Cladonia rei

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Cladonia rei
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Lecanoromycetes
Order: Lecanorales
Family: Cladoniaceae
Genus: Cladonia
Species:
C. rei
Binomial name
Cladonia rei
Schaer. (1823)
Synonyms[1]
List
  • *Baeomyces radicatus var. nemoxynus Ach. (1803)
  • *Cladonia cornuta var. rei (Schaer.) Schaer. (1850)
  • *Cladonia cornutoradiata var. nemoxyna (Ach.) Oxner (1937)
  • *Cladonia fimbriata f. nemoxyna (Ach.) Leight. (1867)
  • *Cladonia fimbriata f. rei (Schaer.) Vain. (1894)
  • *Cladonia fimbriata var. nemoxyna (Ach.) Coem. (1865)
  • *Cladonia nemoxyna (Ach.) Arnold (1888)
  • *Cladonia pyxidata f. nemoxyna (Ach.) Coem. (1863)
  • *Scyphophorus pyxidatus var. nemoxyna (Ach.) Gray (1821)

Cladonia rei, commonly known as the wand lichen, is a species of ground-dwelling, fruticose lichen in the family Cladoniaceae. It is a widely distributed species, having been reported from Africa, Asia, Australasia, Europe, and North America. It is identified by its slightly dirty-colored, rough-surfaced, slender podetia that grow up to 9 cm (3.5 in) tall. Diagnostic characters of the lichen include the continuously sorediate, green-and-brown-mottled, podetia that taper upward to a point, while chemically, it contains homosekikaic and sekikaic acids. Its reduced capacity to bioaccumulate toxic heavy metals from its surroundings, as well as its ability to switch photobiont partners, allows the lichen to colonize and survive highly polluted habitats. There are several other Cladonia species that are somewhat similar in appearance, but can be distinguished either by subtle differences in morphology, or by the secondary chemicals they contain.

Taxonomy[edit]

The species was first described scientifically in 1823 by Swiss lichenologist Ludwig Emanuel Schaerer. It is named after Professor Re from Turin, who had sent the specimens to Schaerer from Italy. In his original description, Schaerer noted the new lichen's similarity to Cladonia gracilis.[2] Schaerer's type specimen, kept at the herbarium of the Conservatoire et Jardin botaniques de la Ville de Genève, contains both homosekikaic and fumarprotocetraric acids.[3] In the genus Cladonia, C. rei is a member of clade Cladonia, subclade Graciles.[4]

In North America Cladonia rei is commonly known as the wand lichen,[5] or the sordid powderhorn.[6]

Synonymy[edit]

In an 1850 publication, Schaerer proposed that the taxon was better classified as a variety of Cladonia cornuta.[7] In 1894, Finnish lichenologist and Cladonia specialist Edvard August Vainio proposed it as a form of Cladonia fimbriata.[8] The two proposed names are now considered homotypic or nomenclatural synonyms of Cladonia rei.[9]

In 1976, Haavard Østhagen proposed that Cladonia nemoxyna, a taxon originally described by Erik Acharius in 1803, should be considered a synonym of Cladonia rei.[3] This nomenclatural possibility had been suggested already a decade earlier by Juha Suominen and Teuvo Ahti when they typified the name in a 1966 publication.[10] This name, and several other with the varietal or form epithet nemoxyna are heterotypic (taxonomic) synonyms of Cladonia rei.[1]

Cladonia subulata, shown here, is difficult to reliably distinguish from C. rei without using chemical techniques.

Cladonia rei is morphologically similar to Cladonia subulata, and the two are difficult to distinguish. In 1993, Paus and colleagues studied all of the morphological characteristics that were used to distinguish between the two species, and concluded that there were none that could sufficiently distinguish between the two, but they could still be considered distinct species due to their different habitat preferences.[11] Leo Spier and André Aptroot conducted a chemical and morphological study on about 350 mostly West European specimens of Cladonia subulata and C. rei. They found about a third of the specimens that had been identified based on inferences about their habitat had been misidentified. They also reported that the long-wave UV test—the standard method for distinguishing between the two species in the field—was unreliable for detecting homosekikaic acid. As a result, many of the previous records of these taxa should also be considered unreliable. They concluded that there was "no indication of any correlation between chemistry and geography, morphology or substratum", and that C. rei should be considered a chemotype of Cladonia subulata, rather than a distinct species. They proposed that C. rei be placed in synonymy with Cladonia subulata, because the latter, as the older of the two names, has priority.[12]

