The Lichens

THE LICHENS

VERNON AHMADJIAN

Department of Biology, Clark University, Worcester, Massachusetts

MASON E. HALE

Department of Botany, Smithsonian Institution, Washington, D.C.

Table of Contents

Cover image

Title page

CONTRIBUTORS

Copyright

LIST OF CONTRIBUTORS

PREFACE

Part I: STRUCTURE AND DEVELOPMENT

Chapter 1: ANATOMY, MORPHOLOGY, AND DEVELOPMENT

Publisher Summary

I Introduction

II Anatomy of the Thallus

III Morphology of the Thallus

IV Vegetative Structures and Their Development

V Influence of Fungus and Alga on the Habit of the Lichen

VI Influence of Fruiting Bodies on the Development of Thallus Tissues

Acknowledgments

Chapter 2: SEXUAL REPRODUCTION

Publisher Summary

I Ascolichens

II Basidiolichens

Chapter 3: SYSTEMATIC EVALUATION OF MORPHOLOGICAL CHARACTERS

Publisher Summary

I Introduction

II Systematic Criteria

III Modifiability and Its Taxonomic Significance

Chapter 4: LICHEN PROPAGULES

Publisher Summary

I Introduction

II Vegetative Propagules

III Sexual Propagules

Acknowledgments

Chapter 5: FINE STRUCTURE

Publisher Summary

I Introduction

II Cellular Structure of the Symbionts

III Symbiotic Relationship between Fungus and Alga

IV Thallus Layers and Surface Structures as Viewed with SEM

V Some Aspects of Changes in Ultrastructure Due to Ecological Conditions

VI Conclusions

Acknowledgment

Part II: PHYSIOLOGY OF THE INTACT THALLUS

Chapter 6: ABSORPTION AND ACCUMULATION OF MINERAL ELEMENTS AND RADIOACTIVE NUCLIDES

Publisher Summary

I Introduction

II Metal Content of Lichens

III Concentration and Retention of Radionuclides

IV Uptake and Translocation of Cations

Chapter 7: PEDOGENETIC SIGNIFICANCE OF LICHENS

Publisher Summary

I Introduction

II Biogeophysical Weathering

III Biogeochemical Weathering

IV Plant Succession and Soil Development

V Conclusions

Acknowledgments

Chapter 8: PHOTOSYNTHESIS AND CARBOHYDRATE MOVEMENT

Publisher Summary

I Introduction

II Photosynthesis by the Intact Lichen

III Interactions between Lichen Symbionts

IV The Mobile Carbohydrate and Its Release

V Fate of the Transferred Carbohydrate

VI Carbohydrate Movement between the Symbionts

VII Conclusions

Acknowledgments

Chapter 9: NITROGEN METABOLISM

Publisher Summary

I Introduction

II Chemical and Biochemical Analyses of Whole Thalli

III Assimilation of Combined Nitrogen

IV Fixation of Elementary Nitrogen

V Translocation of Nitrogen Compounds between the Symbionts

VI The Relationship of Lichens to Other Nitrogen-Fixing Symbiotic Systems

Part III: ENVIRONMENTAL RESPONSE AND EFFECTS

Chapter 10: RESPONSE TO EXTREME ENVIRONMENTS

Publisher Summary

I Introduction

II Determination of Viability and Resistance

III Responses to Environmental Stresses

IV Extreme Habitats of Lichens

V Conclusions

Acknowledgments

Chapter 11: WATER RELATIONS

Publisher Summary

I Introduction

II Water Absorption

III Mechanism of Water Absorption and Water Conduction to the Thallus

IV Water Contents of Thalli

V Water Loss

VI Conclusions

Chapter 12: SUBSTRATE ECOLOGY

Publisher Summary

I Introduction

II Practical Aspects

III Substrate Factors

IV The Lichen–Substrate Interface

V The Effect of Lichens on their Substrate

VI Substrate Specificity

VII Substrates and Speciation

VIII Summary and Conclusions

Acknowledgments

Note Added in Proof

Chapter 13: LICHENS AND AIR POLLUTION

Publisher Summary

I Historical

II Lichen Deserts

III Causes of Lichen Deserts

IV Effect of Environment

V Biological Estimation of Air Pollution

Chapter 14: GROWTH

Publisher Summary

I Introduction

II Techniques of Measuring Growth

III Growth Rates and Life History

IV Conclusions

Part IV: SECONDARY METABOLIC PRODUCTS

Chapter 15: NATURE OF LICHEN SUBSTANCES

Publisher Summary

I Introduction

II Structure of Lichen Substances

III Recent Results

Chapter 16: BIOSYNTHESIS OF LICHEN SUBSTANCES

Publisher Summary

I Introduction

II Biosynthesis

III Conclusion: The State of The Problem

Acknowledgments

Chapter 17: ANTIBIOTICS IN LICHENS

Publisher Summary

I Folklore

II Pharmacopoeias

III Lichen Substances

IV Pharmacological Studies

V Antibiotics in Lichens

Part V: SYMBIONT INTERACTIONS

Chapter 18: RESYNTHESIS OF LICHENS

Publisher Summary

I Introduction

II Developmental Stages of Synthesis

III Physiological Relationships between the Symbionts

IV Lichens Synthesized in Laboratory Cultures

V Factors that Influence Synthesis

VI Conclusions

Chapter 19: EVOLUTIONARY ASPECTS OF SYMBIOSIS

Publisher Summary

I Introduction

II Symbiosis in Retrospect

III Symbiosis Achieved

IV Symbiosis in Prospect

Appendix A: CLASSIFICATION

Appendix B: IDENTIFICATION AND ISOLATION OF LICHEN SUBSTANCES

Appendix C: METHODS OF ISOLATING AND CULTURING LICHEN SYMBIONTS AND THALLI

AUTHOR INDEX

TAXONOMIC INDEX

SUBJECT INDEX

CONTRIBUTORS

V. AHMADJIAN

O.B. BLUM

IRWIN M. BRODO

O.L. GILBERT

MASON E. HALE, JR.

S. HUNECK

I.K. ISKANDAR

T. JAAKKOLA

H.M. JAHNS

L. KAPPEN

K.A. KERSHAW

MARIE-AGNÉS LETROUIT-GALINOU

J.W. MILLBANK

KLAUS MOSBACH

ELISABETH PEVELING

JOSEF POELT

F. BRIAN PYATT

D.H.S. RICHARDSON

JOHAN SANTESSON

G.D. SCOTT

J.K. SYERS

Y. TUOMINEN

K.O. VARTIA

Copyright

COPYRIGHT © 1973, BY ACADEMIC PRESS, INC.

ALL RIGHTS RESERVED.

NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER.

ACADEMIC PRESS, INC.

111 Fifth Avenue, New York, New York 10003

United Kingdom Edition published by

ACADEMIC PRESS, INC. (LONDON) LTD.

24/28 Oval Road, London NW1

Library of Congress Cataloging in Publication Data

Ahmadjian, Vernon.

The lichens.

Includes bibliographies.

1. Lichens. I. Hale, Mason E., joint author. II. Title.

QK583.A35 589′.1 72-13610

ISBN 0–12–044950–1

PRINTED IN THE UNITED STATES OF AMERICA

LIST OF CONTRIBUTORS

Number in parentheses indicate the pages on which the author’s contributions begin.

