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Cladoniaceae

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Cladoniaceae
Cladonia subulata is the type species of the type genus of the family Cladoniaceae
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Lecanoromycetes
Order: Lecanorales
Family: Cladoniaceae
Zenker (1827)[1]
Type genus
Cladonia
P.Browne (1756)
Synonyms[2]

The Cladoniaceae are a family of lichen-forming fungi in the order Lecanorales.[2] It is one of the largest families of lichen-forming fungi, with about 560 species distributed amongst 17 genera. The reindeer moss and cup lichens (Cladonia) belong to this family. The latter genus, which comprises about 500 species, forms a major part of the diet of large mammals in taiga and tundra ecosystems.[5] Many Cladoniaceae lichens grow on soil, but others can use decaying wood, tree trunks, and, in a few instances, rocks as their substrate. They grow in places with high humidity, and cannot tolerate aridity.

Many Cladoniaceae species are characterised by a thallus that has two distinct forms: a scaly or crust-like primary thallus that, depending on the species, can be permanent or temporary, and a secondary fruticose thallus called a podetium or pseudopodetium. Cladoniaceae members form symbiotic associations with green algae from the class Trebouxiophyceae, usually the genus Asterochloris. Six Cladoniaceae species are included in the International Union for Conservation of Nature's Red List of Threatened Species.

Systematics

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Historical taxonomy

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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 recognised 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] In more recent history, significant progress in the knowledge of the taxonomy and biogeography of the family can be attributed to several decades of devoted research by Teuvo Ahti.[12]

Cladoniaceae is now one of the largest families of lichen-forming fungi,[13] with about 560 species distributed amongst 18 genera. The type genus is Cladonia, circumscribed by Irish physician and botanist Patrick Browne in 1756. He included eight 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."[14]

Etymology

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As is standard practice in botanical nomenclature,[15] the name Cladoniaceae is based on the name of the type genus, Cladonia, with the ending -aceae indicating the rank of family. The genus name comprises the Greek word: κλάδος (klādos), meaning "branch", "bud", or "shoot"; and the Latin -ia, a suffix meaning "quality or state of a thing".[16]

Synonymy

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Several phylogenetic studies have shown that Cladoniaceae is a member of the order Lecanorales, and is closely related to the family Stereocaulaceae.[17][18][19][20][21] The family Cetradoniaceae, which was created in 2002 to contain the endangered species Cetradonia linearis,[3] was folded into the Cladoniaceae in 2006.[22]

In 2018, Kraichak and colleagues used a technique called temporal banding to reorganize the Lecanoromycetes, proposing a revised system of classification based on correlating taxonomic rank with geological (evolutionary) age. They synonymised the families Squamarinaceae and Stereocaulaceae with the Cladoniaceae, resulting in a large increase in the number of genera and species.[23] The Squamarinaceae had already been included in the Cladoniaceae by previous authors.[13] Although this reorganisation has been used in some later publications,[2] the folding of the Stereocaulaceae into the Cladoniaceae was not accepted in a recent analysis. As Robert Lücking explained, "merging of the two families under the name Cladoniaceae is not possible without a conservation proposal because Cladoniaceae (Zenker, 1827) is antedated by Stereocaulaceae (Chevallier, 1826) by one year."[24] In a 2021 treatment of the British and Irish Cladoniaceae, the authors also keep these families separate, noting "both families are monophyletic and easily distinguishable on both morphological and molecular terms".[25]

Description

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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 (bushy) or foliose (leafy), and are often dimorphic–consisting of two distinct forms; this particular type of growth is also known as cladoniiform.[26] The primary thallus is ephemeral to persistent, crustose, foliose or squamulose, while the secondary thallus is typically vertical and holds the ascomata.[27] The secondary thallus ranges in height from a few millimetres to more than 25 centimetres (10 in). Some species, however, form neither a primary thallus nor any fruticose structures.[28] As for vegetative propagules, isidia occur very rarely in this family, whereas soredia are common.[25]

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.[27] Their colour is typically dark brown (sometimes pale brown), red, ochraceous, or black.[28] The hamathecium (referring to all hyphae between the asci in the hymenium) consists of sparsely branched paraphyses, and is amyloid. The asci (spore-bearing cells) 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 (club-shaped). Ascospores number eight per ascus, and they are usually non-septate, ellipsoid to more or less spherical in shape, hyaline (translucent), and non-amyloid.[27] 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.[28] The conidiomata are pycnidia; the conidia are non-septate, usually filiform (thread-like), and hyaline.[27]

Chemistry

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In the Cladoniaceae, over 70 different secondary metabolites (lichen products), primarily polyphenols, have been identified. To observe the fluorescence of certain depsides and depsidones, ultraviolet light is directly applied to the specimens. Traditional colour spot tests with reagents like KOH can be ineffective at low concentrations. Consequently, thin-layer chromatography analysis becomes crucial for identifying the major lichen products in the specimens and verifying species identification.[29]

Photobionts

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The symbiotic algal partner (photobiont) of most Cladoniaceae taxa are unicellular green algae, usually in the genus Asterochloris, but occasionally in the genus Chlorella;[29] both of these genera are in the class Trebouxiophyceae. Eleven species of Asterochloris have found to be associated with genus Cladonia; the algal genus – one of the most common lichen symbionts – occurs in the thalli of more than 20 lichen genera.[30] The most common photobionts in this genus that associate with Cladonia are A. glomerata, A. italiana, and A. mediterranea, with some lineages showing dominance in one or several climatic regions.[31] In contrast, Myrmecia was shown to be the main photobiont for the Mediterranean species Cladonia subturgida.[32] The algal genus Trebouxia, a very common lichen photobiont, has not been recorded associating with the Cladoniacae.[28] Some Pilophorus species associate with cyanobacterial symbionts (in addition to their association with green algae) in structures called cephalodia.[29] The cyanobacterial genera Nostoc and Stigonema are involved in these tripartite associations.[28] In a study of several Cladonia lichens collected from Southern Finland, the associated microbial community, which was found to be consistent amongst the different species, consisted largely of Alphaproteobacteria and Acidobacteriota.[33]

