Anaptychia ciliaris

Illustration of "Parmelia ciliaris" by Dutch botanist Jan Kops

According to Annie Lorrain Smith, Anaptypia ciliaris was first mentioned in the botanical literature by the Italian botanist Fabio Colonna in his Ekphrasis (1606), a work notable for its detailed illustrations of plants using copperplate engravings.[3] It was formally described as a new species in 1753 by Carl Linnaeus, as Lichen ciliaris. Linnaeus described it as a somewhat erect, leafy, grey lichen with linear, fringe-like segments that are ciliate (having hair-like structures). He said it resembled a tree moss with notably hairy edges, and with small shield-like structures (apothecia), and cited multiple references that described the lichen in similar ways, emphasizing its larger size, hairy characteristics, and shielded appearance. Linnaeus noted that this lichen is found on trees in Europe.[4] Julius von Flotow is credited by Index Fungorum with the transfer of the taxon to the genus Anaptychia in 1850.[5] A specimen illustrated by Johann Jacob Dillenius in 1742 was selected as the lectotype.[6]

Anaptychia ciliaris is the type species of Anaptychia.[7] This genus was proposed by Gustav Wilhelm Körber in 1848 as a replacement for the name Hagenia, suggested by Franz Gerhard Eschweiler in 1824, but already being used for a plant genus. Körber described genus Anaptychia as follows (translated from Latin): "Apothecia bordered by a resupinate thallus (ascending thallus is channelled)".[8] Although he did not assign a type species himself, A. ciliaris was later designated as type by Louis Pfeiffer in 1872.[7]

Anaptychia ciliaris is greenish when wet and has prominent cilia at the margins of its lobes, or laciniae.

Anaptychia ciliaris has a growth form that bridges the characteristics of foliose and fruticose lichens. While it displays tendencies of both types, its classification often shifts between the two groups. The lichen has a somewhat fruticose habit, attaching to its substrate at a single base point. However, its fronds lay close to the ground, with a dorsiventral internal structure. This includes an upper "fibrous" cortex made of tightly packed, parallel hyphae and an algal layer where the photobionts are interspersed between the cortex and the medulla's looser hyphae. Its lower cortex comprises hyphae running somewhat parallel to the surface. The lichen's upper surface has a greyish hue, while the underside is either greyish or whitish.[17] It tends to be greenish, however, when wet.[18] This lichen species forms loose attachments to its substratum, contributing to the development of extensive colonies that can span up to 15 cm (6 in) or more in diameter. These colonies are characterized by elongated, linear structures that repeatedly dichotomously branch, referred to as laciniae. The laciniae generally have an upward, somewhat ascending orientation towards their tips, measuring over 2 mm (1⁄16 in) in width. They appear either flat or somewhat convex and are covered in fine hair-like structures, giving them a pubescent appearance.[6] The fibrous outer cortex imparts some strength to the laciniae, which are then resulting somewhat upright in habit.[19] Numerous pale, lateral cilia lie along the margins of the lobes.[13] They are dark grey to black, and up to 15 mm (3⁄5 in) long.[14] Sometimes, these long cilia form hapters—aerial attachment organs with highly adhesive hyphae—and after contacting something nearby induces branching and then a spreading sheath; this is quite often another lobe of its own thallus, resulting in entanglement.[20]

Beneath the laciniae, the thallus is decorticate (i.e., it lacks a cortex) and appears paler than its upper surface. The lower surface features irregular veining and is adorned with marginal rhizines, which share the same colour as the thallus. These rhizines measure between 1 and 6 mm (1⁄16 and 1⁄4 in) in length and may be either simple or occasionally branched towards the tips. The laciniae themselves are approximately 300 μm thick. The upper cortex displays irregular thickening, and its lower surface has flexuous contours, occasionally extending downward to the lower surface of the thallus without any medullary covering. The photobiont layer, housing cells measuring 10–15 μm in diameter, is frequently interrupted by the upper cortex, resulting in a discontinuous pattern. The medullary layer is typically very thin and may even be evanescent in some regions. Unlike the upper cortex, the lower cortex is absent in this lichen species.[6]