V. AHMADJIAN,     Department of Biology, Clark University, Worcester, Massachusetts (565, 653)

O.B. BLUM,     Botanical Institute, Academy of Sciences, Kiev, Ukrainian S. S. R. (381)

IRWIN M. BRODO,     Museum of Natural Sciences, National Museums of Canada, Ottawa, Ontario, Canada (401)

O.L. GILBERT,     Department of Landscape Architecture, The University of Sheffield, Sheffield, United Kingdom (443)

MASON E. HALE,     JR., Department of Botany, Smithsonian Institution, Washington, D.C. (473)

S. HUNECK,     Institut für Biochemie der Pflanzen des Forschungszentrums für Molekularbiologie und Medizin der Akademie der Wissenschaften der DDR, Halle/Saale, Germany (495)

I.K. ISKANDAR*,     Department of Soil Science, College of Agricultural and Life Sciences, University of Wisconsin, Madison, Wisconsin (225)

T. JAAKKOLA,     Department of Radiochemistry, University of Helsinki, Helsinki, Finland (185)

H.M. JAHNS†,     Biologische Centrum, Rijksuniversiteit te Groningen, Haren, Netherlands (3)

L. KAPPEN,     Botanical Institute II, University of Wurzburg, Germany (310)

K.A. KERSHAW,     Biology Department, McMaster University, Hamilton, Ontario, Canada (289)

MARIE-AGNÈS LETROUIT-GALINOU*,     Laboratoire de Cryptogamie, Institut de Biologie Végétale, Université Paris VI, Paris, France (59)

J.W. MILLBANK,     Botany Department, Imperial College, London, England (289)

KLAUS MOSBACH,     Biochemical Division, Chemical Centre, University of Lund, Lund, Sweden (523)

ELISABETH PEVELING,     Botanical Institute, University of Münster, Germany (147)

JOSEF POELT,     Institut für Systematische Botanik der Universität Graz, Graz, Austria (91, 599)

F. BRIAN PYATT,     Department of Environmental Sciences, Plymouth Polytechnic, Plymouth, Devon, United Kingdom (117)

D.H.S. RICHARDSON,     Department of Biology, Laurentian University, Sudbury, Ontario, Canada (249)

JOHAN SANTESSON,     Institute of Chemistry, University of Uppsala, Uppsala, Sweden (633)

G.D. SCOTT,     Department of Botany, University of Rhodesia, Salisbury, Rhodesia (581)

J.K. SYERS†,     Department of Soil Science, College of Agricultural and Life Sciences, University of Wisconsin, Madison, Wisconsin (225)

Y. TUOMINEN,     Department of Botany, University of Helsinki, Helsinki, Finland (185)

K.O. VARTIA,     Resident Physician of the State Alcohol Monopoly (Alko), Helsinki, Finland (549)

*Present address: College of Environmental Sciences, University of Wisconsin-Green Bay, Green Bay, Wisconsin.

†Present address: Fachliereich Biologie der Universität, Frankfurt, Germany.

*Present address: Université Paris, Laboratoire de Cryptogamie, Paris, France.

†Present address: Department of Soil Science, Massey University, Palmerston North, New Zealand.

PREFACE

Lichens are nature’s most remarkable alliances. Combinations of certain fungi and algae have been so successful that there are now some 20,000 species of lichens distributed in most of the environmental habitats of the world. Ironically, the success of lichens has caused a major problem for those who study them—the one of identity. Logically, they should be classified with the fungi. Practically, however, this causes difficulties because of the wide differences between the two groups and because of the large number of lichens—they are the single largest group of Ascomycetes. For these reasons mycologists have been reluctant to deal with the lichens, and lichenologists have been content to maintain the separation. In recent years there has been movement toward incorporating lichens in a fungal classification. For example, the sixth edition of the Dictionary of the Fungi includes lichens for the first time. We are encouraged by such action and hope that this volume will stimulate further efforts to integrate lichenized and nonlichenized fungi.

The suggestion for this work came from the editors of the multivolume treatise The Fungi published by Academic Press. The lichenized fungi were not included in these volumes. The editors wanted a treatment that would complement the treatise and we hope that this volume fulfills this goal.

Investigations on lichens have differed from those on fungi. Topics such as genetics, cell biology, and ontogeny dominate mycology but remain virtually untouched among lichenized forms where the emphasis has been on more classic organismic level research and chemotaxonomy. We believe that mycologists have much to learn from their neglected relatives just as lichenologists have from developments in the nonlichenized fungi.

While there are several college-level texts on lichen available, none can match the depth of a multiauthor treatment to which each author brings a voice of authority and imparts some of the excitement in his own specialty. We are aware, of course, that multiauthored texts lack continuity and differ from chapter to chapter in emphasis and approach.

It has been difficult to find authors to cover all of the topics which seem essential. However areas which we consider to be most important are included: structure and development, physiology of the intact thallus, environmental response and effects, secondary metabolic products, and symbiont interactions. The appendices consist of a taxonomic scheme, methods for isolating and culturing lichen symbionts and thalli, and methods for isolating and identifying lichen substances. Hopefully gaps will be filled in future editions of this treatise. A few areas were deliberately omitted; phytosociology, for example, is extensively covered in Barkman’s book.

Ultimately, the real value and usefulness of this treatise derives from the efforts of the individual authors. They have been patient with editorial badgering, deadlines, and other problems that arise when so many authors from different countries come together in a common cause. We can only hope that this pioneering effort brings to the scientific community a new appreciation of the scope and diversity of lichenology.

VERNON AHMADJIAN and MASON E. HALE

Part I

STRUCTURE AND DEVELOPMENT

Chapter 1

ANATOMY, MORPHOLOGY, AND DEVELOPMENT

H.M. JAHNS

Publisher Summary

This chapter reviews anatomy and morphology of the thallus and the vegetative structure and development of the lichens. Most lichens are complex in structure. The layers of the thallus—upper cortex, algal layer, medulla, and lower cortex—are more or less present in all heteromerous lichens. Most lichens are gray or brown when dry. The segregation of lichens can be categorized into the three large groups of crustose, foliose, and fruticose lichens. The thallus of most crustaceous lichens consists of little scales called areoles. The thallus of foliose lichens is formed by flattened lobes, which are heteromerous and dorsoventral in structure. The lobes of fruticose lichens are strap-shaped or threadlike with a radial or dorsiventral thallus. The rhizoidal hyphae, which anchor the thallus by clasping little particles of the substrate, are like the tomental hyphae. Rhizines, having the same function as rhizoidal hyphae, always grow from the underside of the thallus. Vegetative structures emerging from the margin of the thallus and closely resembling the rhizines are called cilia. The mycobiont is responsible for the growth of the thallus. Many lichens develop vegetative organs of dispersal, called isidia, soralia, and hormocystangia. Isidia, formed by crustose, foliose, and fruticose lichens, are small protuberances of the thallus incorporating algal and medullary tissue covered by a cortex. Soralia differ from isidia in being noncorticated. They are powdery breaks in the cortex of the thallus and contain minute soredia. Hormocystangia are swollen areas of the thallus situated at the ends or margins of the lobes in some species of Lempholemma.

