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(American Journal of Botany. 2001;88:788-796.)
© 2001 Botanical Society of America, Inc.

Lateral growth patterns in the Cladoniaceae1

Samuel Hammer2

Division of Science and Mathematics, College of General Studies, Boston University, 871 Commonwealth Avenue, Boston, Massachusetts 02215 USA

Received for publication February 10, 2000. Accepted for publication June 16, 2000.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Lateral growth from the apex of vertical structures is widespread in cladoniiform lichens. In the family Cladoniaceae, it is accomplished through a developmental shift in the meristem, in which growth orientation changes from isotropous to anisotropous. In anisotropous development, the more or less constant relationship among the axial, radial, and circumferential planes of growth is altered during ontogeny. The result is pronounced lateral elongation of the apical meristem, a departure from the isotropous body plan of early ontogeny. Development that favors radial and circumferential growth over axial growth is an innovation that provides ontogenetic flexibility but which also entails the loss of control from a single centralized meristem to one or more meristems. A shift from the constraints of symmetry to the risks and potential of asymmetry and a subsequent diversity of heritable thallus forms reflect evolutionary processes in the Cladoniaceae. Similar morphogenetic activities, which are apparently highly conserved, are shared by species that are presumably only distantly related.

Key Words: Cladoniaceae • development • evolution • growth dynamics • lichen architecture • lichen morphogenesis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Evolution is a struggle between constraint and innovation.—S. J. Gould (1977)

The lichen genus Cladonia P. Browne was first described over two centuries ago, and representatives of the genus were known to the great natural historian Linnaeus. The biology of lichens was not understood by Linnaeus or his scientific descendents, who considered them to be a sort of degenerate plant (Ahmadjian, 1995 ). It was not until the mid-19th century that lichens were understood as a symbiotic relationship between two different organisms, a fungus and a photosynthetic alga or cyanobacterium. Scientists currently recognize ~30 000 lichen species, which, according to the Botanical Code, are named for the fungal partner. Lichens are very widely distributed in habitats throughout the world. Approximately 500 species are classified in some ten genera that comprise the Cladoniaceae, a diverse group that includes the genus Cladonia, with representatives on every continent. The Cladoniaceae are more or less easily recognizable in nature by their distinctive upright habit, the production of cups and branches at their tips, and the fact that they readily colonize roadsides or trailsides where adequate moisture and sunlight are present. However, it is difficult to distinguish the species from one another, in part because of their great morphological variability. The Cladoniaceae are generally considered to be taxonomically problematic and even with the widespread advent of microscopy in the 19th century, it remained difficult to circumscribe the species. Most recently, chemotaxonomy and molecular tools were the preferred means of studying the Cladoniaceae, but contemporary lichenologists have inherited many scientific misconceptions about Cladonia and its allies. Foremost among these is an unfortunate bias against the analysis of morphology as a key to the understanding of lichens.

This paper addresses the problems of morphological analysis in the Cladoniaceae (Ascomycotina) and documents lateral growth in several of the taxa. The study focuses on the ontogeny of the fungal meristem tissue, a bundle of tightly packed, parallel-arranged, thick-walled cells that is present in all of the species and that was discussed in several previous papers (see Hammer, 2000 ). The gross morphology of most of the Cladoniaceae is characterized by an erect thallus verticalis, comprising the lichenized podetium (Ahti, 1982a, 2000 ; Hammer, 1995 ). The growth of the podetium is initiated and controlled by the fungal meristem, which is present from the inception of the podetium through reproductive maturity. Both vertical and lateral development can be traced to the meristem tissue, from which the rest of the hyphae in the podetium are derived (see Hammer, 1993, 1997a, b, c, 1998a ).