Cluster of apothecia with dark brown discs

Apothecia, the reproductive structures of Anaptychia ciliaris, are positioned on the thallus surface and exhibit laminal, stipitate, or subsessile characteristics. These structures typically range in diameter from 2 to 5 millimetres (1⁄16 to 3⁄16 in). Their margins are lacinulate, featuring ciliate lacinules along the edges. The disc of the apothecia appears brown or dark brown and may initially be covered in a white pruina, although this may disappear over time. The receptacle lacks spinules and has a hymenium measuring 150–200 μm in height, which turns blue when treated with iodine. The cortex of the receptacle is irregularly thickened and does not stain with iodine. The asci, which are cylindrical or somewhat clavate, have dimensions of about 120 by 30 μm and typically contain 4–8 spores. The spores themselves are dark brown, ellipsoid in shape with roundish tips, and are more or less constricted at the centre. They measure 17–23 by 28–43 μm in size, with thin and uniformly thickened walls.[6] In their early and undeveloped stages, the spores are oval and filled with granular and mucous substances. Over time, a central partition (the septum) forms, separating these contents, leading to the eventual formation of a two-cell state.[21]

No lichen products have been identified from Anaptychia ciliaris, and it does not react with any of the standard chemical spot tests used to help identify lichens.[6]

The morphology of A. ciliaris changes when exposed to adverse concentrations of ambient levels of air pollutants. It stops producing cilia, and the lobes become shorter and develop a warty upper surface.[22]

Dry individual on the bark of an old deciduous tree

Anaptychia ciliaris is a lichen predominantly observed in Northern Europe, extending its distribution eastward to European Russia, the Caucasus,[6] and northeastern Russia (Murmansk).[28] Its presence also spans Central and Southern Europe, the Canary Islands, and sporadic records in Asia.[29] Specimens from China have been collected from Xinjiang, Gansu, Shaanxi, and Hebei, all at altitudes over 1,800 m (5,900 ft).[30] In Turkey's Lake Abant Nature Park, A. ciliaris emerged as one of the top three lichen species in a biodiversity survey.[31] Furthermore, it is established in various regions of Morocco.[32] However, in the United Kingdom, there has been a discernible decline in its sightings. While it remains a rarity in Ireland, regions like Scotland and northeast England have classified A. ciliaris as locally extinct.[13] Historical records by Smith highlight that, around a century ago, this lichen showed a preference for trees in parklands and along cultivated roadsides.[33] In Finland, where the species is widely distributed, it is most abundant in populated areas, present in parks, alleys, and field edges, but it also occurs on seashore cliffs.[14]

Anaptychia ciliaris displays adaptability in its choice of substrates, predominantly growing on the bark of trees like Quercus rotundifolia, Q. pyrenaica, and Ulmus species. It has also been identified on Pinus sylvestris, P. nigra, and Juniperus oxycedrus.[34] Less commonly, its presence is marked on both calcareous and acidic rocks, as well as gravestones.[13] Additional sightings have been on Acer pseudoplatanus (sycamore) and Fagus sylvatica (beech) trees.[35] In Denmark, it is most commonly found on Fraxinus, followed by Tilia.[22] A noteworthy trait of A. ciliaris is its preference for diffuse light.[36]

In Poland, Anaptychia ciliaris is one of six species listed in the endangered category in the National red list.[37] In the Moscow region, located in the central part of the East European Plain, it is an uncommon species, and it is listed in the 2018 version of the Red Data Book of the Moscow Region. In this area, it is most likely to be found in birch grass-marsh forest. The relatively limited presence of the lichen in this region is attributed to the "transfer of suspended particles, carbon monoxide, nitrogen oxide and dioxide from the city of Moscow".[38] In Austria's Regional Red List, A. ciliaris is classified among the endangered lichens.[35] Although it was once a common sight in Upper Austria, the lichen's decline is attributed to the diminishing availability of its preferred substrate: old, occasionally moss-covered, well-fertilized, and dust-impregnated barks. Contemporary practices often result in the removal of trees before their bark matures to a consistency suitable for A. ciliaris.[39]

Historical North American literature has occasionally mentioned the presence of A. ciliaris, but such references are misinterpretations. In reality, North American instances refer to A. setifera, indicating that A. ciliaris is not native to the continent.[40]