I. Introduction

II. Anatomy of the Thallus

A. Cells

B. Tissues

C. Structure of the Thallus

D. Attachment of the Thallus to the Substrate

III. Morphology of the Thallus

A. Color of the Thallus

B. Growth Forms of the Thallus

C. Development of the Thallus

D. Individuality of the Thallus

IV. Vegetative Structures and Their Development

A. Aeration Pores

B. Vegetative Diaspores

C. Cephalodia

V. Influence of Fungus and Alga on the Habit of the Lichen

VI. Influence of Fruiting Bodies on the Development of Thallus Tissues

References

I Introduction

The thallus of the lichenized ascomycetes exhibits such a complexity of form and color that the inexperienced observer may be forgiven for failing to realize what diverse organisms belong to this group of plants. At the beginning of the nineteenth century botanists were making their first attempts to classify the lichens, and in order to systematize the immense variety of growth habit they first divided the class on the basis of several major growth forms. For example, lichens covering rocks, trees, or soil with a thin, more or less well-developed crust were separated from leaflike species which adhere more or less firmly to the substrate and from upright, branching, bushlike forms. It will become obvious that this principle of classification is more or less arbitrary accentuating only the most striking stages on a scale of continuous development from a primitive to a highly differentiated organism. There are numerous intermediates between the three basic growth forms.

Certainly the growth form of lichen thalli cannot be considered as a principal characteristic on which taxonomy can be based. The foliose lichens, for example, do not form a taxonomic group of related species but only a morphological unity. The lichens of one family, even of one genus, may belong to the crustose, foliose, and fruticose growth form.

A theory proposed by Reinke (1894–1896) suggests that the lichens of different taxonomic groups have developed independently from crustose species to foliose forms and finally to fruticose plants. Fruticose lichens are regarded as the most highly developed peaks of several parallel lines of evolution. This theory, although attractive, is not acceptable. As will be seen, the structure of foliose thalli is not less complicated than that of fruticose thalli. On the contrary, some highly differentiated organs such as cyphellae are confined to foliose genera. For this reason, the foliose and fruticose lichens must be regarded as forms equal in their level of development in a line of evolution leading from a crustose organization to a more highly differentiated habit. Crustose lichens can, with some certainty, be considered as primitive or secondarily derived.

In spite of the above-mentioned objections it is still convenient to divide the lichens into growth forms. The habit being often the most obvious characteristic for distinguishing lichen species, the growth form is the most useful starting point in the construction of artificial keys for their determination.

The habit of a lichen is due not only to the overall growth form, but is often the result of special anatomical characteristics. For example, the shape of the thallus surface depends on the anatomy of the cortex. External appearance and internal structure are interdependent.

The tissues of the thallus consist of certain cell types, which are derived from the simple cells of the fungal hyphae. For a better understanding of the habit and structure of the lichen thallus it is, therefore, convenient to describe the original fungal cell and to follow its development into the specialized cells of which the various tissues and thalli are composed.

II Anatomy of the Thallus

A Cells

The spores of lichenized and nonlichenized fungi germinate and produce hyphae which are divided into cells by means of cross walls called septa. These cells are characterized by their basic cylindrical form and thin walls (Fig. 4). Cells of different hyphae may become secondarily connected. This happens at points where adjacent hyphae touch one another; where their cell walls fuse interconnecting pores are developed. These points of contact between two cells are referred to as anastomoses (Fig. 17). Cells which are connected by pores are chiefly confined to lichens with highly differentiated thalli. In Peltigera, pores can be found in the cross walls between the cells as well as in the anastomoses of the adjacent longitudinal walls. The hyphae of Parmelia are often swollen at the cross septa thereby appearing bone-shaped. The cross septa in this genus are thickened and perforated by pores (Fig. 16).

FIGS. 1–15 Hyphae and tissues. Fig. 1, hyphae with multi-angular cells; Fig. 2, hyphae with globose cells; Fig. 3, hyphae with ellipsoid cells; Fig. 4, branched hyphae with cylindrical cells; Fig. 5, interwoven hyphae in anticlinal arrangement; Fig. 6, interwoven hyphae in periclinal arrangement; Fig. 7, parallel oriented hyphae in periclinal arrangement; Fig. 8, parallel oriented hyphae in anticlinal arrangement; Fig. 9, prosoplectenchymatous tissue developed from anticlinal hyphae with strongly gelatinized walls; Fig. 10, pseudoparenchymatous tissue formed from thin-walled anticlinal hyphae; Fig. 11, fan-shaped arrangement of hyphae; Fig. 12, branched hyphae in a netlike arrangement; Fig. 13, cell lumina of netlike hyphae lying in the homogeneous substance of the gelatinized walls; Fig. 14, prosoplectenchymatous tissue formed by hyphae in a netlike arrangement with gelatinized walls; Fig. 15, pseudoparenchymatous tissue. (Figs. 1–15 from Henssen and Jahns, 1973.)

FIGS. 16–21 Fig. 16, hyphae from the medulla of Parmelia cetrarioides with bone-shaped cross-septa perforated by pores; Fig. 17, hyphae from a rhizine of Peltigera praetextata showing anastomoses and pores; Fig. 18, palisade tissue in the cortex of Roccella phycopsis; Fig. 19, ascus and paraphyses of Coenogonium with club-shaped cells; Figs. 20–21, longitudinal and vertical sections through the thallus of Darbishirella gracillima showing the algal layer and arrangement of cortical hyphae. (Figs. 16–21 from Henssen and Jahns, 1973.)

The fungal cell retains its cylindrical form in loosely organized tissues. In modified lichen tissues the shape of the cells changes because of their special growth and differentiation. Adjoining cells may also influence the shape. For example, cells may be flattened or become angular by the mutual pressure of adjoining developing cells.

In cell differentiation, one of the most important features is the distance between the septa of the hyphae. If the septa are close together, the cells are nearly square in longitudinal section; if the septa are far apart, the cells will appear more rectangular. Many of these cells continue to grow and they begin to swell. The square cells tend to become spherical (Fig. 2) while the rectangular cells take on a more ellipsoid form (Fig. 3). If only one end of the cell swells, it becomes clavate. These asymmetrical cells are often found in the fruiting body at the tips of the paraphyses. In Aspicilia and Coenogonium, for example, several club-shaped cells are formed successively (Fig. 19).

In most lichen tissues the cells show a less regular form than in the ultimate cells of the paraphyses. Usually the lumina are irregularly enlarged and multiangular with thin protuberances (Fig. 1). In cross section these cells are three- to many-cornered and only a part of the cell retains a rounded form.

The shape of the lumen can be influenced by changes in the structure of the wall. Substances may be deposited on the walls or they may become gelatinized and swollen. In this way the cell lumen may be reduced to a thin, often attenuated cavity. In some tissues the cell walls become indistinct and form a homogeneous substance around the lumina (Figs. 9, 13, and 14).

B Tissues

1 DEVELOPMENT OF TISSUES

The structure and development of the tissues depends on the form of the cells and on the particular type of contact between them. This is achieved either by the mutual adherence of the cell walls, by the formation of anastomoses, or by the gelatinization of the cell walls. Other important factors are the direction of growth and the orientation of the hyphae to the surface of the thallus and to each other (Figs. 5–8).