The present study focuses on lateral growth in cladoniiform lichens, but it is also important to summarize vertical growth. The vertical habit is the clearest manifestation of polarized growth in most of the genera, with the exception of Calathaspis Lamb & Weber and Myelorrhiza Verdon and Elix, which are foliose (see Lamb and Weber, 1972 ; Verdon and Elix, 1987 ). Vertical growth requires the production of assimilative hyphae and the subsequent accretion of fungal and lichenized tissue that forms a stipe (podetium) beneath the fungal meristem. The photosynthetic podetium, which is perennial, can grow to several centimeters tall. In most species it is composed of strata of fungal and algal cells that are arranged in more or less concentric layers around a central cavity. Podetia arise from the surface of the thallus horizontalis (primary thallus), which is either leaf-like or crustose, and in many species, podetia persist after the primary thallus has disappeared. Podetia are generally hollow, roughly tubular structures, but the podetia of some species are solid. Podetia generally bear apothecia, and some authors (Jahns, Sensen, and Ott, 1995 ) consider the entire podetium to be composed of ascomatal tissue (but see Hammer, 1993 ). During earliest growth, incipient podetia are composed of a solid mass of fungal tissue. The hollow podetium is a by-product of later development (Hammer, 1993 ), but the growing tips of mature podetia are solid. As the prefix clad (Gr.: clados; branch) implies, podetia in many of the genera, particularly Cladia Nyl., Cladina Nyl., Cladonia Browne, and Ramalea Müller Arg. are branched.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
This study includes species of the lichen family Cladoniaceae representing five genera (Cladia, Cladina, Cladonia, Pycnothelia Dufour, and Ramalea), all of which share the cladoniiform growth habit. Several hundred podetia at all stages of growth were examined, drawn, and photographed. Approximately 100 specimens were air-dried, mounted on aluminum stubs, and sputter-coated with gold for study by scanning electron microscopy (SEM). Photomicrographs were prepared on a Phillips 501 at 10–20 kV at the Museum of Comparative Zoology (Harvard University) and on a Cambridge Instruments Stereoscan 360 lanthium hexa-boride transmitter at 50 pA of electron beam current at 20 kV at the Electron Microscopy Unit (Australian National University). For detailed SEM methods, see Hammer (1996b, 1997c) . Freshly collected material and preserved specimens at the Farlow Herbarium (FH), the National Museum of Natural History, Smithsonian Institution (US), and the National Botanical Garden in Canberra, Australia (CBG) were studied. Most of the specimens collected by the author are deposited at FH and CBG. The specimen of Cladonia perforata A. Evans is deposited at US. The specimens of Ramalea cochleata Müller Arg. are deposited at CBG. Representative specimens include (but are not exclusive to): Cladia aggregata (Sw.) Nyl: Hammer 7034, 7083, 7120; C. schizopora (Nyl.) Nyl.: Hammer 7028, 7075; Cladina subtenuis (Abbayes) Hale & W. C. Culb.: Hammer 3103, 5780, 5815, 6062; Cladonia capitellata (Hook. fil. & Taylor) Church. Bab.: Hammer 7039, 7178; C. cristatella Tuck: Ahmadjian 2366, Culberson 6768, Evans 1858, Hammer 6015; C. fimbriata (L.) Fr.: Hammer 4781, 4853; C. floerkeana (Fr.) Flörke: Hammer 5810, 6021; C. furcata (Huds.) Schrad.: Hammer 3665, 4159, 5036; C. parasitica (Hoffm.) Hoffm. Hammer 5703, 5783, 5821; C. perforata: Llano s.n. (isotype); C. pertricosa Kremp.: Hammer 7033, 7104, 7211; C. prolifica Ahti & S. Hammer: Hammer 1265 (isotype); C. rigida (Hook. fil. & Taylor) Hampe: Hammer 7031, 7070; C. subcervicornis (Vain.) Kernst.: Hammer s.n.; Pycnothelia papillaria Dufour: Hammer 5713, 5768. Ramalea cochleata: Archer 999, Dahl s.n.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Lateral growth is characterized by meristem development in which the radial and circumferential planes of growth are favored over the axial plane of growth. It is observed in both branched and unbranched podetia. In early lateral development, more or less distinct poles become discernable on either side of a solid, curvilinear meristem structure. The poles are generally the foci of lateral growth but intercalary growth can also occur, for example, through tissue folding. The microscopic fungal meristem is the initial site of lateral development, which can be observed during all stages of podetial growth but is most clearly observed in the early stages of meristem ontogeny. Further lateral growth, which is accommodated through growth patterns initiated by the meristem, may be obscured by branching or other gross morphological features. Lateral growth is expressed in a variety of patterns, but it is most apparent in the vermiform shapes that are widely distributed in the Cladoniaceae during early ontogeny.

