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53 Tropcial Bryology 2: 51- 58, 1990

Developmental evidence of acrocarpy in ciliata (Musci: ).

Efrain De Luna, Department of Botany, Duke University, Durham, NC 27706.

Abstract. The growth habit of the Hedwigiaceae has been described variously as acrocarpous, pseudopleurocarpous, or pleurocarpous. Anatomical evidence presented here indicates that is acrocarpous. The archegonia are terminal on the main shoot, and the branching pattern is sympodial. The main axis of each thus consists of a succession of subterminal innovations, rather than a single shoot of indeterminate growth. Since the are plagiotropic and are pleurocarpous in appearance, this growth pattern can be also called pseudo-pleurocarpous.

Resumen. El hábito de crecimiento presente en las Hedwigiaceae se ha descrito como acrocarpo, pseudopleurocarpo, o pleurocarpo. La evidencia anatómica presentada aquí indica que Hedwigia ciliata es acrocarpo. Los arquegonios son terminales en el tallo principal y el patrón de ramificación es simpódico. El eje principal de una planta consiste de una sucesión de inovaciones subterminales, en vez de un tallo principal de crecimiento indeterminado. Dado que las plantas son plagiotrópicas y son pleurocárpicas en apariencia, este hábito también puede denominarse pseudo-pleurocarpo.

Introduction defined by the position of the perichaetia and by the branching pattern. Perichaetial The majority of are modular in position and branching pattern are usually their individual construction as well as in deduced from the mature architecture of their colonial structure. The general the mosses. In some mosses a more detailed appearance of the colony is commonly study has been necessary to understand referred to as the 'life form' (Mägdefrau, the growth habit. Correns (1898), Koponen 1982), whereas the general morphology (1982), Meusel (1935), and Stark (1985) of the individual is often referred to as the have suggested additional morphological 'growth form' (Gimingham and Robin- aspects that can be studied, for example son, 1950; Horikawa and Ando, 1952; phyllotaxy, arrangement of branch Mägdefrau, 1982; Meusel, 1935). In primordia, presence of pseudoparaphyl- addition to growth form, the synonymous lia, and final branch orientation, among terms 'growth pattern', and 'growth habit' others. However, as Schofield and Hébant are also used in this paper. (1984) have stated, ‘branching of gametophores .... has been little studied in Despite the morphological diversity its anatomical aspects’. exhibited by moss gametophores, there are two basic growth forms: acrocarpous The growth habit has been considered of and pleurocarpous (Schofield and Hébant, particular phylogenetic importance in some 1984). These have commonly been moss taxa. For example, several studies 54 have used morphological aspects of growth Vitt, 1986; Frey, 1970; Vitt, 1982). A form as a basis for taxonomic decisions number of authors described Hedwigia (cf. Koponen, 1972, 1979; Nishimura, ciliata as having archegonia terminal on 1985; Sastre-De Jesús, 1987; Tuomikoski main or lateral branches, and they implicitly and Koponen, 1979). Also, Buck and Vitt interpreted it as pleurocarpous (Catcheside, (1986) erected several groups of families 1980; Crum and Anderson, 1981; Ireland, (orders and suborders) based on a 1982; Jones, 1933; Nyholm, 1960; combination of peristomial features, the Sainsbury, 1955; Sim, 1926; Smith, 1978). position of archegonia in relation to the However, Scott and Stone (1976) expli- main shoot, and the type of branching. citly described the growth pattern in H. Moreover, detailed study of the allegedly ciliata as sympodial, 'the stems ending in pleurocarpous growth pattern in Mesotus capsule production and being replaced by (Lindberg, 1873; Allen, 1987 a) was one or two side branches from just below.' helpful in reassigning it to a systematic position among the acrocarpous families. The developmental basis for the growth habit has never been fully described in H. Understanding of the phylogenetic rela- ciliata or in any other species belonging to tionships of the Hedwigiaceae has been this family. It was expected that anatomical limited by uncertainty about the type of study of the perichaetial position and growth habit and the lack of a peristome. branching points of Hedwigia ciliata The purpose of this research was to study would provide a better characterization of the growth form of Hedwigia ciliata the growth habit of the family. (Hedw.) Ehrh. ex P. Beauv., based on developmental anatomy. Recent studies of growth form in plants have stressed the developmental The family Hedwigiaceae has traditionally significance of an architectural analysis included six genera: Hedwigia P.-Beauv., (Hallé et al, 1978). According to Donoghue Hedwigidium B. S. G., Braunia B. S. G., (1981), 'the study of growth patterns is the Pseudobraunia (Lesq. and James) Broth., search for regularities in the construction Rhacocarpus Lindb., and Bryowijkia of plants and the analyses of how such Noguchi (Barthlott and Schultze-Motel, regularities are related to plant form.' 1981; Brotherus, 1925; Vitt, 1982). Although conceived to describe the archi- Current research (De Luna, 1989; in press) tecture of trees, some of the concepts corroborates earlier suggestions to exclude reviewed by Donoghue (1981), Hallé et al Rhacocarpus (Buck and Vitt, 1986) and (1978), Tomlinson (1978) and White Bryowijkia (Vitt and Buck, 1984) from (1984) can be applied to an analysis of the Hedwigiaceae. Thus, the moss architecture. Such a dynamic Hedwigiaceae is treated here as a family approach to morphology helps to identify of four genera of predominantly the structural components and specific saxicolous mosses, with rugose spores, developmental processes that account for globular protonemata, ecostate leaves, the growth form of mosses. papillose, short leaf cells, and eperistomate capsules. Methods