In the tissues the hyphae are either parallel, resulting in a fastigiate arrangement (Figs. 7 and 8), or they are irregularly bent to produce a tissue of interwoven threads (Figs. 5 and 6). Only rarely do the hyphae branch at right angles; usually they branch at an acute angle and form a fan-shaped tissue (Fig. 11). In lichens the most characteristic tissue arrangement is a netlike structure composed of branched, anastomosing hyphae (Figs. 12–14). The cells of this tissue usually have angular or irregular lumina (Fig. 13). This netlike tissue is rarely found in unlichenized ascomycetes and is therefore absent in the description of the textura types given by Korf (1958). The other tissue arrangements described here correspond to the types given by Korf.

2 TYPES OF TISSUES

The development of a true parenchymatous tissue in lichens is rare. Such a tissue is formed by cells dividing in three planes. This kind of cell division, which is characteristic for higher plants, is found in the stroma of some ascolocular fungi and in the muriform ascospores of some lichens, for example, in Polyblastia and Staurothele.

With the exception of these special cases, all lichen tissues are plectenchymatous in origin. The cells divide in only one plane forming cellular hyphal threads. In plectenchyma, the hyphae are loosely interwoven, interconnected by anastomoses, or firmly glued together. The secondary contact between different hyphae can be so close and united that the individual hyphae may be indistinguishable. Some plectenchyma are similar to tissues of higher plants and accordingly are given names that express this resemblance. If the cellular structure of a plectenchyma, consisting of closely packed cells, resembles the parenchyma of higher plants, the tissue is called pseudoparenchymatous or paraplectenchymatous. If the walls of the cells are strongly gelatinized, so that the tissue is similar to prosenchyma (collenchyma) of the higher plants, it is called prosoplectenchymatous.

These two types of compacting tissues can develop from different basic cell forms. For example, a pseudoparenchyma may arise from short, rounded thin-walled cells of different hyphae, which are pressed together, finally forming an unbroken tissue of angular isodiametric cells (Fig. 15). It may be impossible to recognize that this tissue really consists of individual hyphae. In other pseudoparenchymatous lichen tissues the individual hyphae are still discernible (Fig. 10). This kind of tissue develops from elongated swollen cells of loosely interwoven hyphae. In pseudoparenchyma the cell walls may become gelatinized.

Most prosoplectenchymatous tissues develop from plectenchyma with a netlike structure of multiangular or irregularly shaped cells. The walls of the cells gelatinize and become a homogeneous mass in which it is no longer possible to distinguish individual hyphae. Frequently, the shape of the cell lumen changes during the growth of the tissue and accordingly the appearance of the tissue can vary considerably in detail. Not only short-celled hyphae, but also long-celled hyphae in parallel orientation, can form prosoplectenchyma. The cell walls, already connected by anastomoses, may become gelatinized and firmly cemented together.

The hyphae of loosely interwoven plectenchymatous tissues are either irregularly bent or parallel. In tissues with a fastigiate arrangement, the hyphae lie parallel or perpendicular to the surface of the thallus (Figs. 7, 8, 18, 20, and 21). The second type is referred to as a palisade tissue while the perikline structure has no special name.

In some gelatinous lichens, for example in Leptogium, the hyphae are compacted at the surface of the thallus into a pseudoparenchymatous layer which is only one cell thick. Seen from above, this tissue consists either of isodiametric cells pressed together in an unbroken layer or of loosely organized irregular cells (Fig. 22).

FIGS. 22–26 Fig. 22, types of cortex in the Collemataceae. Above: cortex of isodiametric cells in Leptogium sinuatum seen in cross section (left) and from above (right). Middle: primitive cortex of Leptogium apalachense; the cell lumen lies inside a gelatinous substance and forms an irregular pattern when seen from above (right). Below: cortex of Physma byrsinum which is several cells deep in some places. Fig. 23, hairlike thalli of Coenogonium sp. with Trentepohlia as phycobiont; in two places the hyphae gather to form a fruiting body; Fig. 24, hairlike or granular thallus of Coenogonium moniliforme with Physolinum as phycobiont; Fig. 25, hairlike thallus of Cystocoleus niger with Trentepohlia as phycobiont; the alga is completely covered by hyphae; Fig. 26, young perithecium of Porina nucula within a thallus granule; the thallus contains large crystals of calcium oxalate. (Figs. 22–26 from Henssen and Jahns, 1973.)

C Structure of the Thallus

The habit of some primitive lichens, especially of those species where the process of lichenization is not far advanced and the relation between mycobiont and phycobiont is not yet definitely stabilized, resembles the thallus of free-living fungi or algae. In some species, the primitive lichen thalli consist of a loose fungal mycelium enclosing scattered groups of algae, which spreads over the substrate, while other thalli resemble a gelatinous algal colony penetrated and interwoven by fungal hyphae. An example of a thin mycelium with loosely associated algae is the genus Lepraria, a lichen that grows on soil, rocks, or tree bark. Alternatively, the thallus of some species of Collema consists largely of the blue-green alga Nostoc and resembles a colony of this alga (Fig. 66). The hyphae of the mycobiont of Collema grow inside the gelatinous matrix of the phycobiont.

FIGS. 64–68 Fig. 64, zoned thalli of Parmelia centrifuga: ×); Fig. 65, fruticose thallus of Peltula (4 ×); Fig. 66, Gelatinous thallus of Collema subfurvum (1 ×). Fig. 67, umbilicate thallus of Umbilicaria rigida (1 ×); Fig. 68, umbilicate thallus of Dermatocarpon miniatum; the ostioli of the perithecia can be seen as blackpoints (3 ×). (Figs. 64, 67 and 68 from Henssen and Jahns, 1973; Fig. 65 from A. Henssen.)

The lichen thalli described above, characterized by a simple and undifferentiated thallus with irregularly distributed algae, are termed homoiomerous. Only a few lichen genera have this type of thallus. Though the thallus of most lichens is separated into several distinct layers, there exists one other group with an unstratified thallus, which nevertheless is not usually referred to as homoiomerous; these are lichens with extremely short and hairlike thalli consisting of strands of filamentous alga closely wrapped in fungal hyphae (Figs. 23–25).

Most lichens are more complex in structure. The algae are restricted to a particular layer in the thallus and besides the algal zone there is at least one other defined layer, the medulla, which contains no algae. Other layers, a cortex for example, may also be developed. These thalli with a stratified organization are called heteromerous (Fig. 93).

FIGS. 92–95 Fig. 92, soralium of Lobaria pulmonaria; Fig. 93, respiration pore of Nephroma resupinatum; Fig. 94, pseudocyphellae of Cornicularia divergens; Fig. 95, pseudocyphellae of Cetrelia cetrarioides (Figs. 92–94 from Henssen and Jahns, 1973.)

1 ALGAL LAYER

Within the algal layer the contact between the partners of the symbiosis is established. The relations between algae and hyphae vary considerably. Mycobiont and phycobiont are either without direct contact or the hyphae of the fungus more or less completely clasp and surround the algae. In some lichens, cells of the mycobiont are pressed against the algal cells and are called appressoria. In other genera haustoria penetrate the algal cell membrane. Haustoria that penetrate the living cells may kill the algae. In some lichens algae and attacking haustoria divide simultaneously. The two daughter cells of the alga are clasped by two branches of the divided haustorium.

In the algal layer the algae multiply by mitotic cell division and by aplanospores. In Trebouxia, for example, the protoplast of an algal cell divides into several protoplasts, each of which subsequently secretes a cell wall. These aplanospores are freed by the rupture of the wall of the mother cell. The stages of this process can easily be observed in sections of the thallus. Sexual reproduction by zoospore formation has not been observed within the lichen thallus, although the algae produce these motile stages in pure cultures of the phycobiont.

