American Journal of Botany 88(11): 21292131. 2001.

BOOK REVIEW

THE

BIOLOGY OF BRYOPHYTES

BRYOPHYTES ARENT JUST SMALL TRACHEOPHYTES1

BRENT D. MISHLER2
University Herbarium, Jepson Herbarium, and Department of Integrative Biology, University of California, Berkeley, California 94720 USA

The bryophytes, with 20 000 species worldwide, are the most diverse group of land plants except for the owering plants. The group (which may well not be monophyleticsee below) includes three quite distinct lineages (i.e., mosses, hornworts, and liverworts) of familiar species frequently encountered in mesic forests and along streams, as well as a number of less familiar species of tropical rain forests, arctic tundra, and desert boulders. The bryophytes have a basal phylogenetic position among the extant land plants (the embryophytes), remnant lineages surviving today from the spectacular radiation of the land plants in the Devonian Period, some 400 million years ago. The three main bryophyte lineages, plus a fourth, the tracheophytes (i.e., the so-called vascular plants), comprise the entirety of the monophyletic embryophytes, arguably one of the most important lineages to have arisen in earths historythey made possible the colonization of the land by animals and evolved a unparalleled diversity of size, structure, chemistry, and function. Thus, as aptly put by Michael Christianson in the present book, bryophytes preserve three-fourths of what it means to be a land plant (p. 220). The bryophytes are clearly a key to understanding how the embryophytes are related to each other and deciphering how they came to conquer the hostile land environment from their primitive home in fresh waterhabitats still occupied by relatives of the land plants, the green algae (Graham, 1993). Yet despite their diversity, phylogenetic importance, and key roles in the ecosystems of the world, study of many aspects of the biology of bryophytes has lagged behind that of the larger land plants, perhaps because of their small size and the few scientists specializing on the group. This is unfortunate because of the intrinsic scientic interest of these plants. The bryophytes contain some of the most species-rich lineages of land plants, presenting a challenge (as well as opportunities) for understanding processes of evolutionary diversication. They have several biological features making them particularly suited to serve as study organisms in macroevolutionary, population genetic, and ecological research (Mishler, 1988; Shaw, 1991). The plants are complicated enough in ontogeny and mature structure to serve as model systems for studying land plant evolution in general, and yet simple enough morphologically (constructed as they are from easily traceable cell lineages derived from single apical cells) and genetically (given the haploid vegetative plant body) to be readily studied with current techniques. They are in the
1 Bryophyte Biology. A. Jonathan Shaw and Bernard Gofnet [eds.]. Cambridge University Press. 2000. x 476 pp. ISBN 0-521-66097-1 (hardback; $100.00); ISBN 0-521-66794-1 (paper; $35.95). 2 Phone: 510-642-6610, FAX: 510-643-5390, e-mail: bmishler@socrates.berkeley.edu.

great majority of cases (except for some ephemeral species) observable throughout the year; they are also small in size, easily regenerated from fragments, and thus also easy to study in culture. This comprehensive and attractive book, edited by Jon Shaw of Duke University and Bernard Gofnet of the University of Connecticut, will go a long way towards making the biology of these plants more widely known. The wellwritten contributions by many top experts, along with an unusually extensive set of up-to-date literature citations and the well-illustrated nature of most chapters, make this an essential book for the shelves of all botanists, most especially teachers and students. PHYLOGENY The rst four chapters of the book deal appropriately with anatomy, morphology, phylogenetics, and systematics. A wellillustrated and thorough paper by Renzaglia and Vaughn leads off with the hornworts, an enigmatic group that may hold the key for understanding the evolution of fundamental land plant features. Another well-illustrated chapter by Crandall-Stotler and Stotler follows on the liverworts, the most morphologically diversied of the three main bryophyte lineages. A comprehensive morphological cladistic analysis and detailed classication down to the genus level are also provided. The mosses, highly species-rich yet morphologically relatively uniform (at least as compared with the liverworts), are treated in the third chapter by Buck and Gofnet, who also provide a detailed classication down to the genus level. Both of the classications in these two chapters are global in approach and will provide a good starting point for further renement. The fourth chapter, by Gofnet, reviews the many important issues that are at stake in understanding the origin of the land plants. He depicts the controversial state of relationships well and rightly suggests that important character state reconstructions will remain equivocal until relationships among the extant lineages are claried and fossils can be properly interpreted. The phylogeny of bryophytes has attracted interest over a long period of time. In morphological cladistic analyses, the classical group bryophytes appeared not to be monophyletic, in most cladograms with the liverworts being the sister to all other land plants and the mosses more closely related to the tracheophytes than to the hornworts or liverworts (Mishler and Churchill, 1984, 1985; Mishler et al., 1994; Kenrick and Crane, 1997). Most recent molecular cladistic analyses conrm the nonmonophyly of the bryophytes, although the precise interrelationships of the mosses, hornworts, and tracheophytes remain problematic; indeed most possible resolutions of the