The growth habit in the Hedwigiaceae has Populations of Hedwigia ciliata were been variously interpreted as acrocarpous collected on acid rocks in a deciduous (Hedwig, 1801; Bruch et al, 1846), pseudo- forest in the Piedmont of North Carolina pleurocarpous (Frey, 1970; Meusel, 1935), (De Luna 1751, 1752, DUKE). These cladocarpous (Frey, 1970), or populations were kept moist in a large pleurocarpous (Brotherus, 1925; Buck and covered tray and placed in a window-sill

58 displaced by the growth of a subterminal lateral branches. Frequently these branches innovation (Fig. 9). are only small slender buds at the sides of the main shoot (Flowers, 1973). Generally, As the innovation developes, it produces the growth of the main shoot is the same heteroblastic series of leaves that indeterminate and thus branching is is produced by the primary shoot. This monopodial (Buck and Vitt, 1986; heteroblastic leaf series can be used to Flowers, 1973; Schofield & Hébant, 1984), interpret the architecture of mature plants. although a few mosses apparently combine A plant can be recognized as consisting of monopodial and sympodial branching. a chain of innovations. The base of each Most pleurocarpous mosses develop innovation is marked by the presence of plagiotropic shoots; however, some of small juvenile leaves and a sudden change them also develop either erect or pendant in the thickness of the branches. The branches. innovation is slender at its point of attachment to the main shoot. The end of The present description of archegonial an innovation is marked by large mature and branch formation in H. ciliata fits the leaves and a capsule. definition of acrocarpy in mosses. Furthermore, the organization of the shoot The examination of herbarium specimens apex in Hedwigia ciliata is also similar to of other populations of H. ciliata for these that described in other acrocarpous mosses criteria suggests that the same acrocarpous (Berthier, 1972; Frey, 1970, 1974). The growth form is developed regardless of mature plants of H. ciliata are pleurocar- the geographical location, altitudinal pous only in appearance, since they are distribution, size of the colonies, and degree prostrate and bear capsules on what seem of exposure of the habitat. Furthermore, to be very short lateral branches. The observations of additional herbarium results from this study show that the main specimens of other genera in the family axis of this moss is a chain of sympodial suggest that, although size and frequency plagiotropic innovations rather than one of innovations varies, the growth pattern shoot of indeterminate growth. in Hedwigidium, Braunia, and Pseudobraunia is also acrocarpous. Each unit (i.e., innovation) of the main axis of H. ciliata constitutes a module Discussion (sensu White, 1984), since it consists of all the products of an apical cell. Thus, the According to Schofield and Hébant architectural model (sensu Hallé et al, (1984), all acrocarpous mosses are 1978; Tomlinson, 1978) includes repeated characterized by terminal perichaetia on equivalent sympodial units which main shoots of determinate growth. constitute the plagiotropic leader axis (i.e., Branching of the gametophytic shoot is a sympodium), as well as lateral thus sympodial in acrocarpous mosses adventitious branches, also plagiotropic, (Flowers, 1973), with the exception of which develop at the base or medial parts some annual mosses like Bruchia or of each sympodial unit. Pleuridium, that do not branch at all. Branches of an acrocarpous mosses may This type of growth habit has been be orthotropous, i.e., vertically oriented, sometimes called pseudo- pleurocarpous or plagiotropous, i.e., horizontally (Buck and Vitt, 1986; Meusel, 1935). oriented. Anatomical evidence presented here corroborates earlier accounts (Hedwig, In contrast, pleurocarpous mosses are cha- 1801; Meusel, 1935; Bruch et al, 1846; racterized by perichaetia positioned on Scott and Stone, 1976) that described H. 59 ciliata as acrocarpous or pseudo- Hedwigiaceae among the pleurocarpous pleurocarpous. Meusel (1935) also families with diplolepidous peristomes, described Hedwigidium as a pseudo- close to the Leucodontaceae, in the pleurocarpous moss. However, no anato- Isobryales. According to Vitt (1982), mical data on Hedwigidium are available “affinities to the Leucodontaceae are yet. evident in the capsules, basal cells, and leaf characters.” However, the results from It has been suggested that the modular the present study indicate that the structure of mosses can be recognized in Hedwigiaceae may not belong in the herbarium specimens through the Leucodontales or any other group of examination of the heteroblastic leaf series pleurocarpous mosses. that is produced each time a module develops (Mishler, 1986). The available Smith (1978) classified the Hedwigiaceae anatomical data on module formation does in the Orthotrichales, another group with not contradict observations of the hetero- diplolepidous peristomes. A relationship blastic leaf series in H. ciliata. Similarly, to the Orthotrichineae (sensu Vitt, 1984), based solely on observations of herbarium close to Orthotrichaceae, is suggested by specimens, it seems that the growth habit the shape of leaf cells and papillae during in Hedwigidium, Braunia, and shoot development, the type of calyptra Pseudobraunia is also pseudo- development, as well as the acrocarpous pleurocarpous. growth habit.