Development

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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,[34][35][36][37] although the interpretation of results has sometimes been controversial.[28] For example, two 1970 studies by Hans Jahns explored the development of fruiting bodies in Cladonia, significant for understanding the taxonomy and phylogeny within the Cladoniaceae. This work revealed two distinct ontogenetic types based on the formation of generative tissue and its role in developing the characteristic podetium of Cladonia species. This generative tissue, originating in the thallus horizontalis and growing vertically, is crucial for forming the podetium. The study identified variability within species, showing that different species can have more than one ontogenetic type, challenging previous assumptions about the uniformity of development patterns within the genus. This demonstrated variability had implications for the taxonomy and phylogenetic relationships within Cladoniaceae, suggesting a complex evolution of reproductive structures that did not strictly align with previously conceived taxonomic groupings.[38][39]

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, lichenisation 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.[29] 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.[40]

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.[29] The podetia are slow-growing, with an annual growth rate generally ranging from 1 to 15 mm.[41]

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.[42] 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.[43]

Genera

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After more than a century of discovery and research, including recent advances in understanding revealed by molecular phylogenetics studies, the Cladoniaceae encompass 17 genera and about 570 species.[44] In terms of species diversity, the Cladoniaceae stood as the tenth-largest lichen-forming fungal family by 2017.[13] 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

Myelorrhiza was transferred from the Cladoniaceae to the Ramalinaceae by Kistenich and colleagues in 2018.[59] Neophyllis, originally classified in the Cladoniaceae, was transferred to Sphaerophoraceae in 1999.[60]

Habitat and distribution

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Cladoniaceae species have been recorded growing in many habitats and on a diversity of substrates, including soil, tree trunks, and rotten wood.[28] 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.[61] 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.[28]

In his 2000 monograph on the Cladoniaceae of the Neotropical realm, Ahti included 184 species in 4 genera, and showed that that South America is a hotspot of biodiversity for genus Clanodia.[12] Bioclimatic variables significantly influence the distribution of Cladoniaceae species richness in the Neotropics, particularly under conditions of low precipitation and temperature, and high climatic variability. Areas with stable climates and higher temperatures and precipitation tend to support greater species richness.[62] Twenty-six Cladoniaceae species (25 Cladonia and 1 Cladia) are known to occur in the Galápagos Islands. There, some species form mats on lava flows that have developed little soil.[63] A 2013 monograph of Northern European Cladoniaceae treated 100 species (95 Cladonia, 4 Pilophorus, and the monotypic genus Pycnothelia).[64] In the 2021 key to lichen species in Italy, 86 Cladoniaceae are included.[65] In Bulgaria, 55 species in two genera were reported in 2022.[66] In a study of the lichen biodiversity in Kazakhstan's Burabay National Park, the Cladoniaceae made up about 30 percent of the species diversity.[67]

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.[68]

Conservation

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

Each of the six Cladoniaceae species that have been assessed for the global IUCN Red List face a variety of threats impacting their survival. Cetradonia linearis (vulnerable, 2015) is endangered by ecosystem changes in spruce–fir forests, specifically the balsam woolly adelgid's impact on Fraser fir, and changes in humidity regimes and cloud immersion. The species is also vulnerable to threats from logging, mining, and road building if its legal protection status is removed.[69] Cladonia appalachiensis (endangered, 2020) growing on high-elevation Anakeesta Knob rock, faces threats from visitor disruption and changes in cloud cover and humidity.[70] The main threats to Cladonia perforata (endangered, 2003) include habitat loss, hurricanes, and improper fire management, with a single natural event potentially causing substantial subpopulation reduction.[71] Cladonia submitis (endangered, 2020) is primarily threatened by habitat loss and degradation due to land development, particularly around metropolitan areas. Climate change also poses significant risks through altered fire regimes and sea level rise, affecting its pine barren and sand dune habitats.[72] Pilophorus fibula (endangered, 2020) is threatened by habitat loss, alteration of hydrological regimes, recreational damage, and declining water quality.[73] Lastly, Gymnoderme insulare (endangered, 2014), primarily found in old-growth forests in Japan and Taiwan, faces threats from natural hazards like typhoons and is affected by the decline of its tree hosts, Cryptomeria japonica and Chamaecyparis obtusa.[74]

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.[75]

Human interactions and uses

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Some species in the Cladoniaceae have been involved in a profitable export business for decorative uses, with demand reaching thousands of kilograms in various markets. In Europe, Cladonia stellaris is used ornamentally in wreaths, floral decorations and architect's models. In the years 1970–75, an average of nearly 3000 metric tonnes were exported each year from Finland, Norway and Sweden; most of these exports (about 80%) went to West Germany.[76] In Sweden, Cladonia lichens were used historically as a partial insulation for storm windows.[77] The complex net-like structures of the Australasian lichen Pulchrocladia retipora have been described as "of considerable beauty resembling lace or coral", and have been utilised in floral and architectural design.[78]

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Cited literature

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