Illustration of gross morphological features

Anaptychia ciliaris acts as a significant indicator in biomonitoring due to its heightened sensitivity to air pollution. A system was proposed to estimate regional SO₂ emission levels in Denmark and North Germany by checking for the presence, health, and fertility of certain indicator lichens, including the widespread but sensitive A. ciliaris.[22] A similar quantitative scale was implemented in England and Wales. The scale uses zones, numbered from 0 (most polluted) to 10 (least polluted); A. ciliaris is found on eutrophied bark in areas ranked above zone 7, corresponding to an SO₂ level of about 40 micrograms per cubic metre.[41] Historically prevalent in the Netherlands during the 19th century, its population witnessed a steep decline over the course of the 20th century. By that time, its presence had been confined to a few aged trees in specific locations within the country. Nevertheless, 2010 brought forth an unexpected discovery of thriving specimens on post-war ash trees in Brabant. This resurgence can likely be attributed to a combination of decreased levels of air pollution and the ongoing trends of climate warming.[42]

In the realm of environmental science, A. ciliaris offers significant utility. Its degradation of chlorophyll into phaeophytin serves as a method to detect air pollution. One of the strengths of this lichen as a biomonitor lies in its ease of identification and its adaptability to various substrates.[34] Additionally, A. ciliaris has been employed to gauge the lead and cadmium emissions from a municipal solid waste incinerator in France,[43] assess the levels of heavy metals in polluted areas of Greece,[44] and assess levels of air pollution near a lignite power plant.[45]

In Sweden, A. ciliaris has a history of being utilized for monitoring atmospheric pollution.[46] Furthermore, post the Chernobyl disaster, it played a crucial role in the biomonitoring of airborne radioactive fallout. Notably, the caesium-137 activity detected in Anaptychia ciliaris was significantly elevated, reaching levels as high as 14560 becquerels per kilogram.[47]

In the 17th Century, "Cyprus Powder" was used as a toilette powder (a fine powder, often fragranced, that was used for personal grooming and cosmetic purposes) to whiten, scent, and cleanse the hair. It was a blend of oakmoss, Anaptychia ciliaris, and species of Usnea, and was fragranced with ambergris or musk, combined with the essences of roses, jasmine, or orange blossoms.[48]

In the Erkowit region of eastern Sudan, the lichen, known locally as bakour, was mixed with other plants and burned to repel insects.[49]

Research

Vertical section of developing ascogonium in Anaptychia ciliaris, illustrated by German botanist Wilhelm Baur in 1904. a: paraphyses; b: ascogonial hyphae; c: ascogonial cells.[50]

Historically, the lichen Anaptypia ciliaris has played a significant role in various scientific explorations of lichen structure and physiology. In the early days, Joseph Pitton de Tournefort, a French botanist, is believed to have made one of the initial observations of the lichen's distinctive large, dark-colored spores.[51] Holle, in 1849,[52] detailed the development of hyphae from lichen spores, using A. ciliaris as the subject of his study.[53] Shortly after, in 1850 and 1851, the lichen was used by German botanist Hermann Itzigsohn to show the existence of "spermagones" (conidia).[21] Following this, in 1853,[54] German botanist Julius Ferdinand Speerschneider reported his observation of the division of the lichen's photobiont cells (then referred to as gonidia) within a moist thin section of thallus.[55] The sections of the lichen he had cultivated in humid air showed that within two months the hyphae decomposed, whereas the algae not only remained healthy, but grew markedly and divided intensively. Soon after, in the centre of the decomposing section of thallus appeared small, point-like light green structures that transformed into lichen primordia.[56]

Further insights into lichen structure came when Reginald Heber Howe Jr. presented the lichen's cortex as an exemplar of the "fibrous" cortex — a tissue type characterized by long, slender, infrequently branched hyphae growing parallel to the surface.[57] The eighteenth-century work of German bryologist Johann Hedwig added depth to these findings. In his Fundamentum Historiae Naturalis Muscorum Frondosorum from 1784, he described and depicted Anaptypia ciliaris apothecia, its dark-colored septate spores, and pycnidia. He identified minute bodies associated with the organism, measuring approximately 50 μm long and 24 μm thick, as the "semina"[58] — a term which Acharius would later replace in 1803 with "spores".[59]