A pseudo-pleurocarpous growth habit is The Hedwigiaceae has also been classified uncommon, but present in a few groups of among the pseudo- pleurocarpous mosses diverse relationships, notably species in with haplolepidous peristomes, i.e. near the Grimmiaceae and Orthotrichaceae Grimmiaceae (Jones, 1933; Crum, 1976). (Buck and Vitt, 1986), Mesotus However, a peristome is lacking in the (Dicranaceae, Allen, 1987 a), and Hedwigiaceae, so it is difficult to select the Dicnemonaceae (Allen, 1987 b). Since most plausible hypothesis of its ordinal pseudo-pleurocarpy has apparently relationships at present (Crum, 1976). originated independently in several groups, Studies of developmental anatomy of the growth habit alone is of limited value in annular region of the capsule now in pro- assessing the systematic position of the gress may provide a resolution to this Hedwigiaceae. problem.

The Hedwigiaceae has been classified in Besides the potential use of growth pattern three different orders based on several in evaluations of the systematic position of features. For example, the growth form the Hedwigiaceae, it also may help to that resembles pleurocarpy is similar to evaluate the circumscription of the family. that of mosses in the Grimmiales, The available information suggests that Orthotrichales, and Isobryales. The leaf several characters, like spore cells have sinuose walls and are similar to ornamentation, protonemal development, those in the Grimmiales. However, the shoot development, and leaf cell shape multiple papillae are similar to those in the and papillae, are shared only by species in Orthotrichales, and some families in the Hedwigia, Hedwigidium, Braunia, and Isobryales. Finally, the ecostate leaf is an Pseudobraunia. The basic pseudo- additional feature shared with several pleurocarpous pattern is also shared by families in the Isobryales. these four genera. Thus, this information seems compatible with the preliminary Currently, most floristic works include the interpretation that Rhacocarpus and 60

