Cladoniaceae

Cladoniaceae was formally introduced to science in 1827 by German naturalist Jonathan Carl Zenker in a publication of Karl Goebel.[1] Zenker's initial concept of the family included genera that are now recognized as separate families, including Baeomycetaceae, Icmadophilaceae, and Stereocaulaceae.[6] William Nylander included 53 Cladonia species worldwide in his 1860 work Synopsis lichenum.[7] When Edvard August Vainio published his three-volume monograph on the Cladoniaceae (Monographia Cladoniarum universalis, 1887,[8] 1894,[9] and 1897[10]), he included 134 species and subspecies. In his circumscription of the family, the genera Pycnothelia, Cladia, and Cladina were included in the genus Cladonia.[11]

Cladoniaceae is now one of the largest families of lichen-forming fungi,[12] with about 560 species distributed amongst 18 genera. The type genus, after which the family was named, is Cladonia, circumscribed by Irish physician and botanist Patrick Browne in 1756. He included 8 species in his new genus. Of their occurrence, he wrote: "All these species are found in great abundance in the mountains of Liguanea: they grow mostly on the ground, among other sorts of moss, but a few ... species chiefly are found upon the decaying trunks of trees."[13]

In Cladonia coccifera, the conidia are embedded in a scarlet-coloured slime on the margins of the scyphi (cups).

The thallus of Cladoniaceae lichens are fruticose or foliose, and are often dimorphic–consisting of two distinct forms; this particular type of growth is also known as cladoniiform.[22] The primary thallus is ephemeral to persistent, crustose, foliose or squamulose, while the secondary thallus is typically vertical and holds the ascomata.[23] The secondary thallus ranges in height from a few millimetres to more than 25 cm (10 in). Some species, however, form neither a primary thallus nor any fruticose structures.[24]

The ascomata are in the form of an apothecium, and are biatorine, meaning they are of the lecideine type – light in colour and soft in consistency. They often have a reduced margin.[23] Their colour is typically dark brown (sometimes pale brown), red, ochraceous, or black.[24] The hamathecium (referring to all hyphae between the asci in the hymenium) consists of branched paraphyses, and is amyloid. The asci are somewhat fissitunicate, meaning they have two layers that separate during ascus dehiscence. The ascus structure consists of an apical dome and a tube (both of which are amyloid), which is cylindrical to clavate. Ascospores number eight per ascus, and they are usually non-septate, ellipsoid to more or less spherical in shape, hyaline, and non-amyloid.[23] Except for a few genera that produce septate ascospores (Calathaspis, Pycnothelia and Pilophorus), the hymenium does not generally have characters that are useful in taxonomy.[24] The conidiomata are pycnidia; the conidia are non-septate, usually filiform (thread-like), and hyaline.[23]

Cladonia coniocraea (left) has subulate podetia, while the podetia of Cladonia fimbriata (middle) feature cup-shaped scyphi, commonly called "pixie cups", Cladonia cervicornis (right) has a more complex branching pattern.

The development of several Cladoniaceae genera have been studied in detail,[28][29][30][31][32][33] although the interpretation of results has sometimes been controversial.[24] Cladoniaceae species begin development with the formation of a prothallus – a fungal layer upon which an algae-containing thallus will develop. It comprises the hyphae from the germination of an ascospore. After the protothallus contacts the alga, lichenization begins with the development of small squamules (scale-like thallus segments) that make up the primary thallus. Most Cladoniaceae have a mixed thallus, consisting of two parts: a base, parallel to the substrate, called the primary thallus and the other erect, the secondary thallus. The primary thallus is squamulose (scaly) or crustose (crustose-like). The secondary thallus consists of vertical structures that are shrubby and hollow, although they can be solid in rare cases. If these structures are made of generative tissue, they are called podetia; when they are made of vegetative tissue, they are called pseudopodetia. The morphology of these structures determines to a large part the taxonomy of the Cladoniaceae, which can range from simple to very complex branching patterns.[25] Cladonia minisaxicola, found in the mountains of Bahia (Brazil) is the only species in that large genus that is completely crustose and does not develop podetia.[34]

The tips of the podetia have a wide range of morphology in the Cladoniaceae. They can be straight, tapering from a wide base to a point (called subulate), or flaring on cup-shaped scyphi. The scyphi are sometimes closed, or have a central perforation, forming structures called funnels.[25] The podetia are slow-growing, with an annual growth rate generally ranging from 1 to 15 mm.[35]

