Podetium Development in the Lichen Genus Cladia

Transactions of the Royal Society of New Zealand : Botany, Volume 3, Issue 9, 30 November 1966, Page 161

Podetium Development in the Lichen Genus Cladia

D. J. Galloway,

By

Biochemistry Department, University of Otago, Dunedin.

[Received by the Editor, 28 January 1966.]

Abstract

It is shown that plants of Cladia aggregata, C. retipora and C. sullivanii arise from a primary thallus which is usually evanescent but can be persistent, as for example in C. retipora. The’ genus is separated from Cladonia on the basis of possessing pseudopodetia. It is suggested that Cladia should be incorporated in the family Glathrinaceae as advocated by Duvigneaud (1944), rather than in the Cladoniaceae. It is further suggested that Stereocaulon and Thysanothecium are related to Cladia possibly through divergent development from a common primitive Lecideacean ancestor near to the genera Toninia, Psora or Sphaerophoropsis. Podetial development is discussed with particular reference to differences between Cladia and Cladonia. The known occurrences of primary thalli are recorded. The possible occurrence of hybrids of C. aggregata and C. sullivanii strengthens evidence for their being nonspecific.

Introduction

The stalks (podetia) supporting the fruiting bodies of fruticose lichens are known to arise in two different ways: as outgrowths either of the apothecial tissues (true podetia) or of the thallus tissues supporting the apothecia (pseudopodetia). It is a diagnostic feature of the Cladoniaceae that the plant is composed of a horizontal primary thallus, crustaceous, squamulose or foliaceous, and a vertical, fruticose secondary thallus, the podetium, on which are borne the apothecia. The stalk of the true podetium is composed of the hypothecium which is prolonged into a solid or hollow cartilaginous column whose extremity is expanded into a club-shaped structure bearing the hymenial tissues. The hyphae of the podetial stalk can become lichenised, thus in the presence of appropriate phycobionts they compose a ± complete assimilatory thalline covering which may often be overlain by a fungal cortex.

Wainio (1922) suggested that the podetium in Baeomyces had evolved through the lichenisation of the carpogenic pedicels of a group of ascomycete fungi (the Helvellaceae) and Duvigneaud (1944) supported this view. In Baeomyces the podetium remains simple and short, much like the stalk of the putative fungal ancestor. It is composed of cartilaginous tissue and is solid or slightly fistulose.

The thalline covering is evanescent or discontinuous or it may be restricted to small scattered squamules. The podetia of Cladonia may be considered as a further development of the Baeomyces type. They are typically hollow and may be much branched with a thalline covering (mantle of mycobiont and phycobiont) which is well developed and often surrounds the cartilaginous stalk as a continuous layer; alternatively the mantle may be divided into squamules or may disintegrate into soredia. The extensive development of phycobiont-containing tissue tends to obscure the fact that the podetium of Cladonia has a carpogenic origin similar to that of Baeomyces which, not having a thalline covering, cannot be considered as other than a prolonged apothecial stalk. Weisse (1936) has shown that species of Cladonia, grown under glass in shade and shelter, form podetia quite without thalline coverings and reduced to cartilaginous axes which are just apothecial stalks. Clearly the colonisation of the podetium by the phycobiont layer is a secondary process. Conversely, some species of Baeomyces in certain environmental conditions form a thalline podetial covering which may even be well developed. Indeed the New Zealand species B. fungoides (Sw.) Ach. nearly always has such a covering. Thus Baeomyces and Cladonia have a closely related structure. A third genus, Pilophoron, probably has similar podetia with a carpogenic origin. Lamb (1951) records that in the Japanese species Pilophoron nigricaule Sato, the podetium is indeed the developed hypothecium. In spite of the occurrence of cephalodia, Pilophoron appears to be more closely related to Baeomyces than to Stereocaulon.