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four major land plant lineages have been supported by one molecular data set or another (as shown nicely in g. 4.1 in Gofnets chapter). It is clear that this is yet another example of a deep phylogenetic radiationwhatever the relative relationships among the four lineages truly are, the periods of shared history are extremely brief as compared to the long separate history of lineages afterwards. In my opinion, a satisfactory result in such cases can only come from extensive total evidence analyses that include large sets of unlinked genes and morphology, including fossil taxa that can help break up long branches (Mishler, 2000). Nucleotide sequence data are subject to considerable homoplasy in such deep reconstructions because of their sheer simplicity (Mishler, 1994), thus of particular promise are much more complicated characters derived from comparative genomics (rearrangements, inversions, duplications, etc.). Further development of these over the next few years should shed much light on this and other difcult phylogenetic problems. CHEMISTRY, GENETICS, AND PHYSIOLOGY The second four chapters of the book deal with the inner workings of bryophytes. Their incredibly rich chemistry is reviewed by Mues, in very accessible text and gures for the nonspecialist. Molecular genetics of mosses is a rapidly accelerating eld, reviewed here by one of its leaders, David Cove. In addition to a long history of classic genetic studies, mosses are the only plants for which homologous recombination can be used as a practical tool in genetic studies, suddenly making them hot subjects for study of gene function in biotechnology. This is an area certain of rapid growth in the future that should also benet understanding of development, morphology, physiology, and evolution. The morphogenetic context is reviewed well by Christianson in the following chapter, again with an eye towards making the information broadly available to nonspecialists. Proctor follows with a ne review of physiological ecology, here emphasizing water relationships, and appropriately so, because of the unusual way in which bryophytes relate to water in their environment. In a recent review, Oliver, Tuba, and Mishler (2000) showed that vegetative desiccation tolerance was primitively present in the land plants (as seen today in all bryophytes), but was then lost in the evolution of tracheophytes. The initial evolution of vegetative desiccation tolerance was a crucial step required for the colonization of the land, but that tolerance came at a cost, since metabolic rates are lower in tolerant plants as compared to plants that dont maintain costly mechanisms for tolerance. Thus, the loss of tolerance might have been favored along with the internalization of water relationships that happened as the vascular plants became more complex. However, at least two independent evolutions (or re-evolutions) of desiccation tolerance occurred in Selaginella and in the ferns. Within the Angiosperms, at least eight independent cases of evolution (or re-evolution) of desiccation tolerance occurred. The time scale of desiccation, rehydration, and responsiveness are different in different lineages each time the general phenotype was re-evolved. Deciphering the physiological mechanisms and genes behind these complex phenotypes will be aided by a phylogenetic approach and will have both intellectual and economic applications.