Branching in the Cladoniaceae occurs on the podetium due to the growth dynamics of fungal meristem tissue at its apex. Two primary branching patterns exist: one where branches emerge from late divisions of a large meristem that alters its shape, and another where branches come from small meristems that split early but maintain their shape. These meristem growth dynamics are crucial for interpreting phylogeny in Cladoniaceae mycobionts, with the trend towards smaller, early-splitting meristems seen as an evolutionary advancement.[36] In cladoniiform lichens, especially within the Cladoniaceae, a shift in meristem growth from isotropous (having uniform properties in all directions) to anisotropous (having properties that differ depending on the direction in which they are measured) leads to pronounced lateral elongation of the apical meristem. This change offers developmental flexibility, transitioning from a symmetrical growth to a more varied, asymmetrical growth, hinting at evolutionary processes within the Cladoniaceae. Despite this variability, such morphogenetic activities appear to be highly conserved even among species that are presumably distantly related.[37]

Cladoniaceae species have been recorded growing in many habitats and on a diversity of substrates, including soil, tree trunks, and rotten wood.[24] In a few cases, Cladoniaceae can grow on rocks, such as Cladonia salmonea which grows on the rock faces of vertical cliffs, or Cladonia pyxidata, which can grow on thin soil on rocks.[38] They are absent from very dry regions. The range of their habitats includes boreal forests, bogs, temperate forests, the tundra of the Arctic and Antarctic, man-made habitats (e.g. roadsides), tropical highlands, and the sandy tropical lowlands of the Amazon rainforest.[24] Twenty-six Cladoniaceae species (25 Cladonia and 1 Cladia) are known to occur in the Galapagos Islands. There, some species form mats on lava flows that have developed little soil.[39] A 2013 monograph of Northern European Cladoniaceae treated 100 species (95 Cladonia, 4 Pilophorus, and the monotypic genus Pycnothelia).[40] In the 2021 key to lichen species in Italy, 86 Cladoniaceae are included.[41]

A study on the distributional ecology of Cladina and Cladonia in western North America found that the Coast Mountains of British Columbia act as a key phytogeographic barrier. This results in distinct oceanic and continental taxa groupings on either side. The research also suggests that the southern boundaries of certain species may be determined more by historical rather than purely ecological factors, indicating possible range expansions.[42]

Cladonia perforata has been an endangered species on the IUCN redlist since 2003.

Five Cladoniaceae species have been assessed for the global IUCN Red List: Cetradonia linearis (vulnerable, 2015),[43] Cladonia appalachiensis (endangered, 2020),[44] Cladonia perforata (endangered, 2003),[45] Pilophorus fibula (endangered, 2020),[46] and Gymnoderme insulare (endangered, 2014).[47] On the red list of China's macrofungi, Cladonia delavayi (vulnerable), Cladonia pseudoevansii (critically endangered), Gymnoderma coccocarpum (endangered), and Gymnoderma insulare (endangered) are the representatives of the Cladoniaceae.[48]

After more than a century of discovery and research, including recent advances in understanding revealed by molecular phylogenetic studies, the Cladoniaceae encompass 17 genera and more than 550 species. This is a list of the genera contained within the Cladoniaceae, based on the Catalogue of Life; this includes taxa formerly classified in the Squamarinaceae, but does not include the Stereocaulaceae. Following the genus name is the taxonomic authority, year of publication, and the number of species:

Pilophorus acicularis

Pycnothelia papillaria

• Calathaspis I.M.Lamb & W.A.Weber (1972)[49] – 1 sp.
• Carassea S.Stenroos (2002)[15] – 1 sp.
• Cetradonia J.C.Wei & Ahti (2002)[3] – 1 sp.
• Cladia Nyl. (1870)[50] – ca. 27 spp.
• Cladonia Hill ex P.Browne (1756)[13] – ca. 500 spp.
• Heteromyces Müll.Arg. (1889)[51] – 1 sp.
• Metus D.J.Galloway & P.James (1987)[52] – 3 spp.
• Muhria P.M.Jørg. (1987)[53] – 1 sp.
• Notocladonia S.Hammer (2003)[54] – 2 spp.
• Paralecia Brackel, Greiner, Peršoh & Rambold (2015)[55] – 1 sp.
• Pilophorus Th.Fr. (1857) – 17 spp.
• Pulchrocladia S.Stenroos, Pino-Bodas, Lumbsch & Ahti (2018)[24] – 3 spp.
• Pycnothelia Dufour (1821)[56] – 2 spp.
• Rexiella S.Stenroos, Pino-Bodas & Ahti (2019)[57] – 1 sp.
• Sphaerophoropsis Vain. (1890)[58] – 2 spp.
• Squamella S.Hammer (2001)[59] – 1 sp.
• Thysanothecium Mont. & Berk. (1846)[60] – 3 spp.

Myelorrhiza was transferred from the Cladoniaceae to the Ramalinaceae by Kistenich and colleagues in 2018.[61] Neophyllis, originally classified in the Cladoniaceae, was transferred to Sphaerophoraceae in 1999.[62]