The thickness of the algal layer varies in different lichen genera and the position of the algal zone in the thallus is not invariable. The algae are situated in that part of the thallus where the hyphae are sufficiently loosely interwoven to leave enough space for the algae and where they have an optimum light intensity. The algae are therefore seldom located at the surface or deep within the thallus. The fact that the algae are not strictly confined to a specific layer of the thallus becomes apparent if, by chance, the position of a lichen thallus is changed in nature. If a lobe of a foliose thallus is reversed, the algal layer, which usually lies near the upper surface of the thallus, migrates to the new upper surface and establishes itself inside a tissue which was originally part of the medulla in the lower part of the thallus before reversal (Jahns, 1970).

2 MEDULLA

The medulla consists of loosely interwoven hyphae in a periclinal arrangement. The hyphae are in general only weakly gelatinized and often have a fibrous or a cottony appearance. The medulla has a greater water-holding capacity than any of the other tissues and is a region of food storage. The individual hyphae are not easily moistened and this, together with their loose interweaving, facilitates gas exchange within the thallus. Many lichen substances are deposited extracellularly in the medulla and other layers of the thallus. Besides the deposits of typical lichen substances the thallus may be interspersed with large crystal clusters of calcium oxalate. This occurs, for example, in species of Cladonia, Porina, and Usnea (Fig. 26).

In some fruticose lichens, such as Usnea which has a radial arrangement of the tissues, a central axial strand can be distinguished internal to the medulla (Fig. 46). The structure of the central axis is dense and consists of paraplectenchymatous or prosoplectenchymatous tissue giving considerable tensile or skeletal strength to the thallus. In other genera, i.e., Alectoria, Cladonia, and Ramalina, the central axis is absent. Its place can be taken by a central hollow or by gelatinous or spongy tissues. In Letharia a central cord is formed by fusion of several smaller strands (Fig. 29).

FIGS. 27–31 Fig. 27, part of a cross section of the radial thallus of Sphaerophorus globosus showing a strongly gelatinized cortex; Fig. 28, cross section of the thallus of Sphaerophorus melanocarpus showing cortical hyphae with gelatinized walls in a netlike arrangement; Fig. 29, cross section of the thallus of Letharia vulpina with a central cord formed by several smaller strands; Fig. 30, cross section of the isolateral thallus of Ramalina siliquosa. The algal cells are either situated in the medulla or in the cortex; Fig. 31, the double cortex of Ramalina siliquosa. (Figs. 27–31 from Henssen and Jahns, 1973.)

FIGS. 39–46 Fig. 39, thallus of Parmeliella plumbea with dark, hairy prothallus (2 x); Figs. 40–41, netlike tomentum on the underside of Anzia ornata (65 × and 330 ×); Fig. 42, thallus of Physconia grisea covered with white pruina (9 ×); Fig. 43, black prothallus of Rhizocarpon geographicum growing on white quartz stone; at some places squamules of the thallus have developed (15 ×); Fig 44, lower surface of the thallus of Peltigera venosa showing black veins (3 ×); Fig. 45, thallus of Diploschistes covered with whitish pruina and bearing apothecia (18 ×); Fig. 46, longitudinal section through the thallus of Usnea ceratina showing the central cord (140 ×). (Figs. 39–42 and 44–46 from Henssen and Jahns, 1973).

In fruticose thalli which are held upright by the tube-shaped cortex, the cortical hyphae are either arranged netlike or periklin or they form a palisade tissue (Figs. 18, 27, and 28).

3 CORTEX

Lichens which consist only of medulla and algal layer have a granular or powdery appearance. Most lichens are protected by a cortical layer which is sometimes pigmented and always covers the upper side of the thallus and sometimes also the lower surface. The cortical layers are comparable to the epidermis of a green leaf. The thickness of the cortex varies in different lichen genera and the layer does not always form a continuous stratum. For example, in Ramalina and Solorina, the cortex can be broken by clefts or can be thinner in places thereby allowing the algae to penetrate into the covering layer (Figs. 30 and 115).

FIGS. 115–118 Fig. 115, section through the thallus of Solorina crocea. The cells of the Coccomyxa phycobiont reach into the cortex at several places. The Nostoc phycobiont (black) forms a layer beneath the green algae; Fig. 116, sacculate cephalodium of Stereocaulon coniophyllum containing Scytonema. The terminal cells of the hyphae forming the wall are swollen; Fig. 117, apothecium of Collema coilocarpum with basal supporting tissue formed by the anchor hyphae; Fig. 118, development of isidia in a soralium of Alectoria nidulifera. (Figs. 115–118 from Henssen and Jahns, 1973.)

All tissue types can build a lichen cortex. Occasionally, two different tissues form a cortex which then appears as a two-layered structure. For example, in Ramalina siliquosa the outer part of the cortex is formed by a few parallel to reticulately orientated hyphae, connected by anatomoses. The rest of the thick cortex is formed of hyphae with gelatinized walls with a fastigiate arrangement. The hyphae of the two tissues lie at right angles to one another (Fig. 31).

The homoiomerous thalli of some gelatinous lichens show a few of the phylogenetic steps by which a cortex has been formed. Most species of Collema have a simple uncorticated thallus, but in some species the first stages in the development of a primitive cortex can be observed. Hyphae growing from the inner part of the thallus towards the surface bend at right angles and continue their growth parallel to the surface but still inside the gelatinous substance of thallus (Fig. 33). The species of Leptogium show all steps of development from a cortex formed by loosely organized irregular cells to a layer of isodiametric cells pressed together forming an unbroken stratum. In Leptogium the cortex is always formed outside the gelatinous substance of the thallus. In this genus the cortex is usually one cell thick (Fig. 22) but in some related genera it is several cells deep.

FIGS. 32–38 Fig. 32, hairs on the lower side of the thallus of Leptogium americanum resembling a string of pearls; Fig. 33, development of the cortex in Collema occultatum; Fig. 34, thallus of Peltigera horizontalis with a smooth cortex; Fig. 35, thallus of Peltigera scabrosa with a granular cortex; Fig. 36, podetia of Cladonia showing dispersal of soredia; the upper part of the podetia is ecorticate and completely sorediate (S, soredia; C, cortex); Fig. 37, thallus of Peltigera canina covered with hyaline hairs; Fig. 38, bushlike group of podetia of Cladonia showing distribution by fragmentation of the thallus (a, zone of growth; b, older parts of the podetia which do not grow; c, decaying podetia; f, fragmentation). (Figs. 32–35 and 37 from Henssen and Jahns, 1973; Figs. 36 and 38 from Hennipman, 1969.)

VEGETATIVE STRUCTURES OF THE CORTEX.

The anatomy of the lower cortex of the thallus can differ from that of the upper cortex even in the same species. The shape of the outermost cells of the cortex has an important influence on the habit of the lichen. The surface is often covered with a thin homogenous cuticle, but in a number of lichens the outermost cells become necrotic and give the thallus a scurfy appearance. These tiny granules are called pruina. They may also be an accumulation of carbonates and oxalates. For example, the margins of foliose thalli of Physconia and the disks of the apothecia in particular are covered with a whitish dust (Figs. 42 and 45).