ECOLOGY, EVOLUTION, AND BIOGEOGRAPHY The nal ve chapters in the book deal with bryophytes in relation to the environment in ecological and evolutionary processes. Bryophytes are in unusually intimate contact with their microenvironment, as shown by Bates in an extensive review of mineral relationships, natural substrates, and human sources of pollutants. Peatland ecosystems, the primary habitats that are actually dominated by bryophytes, are reviewed by Vitt in the next chapter. He uses particularly informative diagrams and ordinations to visualize species composition (not all Sphagnum by any means) in relation to the most important environmental variables. ONeill then tackles a timely topic in the following chapter, on the role of bryophyte-dominated ecosystems in the worlds carbon budget. It turns out that northern peatlands and other bryophyte-dominated habitats contain some of the globes largest carbon reservoirs, considerably more than tropical rainforests, for example. The possibility of a positive feedback loop, with global temperature increase possibly leading to carbon release from peatlands, is a matter of great concern. Shaw follows with a chapter that looks at population-level evolutionary processes in bryophytes, whose unique biology means that certain dogmas received from studies of the larger land plants dont apply (more below). The nal chapter in the book is a concise overview by Tan and Pocs of bryogeogra phy. They also address conservation issues, in addition to illustrating the major distributional patterns. Bryophytes tend to have distributional ranges that correspond to historical biogeographic patterns of tracheophytes (Crum, 1972; Schoeld, 1983), but intriguingly, species of bryophytes (at least with currently prevailing species concepts in the group) tend to be relatively more widely distributed. As discussed by Shaw (1991, and his chapter in the present book), there is an evident disconnect between molecular variation among populations, which varies at about the level you would expect from angiosperm studies, and morphological variation, which is often much less than one might expect. This may indicate that developmental constraints play an unusually important role in maintaining the morphological integrity of bryophyte species and higher taxa (Mishler, 1985). Bryophyte species tend to be highly specic for particular microenvironments (responding to such features as temperature, light and water availability, substrate chemistry, etc.), making them good ecological indicator species. Thus, bryophytes are attracting much attention recently from applied ecologists and conservation biologists. For example, in addition to their role in the global carbon cycle as mentioned above, bryophytes appear to be an ecological keystone group in the temperate rainforest that extends along the coast from southern Alaska to northwestern California. Throughout this region, the mass of bryophytes on angiospermous trees in riverine corridors is almost as great as any place in the world. Nadkarni (1984) suggested that bryophytes in such areas provide a major buffer allowing measured loss of minerals from the tree to the soila loss slow enough to allow almost complete reabsorption by the tree. CONCLUSION: A RADICAL VIEW OF BRYOPHYTE BIOLOGY, OR MOSSES ARE FROM MARS, VASCULAR PLANTS ARE FROM VENUS Let me conclude with a personalized summing up, addressing the question: in what ways does bryophyte biology dif-

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ferent from that of the larger tracheophytes? The short answer: in almost every way possible! The groups didnt evolve on different planets, but their differences could almost make you think they did. They certainly adopted very different approaches to being a land plant on this planet. As discussed above, many aspects need much more study, but what is known about bryophyte biology suggests that in general the bryophytes differ in most ways in their biology, ecology, and evolution from tracheophytes. I will go through these contrasts in list form below, in hopes they can summarize how different major lineages have solved the problem of life on land, in a way useful for teaching about these remarkable little plants. Major differences in bryophyte biology from tracheophytes include: 1. Haploid dominance in the alternation of generations. The green, vegetative part of the life-cycle in bryophytes is haploid. Without the genetic benets of dominance, genes acting in the gametophyte are presumably subject to relatively severe selection. 2. Extensive phenotypic plasticity. Studies have shown that bryophytes tend to have very high amounts of morphological and physiological plasticity. This may compensate for their demonstrated low levels of ecotypic differentiation (perhaps due to haploidy). 3. Poikilohydry and desiccation tolerance. Poikilohydry is the rapid equilibration of the plants water content to that of the surrounding environment, while desiccation tolerance is the ability of a plant to recover after being air-dry at the cellular level. All bryophytes have these abilities to some extent, but as discussed above, this was lost in the larger, more complex, and endohydric tracheophytes. 4. Need for free water for sexual reproduction. A residual feature of the early land plants is the constraint imposed by the swimming sperm. Swimming gametes have short dispersal distances that leads to frequent inbreeding in monoicous species and lack of sporophyte production in dioecious species. 5. The clump as a super-organism. Many mosses and some liverworts are essentially social organisms. This results from the combination of clonal growth, poikilohydry, and external water conduction. The plants in a clump are subject to natural selection as a group. Intimate contact of each vegetative cell with the environment, due to poikilohydry, lends itself to interplant chemical communication via pheromones. 6. Heavy reliance on asexual reproduction. Due to the difculty of achieving fertilization, many bryophytes have evolutionarily lost functional sexuality. Since bryophytes grow from an apical cell, somatic mutation allows genetic variation even within clones. 7. Small stature and the occupation of microhabitats. Small size, lack of roots, and poikilohydry means that bryophytes are in a close relationship with only their immediate microenvironment. Over geological time, they may be less inuenced by climatic change, and linger in refugial habitats. 8. Less selection pressure from the biotic component of the