Some studies published soon challenged Spier and Aptroot's proposal. Authors of a study of this taxon in Poland argued that the species should remain distinct, largely because "Their conclusions were based on material mostly from the Netherlands, with rather scanty representatives from other countries". After analysing almost 800 collections, they determined that 90% of the 228 specimens of C. rei had been misidentified, a figure they attributed to the original collectors not having corroborated their determinations with thin layer chromatography to accurately assess the chemistry.[13] In 2010, a molecular phylogenetics study, showed the subclade of C. subulata to be distinct from C. rei. The authors propose that the determining chemical feature for C. rei is the presence of homosekikaic acid.[14] Additional molecular support for separate species in another study also used scanning electron microscopy of the stereome surfaces that revealed distinct differences between the two species.[15]

Description[edit]

Photograph of a herbarium specimen taken through a dissecting microscope (x12) showing terminal apothecia

Primary squamules are small and inconspicuous, often disappearing.[5] Podetia are gray-green to olive, sometimes browned, slender, coarsely or finely sorediate on the upper half.[5] They have dimensions in the range of 2–9 cm (13⁄16–3+9⁄16 in) tall by 1–2 mm (up to 3.5 mm) thick.[16] They have with narrow, symmetrical, or, more frequently lopsided cups, proliferating at the margins to resemble a star or magic wand.[5] Pale to dark brown apothecia are common on proliferations along the cup margins.[5] It is prudent to take heed of Spier and Aptroot's thoughts: "There is much individual variation between the specimens, which can vary from nearly unbranched to cup-shaped, from slender (less than 1 mm thick) to robust (reaching 5 mm) and from low (average height below 2 cm) to high (height over 5 cm, clearly higher than the surrounding Cladonia species). The distribution of these forms over the chemotypes is on the whole largely similar and differentiating characteristics could not be found."[12] Further, it is known that growth in contaminated sites can influence the growth and development of the Cladonia thalli, sometimes resulting in features that do not coincide with the normal taxonomic definition of the species.[17] This phenomenon has been documented with Cladonia rei.[18]

Chemistry[edit]

Chemical spot tests are undergone for identification. C.rei responds to P+ red for fumarprotocetraric acid, P− and UV+ white for homosekikaic acid.[5] PD reactions also turn C.rei yellow in low presences of fumarprotocetraric acid.[13] [19]

Cladonia rei invariably contains homosekikaic acid; sometimes it also has fumarprotocetraric acid. It also has smaller amounts of sekikaic acid, and well as trace amounts of the accessory substance 4'-O-methylnorhomosekikaic acid. The positive fluorescence of an ultraviolet test is traditionally used to detect the presence of homosekikaic acid. It can also be tested using the ferric chloride chemical spot test, which produces a violet-coloured spot if positive.[15] Other compounds that have been found in the lichen include antheraxanthin, astaxanthin, α-carotene, ε-carotene, β-cryptoxanthin, lutein, lutein epoxide, and violaxanthin.[20]

Similar species[edit]

Cladonia subulata and Cladonia ochrochlora are similar species that can be distinguished by their secondary chemistry. Fumarprotocetraric acid is the only main lichen metabolite in C. subulata. Another lookalike, Cladonia glauca, contains squamatic acid, a substance that causes it to glow white when lit with a UV light. It also has a narrow longitudinal slit in most podetia.[4] Lots of details available.[11] Cladonia cenotea might be closely related.[15] Cladonia coniocraea and Cladonia cornuta tend to have larger primary squamules and do not normally proliferate at the cup margins; neither contains homosekikaic acid.[5]

Cladonia lookalikes

Habitat and distribution[edit]

