical biases rather than biological evidence (see Hammer, 1998a
). However, the morphology and morphogenesis of the Cladonia fungus (as represented by its meristem tissue) are consistent, conserved, and species specific (for examples see Hammer, 1997a,
c, d, e).
The present study focuses on the growth dynamics of an exclusively fungal component of Cladoniaceae podetia, which was described in previous papers as a meristem (Hammer, 1996a, 1997a, d
; see Table 1). The fungal meristem is a bundle of tightly packed hyphae found at growing tips of Cladoniaceae podetia (Hammer, 1993
). The tissue undergoes morphogenic processes that influence and contribute to podetial form, and it is therefore considered as an apical meristem in the sense of Barlow (1989)
. Similar to plant meristems, the cells of the Cladonia meristem give rise to other cells through successive divisions, and it determines branching patterns of the podetium (Hammer, 1995a
). Unlike the podetium, which is photosynthetic, the meristem is not lichenized (see Ahmadjian, 1993
). Most of the meristem tissue lacks an immediate contact with the algal photobiont (Trebouxia spp.) and can therefore be considered to represent the Cladonia fungus in the strict sense. The morphology of the mature lichenized podetium (which can be several centimetres tall) is difficult to interpret accurately, but the morphology of the meristem is easier to interpret for several reasons. The meristem expresses the morphology of the fungus at the tissue level, in a structure that is 50–100 µm in diameter. In mature thalli, meristem tissue at the branch apices reiterates the earliest growth stages of the young podetium. It is therefore available for study at all growth stages. Finally, meristems are less affected by selective pressures than mature structures (and therefore less variable), providing a reliable set of characters for systematists (see Sachs, 1982
). The goal of this paper is to analyze the growth dynamics of several Cladoniaceae genera in order to provide characters for further systematic studies.
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Cladoniaceae species representing four genera (Cladia, Cladina, Cladonia, and Pycnothelia) were studied. Several hundred thalli were examined, drawn, and photographed. Scanning electron microscopy (SEM) photographs were prepared from several hundred specimens. Selected specimens were air-dried, mounted on aluminum stubs, and sputter-coated with gold for study by scanning electron microscopy (SEM) (Phillips 501 at 10–20 kV). For detailed SEM methods, see Hammer (1996d, 1997c)
. Freshly collected material and preserved specimens at the Farlow Herbarium (FH) and the Smithsonian Institution (US) were studied. Representative specimens include (but are not exclusive to): Cladia retipora (Labill.) Nyl.: Constable L53, Taylor L-36,145, Wright 5591, Hoogland 10,048; Cladina rangiferina (L.) Nyl.: Hammer 3182, 5731, 5764, 6064; Cladonia boryi Tuck.: Hammer 5701, 5830; C. floerkeana (Fr.) Flörke: Hammer 5810, 6021; C. floridana Vain.: Hammer 5800, 5807; C. gracilis (L.) Willd. subsp. turbinata (Ach.) Ahti: Hammer 3688, 5192, 5554; C. perforata A. Evans: Llano s.n. (isotype); C. prolifica Ahti & S. Hammer: Hammer 1265 (isotype); 2067, 2169, 2367; Pycnothelia papillaria Dufour: Hammer 5713, 5768. Nine species are included in this paper, and many more species were studied and considered for this study, as cited throughout. References to other representative specimens may be found in Hammer (1994, 1995b, 1996b)
. The terminological conventions for lichen morphogenesis are still developing. Certain aspects of terminology, particularly a comparison of plant terms that might be applied to Cladoniaceae lichens, were discussed in Hammer (1997a, c)
. It is important to note that the term "branch" is used in a very broad sense here. Podetia elongate and display a branch-like growth form, but there is no vascular system and therefore no vascular trace leading to appendages as in the branching systems of plants (see Bell, 1991
).