environment than from the physical component. Vagility and establishment abilities of bryophytes are relatively poor. Available substrates are not lled in most mesic and xeric environments (although they may be in some hydric environments). The presence of other bryophytes nearby often appears benecial to growth. 9. Relatively slow evolutionary rates in morphology. The fossil record of bryophytes indicates that ancient forms are very similar to modern ones. Biogeographically, bryophytes tend to follow the same historical patterns of disjunction as tracheophytes, but at a lower taxonomic level. This may indicate that developmental constraints play an unusually important role. The overall effect of these features on the evolutionary ecology of bryophytes makes them profoundly different. By studying bryophytes and comparing their lifestyle to that of tracheophytes, the student can learn to observe structure closely, think critically about evolutionary inferences, and comprehend how different lineages can take different functional paths in response to the same stimuli. Let us hope this book will lead more students to study and enjoy this most wonderful group of plants. LITERATURE CITED
CRUM, H. A. 1972. The geographic origins of the mosses of North Americas deciduous forest. Journal of the Hattori Botanical Laboratory 35:269 298. GRAHAM, L. E. 1993. The origin of land plants. Wiley, New York, New York, USA. KENRICK, P., AND P. R. CRANE. 1997. The origin and early diversication of land plants: a cladistic study. Smithsonian Institution Press, Washington, D.C., USA. MISHLER, B. D. 1985. The morphological, developmental, and phylogenetic basis of species concepts in bryophytes. Bryologist 88:2072l4. MISHLER, B. D. 1988. Reproductive ecology of bryophytes. In J. Lovett Doust and L. Lovett Doust [eds.], Plant reproductive ecology, 285306. Oxford University Press, London, UK. MISHLER, B. D. 1994. Cladistic analysis of molecular and morphological data. American Journal of Physical Anthropology 94:143156. MISHLER, B. D. 2000. Deep phylogenetic relationships among plants and their implications for classication. Taxon 49:661683. MISHLER, B. D., AND S. P. CHURCHILL. 1984. A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406424. MISHLER, B. D., AND S. P. CHURCHILL. 1985. Transition to a land ora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1:305328. MISHLER, B. D., L. A. LEWIS, M. A. BUCHHEIM, K. S. RENZAGLIA, D. J. GARBARY, C. F. DELWICHE, F. W. ZECHMAN, T. S. KANTZ, AND R. L. CHAPMAN. 1994. Phylogenetic relationships of the green algae and bryophytes. Annals of the Missouri Botanical Garden 81:451483. NADKARNI, N. M. 1984. Biomass and mineral capital of epiphytes in an Acer macrophyllum community of a temperate moist coniferous forest, Olympic Peninsula, Washington State. Canadian Journal of Botany 62:2223 2228. OLIVER, M. J., Z. TUBA, AND B. D. MISHLER. 2000. The evolution of vegetative desiccation tolerance in land plants. Plant Ecology 151:85100. SCHOFIELD, W. B. 1983. Bryogeography of the Pacic Coast of North America. Journal of the Hattori Botanical Laboratory 55:3543. SHAW, A. J. 1991. Ecological genetics, evolutionary constraints, and the systematics of bryophytes. Advances in Bryology 4:2974.