Cladonia rei is a terricolous lichen that grows in soil, although more rarely it is found on rotting wood,[16] and there are few records of it growing on other substrates, including rock, plastic,[12] old straw, and mosses over rocks.[13] It prefers open areas with low humus content and a substrate with a more or less neutral soil pH.[15] often in dry and sunny places like grasslands, heaths and wastelands.[21] Another favoured habitat is limestone cliffs and limestone meadows, although the lichen is also found in disturbed areas, such as road embankments, gravel pits, or house ruins.[22] It is a pioneer species: able to quickly colonise bare ground, particularly in disturbed and anthropogenic habitats.[21] In some cases, it can grow on impoverished soil with high heavy metal content. In Krompachy (Slovakia), the lichen, along with the moss Ceratodon purpureus, was found to be very abundant in bare acid soil near copper smelters, where all vascular plants were severely damaged or have disappeared.[23] It is prevalent in temperate or somewhat arid regions, and does not occur in the Arctic or the Antarctic.[15] The lichen was used as a case study for a large-scale biodiversity monitoring program in Alberta, Canada. Historical records and collections suggested that the lichen was broadly distributed but rare in the province, but more recent material from surveys conducted by the Alberta Biodiversity Monitoring Institute showed that its distribution is entirely limited to the dry mixed grassland, northern fescue grassland and aspen parkland natural regions, where it is relatively common.[24]

Cladonia rei growing in sand amongst mosses and other Cladonia species, in Buckhorn State Park, Wisconsin, USA

It is a widespread species, with a range extending to Europe, Africa, Asia, Australasia, North America,[22] and South America. It is widely distributed in Europe, having been recorded in Austria, Belgium and Luxemburg, Czech Republic, Estonia, Lithuania, Norway, Poland, Slovakia, Spain, and Sweden.[13] More recently, it was reported from Armenia,[25] from the coastal sand-dunes of Portugal,[26] and, in 2021, from the Pyrénées-Orientales in the French Mediterranean region.[27] Its Australasian distribution includes both Australia[13] and New Zealand.[20] It was reported as new to India in 2002.[28] In 2006 it was recorded from Iran[29] and Turkey.[30]

In the United States, it has been considered by some authors to be widely distributed in the northwestern part of the country, but probably because of misidentification with the much more common C. ochlorochlora and C. verruculosa. Samuel Hammer suggests that the actual range in the region is limited to interior localities east of the Cascade Mountains, in Idaho and Washington.[31]

Pollution tolerance[edit]

Because the lichen has often been recorded growing in extremely contaminated post-smelting slag dumps, its bioaccumulative abilities have been studied. The lichen has developed a restrained heavy-metal accumulation pattern that limits its exposure to these toxic compounds, and helps it to colonise these contaminated sites.[18] Efficient methods have been developed for extracting arsenic compounds from this species; in an arsenic-contaminated environment, Cladonia rei was shown to contain arsenous acid, arsenic acid, methylarsonic acid, dimethylarsinic acid, arsenobetaine, and trimethylarsine oxide.[32] Its high genetic variability within a single population is suggestive of great potential for colonising anthropogenic habitats, and underlies the role of this lichen as a pioneer in the early stages of natural regeneration of these contaminated sites.[33] Cladonia rei has a low bioaccumulation factor, meaning it is classified as a weak accumulator of heavy metals. Its erect and fruticose growth form help it survive in this polluted environment, due to the decrease in metal content along the vertical gradient of the thallus.[34] The level of cell membrane damage in the lichen is dependent on the heavy level concentrations of the polluted site. The amount of cell damage can be measured experimentally by determining relative electrical conductivity, and thus, this physiological parameter can serve as an early warning indicator for detection of elevated metal concentrations in soil.[35]

A phytosociological study of the pioneer cryptogamic communities associated with Cladonia rei in Polish post-smelting dumps showed the frequent co-occurrence of Diploschistes muscorum and Cladonia conista. In non-polluted sites, typical lichen associations include C. chlorophaea, C. fimbriata, C. pyxidata, Ceratodon purpureus, and Peltigera didactyla.[21] In northeastern North America, it is noted to be a common pioneer species in old field succession, along with Cladonia cristellata and Cladonia polycarpoides.[5] It is also a characteristic species of cryptogamic communities in dry grasslands of Saskatchewan,[36] and anthropogenic habitats in Germany.[37] Some cryptogamic communities, including those involving C. rei, are quite similar in Europe and North America, even though the vascular plant species composition often differs considerably.[21]