RESULTS
Overview of podetial development
In species of Cladoniaceae the first structure that emerges from the primary thallus (squamule or crust) is a solid bundle of tissue composed exclusively of fungal cells. The shape of the bundle is roughly spheroidal to obconical. The tissue, which is meristematic, gives rise to the fungal hyphae that comprise the erect secondary thallus (podetium). The vertical growth of the podetium is concomitant with lichenization of the surface of the podetium distal to the meristematic apex. Thus, hyphae that are produced by the meristem come into contact with algal photobiont cells, but the meristem bundle remains exclusively fungal throughout development. A lacuna generally develops in the podetial structure distal to the apex, which results in a hollow podetium in most species. Lateral growth of the podetium (widening) occurs primarily through meristem enlargement and deformation, and this results in various cup-like, flabelliform, and hood-like shapes that characterize many species of Cladoniaceae. Meristem divisions produce the branch-like proliferations studied in this paper.
Branching from a large meristem
In earliest ontogeny (Fig. 1) the undivided meristem of Pycnothelia papillaria is >100 µm in diameter. Early in ontogeny a transverse fissure, which divides two growth regions, forms across the top of the meristematic tissue. Further apical growth appears to bud from parts of the tissue. The meristem, which is >100 µm in diameter, resembles a hood at this stage (Fig. 2), and this shape is carried through to maturity. As growth continues, the meristem splits incompletely into large, indistinct bundles. The apex of the developing podetium is composed of the largest meristem bundle. This bundle leads the podetium in reflexed growth (Fig. 3) as faster growing regions begin to grow downward. Branching in P. papillaria is restricted to a series of three or four divisions that produce a bluntly digitate-furcate branching pattern (Fig. 4). The final divisions are dichotomous and are roughly parallel to the growth plane. The apical branches of mature podetia are somewhat flattened, and hymenial tissue is borne on their lower side. At maturity, the apical tissue is >100 µm in diameter. Mature podetia, which are ~1 cm tall, are strongly reflexed and somewhat dorsiventral (Figs. 5–6). They resemble the primary squamules of Cladonia species, which are either reflexed or upturned, and which are always dorsiventral. Branching in P. papillaria is determinate, and the mature podetium is digitate-cucullate.
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The vertical growth of the podetium in Cladia retipora proceeds from two daughter meristem bundles that split very early in ontogeny (Fig. 37). The resulting bundles continue to split dichotomously, producing characteristic groups of three meristem bundles. The development of same-age bundles is unequal, and ontogenetic differences are more pronounced as the meristem bundles grow farther apart. Splitting is not synchronized between bundles of approximately the same age (Figs. 38–39). One meristem bundle or one side of the podetium grows beyond the others (Fig. 40, arrows). Subtly articulated torsion of the meristem is apparent during early ontogeny, as evidenced by the relative angle at which the meristem bundles are oriented to one another (Fig. 40). Perforations between meristem bundles occur later in ontogeny, and perforations that are ontogenetically unrelated to the central perforation arise early in the lichenized tissue distal to the meristem (Figs. 41–42).
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Branching as an adaptive feature
The period in evolutionary history in which lichens made their initial appearance in terrestrial ecosystems is not known, and the absence of a fossil record makes it difficult to assess evolutionary trends in lichens. Molecular data support the traditional assumption that lichens, a polyphyletic life form, arose a number of times, perhaps under widely differing ecological conditions (Gargas et al., 1995
). How have environmental conditions influenced lichen evolution? As perennial multicellular organisms, lichens in the Cladoniaceae are subject to selective pressures involving photosynthesis, reproduction, and resource acquisition that are similar to those of plants. Lichen fitness may be linked to meeting the demands of those pressures, and the morphological innovation of branching may have arisen in the Cladoniaceae as a response to these pressures. For example, lichen fungi depend upon the photobiont host for their fixed carbon (Ahmadjian, 1964, 1993
; Brown, 1985
). It follows that light requirements would influence the evolution of lichen form (see Hammer, 1996a, 1997a, c, d
) as is the case with bryophytes (Rothwell, 1995
