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A herbarium specimen of the lichen Leptogium cyanescens, magnifed 40X, with lobule-shaped isidia.

An isidium (plural: isidia) is a minute, cylindrical or branched outgrowth found on the thallus of certain lichen species. Isidia primarily function as a means of vegetative propagation, allowing the lichen to spread and colonize new substrates. It is a diaspore–a reproductive propagule comprising both fungal and algal components. An isidium mirrors the anatomical structure of the parent thallus from which it arises, in that it is surrounded by a cortex. It is this latter feature that contrasts it with soredia, a similar reproductive structure that lacks a cortex. In some cases, the term isidium is used rather broadly, to include all propagules with a cortex, even ones that are only externally similar, such as dactyls or pseudoisidia.

Isidia have a diverse morphology, ranging in shape from spherical and cylindrical to club-shaped, with sizes typically between 0.01 to 0.03 mm in diameter and 0.5 to 3.0 mm in height. Their appearance can vary, being smooth to knobby or shiny to matte, with some lichens featuring hollow, inflated-looking isidia. Less often, isidia are compressed and spathulate, squamose (scaly), or even shield-like ("peltate"). Differentiating between isidia and other lichen outgrowths can be challenging, as they can resemble juvenile isidia or other thalline structures. While some isidia detach easily or transform with age, others remain permanently attached to the thallus, likely increasing its surface area. Isidia that have broken off can be carried by wind, water, or animals (such as getting stuck on bird feet or entangled in animal fur). When these land in a conducive environment, they can give rise to new thalli. While isidia are still connected to a thallus, they enhance its surface area, thereby aiding in gas exchange and photosynthesis.

About 25–30% of foliose (leafy) or fruticose (bushy) lichens form isidia.[1] Features of isidia are reflected in the species epithets of many lichens, both indirectly, and explicitly.

Morphology[edit]

Closeup of the pustulate isidia that are characteristic of Flavoparmelia baltimorensis; scale bar = 1 mm

The visual characteristics of isidia vary widely. These tiny protrusions can be spherical (globose), cylindrical, scale-like (squamulose, coralloid,[2] club-shaped (claviform), disc-shaped (disciform), cup-shaped (cupuliform),[3] and wart-shaped verruciform.[4] They range from 0.01 to 0.03 mm in diameter and 0.5 to 3.0 mm in height.[5] Their colour, especially at the apex, often differ from non-isidiate sections, and they can be simple or branched. Surfaces range from smooth to knobby, and shiny to matt.[4] Most isidia are solid, but some lichens feature hollow, inflated isidia. Soralia and isidia formation can overlap, with soralia growing at the tips of isidia and isidia developing within a soralium, where the loose network becomes compact and forms a secondary cortex.[2]

The isidia of the foliose lichen Pseudocyphellaria horridula are distinct, emerging vertically from the lobes and growing up to 10 mm. These large isidia create a distinctive fish bone pattern on the lobes.[6]

Parmelina pastillifera has distinctive isidia. This greyish foliose species has a central part with button-shaped, brown to black protuberances that have a flat or slightly concave, warty surface. These protuberances break off easily, leaving crater-shaped depressions, distinguishing P. pastillifera from P. tiliacea, which has smaller, globose to cylindrical black isidia on its older, central parts.[7]

the gelatinous lichen Collema subflaccidum has prominent globular isidia.

Differentiating isidia and other outgrowths can be challenging, as some lichens have similar warts and papillae. Old isidia may resemble foliose outgrowths (lobuli) and can transition to fibrils or small lateral branches. In some lichens, old isidia can transform into other structures without detaching. Only a few lichens actively disperse isidia through cortical base degeneration. The isidia of many crustose lichens, like Pertusariaceae, detach easily, while others remain attached until the thallus dies. In many gelatinous and foliose lichens, the isidia stay attached to the thallus permanently, likely increasing the surface area.[2] Consoredia are clusters of incompletely separated soredia; soralia with many consoredia may be mistaken for isidia clusters.[8] Sometimes, isidia may break down to soredia and consoredia. Species like Pertusaria coccodes may rarely produce both isidia and soredia.[9] "Sorediate isidia" refers to isidia that erupt into soredia, typically at the tips. "Isidiate (or isidioid) soredia" describes soredia that look like isidia but lack a cortex and arise from distinct soralia. Du Rietz used "isidiate soredia" for the fragile isidia of Xanthoparmelia loxodes and X. verruculifera,[10] but the term is inaccurate, as no soredia form.[11] Soredial granules growing like isidia on the parent thallus are common in the Physciaceae.[12]

Formation and development[edit]

Isidia proliferate on the surface of this Pseudevernia furfuracea
Isidia are abundant on the lobe margins of this Peltigera praetextata

Isidia formation and development wary widely, influenced tissue initiation and environmental conditions. In many lichens, isidia begin with medullary or algal hyphae intruding between cortical hyphae, transporting algal cells upwards to form a protuberance. Initially lacking a cortex, this forms later as the process matures. This development is common in pseudocyphellae, where outgrowing hyphae are not constrained by a cortex.[2]

Experimental studies on Pseudevernia furfuracea reveal that isidia formation involves high cellular turnover in both symbiotic partners, with increased asexual spore production in algae and proliferation of medullary hyphae. These isidia are metabolically active, showing heightened photosynthesis and dark respiration rates.[13]

In Peltigera praetextata, isidia form only at sites of cortical injury, which can be experimentally induced by making incisions on the thallus. Some researchers suggest calling these foliose outgrowths "lobuli" due to their regenerative role.[2]