Here C. rei is a component of a biological soil crust in Wisconsin, USA

Ecology[edit]

Epicladonia sandstedei is a lichenicolous fungus that parasitises Cladonia rei.[38]

In a study of the oribatid mite communities associated with three Cladonia species in a heavily contaminated habitat, Cladonia rei was shown to provide a good habitat for mites. Because of the great variation in the growth forms of its podetia, densely covered with propagules such as corticated granules, squamules and microsquamules as well as numerous non-corticated, farinose-to-granular soredia, the surface area/volume ratio of the lichen is higher compared to other studied Cladonia species. The rugged surface texture provides more microhabitats for both mites and the particles of organic matter that are their diet. This contrasts with Cladonia cariosa and Cladonia pyxidata, which have a less diverse morphology, and a lower diversity of oribatid inhabitants.[39]

The photobiont partners of Cladonia rei are to some extent dependent upon the environment. Although both Asterochloris and Trebouxia can associate with the fungus, and "the presence of Trebouxia was directly related to anthropogenic sites with technogenic substrates, and the proportion of lichen specimens with these algae clearly depended on the level of heavy-metal soil pollution and the habitat type. Although Cladonia lichens were previously thought to be restricted to Asterochloris, they are able to start the relichenization process with Trebouxia under specific habitat conditions and to establish a stable association with these algae when colonization of disturbed sites takes place."[40]

See also[edit]

References[edit]