Lateral growth in the Cladoniaceae is preceded by two early ontogenetic events. First, the roughly globose apical meristem enlarges to >100 µm in diameter. Enlargement is the most common precursor to morphogenetic change in the meristem tissue and occurs in most species irrespective of their morphology. The second event is the development of a transverse fissure that disrupts the continuity of the enlarging meristem tissue. The fissure, which is apparently the result of differential rates of cell growth in the surrounding region, generally signals the beginning of lateral growth. In some species a roughly helical, undivided vermiform structure can be observed in earliest ontogeny, without the development of the transverse fissure. Lateral growth is an ontogenetic shift in the meristem, which changes from a roughly globose form to intermediate toroid (doughnut-shaped) or reniform (kidney-shaped) structures. These structures are generally the products of synchronized growth and in some cases, the development of vermiform structures is also part of synchronized vertical/horizontal development of the podetium.

Generally, the development of the vermiform structure signals a disruption of synchronized isotropous growth. For example, Cladonia subcervicornis is characterized by helical vermiform growth, which can be detected during earliest ontogeny (Fig. 1). Lateral growth in C. subcervicornis occurs when the synchronized growth activities of the meristem have been interrupted, for example, after the meristem initial has enlarged and partially split (Fig. 2). In other species, for example Cladina subtenuis or Cladonia floerkeana, lateral growth is linked to the early stages of meristem splitting, which precedes the development of branches or branch-like proliferations (Figs. 3, 4). During later ontogeny of the meristem, the development of vermiform structures represents a loss of centralized control over growth. For example, when the meristem of C. fimbriata splits, the initial toroid-annular structure changes to a crenate-vermiform structure (Fig. 5). The meristem later splits into smaller, independently controlled bundles. In other species, the vermiform structure is linked to the overall pattern of the developing meristem, which is expressed by pulses of growth. For example, the synchronized meristem divisions of C. perforata result in temporary, reiterating reniform shapes (Fig. 6). Vermiform structures are part of a larger pattern of lateral growth in other species as well. For example, the meristem of C. parasitica splits and grows outward concomitantly, producing distinct reniform shapes (Fig. 7), a common pattern in the Cladoniaceae (see Figs. 3, 6, and 9–16). Reniform structures can also occur as part of a synchronized division of a toroid meristem, as in C. floerkeana (Fig. 8).