In the subsequent century, the study of Anaptypia ciliaris continued to evolve. In 1894, Pierre Augustin Dangeard focused on the origin and progression of asci in lichens using Anaptypia ciliaris as his specimen.[60] René Maire delved into the realm of cellular biology, observing nuclear division within an ascospore before the formation of a septum.[33] Beyond its cellular significance, the lichen's utility was also explored. In 1825, Joseph Placide Alexandre Léorier chronicled the endeavors of Roy of Tonnerre, who pioneered a technique to produce alcohol from lichens, notably Anaptypia ciliaris. This innovation was particularly remarkable given that lichens, in contrast to fruits or grains, typically lack abundant sugars typically used in traditional alcohol production.[61]

More recent research on Anaptychia ciliaris has revealed a spectrum of potential biological activities. The lichen's extracts have been assessed for antibacterial and insecticidal efficacy against specific pathogenic bacteria and the mosquito Culiseta longiareolata larvae, with the findings indicating moderate larvicidal properties.[62] Other research showed the lichen's modest antioxidant capabilities, particularly in combating oxidative stress induced by AFB1 in human lymphocytes.[63] When tested against fish bacterial pathogens, A. ciliaris demonstrated antibacterial actions, particularly towards Aeromonas hydrophila, Streptococcus agalactiae, Enterococcus faecalis, and Lactococcus garvieae.[64] Lastly, the presence and concentration of active metabolites in A. ciliaris, inclusive of numerous antioxidants, were observed to differ based on its tree-substrate.[65]

The mycobiont of Anaptychia ciliaris can be cultivated in axenic (pure) culture. More than 100 years ago, Finnish phycologist Harry Warén described the fungal partner of A. ciliaris (then known as Physcia ciliaris) grown from spores, which he described as having compact mycelia and large globular cells in which erroneously thought to observe the presence of chlorophyll.[66][67] To initiate spore growth, researchers place apothecia from the lichen in proximity to the underside of an inverted petri dish; if the asci and ascospores are mature, the spores will be ejected onto the petri dish and begin germinating.[68] Expanding on these findings, subsequent research explored the growth conditions of A. ciliaris. The spores displayed a distinct dispersal pattern, often sticking to the growth medium individually–a pattern observed in other species and common within specific lichen families. Unlike many lichens that refrain from releasing spores in lab conditions, the apothecia of A. ciliaris consistently did so, suggesting indicate that the apothecia were sexually mature, and that both the collection season and laboratory conditions were conducive to sporulation. On average, these spores took six to seven days to begin germination.[69]

Furthermore, this lichen species displayed heterogeneous spore production despite having apothecia of approximately the same size, underscoring the impact of its heterothallic life cycle, which allows for cross-fertilization and genetic recombination. The study also revealed that glucose inhibited spore germination, consistent with prior observations. Additionally, the mycobiont's early growth stages benefited from the presence of carbon sources, leading to more robust filamentous development. These findings align with the known slow growth rate of lichens and their capacity for apothecia of various ages on a single thallus, contributing to genetic diversity. Various culture media influenced the lichen's morphological and metabolic characteristics, and pigmentation synthesis was linked to the availability of sugars and sugar alcohols. The study recommended optimal culturing conditions for this species, emphasizing the importance of media composition in shaping growth patterns and metabolic processes.[69]

Anaptychia ciliaris interacts with a range of lichenicolous organisms, which are species that live on, and often parasitize, lichens. Among the fungi that parasitize A. ciliaris is Tremella anaptychiae, a species described in 2017. This fungus yields spherical or tuberculate fruit bodies that vary in colour from cream, pinkish, to brownish or blackish and are found in regions like Italy, Macedonia, Spain (including the Canary Islands), Sweden,[29] and Greece. Meanwhile, Catillaria mediterranea, a lichen with a reduced thallus,[70] and Monodictys anaptychiae, a rare hyphomycete, are known to grow on A. ciliaris. The latter may exclusively target A. ciliaris, leading to thallus surface damage and discoloration.[71][72] In the UK, the subspecies Anaptychia ciliaris mamillata often exhibits numerous tiny black dots on its lobes due to parasitism by Stigmidium hageniae.[13] Additionally, A. ciliaris is infected by other lichenicolous fungi such as Pronectria tincta.[73]