Lamb (1951) has shown that in the Stereocaulaceae the podetium is not homologous with that of Baeomyces or Cladonia. It is a columnar projection of thalline tissue, in which all the tissues of the thallus take part and not the lichenised apothecial stalk borne upon the crustaceous or squamulose primary thallus. Similarly in the genus Thysanothecium (Nylander, 1858) the podetium consists of an outer cartilaginous fungal cylinder, which may be slightly perforate, lined internally by a layer containing the phycobiont. In T. hookeri there is a granular primary thallus and in T. hyalinum a squamulose one. These primary thalli develop short thick, simple or branched structures which are always terminated by a large apothecium. From their anatomical structure these are not apothecial stalks but direct outgrowths of the primary thallus tissues, i.e., they are pseudopodetia.

It is the purpose of this paper to give an account of the development of podetial structures in the genus Cladia. The relation of Cladia to members of the families Cladoniaceae and Stereocaulaceae (discussed above) is suggested, in the hope that the taxonomic position of the genus may be clarified.

Development of Podetia in Cladia

The investigation of podetial development in Cladia has been held up for many years by the lack of primary thalli. These were supposed to be absent from the genus. In 1958, specimens of Cladia retipora (collected by William Martin from the Longwood Range, Southland) were shown to have a primary thallus of minute squamules; this was confirmed by A, W. Evans. Since then, I have discovered and investigated primary thalli of C. aggregata, C. retipora and C. sullivanii from several different localities.

The primary thalli of Cladia are squamulose or bullate. Under high magnification (X 50) the substratum in the vicinity of the primary thallus is seen to be covered with minute farinose primordial granules (150/x). In C. retipora the granules are white and in C. aggregata and C. sullivanii the granules are greenishbrown. The granules later coalesce into more obvious nodular-papillose structures (0.3-o.smm diameter) which constitute the visible primary thallus. In C. retipora

the primary thallus is persistent and consists of small inflated squamules usually lobed. The squamules are not dorsiventral; the lobes appear to be meristematic regions from which the podetia arise. The podetia are at first cylindrical but soon become branched and reticulate. The primary thallus nodules are pale grey-white or yellow, tinged apically with brown, and have an average diameter of c. o.2mm (see Plate la).

The primary thalli of C. aggregata and C. sullivanii are small, erect, usually greenish-brown cylindrical structures up to o.smm in height. The apices of these bullate primary thalli are tinged a dark brown and from them growth and branching of the podetium apparently commences (see Plate 1, fig. 2, and Plate 2).

The primary thalli of all three species have an upper cortex c. 5—15//, thick composed of conglutinate hyphae at right angles to the surface merging into a rather diffuse algal zone of c. 30//, thickness, in which the phycobiont is Trebouxia. The medulla c. 80//, thick is composed of loosely packed interwoven hyphae. There is no cartilaginous lining present. Podetium development was studied in primary thalli of C. retipora collected from a sub-alpine Leptospermum bog at Makarewa, Southland, New Zealand. It was found that the thin conglutinate hyphae of the upper cortex proliferate to initiate the podetium. This multiplication and extension of the cortical cells is accompanied by a similar proliferation of algal cells which spread upwards into, or perhaps are drawn upwards by, the developing podetium. In Cladia, therefore, the podetium originates in the upper cortex but contains all the anatomical layers of the primary thallus, of which it is a direct continuation or branch and not merely an extension of the hypothecium ± covered with thalline granules as in Cladonia. The podetia in Cladia must therefore be considered to be pseudopodetia.

Development of Podetia in Cladonia

The primary thalli of Cladonia sens. str. exhibit three ± well defined anatomical regions arranged in strata as in other dorsiventral foliose lichens: upper cortex, algal layer and medulla. The upper cortex is composed of ± vertical conglutinate hyphae. In the algal layer the phycobiont, usually Trebouxia, may be present continuously or in discrete colonies. The medulla is formed of thick-walled, often conglutinate hyphae. The podetia are secondary outgrowths, developing from the upper surface or rarely from the margins of the primary thallus. Podetial development is endogenous and is initiated by fungal hyphae in the phycobiont layer which proliferate and unite to form a strand of filaments below the upper cortex, but above the phycobiont layer. This podetial primordium extends in length and width, the basal portion growing downwards and eventually displacing the phycobiont layer, while the upper portion, as a compact cylinder, forces its way through the upper cortex. The upper cortex forms no part of the developing podetium, but together with the phycobiont layer is deflected upwards as a sheath around the base of the podetium. The development of the podetium of Cladonia is analogous to the apothecial development of Lecidea, but instead of spreading outwards on reaching the surface as does the Lecideine apothecium, the podetium remains erect. The podetium, which in origin is thus an apothecial stalk, is usually colonised with phycobiont tissue which spreads upwards from the primary thallus. The podetium thus becomes photosynthetic and is a secondary thallus. Its vegetative development can be correlated with the reduction of the primary thallus which in many species, bears little relation in size or persistence to the podetium. The structure and development of podetia has been discussed by Smith (1921).