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  		 Figs. 1–8. Early ontogeny in several species (SEM). 1, 2. Early polarized growth of Cladonia subcervicornis. The incipient podetium grows vertically by a roughly helical accretion of tissue (Fig. 1 ). The meristem has split into two parts. The larger, deformed toroid meristem is curvilinear. Developing poles of the vermiform structure are indicated by arrows (Fig. 2 ). 3. Splitting meristem bundles of Cladina subtenuis. Arrows indicate poles of lateral growth. 4. Developing polarity in the meristem of Cladonia floerkeana. Lateral growth is accomplished through splitting (inward-facing arrows) and through enlargement and deformation (outward-facing arrows). Note similarity of meristem bundle at left to that in Fig. 1 . 5, 6. Deforming toroid-vermiform meristems of C. fimbriata (Fig. 5 ) and C. perforata (Fig. 6 ). Separate meristem bundles form through divisions of the larger structure. Arrows indicate indistinct poles in Fig. 5 . In C. perforata divisions in the meristem (inward-facing arrows) form vermiform structures that split further. Lateral growth indicated by outward facing arrows. The perforation (center) suggests that meristem development and splitting are reiterated. 7, 8. Vermiform-reniform growth in C. parasitica (Fig. 7 ) and C. floerkeana (Fig. 8 ). Lateral growth in C. parasitica is accomplished through splitting (inward-facing arrows) and outward growth (outward-facing arrows). Reniform meristem structures at right may split, leading to vertical growth, or they may elongate, forming vermiform structures that lead to lateral growth. Compare to structures in Figs. 6 and 8 . Note reniform meristem structures at top of Fig. 8 . Scale bars for Figs. 1–2, 6–8 = 100 µm. Scale bars for Figs. 3–4 = 50 µm. Scale bar for Fig. 5 = 10 µm

 
Lateral growth and the development of vermiform structures are also part of the morphogenetic pattern in branched species. For example, the meristem of Cladonia furcata shows patterns of splitting and stretching that result in the lateral growth of the thallus (Fig. 9). Lateral growth in C. furcata can be traced to vermiform meristem structures that are produced in very early ontogeny, immediately after the subglobose meristem bundle of earliest ontogeny has split (Fig. 10). These meristem structures, which are the products of early splitting, appear to be stretched laterally, and their orientation influences the later development of the thallus. Similarly, the overall pattern of development in C. prolifica reiterates the earliest ontogeny of a few meristem bundles. Large meristem structures in C. prolifica, which are themselves roughly vermiform (Fig. 11), split into smaller reniform-vermiform shapes (Fig. 12). These grow in turn to produce the larger meristem structure that influences the overall shape of the thallus. In C. prolifica, as in other species of the Cladoniaceae, the average size of the collective meristem bundles is relatively stable.



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  		 Figs. 9–16. Vermiform growth in branched species (SEM). 9, 10. Macroscopic habit of young C. furcata (Fig. 9 ). Arrow indicates meristem bundles in Fig. 10 . 11, 12. Ontogeny of C. prolifica (Fig. 11 ) with apical meristem bundles at tips of numerous branches (Fig. 12 ). Inward-facing arrows indicate earlier meristem splits, and outward growth is indicated by outward-facing arrows. 13, 14. C. capitellata, with apical meristem bundles at tips of numerous branches. Compare the interior cavity at center of podetium (Fig. 13 ) with the interior space of the vermiform meristem in Fig. 11 . Perforations at branch junctures reiterate, together with the growth pattern. Some elongation of the thallus is apparent in the mature podetium, but vermiform growth is not distinct. Arrow indicates meristem bundles enlarged in next figure. Inward-facing arrows in Fig. 14 indicate initial split in meristem. Outward-facing arrows indicate lateral meristem. 15, 16. Cladia aggregata, with numerous branches, characteristic perforations, and toroid-reniform meristem structures at branch tips. Inward-facing arrow of Fig. 16 indicates initial split, outward-facing arrows indicate outward growth of meristem tissue. Scale bar for Figs. 9, 11, 13, 15 = 1 mm. Scale bar for Fig. 10 = 100 µm. Scale bar for Fig. 12 = 0.5 mm. Scale bar for Fig. 14 = 100 µm. Scale bar for Fig. 16 = 50 µm

 
Lateral meristem growth at the macroscopic level reflects growth patterns that are established in very early ontogeny (Fig. 11). Similar to C. prolifica, a reiterating pattern of meristem splitting and outward growth of vermiform structures is present in the branched species C. capitellata (Figs. 13, 14). The tension between splitting and stretching meristem structures is present in earliest ontogeny (Fig. 14), and this tension is reiterated in the gross morphology of the podetium (Fig. 13). In C. aggregata as in other branching species, the meristem elongates before lateral expansion occurs, and lateral polarized growth is obscured in the branched thallus (Fig. 15). Lateral growth in these species is an intermediate ontogenetic stage, after which the meristem splits again, renewing the axial growth pattern. However, evidence of lateral growth, including vermiform meristem shapes, persists in mature podetia (Figs. 11, 13). The meristem tissue at branch tips thus displays growth dynamics of splitting and stretching that characterize lateral growth in nonbranching species (Fig. 16).