Some cortical cells may continue their growth and develop into thin, hyaline hairs (Fig. 72), each consisting of one or more cells. The hairs are long and pointed or branched and connected by anastomoses (Fig. 37). In some species the cells of the hairs are globose and resemble a string of pearls (Fig. 32). Hairs may form a felted, hirsute, or cottony mat called a tomentum (Figs. 83, 85, and 123). Many foliose species, especially those without a cortex or with only a poorly developed one, are characterized by a tomentum on the lower surface of the thallus. Peltigera and Lobaria are well-known examples of this type. The tomentum can become a thick, spongy layer of netlike branched hairs as in Anzia (Figs. 40 and 41). The blackened hypothallus of Parmeliella and Pannaria also resembles a tomentum (Fig. 39). The thalli of some crustose lichens bear bristly hairs.

FIGS. 69–74 Fig. 69, fruticose thallus of Cladonia impexa (1 ×); Fig. 70, fruticose thallus of Ramalina fraxinea (1 ×); Fig. 71, fruiting bodies of Baeomyces placophyllus (9 ×); Fig. 72, hairy thallus of Teloschistes flavicans (10 ×); Fig. 73, thallus of Cetraria cucullata bearing apothecia (1 ×); Fig. 74, thallus showing holdfast of Ramalina curnowii (1 ×); (Figs. 71 and 74 from Henssen and Jahns, 1973.)

FIGS. 83–88 Fig. 83, cyphellae on the tomentous underside of Sticta (20 ×); Fig. 84, pseudocyphellae of Cornicularia divergens (16 ×); Fig. 85, tubercles on the underside of the tomentous thallus of Nephroma (8 ×); Fig. 86, areation pore of Parmelia aspidota (200 ×); Fig. 87, young isidia of Collema flaccidum in section (350 ×); Fig. 88, hormocystangium of Lempholemma versiculiferum (60 ×). (Figs. 83, 84, and 86–88 from Henssen and Jahns, 1973.)

FIGS. 119–125 Underside of an apothecium of Peltigera leucophlebia with small patches of cortical tissue (5 ×); Fig. 120, undersides of apothecia of Peltigera aphthosa completely covered by cortical tissue (5 ×); Fig. 121, smooth cortex of Peltigera horizontalis (10 ×); Fig. 122, granular cortex of Peltigera scabrosa (15 ×); Fig. 123, hairy cortex of Peltigera canina (15 ×); Fig. 124, cephalodia of Peltigera aphthosa (20 ×); Fig. 125, thallus of Placopsis gelida bearing cephalodia and soralia. A small cephalodium has been formed near the main thallus and is half surrounded by a small scale of the thallus (8 ×). (Figs. 120–123 and 125 from Henssen and Jahns, 1973.)

The form of the marginal cells of the cortex, and as a result the habit of the thallus, may vary in closely related species. In Peltigera horizontalis all marginal cells of the cortex end in an unbroken layer, covered by a gelatinous cuticle (Fig. 34). The thallus appears smooth and glossy (Fig. 121). The cortex of Peltigera scabrosa is characterized by little granules (Fig. 122), each consisting of several cells equivalent to abbreviated bundles of hyphae which have grown above the general surface of the thallus (Fig. 35). In Peltigera canina the cells of the cortex end in interwoven, unorientated hyaline hairs (Fig. 37) giving the thallus its felted appearance (Fig. 123).

The upper surface and the lower surface of foliose lichens can be covered by netlike veins (Fig. 44). For example, the underside of Peltigera always has veins of a spongy and felted appearance. In this genus the veins are formed by the medullary hyphae multiplying at certain places. In Hydrothyria, an aquatic lichen belonging to the same family as Peltigera, the veins consist of single medullary hyphae with strongly enlarged cell lumina.

The layers of the thallus—upper cortex, algal layer, medulla, and lower cortex—are more or less present in all heteromerous lichens. Those lichens with a radially organized thallus are no exception. Here the only difference is that the medulla lies in the center of the thallus and is enclosed by a cylindrical algal layer and cortex. The medulla may have a hollow center or an axial strand.

Foliose lichen thalli resemble the leaves of higher plants. The cortex of the lichen corresponds to the epidermis and the algal layer to the palisade layer. The cyphellae and pseudocyphellae of lichens have the same function as the stomata of the leaf, while their anatomical structure resembles the lenticels of higher plants. There are significant differences in thallus thickness between lichen specimens growing in the shade and others exposed to the sun (Scott, 1971). For example, thalli of Xanthoria parietina growing on shaded tree trunks are thinner than thalli growing on exposed rocks, a feature corresponding to the sun and shade leaves of angiosperms. Not only the thickness of a lichen thallus as a whole, but also the relative thickness of the different layers, varies under different circumstances. The cortex and medulla of lichens growing in the shade are thinner while the algal layer is thicker than in specimens exposed to the sun.

D Attachment of the Thallus to the Substrate

The thallus of homoiomerous lichens is fastened to the substrate by the basal hyphae. The same simple way of attachment also is found in some heteromerous lichens. The rhizoidal hyphae, which anchor the thallus by clasping little particles of the substrate, are like the tomental hyphae. Lichens growing on soil incorporate grains of sand between the hyphae of the lower part of the thallus.

Rhizines have the same function as rhizoidal hyphae. They are composed of bundles of more or less parallel aligned hyphae and develop in three different ways. In some lichens, i.e., in the Parmeliaceae, the hyphae of the rhizines are cemented together as soon as they start to develop. They form a direct elongation of the cortex tissue. The walls of the hyphae are glued together by gelatinization. When the tip of the rhizines reaches the substrate the growing hyphae spread and form a disklike holdfast attaching the lichen to the substrate (Fig. 51). In this disk the hyphae and particles of the substrate are glued together. In other groups of lichens, for example, in the Peltigeraceae and Stictaceae, young rhizines consist of loosely associated hyphae, which later become closely connected by anastomoses. The mature rhizines of this type may spread at their tip and become brushlike (Fig. 53). In Leptogium the rhizines are formed by a tuft of individual hyphae not connected with one another.

FIGS. 47–53 Fig. 47, underside of Umbilicaria pustulata with central holdfast (1.5 ×); Fig. 48, bulbate cilia at the margin of apothecia of Parmelia abstrusa (25 ×); Fig. 49, squarrose rhizines of Parmelia ecuadoriensis (25 ×); Fig. 50, thallus of Heterodermia leucomela with long dark cilia (8 ×); Fig. 51, rhizine of Parmelia sulcata showing point of attachment to the substrate (50 ×); Fig. 52, dichotomous rhizines of Parmelia revoluta (25 ×); Fig. 53, rhizines of Peltigera aphthosa (12 ×). (Figs. 47, 49–51, and 53 from Henssen and Jahns, 1973.)

To what extent rhizines can transport dissolved mineral or organic metabolites from the substrate to the thallus has not yet been established. Probably there is some correlation between the type of rhizine and its ability to transport water which varies considerably. For example, the compact rhizines of Parmelia are not quickly wetted by water while the treelike rhizines of Peltigera function like a wick.

Rhizines always grow from the underside of the thallus. Vegetative structures emerging from the margin of the thallus and closely resembling the rhizines are called cilia. The habit of rhizines and cilia varies in different genera. The simplest type is an unbranched strand of hyphae (Figs. 50 and 51). Branched rhizines and cilia are of a squarrose or dichotomous type (Figs. 49 and 52). Short cilia can have a bulbate inflated base (Fig. 48).