Status and Affinities of the Genus Cladia

In his “ Synopsis lichenum Novae Galedoniae ” Nylander (1867) included three genera in the Tribe Gladoniei (the modern family Cladoniaceae) :

1. Heterodea 2. Cladonia 3. Cladina

Of these, Cladina comprised three species formerly in the genus Cladonia : —

C. sylvatica var. pyncnoclada (Pers.) Nyl. C. aggregate (Eschw.) Nyl. C. retipora (Ach.) Nyl,

In a footnote he commented “ In the genus or subgenus Cladina the thallus is non-foliaceous ”. It appears that he was undecided as to the exact status, generic or subgeneric, of this group of plants. By non-foliaceous (“ efoliolosus ”) he clearly meant that there was no primary thallus in what he called Cladina. He amended his description of the genus in a later paper (1870) while describing Ramalina jauanicum. “R. javanicum (Nyl.)—the thallus ( c. Imm in thickness towards the base) is usually fuscous-red or blackened towards the base, smooth, slightly perforated from there. The appearance is almost that of Cladia aggregata —thin but less stoutly branched . . . , with another distinct corticate layer . . . ; in Cladia aggregata the entire corticate layer is composed of thickly conglutinate longitudinal filamentous hyphae, which texture immediately makes Cladia a genus entirely distinct from Cladonia and containing C. schizophora, C. aggregata and C. retipora

Thus, of his original genus Cladina only C. sylvatica var. pyncnoclada remained, the other two species being transferred to the new genus Cladia together with C. schizophora. From his descriptions of 1867 and 1870 it is clear that the points which, in Nylander’s opinion, distinguished Cladia from Cladonia were the absence of a primary thallus, and the absence of the supporting cartilaginous (chondroid) layer lining the central canal of the podetium.

In 1883 Muller-Argov. renamed the genus, calling it Clathrina and adding to Nylander’s original three species two more, C. sullivanii and C. jerdinandii, which is closely related to if not a subspecies of C. retipora. Since that time Cladia schizophora has usually been placed in Cladonia section Chasmariae and C. aggregata, C. retipora and C. sullivanii have usually been grouped together in the genus Cladonia as the sub-genus Clathrina (Wainio, 1887; Zahlbruckner, 1927; Sandstede, 1938; Mattick, 1938, 1940; Martin, 1958 a, 1958 b).

Duvigneaud in 1944 advocated generic status for this group of plants, under Nylander’s original name Cladia, and the accommodation of the genus in a new family the Clathrinaceae. His views have been endorsed by Dodge (1948), Lamb (1954) and Martin (1962, 1965).

The genus Cladia has generally been considered to be a member of the Cladoniaceae; in its anatomical structure, however, it has rather less in common with Cladonia than with the Usneaceae. There is no cartilaginous (chondroid) layer present in Cladia; instead, the cells of the cortex confer mechanical strength and rigidity. The mechanical tissue in Cladia forms an external cartilaginous cylinder similar to the cortical cartilaginous layers of Alectoria, Ramalina and Oropogon {Usneaceae) . The algal layer is found on the inside of the strengthening layer and there is a loose woolly medulla, as in the Usneaceae, except Usnea where the

medulla is a strong cartilaginous strand. Nylander (1870) perhaps recognised Cladia as distinct from the Cladoniaceae when he placed it near to Ramalina.