Lateral growth leads to variable thallus shapes. In Cladia schizopora vermiform morphology is pronounced during all phases of growth, and the meristem develops in a distinctly helical pattern (Figs. 17, 18). The habit of C. schizopora results from both vertical and lateral growth. Where small portions of the meristem split from the larger tissue, branchlike proliferations arise. Similarly, lateral meristem growth and the development of the vermiform shape produce a range of morphologies in Cladonia pertricosa (Fig. 19) and C. cristatella (Fig. 20). In both species, meristems split frequently resulting in plasticity of form in mature podetia. In C. pertricosa (Fig. 19) the vermiform habit combines with a flattened, leaf-like meristem morphology. The combination of lateral growth, vermiform meristem shapes, and the large, morphologically undifferentiated subapical meristem tissue results in tremendous variability in C. pertricosa. Mature specimens of this species range from very narrow branched forms (<0.5 mm wide) to highly expanded podetia (>5 mm wide). Similarly, radial splitting and stretching in C. cristatella produce a number of meristematic growing regions. The development of separate meristem bundles, most of which are subglobose in earliest ontogeny, results in the variable podetial height, width, and branching in C. cristatella. In C. rigida (Figs. 21, 22) the meristem is initially roughly symmetrical. It later develops vermiform regions that expand, grow asymmetrically, and split (Fig. 22), producing a variety of podetial shapes. Branching and vertical growth result through splitting, and the large meristem may continue to add cells, change its growth orientation, or provide new branches through further splitting. The vermiform structure is pronounced in very young thalli of Pycnothelia papillaria (Fig. 23). The meristem expands laterally for much of early ontogeny and vertical growth is restricted in the mature thallus. Ramalea cochleata shows lateral thallus elongation as well as branching (Fig. 24), along with persistent toroid meristem shapes. Developmental patterns in R. cochleata result from meristem growth dynamics as described above.



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  		 Figs. 17–24. Well-developed vermiform growth in various species (SEM). 17, 18. Toroid-vermiform development with helical growth habit in Cladia schizopora meristem, showing extraordinary length of the vermiform structure. 19. Reniform-vermiform meristem structures in Cladonia pertricosa. Large undulating meristem structure in background is well developed, while structures in foreground are immature. Foreground structures will enlarge while background structure splits. 20. Undulating vermiform meristem of C. cristatella developing from subglobose precursor with many incipient divisions radiating from the structure. Note several foci of growth (raised areas). 21, 22. Ontogeny of C. rigida. Umbonate meristem structure inside of toroid meristem (Fig. 21 ) and deformed toroid-vermiform meristem (Fig. 22 ). 23. Very early ontogeny of vermiform meristem structures of podetia of Pycnothelia papillaria. Protruding hairlike structures may be trichogynes. 24. Developing vermiform-toroid meristem structures of Ramalea cochleata. Scale bar for Figs. 17–19 = 100 µm. Scale bar for Figs. 20–24 = 50 µm