) and vascular plants (Niklas, 1994, 1997
). The sexual processes of lichen fungi are poorly understood (Hale, 1974
; Hammer, 1993
), but it is assumed that the mycobionts of lichens in the Cladoniaceae function in ways that are similar to other inoperculate discomycetes (Corner, 1929, 1930a, b
; Jahns, 1970
; Jahns and Beltman, 1973
; Letrouit-Galinou, 1966, 1968
; Nash, 1996
). If this is the case, adaptations that increase the potential for diaspore production and dissemination would predictably increase fitness. Finally, lichens are generally considered to be "pioneer" organisms that grow in harsh conditions, for example on bare rock. While this is true of many species, lichens in the Cladoniaceae inhabit and may have evolved upon organic substrates as well (Brodo, 1973
). Most species in the Cladoniaceae live near or among plants. They are relatively slow-growing and must therefore accommodate their light and space requirements to the restrictions imposed by neighboring plants. While crustose lichens are often the dominant life form in high-light environments (D. Galloway, personal communication), branched lichens are more common in attenuated light, for example among or under plants. The thalli of species in the Cladoniaceae establish and persist upon plant parts and organic substrata such as rotting wood, twigs, leaf litter, and soil (Hammer, 1993, 1996c, 1997b
). Thus, they possess a distinct functional relationship to plants. Apomorphic features of thallus ontogeny such as erect podetia and the branching habit may have increased the evolutionary fitness of the species through greater photoreceptivity (Hammer, 1997a
), increased reproductive opportunities (Jahns, 1984
), and efficient water relations (Ott, Mechmann, and Jahns, 1993
). The podetium can be considered as a structure whose reproductive function has been partially changed to a photosynthetic function. This diversification has predictably led to complications in interpreting the morphology of the Cladoniaceae. As discussed by Corner (1958)
, the transference of biological function through evolution may lead to difficulties in interpreting phylogeny, and this problem is amply reflected in studies of the Cladoniaceae.
Morphological evidence for branch evolution in the Cladoniaceae
Persistent, large, unspecialized meristems
If the family Cladoniaceae represents a monophyletic grouping, then we should be able to hypothesize evolutionary trends on the basis of known patterns of morphogenesis (see Tomlinson, 1984a, b
, for discussions of this issue in vascular plant taxonomy). Podetia are formed by the development of the fungal meristem, and branches arise ontogenetically from divided fungal meristems in the Cladoniaceae. Do podetium and branch ontogeny indicate evolutionary novelties from which we can infer evolution in the Cladoniaceae? Is it possible that similar phenomena exist in other lichens? Meristem or meristem-like activity is almost certainly present in other lichen groups, and it may not represent an autapomorphy in the Cladoniaceae. Further studies should include consideration of the phenomena of growth dynamics in other lichen groups. However, meristem size and developmental patterns as described above do provide insights within the context of Cladoniaceae systematics. For example, persistent, large, undivided, or little-divided meristems produce short podetia that are unbranched or little-branched. The mature podetia of "large-meristem" species such as Pycnothelia papillaria and Cladonia strepsilis (Ach.) Grognot (see Hammer, 1999
) resemble primary squamules, which are the developmental precursors of podetia. The podetia of "large-meristem" P. papillaria and Cladonia incrassata Flörke (see Hammer, 1997e
) are strongly reflexed, with a downward-facing hymenium that resembles those of the outgroup genus Thysanothecium Mont. & Berk. Large meristems, whether they are spheroidal or toroidal, provide strong, centralized control over the growth of the thallus (Hammer, 1996a
). Generally, they constrain vertical growth of the podetium. When large meristems split, their control over podetial growth and synchronization is weakened. For example, in C. cervicornis (Ach.) Flot. and its allies, vertical podetial growth exceeds lateral growth when the meristems split (see Hammer, 1996a
). In a related phenomenon (see C. prolifica above), the difference in the progression of development between meristem bundles increases as the physical distance between the bundles (and their distance from the apex of the podetium) increases. The suite of morphological characters that arise from a persistent, large meristem is considered here as primitive. Such features include squamule-like, little-branched, reflexed podetia that are relatively short (<2 cm).