Unbranched cilia, for example in Usnea, are sometimes called fibrillae (Fig. 76) and short pin-shaped protuberances are named papillae. As it is unknown whether there are any fundamental differences between these vegetative structures, it is really impossible to give a meaningful definition of the different names.

FIGS. 75–77 Fig. 75, thallus of Usnea longissima ×); Fig. 76, thallus of Usnea ceratina; note fibrillae on the apothecial margins (2.5 ×); Fig. 77, Sticta filix; the dark fruticose thallus with Nostoc as phycobiont bears the foliose thallus which has a green phycobiont (2 ×). (Figs. 75–77 from Henssen and Jahns, 1973.)

Some lichens, especially those growing on rocks or tree bark, are attached by a disklike holdfast (Figs. 47 and 74).

III Morphology of the Thallus

A Color of the Thallus

Most lichens are gray or brown when dry. In wet thalli the color of the algae can be seen more distinctly through the cortex and these lichens become more or less green. Many species are brightly colored by incrustations of special lichen pigments in the cortex. For example, the orange or yellow substance called parietin is found in the Teloschistaceae. Green and yellow tints are common in lichens while red, blue, and violet colors are rare. Many of these pigments are not confined to a single genus but often occur widely throughout the lichens. They are absent in most gelatinous lichens and rare in pyrenocarpic species.

B Growth Forms of the Thallus

The segregation of lichens into the large groups of crustose, foliose, and fruticose lichens has already been mentioned. However, the hairlike or filamentous lichens with their short, thin branches and the gelatinous lichens form two extra groups which are not satisfactorily incorporated into one of the three main types. The gelatinous lichens are cartilaginous when dry, but immediately swell and become gelatinized in wet conditions. To a certain extent all lichens, which are hard and brittle when dry, may swell when wet and become soft and flexible. When the traditional classification into growth forms is applied to all the different species of lichen, intermediate forms are usually arbitrarily placed in that group to which the majority of closely related species belong.

1 CRUSTOSE LICHENS

Crustose lichens never possess a lower cortex. They are attached to soil, rock, or tree bark by the hyphae of the medulla and the contact is so intimate that they are practically inseparable from the substrate. A patch of crustaceous lichen may belong to one species and yet be composed of many individuals which have fused together. Simple crustose lichens are homoiomerous. They lack a cortex and are therefore granular in structure. The mycelium spreads over the substrate in a thin filamentous mat enclosing the algae.

The thallus of most crustaceous lichens consists of little scales called areoles (Fig. 54). The lower hyphae of the areoles usually grow faster than the main part of the thallus and form a thin spreading layer around it. This mat of hyphae is usually dark in color and is called a prothallus (Fig. 43). The name hypothallus, also previously used for this structure, is more correctly applied to the thin filaments which link the areoles of the inner part of the thallus. A cracked surface in lichens may develop in one of two ways. In many species the thallus is initiated evenly and becomes cracked, often incompletely, at a later stage. In other groups of lichens, small defined areas of the thallus develop on an advancing prothallus appearing as separate entities and gradually becoming more closely compacted towards older parts of the thallus (Fig. 43).

FIGS. 54–60 Fig. 54, areolate thallus of Lecanora frustulosa (2 ×); Fig. 55, endolithic thallus of Lecidea; the black apothecia emerge from the stone (0.6 ×); Fig. 56, thallus of Acarospora oxytona with effigurated margin (3 ×); Figs. 57–58, placoid thallus of Xanthopeltis rupicola seen from above (with apothecia) and from below (with umbilicus) (3 × and 3 ×); Fig. 59, squamulose thallus of Lecidea scalaris, the margin of the squamules becoming sorediate (8 ×); Fig. 60, umbilicate thallus of Glypholecia scabra (1 ×). (Figs. 54 and 57–60 from Henssen and Jahns, 1973.)

Lichens with very small areoles are frequently homoiomerous. Bigger areoles begin to show the first signs of a differentiation into layers. The algae are accumulated in the upper part of the thallus, and at the surface a kind of cortex is formed by necrotic, gelatinized cells. This layer of dead cells is continuously sloughed off, but is always reformed by the growth of the thallus. An example of this type is Acarospora. Other crustose lichens, especially the intermediate forms between the crustose and the foliose type, have a true heteromerous thallus. The cortex may cover only the upper surface of the thallus or it also may include the margin of the individual areoles.

An extreme example of the crustose type are lichen thalli which grow completely inside their substrate, whether it be wood or stone. Species growing inside rock are called endolithic, and those penetrating wood are termed endophloeodic. Sometimes the thallus of these lichens can be seen as a discoloring of the substrate (Fig. 55), but frequently only the ascocarps in pits or on the surface of rock or bark indicate the presence of a lichen. The hyphae of endolithic lichens appear to excrete lichen substances which are able to dissolve the stone and thus make it possible for hyphae and algae to penetrate several millimeters into the rock. Species growing inside limestone develop special oil cells that are intercalated along the hyphae. The irregularly swollen cells appear clustered with oil drops.

2 INTERMEDIATE FORMS BETWEEN CRUSTOSE AND FOLIOSE LICHENS

In some crustose lichens elongated, small lobes replace the areoles. These lobes can be fastened to the substrate by the entire lower surface or the margin of the thallus can be free and ascending. Different combinations of these characteristics lead to a variety of described growth types.

If the margin of the thallus consists of small, elongated lobes while the inner part is composed of small areoles, the lichen is said to have an effigurated margin (Fig. 56). If the whole thallus is formed by elongated lobes, the lichen belongs to the placoid type. Thalli of the effigurate and placoid type are closely appressed to the substrate by their whole lower surface. The squamulose thallus of some species of Heppia, Lecanora, Lecidea, and Placynthium consists of little scales. At one side their margin separates from the substrate and bends upwards (Fig. 59). Several scales can be arranged in a rosette. The squamules may overlap like the tiles of a roof and are then imbricate.

Further development of the squamulose thallus is seen in peltate lichens. In this type only the central part of the scales is fastened to the substrate, the whole margin becoming free. Lichens of this type have more or less the same habit as the umbilicate foliose genera (Figs. 57, 58, and 60). The scales and lobes of some squamulose and peltate thalli are bent upwards and begin to resemble fruticose growth forms. For example, some species of Peltula with upright lobes and with a corresponding radial anatomy could be classified as having a fruticose growth habit (Fig. 65).

3 FOLIOSE LICHENS

The thallus of foliose lichens is formed by flattened lobes, which are heteromerous and dorsoventral in structure. Two principal types, the laciniate and the umbilicate growth form, can be distinguished. Laciniate thalli adhere more or less firmly to the support on which they grow. Either the whole lower surface is in contact with the substrate or the margin of the lobes becomes free and bends upwards. The thalli are usually attached by rhizines or rhizoidal hyphae. The umbilicate lichens are platelike and attached by a central discoid holdfast called the umbilicus (Fig. 47).

a LACINIATE FOLIOSE LICHENS.