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Polarized growth, in which enlargement is accomplished through elongation, has long been a subject of interest in botany, and it possesses its own history within the context of mycology. However, lichen fungi have not been considered in this context. De Bary (1887) pioneered the study of polarized growth in fungi, and it has since been documented at the cellular level (Bartnicki-Garcia, 1986, 1990 ; Bartnicki-Garcia et al., 1995 ), at the level of the tissue (Buller, 1931, 1934 ; Corner, 1932 ; Willets and Bullock, 1992 ), and in the context of the aggregate colony (Rayner, 1997 ; Rayner, Watling, and Frankland, 1985 ). Polarized growth in filamentous fungi is observed in apical hyphal cells. Cytoplasmic resources and the well-documented Spitzenkörper (a small, densely staining body found close to the cytoplasmic membrane; see Hawksworth et al., 1995 ), are concentrated at the actively growing cell tip, which advances through or toward nutritional resources (Bartnicki-Garcia et al., 1995 ). Growth in fungal hyphae, which is essentially unidimensional, allows for the migration of otherwise sessile fungi through nutritional substrates (Rayner et al., 1985 ). It also accommodates fungal movement through aerial and subterranean space in pursuit of nutrients. It confers a selective advantage where resources are limited, and it may have thus contributed to the explosive radiation of filamentous fungi in terrestrial environments. Most of the research on polarized growth in fungi has focused on taxa in the Ascomycotina (ascomycetes) and Basidiomycotina (basidiomycetes). Lichen fungi, which are included within these groups (and which comprise a large part of the Ascomycotina), have not been considered by most authors (but see Reinke, 1895, 1896 ). In part, the growth dynamics of lichen fungi have been ignored because lichens are considered as symbiotic entities in which the component parts are not considered separately. Thus the biology of lichen fungi, for which the symbiotic "species" are named, has not been studied adequately. Further, lichen development has barely been studied because lichen morphology is often dismissed as too difficult to analyze for taxonomy, where most of the scientific work on lichens has been concentrated. The phenomena of growth and morphogenesis in lichen fungi are in need of further elucidation.

Rayner (1997) described polarized growth in fungi as a process of "breaking symmetry," a characterization that can be applied to morphogenesis in lichens. Axial polarized growth results in the development of characteristic vertically oriented cladoniiform lichens. It is part of the controlled, highly synchronized pulse that characterizes the early ontogeny of the apical meristem in the Cladoniaceae. Lateral development, which can be interpreted as a sort of polarized growth, occurs when pulsed growth is perturbed, for example by meristem splitting. In some species, pulsed growth resumes later in ontogeny, producing further morphological complications. Lateral polarized growth and the concomitant loss of thallus symmetry have important implications for morphological analysis in lichens as well as in plants (see Green, 1999 ). Variability directly affects any taxonomic system that is based on morphological evidence, and this is exemplified in the Cladoniaceae. In both plants and lichens, morphogenetic plasticity and its underlying mechanisms must be recognized when considering variation and variability (see Green, 1984 ). Information on shared morphogenetic pathways can provide a tool for building phylogenetically based classification systems (see Tomlinson, 1984a, b ). The pathway that includes lateral development results in a great variety of shapes in the Cladoniaceae. Naturally, this complicates taxonomic decision-making. Meristematic control is weakened or lost when splitting occurs (see Hammer, 1996a ), giving rise to shapes that are relatively difficult to predict, much less assign to a given taxon. Thus, complex patterns of morphological variability are introduced through relatively simple morphogenetic phenomena. In the Cladoniaceae, growth patterns that "break symmetry" introduce morphological complexity.

A previously undescribed form of lateral growth in lichens is the vermiform meristem. It is roughly horizontally oriented, and its morphology is the result of splitting and the subsequent elongation of the initially subglobose meristem. In most species, the vermiform shape is microscopic and limited to the activity of a single (usually apical) fungal meristem. However, in at least one species (Cladina evansii Abbayes [Hale & W. C. Culb.]), the form of the entire macroscopic clonal thallus, which may approach a meter in diameter (personal observation) changes from subglobose to vermiform, a feat that is presumably accomplished through the activity of hundreds of apical meristem bundles. While vermiform meristems are a temporary stage in some species (they split to produce smaller meristem bundles of various shapes), the vermiform shape is a persistent characteristic in others. The development of vermiform shapes, which are common in the hyphae and hyphal aggregations of filamentous fungi, provide a morphogenetic link between the Cladoniaceae and their fungal ancestors. The lateral development of an aggregation of hyphae (the meristem tissue) in the Cladoniaceae recalls the growth habit of individual hyphae that characterize most filamentous fungi.