Modified "large" meristem ontogeny
Toroidal meristems are modified "large" meristems that may produce tall or short podetia. They are found in many species of branched (as well as unbranched) taxa in the Cladoniaceae, and it is possible that more than one lineage arose from an ancestral species with a toroidal meristem structure. In one lineage, represented here by C. boryi and C. perforata [included in section Unciales (Del.) Oxner ex Ahti], the toroidal meristem structure persists throughout the ontogeny of the podetium. The branches of these species are produced when the toroidal meristem splits. In mature podetia, branches may be relatively long (C. boryi) or short (C. perforata). Mature podetia may be roughly symmetrical, as in C. boryi, or they may be asymmetrical, as in C. perforata. Generally, perforations are present at the axils of branches. Scyphus-like structures are uncommon, but in some species, for example C. boryi, they are characteristic of mature podetia. The growth pattern of C. boryi, particularly the formation of the toroidal meristem structure, is more specialized than the growth pattern in Pycnothelia. However, the persistent toroidal structure, which remains relatively thick throughout ontogeny, represents a relatively primitive habit in the Cladoniaceae.
In the second lineage, which is represented by a toroidal-annular meristem conformation, cup-forming podetia are produced by the synchronization of vertical growth and meristem widening early in ontogeny. The meristem generally thins to an "annular" shape as its circumference widens. This represents a reduction of the meristem and is considered here as an apomorphic character for a group that includes C. gracilis and many of the species presently classified within section Cladonia such as C. chlorophaea (Flörke ex Spreng.) Sommerf., C. fimbriata (L.) Fr., C. ochrochlora Flörke (see Hammer, 1993
), and C. pyxidata (L.) Fr. It also includes species that are presently classified in section Cocciferae such as C. pleurota (Flörke) Schaer. and C. coccifera (L.) Willd. In all of these species, the meristem persists as an annular structure throughout ontogeny, and as the circumference of the meristem expands, the lichen tissue within the circumference is generally persistent. In verticillate species such as C. cervicornis and C. verticillaris (Raddi) Fr. (see Hammer, 1996a
), the annular meristem is further reduced through splitting, and some of the tissue within the circumference of the meristem also retains meristematic properties. Further tiers of podetia generally arise from that tissue. Podetial growth in all of these species is determinate as long as the meristem remains undivided, resulting in cup-like podetia at maturity. However, podetial growth in verticillate podetia becomes indeterminate when the meristem splits. Branches can form in any of these species when the meristem splits and in some species, for example C. dimorpha Hammer, C. gracilis, C. grayi G. Merr., and C. phyllophora (L.) Hoffm., the initial cup-like podetium characteristically gives rise to branches (see Hammer, 1997d
).
The developmental process in Cladonia prolifica and C. subcervicornis (Vain.) Kernst. (see Hammer, 1998b
) is a derivation of the pattern described immediately above. Instead of forming cup-like podetia, development in C. prolifica is based on a sequence of early divisions of the meristem. The divisions produce a helical arrangement of meristem structures, by-passing the cup-forming stage that was described for the previous species. The largest meristem structure, which is generally at the apex of the podetium, leads vertical growth. The branches are relatively short, but the vertical growth of the mature podetium is pronounced. The helical growth form that was laid down by the dividing meristem is present in mature podetia. Occasional cup-like forms may persist in species with this growth form, but they are infrequent and indistinct.
Small meristems are produced ontogenetically from large meristems through splitting. In species such as Cladina rangiferina, Cladonia floridana, and Cladia retipora, which are considered here to be evolutionarily advanced, the developmentally intermediate toroid-annular structure is circumvented. Meristem divisions, which direct podetial development and branch formation, are frequent in these species. Early splitting of the meristem, which is an evolutionarily advanced feature, produces early podetial branching. Helical growth, which represents an intermediate evolutionary advance in species such as Cladonia prolifica, is present in the very early ontogeny of species like Cladina subtenuis (Abb.) Hale & W. L. Culb. (see Hammer, 1997a
), as well as in species of Cladia, but it is not seen in later development. Vertical growth in these species, which may reach several centimetres in height, is pronounced. The species are characterized by luxuriant branching and the branches may function as colonizing structures (Hammer, 1997b
).