  1. ^ a b "Synonymy: Cladonia rei Schaer., Lich. helv. spicil. 1: 34 (1823)". Species Fungorum. Retrieved 16 January 2022.
  2. ^ Schaerer, L.E. (1823). Lichenum Helveticorum Spicilegium. Pars 1. Sect. 1 (in Latin). p. 34.
  3. ^ a b Østhagen, Haavard (1976). "Nomenclatural note on Cladonia nemoxyna". The Bryologist. 79 (2): 242–246. doi:10.2307/3241924. JSTOR 3241924.
  4. ^ a b James, P.W. (2009). "Cladonia". In Smith, C.W.; Aptroot, A.; Coppins, B.J.; Fletcher, A.; Gilbert, O.L.; James, P.W.; Wolseley, P.A. (eds.). The Lichens of Great Britain and Ireland. London: British Lichen Society; Natural History Museum. pp. 309–338. ISBN 978-0-9540418-8-5.
  5. ^ a b c d e f g h Brodo, Irwin M.; Sharnoff, Sylvia Duran; Sharnoff, Stephen (2001). Lichens of North America. Yale University Press. p. 269. ISBN 978-0-300-08249-4.
  6. ^ Goward, Trevor (1999). The Lichens of British Columbia: Illustrated Keys. Part 2–Fruticose Species. Victoria, B.C.: Ministry of Forests, Research Program. ISBN 0-7726-2194-2. OCLC 31651418.
  7. ^ Schaerer, Emanuel (1850). Enumeratio critica lichenum europaeorum (in Latin). Bern: Sumtibus Auctoris Excudebat Officina Staempfliana. p. 196.
  8. ^ Wainio, Edvard August (1894). Monographia Cladoniarum universalis: II. Acta Societatis pro Fauna et Flora Fennica (in Latin). Vol. 10. p. 305.
  9. ^ "Homotypic Synonyms. Basionym Name: Cladonia rei Schaer., Lich. helv. spicil. 1: 34 (1823)". Index Fungorum. Retrieved 18 January 2022.
  10. ^ Suominen, Juha; Ahti, Teuvo (1966). "The occurrence of the lichens Cladonia nemoxyna, C. glauca and C. polycarpoides in Finland". Annales Botanici Fennici. 33 (3): 418–423. JSTOR 23724278.
  11. ^ a b Paus, Susanne; Daniels, Fred J.A.; Lumbsch, H. Thorsten (1993). "Chemical and ecological studies in the Cladonia subulata complex in Northern Germany (Cladoniaceae, lichenised Ascomycotina)". In Feige, G.B.; Lumbsch, H.T. (eds.). Phytochemistry and Chemotaxonomy of Lichenized Ascomycetes – A Festschrift in Honour of Siegfried Huneck. Bibliotheca Lichenologica. Berlin, Stuttgart: J. Cramer. ISBN 978-3-443-58032-2.
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  13. ^ a b c d e Syrek, Magdalena; Kukwa, Martin (2008). "Taxonomy of the lichen Cladonia rei and its status in Poland". Biologia. 63 (4): 493–497. doi:10.2478/s11756-008-0092-1. S2CID 34668889.
  14. ^ Dolnik, Christian; Beck, Andreas; Zarabska, Daria (2010). "Distinction of Cladonia rei and C. subulata based on molecular, chemical and morphological characteristics". The Lichenologist. 42 (4): 373–386. doi:10.1017/s0024282910000071. S2CID 84036053.
  15. ^ a b c d e Pino-Bodas, Raquel; Burgaz, Ana R.; Martín, María P. (2010). "Elucidating the taxonomic rank of Cladonia subulata versus C. rei (Cladoniaceae)". Mycotaxon. 113: 311–326. doi:10.4248/113/311 (inactive 31 January 2024).{{cite journal}}: CS1 maint: DOI inactive as of January 2024 (link)
  16. ^ a b McCune, Bruce; Geiser, Linda (1997). Macrolichens of the Pacific Northwest (2nd ed.). Corvallis: Oregon State University Press. p. 74. ISBN 0-87071-394-9.
  17. ^ Osyczka, Piotr; Boroń, Piotr; Lenart-Boroń, Anna; Rola, Kaja (2017). "Modifications in the structure of the lichen Cladonia thallus in the aftermath of habitat contamination and implications for its heavy-metal accumulation capacity". Environmental Science and Pollution Research. 25 (2): 1950–1961. doi:10.1007/s11356-017-0639-1. PMC 5766729. PMID 29105035. S2CID 6148896.
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  21. ^ a b c d Rola, Kaja; Osyczka, Piotr; Nobis, Marcin (2014). "Cryptogamic communities dominated by the lichen Cladonia rei— a case study of Polish post-smelting dumps in a worldwide context". Herzogia. 27 (1): 121–135. doi:10.13158/heia.27.1.2014.121. S2CID 86267121.
  22. ^ a b Stenroos, Soili; Ahti, Teuovo; Lohtander, Katileena; Myllys, Leena (2011). Suomen jäkäläopas [Finnish lichens] (in Finnish). Helsinki: Kasvimuseo, Luonnontieteellinen keskusmuseo. p. 166. ISBN 978-952-10-6804-1. OCLC 767578333.
  23. ^ Hajdúk, J.; Lisická, E. (1999). "Cladonia rei (lichenizované askomyéty) na stanovistiach kontaminovanych imisiami z Kovohút Krompachy (SV Slovensko)" [Cladonia rei (lichenized Ascomycotina) on heavy metal-contaminated habitats near copper smelters at Krompachy (NE Slovakia)]. Bulletin Slovenskej Botanickej Spolocnosti. 21: 49–51.