From an ontogenetic perspective, lateral polarized growth and, in particular, the development of vermiform meristem shapes are innovations that change the growth pattern of cladoniiform lichens from an isotropous to an anisotropous orientation. Lateral growth appears to occur through heritable endogenous signals, but it may also occur as a response to exogenous conditions such as light. Lateral growth can thus be analyzed in the context of selective pressures such as nutritional constraints. Studies of fungal systems provide several examples. For instance, polarized growth in fungi can be considered in a nutritional framework as a morphogenetic response to biochemical signals (Crawford and Ritz, 1994 ). Rayner et al. (1985) described polarized growth in the context of linear migratory organs such as "cords, threads, strands, rhizomorphs, and pseudorhiza" that develop in response to nutritional cues. Similar growth patterns in the underground prothallus in lichens were discussed in Hammer (1996b, 1997c) . Aggregations of (mostly underground) hyphae behave more or less like individual fungal cells, particularly as regards lateral growth. They provide filamentous fungi with relative freedom of "movement" through their elongation. Can a similar concept of "migratory organs" be extended to include the aboveground lichen fungus, which, like nonlichenized fungi, is sessile? What are the constraints that must be considered in posing such a question?

The movement of the fungal meristem is constrained by at least three factors. First, its apical position on the erect podetium means that the meristem is essentially an aerial structure. Thigmotropic growth, which is common in fungi, is therefore impossible. Second, gravitropism, which is observed in shaded portions of the photosynthetic thallus, would limit lateral growth that exceeds the width of the supporting podetium. Finally, the subglobose meristem is prevented from migrating by its obvious attachment to the podetium. At 50–100 µm diameter, the meristem is the approximate size of a fungal spore, but as part of the podetium it is perforce sessile. While vegetative propagules such as soredia, which are approximately the same size as the meristem, are easily carried through space by a variety of agents, the fungal meristem is nonmotile. What are the innovations by which it overcomes the constraints of immobility? Lateral growth, which is accomplished through meristem splitting and the development of vermiform structures, provides a mechanism by which the meristem serves as a slow-motion engine of movement. By splitting and "stretching" the meristem can direct thallus growth and "movement" in response to nutritional requirements. However, the cost of mobility is the loss of centralized meristem control.

How does meristem ontogeny reflect the evolutionary history of the Cladoniceae? Lateral growth and expansion at the apex of the podetium may represent an evolutionary advance over underground lateral growth, which is characteristic of nonlichenized fungi and which presumably evolved earlier. Similarly, the development of the vermiform meristem shape from a subglobose precursor may represent an apomorphy in the Cladoniaceae that presumably developed in response to selective pressures (Hammer, 2000 ). Vermiform growth forms are widely distributed among the Cladoniaceae, but like many other morphological trends in the group (see Ahti 1982a, b ; Stenroos and DePriest, 1998 ) their importance has not been recognized.

Lichen thalli are aggregate colonies of fungal and photobiont cells, and lichen activities reflect interactions between the partners. However, the earliest ontogeny of the thallus, while it may involve signals from the photobiont, is a phenomenon that appears to be restricted to fungal cells and tissue. The earliest growth of the fungal meristem results in morphological patterns that are difficult to observe in later thallus form, and as a consequence, whole-thallus morphology is difficult to interpret. Growth dynamics of the thallus are thus best understood at the level of the fungal meristem and its activity. Subtle morphogenetic trends like meristem-initiated growth are later reflected in the gross morphology of the podetium but vermiform meristem development, which is widespread in early ontogeny (see Hammer, 1998b, 1999 ), is less discernable at the whole-thallus level. A comparison with nonlichenized fungi shows that lateral polarized growth and vermiform shapes are underlying, highly conserved morphogenetic trends. Thus, it is important to note that morphogenetic similarities to nonlichenized fungi present certain contradictions that have led to problems in "rooting" morphogenetic trends in cladoniiform lichens (Ahti, personal communication). While the vermiform meristem represents an ontogenetic advance over the subglobose meristem habit in lichens, it can also be interpreted broadly as a plesiomorphic or homoplasic fungal characteristic.