Establishing character polarity on the basis of morphogenesis in the Cladoniaceae
The issue of polarity among characters has a long history of controversy (see Stevens, 1980
), and it is still perceived as a problem in the Cladoniaceae (DePriest, 1995
; Stenroos, Ahti, and Hyvönen, 1997
). Polarity among traditional taxonomic characters such as gross thallus morphology and secondary chemistry has not been useful in establishing evolutionary trends in the group. Gross morphology was interpreted phylogenetically by Vainio (1897)
and by Mattick (1938, 1940)
but resulted in groupings that were partially artificial. The central concept of "open" vs. "closed" branch axils that these authors used added confusion to Cladoniaceae taxonomy and delimited nonmonophyletic groups (see Choisy, 1929
; Hammer, 1995a, 1998a
). Further, in mature podetia, these morphological features are difficult to interpret because of variable growth. Secondary substances, which have been invoked in phylogenetic models for the Cladoniaceae (for examples, see Ahti, 1966
; Culberson, 1986
), are not apomorphic within the mycobionts of the Cladoniaceae. Therefore, the analysis of secondary chemistry is not a particularly effective criterion for outgroup comparison or for establishing evolutionary trends in the group. Finally, terminological usage, which is implicit within phylogenetic studies in the Cladoniaceae, remains problematic. One example is the controversy over the terminology of the lichenized stipe (whether podetium or pseudopodetium), which can be traced to Lamb (1954)
. The concept is more semantic than biological, since no conclusive evidence has been established for distinguishing a podetium from a pseudopodetium (see Galloway, 1966
; Jahns, 1970
; Jahns and Beltman, 1973
; Ahti, 1982b
; Hammer, 1993
). Efforts to distinguish between the "true" podetium and the pseudopodetium have led to an unproductive either-or interpretation of Cladoniaceae morphology of the sort that Sattler (1990, 1992)
discussed for vascular plants.
A phylogenetic model requires that criteria for evolutionary trends based on polarity among character states be established, and in the Cladoniaceae, some of these criteria can be based on meristem ontogeny. For example, large meristems split to produce smaller meristems, and this morphogenetic feature, which is universal in the Cladoniaceae, may be used to establish polarity in the group. Polarity in the Cladoniaceae can be determined on the basis of apomorphic developmental processes of the fungal meristem, which are reflected in the morphology of mature podetia. For example, the genus Thysanothecium, with its nonbranching, strongly reflexed, squamule-like podetium, and persistent, large meristem, is considered as an outgroup to the branched taxa discussed here. Pycnothelia, which is characterized by a large meristem, limited determinate branching, strong podetial reflexion, and squamule-like podetia can be considered as a sister taxon to the genera Cladia, Cladina, and Cladonia. The central ontogenetic feature of Thysanothecium and Pycnothelia is a large meristem, a plesiomorphic character that is shared with certain Cladonia species, but which is absent in the genera Cladia and Cladina (Table 2). The developmental shift of the meristem from a large, undivided bundle to smaller bundles is considered as an evolutionarily derived process. The evolutionary trend toward early-dividing meristem bundles is another apomorphy. The formation of a toroid-annular meristem is an intermediate stage representing both a reduction in meristem size and a specialized meristem shape that is absent in Thysanothecium and Pycnothelia. The reduction of the toroidal shape to an annular meristem shape is a further stage. Both the toroidal meristem and the annular meristem have the potential to split into smaller bundles, although they may not split at all. Meristem division in these taxa occurs relatively late, after the initiation of the toroidal or annular meristem structure. When splitting occurs it results in elongate proliferations or branches, but generally proliferations and branches lead to further toroidal-annular shapes. The phenomenon of branching without the formation of a toroidal-annular meristem may represent a neotonous development in the Cladoniaceae (see Tomlinson, 1984b
, for a relevant discussion of "neotonous metamorphism" in plants). Heterochrony, which has been documented in the Cladoniaceae (see Hammer, 1997c
), is a key to understanding the evolution of morphogenesis in the group.
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FOOTNOTES
1 The author thanks D. H. Pfister, J. Warnement, and P. DePriest for providing access to collections at the Farlow Herbarium and Reference Library and the National Museum of Natural History (Smithsonian Institution), Mr. Edward Seling for assistance in the preparation of SEM micrographs for this paper, and T. Ahti and D. Galloway for reading and comments upon earlier drafts of the manuscript. Grants from the National Geographic Society (6052-97) and the National Science Foundation (DEB-9712484) assisted in the support of this research. 
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