The laciniate lichens form an extremely polymorphous group. Their habit and the mode of attachment of the thallus vary and their anatomy is the most complex of all lichens. Some are very large plants. Lobes of Lobaria pulmonaria (Fig. 61) may reach a length of 30 cm and multilobed thalli of Parmelia (Fig. 62) reach ½ m in diameter (Fig. 64). The thalli of Lobaria are covered on both sides by a cortex, while in Peltigera (Fig. 63) the cortex is restricted to the upper side, the underside being tomentose with veins. In Parmelia the whole lower surface of the thallus or only part of it is attached to the substrate by rhizines. Rhizines, cilia, veins on the thallus surface, and other vegetative structures are common in foliose lichens. The cortex layers are derived from different types of tissue.

FIGS. 61–63 Lobaria pulmonaria×); Fig. 62, foliose, laciniate thallus of Parmelia quercina (2.5 ×). Fig. 63, foliose laciniate thallus of Peltigera canina ×). (Figs. 61 and 62 from Henssen and Jahns, 1973.)

b UMBILICATE FOLIOSE LICHENS.

Umbilicate lichens have a disklike thallus that is attached to the substrate with a central holdfast. The holdfast causes a small depression in the surface of the thallus. All species of Umbilicaria (Fig. 67) have this type of thallus, as the name of the genus indicates. An umbilicate thallus occurs in other lichens which are not closely related to Umbilicaria, as, for example, in the pyrenocarpous genus Dermatocarpon (Fig. 68) and in the gymnocarpous genera Glypholecia, Omphalodium, and Xanthopeltis (Figs. 57, 58, and 60). The thallus of Umbilicaria is heteromerous and fully corticated. Many species also are characterized by a veined or rugose thalline surface.

4 INTERMEDIATE FORMS BETWEEN FOLIOSE AND FRUTICOSE LICHENS

The thalli of foliose lichens of the laciniate type, for example, those of Cetraria (Fig. 73), are sometimes nearly erect so that they are often considered to be fruticose. The lobes are fastened by the lower surface and in older thalli the base begins to rot. This further proves the arbitrariness of classification based on thallus types.

5 FRUTICOSE LICHENS

The lobes of fruticose lichens are strap-shaped or threadlike with a radial or dorsiventral thallus. Ramalina (Fig. 70) and Roccella (Fig. 79) are good examples of strap-shaped, radial thalli, while Usnea (Fig. 75) consists of thin strands up to 5 m long. Evernia and Pseudevernia have strap-shaped, dorsiventral thalli.

FIGS. 78–81 Fig. 78, cup-shaped podetia of Cladonia chlorophaea growing from a foliose primary thallus; the older podetia bear apothecia (3 ×); Fig. 79, thallus of Roccella fuciformis with soralia (1 ×); Fig. 80, pseudopodetia of Stereocaulon alpinum with phyllocladia and apothecia (7 ×); Fig. 81, Pilophorus strumaticus; upright pseudopodetium bears black apothecia; note black cephalodium on the thallus (25 ×); (Figs. 78–80 from Henssen and Jahns, 1973.)

Many strap-shaped and radiate thalli are attached to the substrate by a holdfast (Fig. 74). Some long, pendulous, threadlike strands of certain species of Usnea hang from the branches of trees, without any organized attachment to the bark. Of these, Usnea longissima may reach a length of several meters. Other fruticose lichens that grow on soil form little cushions which consist of separated upright lobes. Frequently, they are not attached to the soil. Some species degenerate at the base and become completely free. They may be dislodged by the wind and blown over the ground. Good examples of this type are species of Cladonia, sect. Cladina, and Cornicularia.

The stiffness of fruticose lobes is achieved by two different types of basic construction. In some lichens the hyphae of the cortex serve as supporting tissue. They form a cylindrical tube at the lateral edge of the thallus, while the center of the lichen is hollow or filled with a cottony medulla. This type of construction serves to keep the plant upright and to withstand lateral pressure. The supporting tissue is a prosoplectenchyma or pseudoparenchyma with the hyphae being closely cemented. In the second type of fruticose lichen the supporting tissue is situated in the center of the medulla. A central cord or axial strand is constructed from thick-walled, perpendicular, agglutinated hyphae. Usnea has a single threadlike elastic cord, while other lichens develop several individual strands which later fuse. This central axial strand gives the requisite tensile and skeletal strength to pendulous lichens.

6 LICHEN THALLI WITH A TWOFOLD CHARACTER

In some lichens the thallus consists of a horizontal part lying on the substrate and of a vertical, fruticose part, bearing the fruiting bodies. The horizontal thallus can be crustose, as in some species of Baeomyces (Fig. 71) or foliose, as in Cladonia (Fig. 78). The horizontal thallus of a lichen may be evanescent, being only found in a very young specimen, disappearing as it matures. The adult lichen consists only of a vertical fruticose thallus (Fig. 69).

The twofold thallus has been independently developed in several lichen families and can be of different origin. In Cladonia the thallus verticalis is formed from the generative tissue, a tissue which surrounds the sexual organs and usually gives rise to the ascocarp. Thus, the thallus verticalis of this genus is ontogenetically a part of the fruiting body. This kind of fruticose stalk is called a podetium. The podetia may be simple or richly branched with pointed apices or apical cups.

The development of the thallus verticalis in Stereocaulon (Fig. 80) and Pilophorus (Fig. 81) is different. A part of a squamule of the thallus horizontalis or a complete granule of the thallus grows vertically upwards and develops into a simple or branched more or less erect thallus verticalis. The primordium of the fruiting body is formed only at the top of this stalk. The generative tissue builds only the ascocarp while the thallus verticalis is differentiated from vegetative thallus tissue. This kind of stipe is called a pseudopodetium.

7 HAIRLIKE THALLI

The habit of hairlike lichens, with their threadlike thalli, resembles that of fruticose lichens. These lichens, however, are much smaller and usually not more than a few millimeters high. In contrast to most lichens, the habit is principally determined by the phycobiont. Filamentous algae, belonging to the Chlorophyceae or the Cyanophyceae, are more or less closely ensheathed by hyphae of the mycobionts (Figs. 23–25).

8 GELATINOUS LICHENS

The consistency and growth form of gelatinous lichens are for the most part determined by the blue-green phycobiont. The characteristic swelling of the wet thallus is due to the gelatinous sheath of the phycobiont. Frequently, the structure of the thallus is homoiomerous but the anatomy is different from the homoiomerous crustaceous lichens. In crustose lichens the algae are scattered in a mycelium of loosely interwoven hyphae, while the hyphae of gelatinous lichens usually grow inside the gelatinous algal substance that fills the thallus. The hyphae often do not touch the algae. The lateral margin of the thallus is also sometimes formed by the gelatinous sheath of the algal cells.

In some genera the fungus provides a cortex at the surface of the thallus. A gradation of differentiation can be found among genera of the Collemataceae. Most species of Collema are noncorticate, but in some species vertically oriented hyphae reach the surface of the thallus, bend at right angles, and spread parallel to the surface (Fig. 33). Leptogium has a cortex which is one cell layer thick. It consists of irregularly formed cells which are arranged in either a broken pattern or in a regular layer of isodiametric cells when viewed from above (Fig. 22). The cortex of other lichens belonging to the Collemataceae is several cell layers thick.

All types of growth forms are found in the gelatinous lichens. Most species are very small and only the foliose thalli reach a diameter greater than 10 cm (Fig. 66). The color of the thallus is olive-green, blackish, or gray. The bright colors of lichen substances or pigments are not present in this group. Some species are red or violet when wet, but this