Morphogenesis in the Cladoniaceae reflects the evolutionary history of the group from a biogeographical perspective as well. Developmental pathways and their subsequent shapes are shared by taxa of the Cladoniaceae that are presumably only distantly related and that are also separated by enormous geographical barriers. This suggests that "form-building," the combined phenomena of morphological divergence and speciation that were described in the context of panbiogeograpy by Craw, Grehan, and Heads (1999) , is a conserved process in the Cladoniaceae. Growth dynamics and the resulting meristem shapes of diverse taxa as illustrated by the figures in the present study are remarkably similar. For example, the nearly radial vermiform meristem of Cladonia cristatella, an endemic species of eastern North America, is comparable to the meristem structure of C. rigida, an Australasian endemic. The meristems of both species change their form through the undulations of an annulus, a specialized pattern of "tissue folding" that was described in vascular plants by Green, Steele, and Rennich (1998) . The bow-tie shaped central perforation in C. capitellata, an endemic Australasian species, is identical to the interior space created by the growing meristem of C. prolifica, which is endemic to western North America. The shapes of both species are influenced by similar processes of growth dynamics that involve meristem splitting and stretching. The vermiform-reniform meristem of Cladonia perforata, an endemic species of the southeastern United States, is comparable to the shapes that are produced in podetia of the genera Cladia, Ramalea, and Pycnothelia. These findings suggest that the species of the Cladoniaceae can be characterized by homologous, highly conserved developmental pathways.

What is the origin of meristem ontogeny in the Cladoniaceae? Polarized growth is a universal biological phenomenon, expressed in a unique fashion by the Cladoniaceae but doubtless not exclusive to the group. For example, Barlow (1992) discussed the flow of information that dictates cell orientation and differential plant growth. Baluska, Volkman, and Barlow (1998) documented how changes in cytoskeletal networks altered the orientation of cell growth and its expression in polarized plant body development. Similarly, the polarized apical growth that is characteristic of fungal hyphae may influence differential growth in lichens. The activities of the Spitzenkörper in filamentous fungi have been linked to the development of the hyphal cytoskeleton and subsequent polarized growth of the cell. It is feasible that in lichenized fungi, meristematic cells (and cells leaving the meristematic region) would possess Spitzenkörper that influence cytoskeletal activity and subsequent cell orientation. The activities of the fungal Spitzenkörper as well as those of the lichen meristem are presumed to be a response to nutritional signals. It makes sense that in photosynthetic lichens, light acquisition would play an important role in directing growth. Morphogenesis in the Cladoniaceae is flexible, and it requires a flexible system of meristem cell orientation. In lichens as in plants, changes in cytoskeletal orientation may accommodate the development of photosynthetic tissue on various planes. Barlow (1989) stated that the mechanism of control over differential growth lies in a level lower than that in which it is expressed. This is apparent in the Cladoniaceae, where thallus form is influenced by the activities of the fungal meristem. Further studies would benefit from a focus on the ultrastructure of meristematic cells in the Cladoniaceae and their response to light cues.


   FOOTNOTES
 
1 The author thanks D. H. Pfister and J. Warnement for providing access to collections at the Farlow Herbarium and the Botany Libraries at Harvard University; R. Heady and E. Seling for assistance in the preparation of SEM micrographs for this paper; and T. Ahti, P. W. Barlow, S. Tucker, and W. A. Weber 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. Back

2 cladonia{at}bu.edu Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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