Bryowijkia should be excluded from the North America. Columbia University Press. Hedwigiaceae, and that the Hedwigiaceae De Luna, E. 1989. Shoot ontogeny in the Hedwigiaceae includes only the species currently included (Musci). Amer. J. Bot. 76(6): 6. in Hedwigia, Hedwigidium, Braunia and —————. in press. Protonemal development in the Hedwigiaceae Pseudobraunia. However, the (Musci) and its systematic significance. Syst. Bot. circumscription of the family is a Donoghue, M. 1981. Growth patterns in woody plants with taxonomic problem still under study. examples from the genus Viburnum. Arnoldia 41: 2-23. Flowers, S. 1973. Mosses: Utah and the West. Provo: Brigham Acknowledgements. Young Univ. Press. Brent D. Mishler and Lewis E. Anderson Frey, W. 1970. Blattentwicklung bei Laubmoosen. Nova provided supplies and facilities for this Hedwigia 20: 463-556. study. I especially thank Melvin Turner ———. 1974. Vergleichende Entwicklungsgeschichtliche and Owen Schwartz for their advice with Untersuchungen an Laubmoosblättern als Beitrag zur anatomical techniques. L. E. Anderson, Systematik der Laubmoose. Bull. Soc. Bot. France 121: 29-34. B. D. Mishler, and Angela Newton Gimingham, C. H. & E. T. Robinson. 1950. Preliminary suggested improvements on the investigations on the structure of bryophytic communities. Trans. manuscript. A pre-doctoral fellowship Brit. Bryol. Soc. 1: 330-344. from CONACYT Mexico (reg. 52678) is Hallé, F., R. A. A. Oldeman & P. B. Tomlinson. 1978. deeply appreciated. Tropical trees and forests: an architectural analysis. Berlin: Springer Verlag. Hedwig, J. 1801. Species Muscorum frondosorum descrip- Literature. tae et tabulis aenis. LXXVII. Leipzig. Horikawa, Y. & H. Ando. 1952. A short study on the Allen, B. 1987 a. A revision of the genus Mesotus (Musci: growth-form of bryophytes and its ecological significance. Hikobia Dicranaceae). J. Bryol. 14: 441-452. 1: 119- 129. ————. 1987 b. A revision of the Dicnemonaceae (Musci). J. Ireland, R. R. 1982. Moss flora of the Maritime provinces. Hattori Bot. Lab. 62: 1-100. Nat. Mus. Canada Publ. Bot. 13. Barthlott, W. W & W. Schultze-Motel. 1981. Zur Johansen, D. A. 1940. Plant microtechnique. McGraw Hill. Feinstruktur der Blattoberflachen und systematischen Stellung New York. der Laubmoosgattung Rhacocarpus und anderer Hedwigiaceae. Jones, G. N. 1933. Grimmiaceae. In: A. J. Grout. Moss flora Willdenowia 11: 3-11. of North America north of Mexico. Vol. II. part i: 1-65. Berthier, J. 1972. Recherches sur la structure et le developp- Koponen, T. 1972. Rhytiadelphus japonicus and R. subpinna- ment d’apex du gameyophyte feuille des mousses. Rev. Bryol. tus. Hikobia 6: 18-35. Lichénol. 38: 421-551. —————. 1979. Contributions to the East Asiatic bryoflora. III. Brotherus, V. F. 1925. Musci (Laubmoose). In: A. Engler & Hylocomium himalayanum and H. umbratum. Ann. Bot. Fennici K. Prantl (eds). Die natürlichen Pflanzenfamilien 1(3): 712-723. 16: 102-107. Bruch, P., W. P. Schimper & W. T. von Gümbel. 1846. —————. 1982. Rhizoid topography and branching patterns in Bryologia Europaea, seu genera muscorum europaeorum moss . Nova Hedwigia 71: 95-99. monographice illustrata. Vol. III. Stuttgart. Lindberg, S. 0. 1873. Remarks on Mesotus Mitten. J. Linn. Buck, W.R. & D. H. Vitt. 1986. Suggestions for a new Soc. Bot. 13: 182-185. familial classification of pleurocarpous mosses. Taxon 35: 21-60. Mägdefrau, K. 1982. Life-form of Bryophytes. In: A. J. E. Catcheside, D. G. 1980. Mosses of South Australia. Hand- Smith (ed). Bryophyte Ecology. Chapman and Hall. pp. 45-58. book of the flora and fauna of South Australia. Goverment Meusel, H. 1935. Wuchsformen und Wuchstypen der euro- Printer. pischen Laubmoosen. Nova Acta Leop. N. F. 3(12): 123-277. Correns, C. 1898. Ueber Scheitelwachsthum, Blattstellung Mishler, B. D. 1986. Ontogeny and phylogeny in Tortula und Astanlagen des Laubmoosstämmchens. Festschrift für (Musci: Pottiaceae). Syst. Bot. 11: 189-208. Schwendener, 385-410. Berlin, Borntraeger. Nishimura, N. 1985. A revision of the genus Ctenidium Crum, H. A. 1976. Mosses of the Great Lakes forest. (Musci). J. Hattori Bot. Lab. 58: 1-82. University of Michigan. Ann Arbor. Nyholm, E. 1960. Illustrated Moss Flora of Fennoscandia. Crum, H. A. & L. E. Anderson. 1981. Mosses of Eastern Vol. 2, fasc. 4: 235-250. Sainsbury, G. O. K. 1955. A handbook of New Zealand mosses. Royal Soc. of New Zealand. Bull. 5: 331-335. Sastre-de Jesús, I. 1987. Revision of the Cyrtopodaceae and transfer of Cyrtopodendron to the Pterobryaceae. Mem. N. Y. Bot. Gard. 45: 709-721. Schofield, W. D. & C. Hébant. 1984. The morphology and anatomy of the moss gametophore. In: R. M. Schuster (ed). New Manual of Bryology 2: 627-657. Hattori Botanical Laboratory, Japan. Scott, G. A. M. & I. G. Stone. 1976. The mosses of Southern Australia. Academic Press. Sim, T. R. 1926. The Bryophyta of South Africa. Trans. Royal Soc. of South Africa 15: 348-353.