In the Gyclocarpineae mature apothecia can be one of two different developmental types, Lecideine or Lecanorine. In the Lecideine apothecium the hyphae from the upper medulla grow as a compact column through the algal zone to the surface of the thallus, spread radially, then curve upwards to form the outer wall or proper margin around the spore-bearing tissues; algal cells are absent both from below the hypothecium and in the margins. In the Lecanorine apothecium, by contrast, the developing hyphae from the medulla often carry algal cells with them which multiply and spread as a second algal layer under the hypothecium. Both the outer cortex and the initial algal zone of the thallus are associated with the column of medullary hyphae from the start of apothecial development, and grow up along with it, providing the outer part of the apothecium with an additional thalline margin continuous with the thallus itself. According to Duvigneaud (1944) the apothecia of Cladia are Lecideine with a brown disc and margin. He observes that the hypothecium is not borne directly upon the podetial tissues, but on the cone-shaped amphithecium which is formed on the extremity of the podetium. Phycobionts appear and proliferate between the conical amphithecium and the supporting podetial tissues. Thus the superficially Lecideine apothecia of Cladia are partially Lecanorine. However, apothecia of the Usneaceae are typically Lecanorine, so that the placing of Cladia in a separate family, Glathrinaceae, is certainly merited.

In a recent paper Martin (1965) separated Cladia from Cladonia on morphological and chemical grounds. Since both of these criteria can fluctuate widely with environmental conditions it is preferable to separate the two genera on the more fundamental basis of their different development, since this is a more constant expression of genetic constitution. The nature of the podetia shows that Cladia is a distinct genus whose podetial development (thalline) is different from that of Cladonia (carpogenic) and nearer to that of Thysanothecium and Stereocaulon to which it is probably more closely related.

A further point of interest is that the lobular-squamulose primary thallus of C. retipora is common and more persistent than those of C. aggregata and C. sullivanii. Moreover the bullate, cylindrical primary thalli of C. aggregata and C. sullivanii are morphologically alike but quite distinct from the corresponding squamulose structures in C. retipora. The extreme polymorphism of C. aggregata in New Zealand and of C. sullivanii in Tasmania make it not improbable that C. aggregata and C. sullivanii are varieties of the same species. In a Leptospermum heath in Stewart Island I have observed a series of species intergrading almost completely between C. aggregata and C. sullivanii. This suggestion of hybridism may be useful in assessing the distinctness of the two species.

The members of the Cladoniaceae are assumed (Wainio, 1887; Watson, 1928) to have evolved from the Lecideaceae; this assumption is based on a comparison of fruiting structures and the nature of the primary thallus. There is a strong similarity between Cladoniaceae and some crustaceous species of the section Biatora (Lecidea ) in which the apothecia, as in the Cladoniaceae, are waxy, ± light coloured and without a thalline margin. Since Cladia has many affinities with the Cladoniaceae (as well as the Usneaceae) and has a ± Lecideine apothecium it is probable that this genus also is derived from a Lecideacean ancestor. The primary thallus of C. retipora has much in common with the squamulose thallus of Psora (Lecidea) while the Lecideacean genera Toninia and Sphaerophoropsis are very similar to the small bullate cylindrical primary thalli of C. aggregata and C. sullivanii. It may be that Cladia, Thysanothecium and Stereocaulon have arisen by divergent development from one of these Lecideacean ancestors.

Distribution of Primary Thalli of Cladia

Primary thalli of Gladia spp. are probably rather rare, but are widespread. So far they have been found in the following localities:

Cladia aggregata (Sw.) Nyl.

Otago; Silver Peaks. Southland: Tussock Creek, Makarewa, Awarua Bog. Stewart Island: Rakeahua Flats.

Cladia retipora (Laßill.) Nyl.

Otago: Silver Peaks. Southland: Longwood Range (Wm. Martin), Tussock Creek, Makarewa. Stewart Island; Rakeahua Flats. Cladia sullivanii (Mull. Argov.) Martin

Stewart Island: Rakeahua Flats. West Otago: Forgotten River Gorge.

Acknowledgments

The author wishes to thank P. W. James, Department of Botany, British Museum (Natural History) and T. W. Rawson, Botany Division, D.5.1.R., Lincoln, for assistance with literature; B. P. Connor, O.U. Medical School Photographic Unit, for photographs, and G. A. M. Scott, Botany Department, University of Otago, for his helpful criticism and advice.

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