  24. ^ Haughland, Diane L.; Hillman, Ashley; Azeria, Ermias T. (2018). "Tackling rarity and sample bias with large-scale biodiversity monitoring: a case study examining the status, distribution and ecology of the lichen Cladonia rei in Alberta, Canada". The Lichenologist. 50 (2): 211–230. doi:10.1017/s0024282918000099. S2CID 13843040.
  25. ^ Gasparyan, Arsen; Sipman, Harrie J.M.; Brackel, Wolfgang Von (2014). "A contribution to the lichen-forming and lichenicolous fungi flora of Armenia". Willdenowia. 44 (2): 263–267. doi:10.3372/wi.44.44208. S2CID 84745586.
  26. ^ Vaz, Ana Sofia; Marques, Joana; Pradinho Honrado, João (2014). "Patrones de diversidad liquénica en las dunas arenosas de la costa del norte de Portugal". Botanica Complutensis. 38: 89–96. doi:10.5209/rev_bocm.2014.v38.45776.
  27. ^ Giardi, Léo (2021). "Une espèce de lichen nouvelle pour la région méditerranéenne française : première observation documentée de Cladonia rei Schaer., 1823 dans les Pyrénées-Orientales" [A new species of lichen for the French Mediterranean region: first documented observation of Cladonia rei Schaer., 1823 in the Pyrénées-Orientales]. Carnets botaniques (in French). 65. doi:10.34971/1h5x-7k73. ISSN 2727-6287.
  28. ^ Ahti, Teuvo; Dixit, P.K.; Singh, K.P.; Sinha, G.P. (2002). "Cladonia singhii and other new reports of Cladonia from the Eastern Himalayan Region of India". The Lichenologist. 34 (4): 305–310. doi:10.1006/lich.2002.0404. S2CID 86476787.
  29. ^ Ahti, T.; Sohrabi, M. (2006). "A synopsis of Iranian Cladonia (Lichenes)". Flora Mediterranea. 16: 139–144.
  30. ^ Yazıcı, Kenan (2006). "Three new lichens from Turkey". Mycotaxon. 97: 345–348.
  31. ^ Hammer, Samuel (1995). "A synopsis of the genus Cladonia in the Northwestern United States". The Bryologist. 98 (1): 1–28. doi:10.2307/3243636. JSTOR 3243636. S2CID 84727928.
  32. ^ Mrak, Tanja; Šlejkovec, Zdenka; Jeran, Zvonka (2006). "Extraction of arsenic compounds from lichens". Talanta. 69 (1): 251–258. doi:10.1016/j.talanta.2005.10.011. PMID 18970562. S2CID 23879365.
  33. ^ Osyczka, Piotr; Rola, Kaja; Lenart-Boroń, Anna; Boroń, Piotr (2014). "High intraspecific genetic and morphological variation in the pioneer lichen Cladonia rei colonising slag dumps". Open Life Sciences. 9 (5): 579–591. doi:10.2478/s11535-014-0286-1. S2CID 11819539.
  34. ^ Osyczka, Piotr; Rola, Kaja; Jankowska, Klaudia (2016). "Vertical concentration gradients of heavy metals in Cladonia lichens across different parts of thalli". Ecological Indicators. 61 (2): 766–776. doi:10.1016/j.ecolind.2015.10.028. S2CID 85969600.
  35. ^ Osyczka, Piotr; Rola, Kaja (2019). "Integrity of lichen cell membranes as an indicator of heavy-metal pollution levels in soil". Ecotoxicology and Environmental Safety. 174: 26–34. doi:10.1016/j.ecoenv.2019.02.054. PMID 30818257. S2CID 73499817.
  36. ^ Looman, Jan (1964). "Ecology of lichen and bryophyte communities in Saskatchewan". Ecology. 45 (3): 481–491. doi:10.2307/1936101. JSTOR 1936101. S2CID 86504694.
  37. ^ Paus, Susanne M. (1997). Die Erdflechtenvegetation Nordwestdeutschlands und einiger Randgebiete [The lichen vegetation of Northwestern Germany and some adjacent areas. Their vegetation ecology under consideration of the chemistry of selected species]. Bibliotheca Lichenologica (in German). Vol. 66. Berlin/Stuttgart: J. Cramer. pp. 68–73. ISBN 978-3-443-58045-2.
  38. ^ Zhurbenko, M.P.; Pino-Bodas, R. (2017). "A revision of lichenicolous fungi growing on Cladonia, mainly from the Northern Hemisphere, with a worldwide key to the known species". Opuscula Philolichenum. 16: 188–266.
  39. ^ Skubała, Piotr; Rola, Kaja; Osyczka, Piotr (2016). "Oribatid communities and heavy metal bioaccumulation in selected species associated with lichens in a heavily contaminated habitat". Environmental Science and Pollution Research. 23 (9): 8861–8871. doi:10.1007/s11356-016-6100-z. PMC 4850176. PMID 26810668.
  40. ^ Osyczka, Piotr; Lenart-Boroń, Anna; Boroń, Piotr; Rola, Kaja (2020). "Lichen-forming fungi in postindustrial habitats involve alternative photobionts". Mycologia. 113 (1): 43–55. doi:10.1080/00275514.2020.1813486. PMID 33146594. S2CID 226251647.
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