Some isidia from from a protuberance of the thalline cortex, with tissue from the algal layer advancing into this protrusion. In some cases, isidia originate from cortical hyphae that ensnare free-living algae, which are then encapsulated by the outgrowing hyphae. Connections to the internal thallus layers are secondary. This process resembles cephalodia, highlighting the adaptability of lichen tissues.[2]

In gelatinous lichens, isidia begins with the active division of algal cells at the thallus periphery. In non-corticate lichens, this triggers a small protuberance soon invaded by hyphae. In corticate lichens, increased algal proliferation stimulates cortical cell division, ensuring the thalline protuberance is uniformly coated with a cortical layer.[2]

Regeneration[edit]

Although many isidia do not primarily aid in vegetative propagation, they are crucial for regeneration. On aging thalli, isidia can sprout into new lobes. For example, a study on Parmotrema tinctorum found that isidia placed in nylon bags on Cryptomeria japonica trunks formed protuberances within six months, eventually maturing into lobules with rhizines and lichen compounds by the end of the year.[14] Similarly, the isidia of Peltigera praetextata formed small juvenile thalli in 4–5 months when sown into soil, with larger thalli appearing after eight months.[15]

It is commonly believed that after dissemination, isidia deconstruct into a loose association of fungal and algal cells before forming a new thallus.[2] However, some species contradict this. Phyllophiale pastillifera isidia rapidly develop into a thallus shortly after detachment.[7] Similarly, Lobaria pulmonaria isidia germinate directly into young thalli without a dedifferentiation phase.[16]

While isidia are less conducive to dispersion than soralia due to their weight, their protective cortex makes them resilient in adverse conditions. Larger lichen fragments regenerate faster but are harder to disperse.[2]

In the foliose lichen Parmelia saxatilis, mature isidia evolve into new thalline scales on the thallus surface. These emergent scales rejuvenate growth by overlapping older thalli like tiles, using the tissue from older, deceased lobes as a water reservoir.[2]

Transplantation studies[edit]

Lichen transplantation is a restoration technique employed to introduce or reintroduce lichens to areas where they've been depleted or to new environments where they can be beneficial. This method aims to enhance ecosystem recovery and may serve various purposes, from environmental remediation to conservation efforts. Isidia, given their role in lichen propagation, have become valuable assets in such transplantation studies.

For instance, isidia from the foliose lichen Xanthoparmelia tinctina were used in an attempt to rehabilitate an abandoned asbestos mine. The goal was to introduce lichens to cover and stabilize the surface, reducing the exposed asbestos surface area and thereby mitigating the dispersal of hazardous airborne fibers. Unfortunately, achieving robust colonization was a challenge, with running water and debris posing significant hurdles.[17]

From a conservation perspective, Parmotrema crinitum isidia were cleverly combined with surgical gauze fibers to facilitate effective substrate attachment during transplantation. On the other hand, Sticta sylvatica required a considerable 24-month period post-transplantation to generate small lobules from its isidia.[18]

Function and ecological role[edit]

  • Role of isidia in lichen reproduction.
  • Advantages of having isidia for lichen colonization and distribution.
  • Interaction with surrounding environment and other organisms.

Vegetative propagules like isidia can probably germinate in a broader range of habitats than ascospores or conidia, since they do not require a resynthesis of the symbiosis.[19]

Leptotrema and Graphina rely on isidia to facilitate the aeration of their thallus. The apex of the isidia in these species contains hyphal tissue that is made porous and loosened, providing a transition point to a respiratory pore. When the isidia detach, they leave behind a respiratory pore that resembles a crater. This pore can be sealed by a secondary cortex that forms during subsequent development.[2]

Types and variations[edit]

Isidia that occur on Usnea, such as these on the branch S. ceratina, are sometimes referred to as isidomorphs.

Isidia present in various forms and structures, each providing unique insights into lichen biology and taxonomy. In his 1992 monograph of the bark-dwelling, sorediate and isidiate crustose lichens of Norway, Tonsberg broadly defined isidia as "all globose to elongate, usually projecting, corticate diaspores with a basal point of attachment", and further defined several types.[4] He delineated these as follows:

The first group comprised isidia that were initiated beneath the upper cortex and seemed to burst through the thallus cortex. Such isidia, continuously developed, pushed older ones outward with younger isidia forming beneath. They lacked a primary cortex, with cortex differentiation being secondary. This resulted in homoiomerous isidia, meaning their interiors contained both hyphae and algae without a medullar central core. The mature isidia were surrounded by ecorticate tissue in rounded patches, often located at tuberculae tips. This was observed in species like Pertusaria flavida, P. coccodes, and P. coronata.[4]

Pseudevernia consocians has claviform (club-shaped) isidia.[3]

Some isidia connected continuously with the surrounding thallus cortex and seemed to originate from it. This was seen in species like Pertusaria corallina, P. oculata, and P. dactylina. These isidia were heteromerous, meaning they had a white medullary core surrounded by an algal layer. This formation mode differs anatomically from the homoiomerous isidia of the foliose species Lasallia pustulata and Parmelia tiliacea, which are also derived from the thalline cortex.[4]

A few areolate species displayed isidiiform areolae, which are more or less spherical to cyclindrical, and easily detached or broken. Examples include Caloplaca herbidella and Placynthiella icmalea. The latter's isidia-like areolae were termed "blastidia", as they resembled consoredia but remained attached at the base to the substrate. The entire areola of Placynthiella icmalea was identified as a blastidium.[4]

An isidiomorph is a structure that resembles an isidium, but is formed as an outgrowth of the medulla rather than the cortex. It is associated with soralia of species in the genus Usnea.[20]

Schizida and thlasidia[edit]

Josef Poelt introduced the terms schizidia and thlasidia to categorize specific diaspores and isidia-like structures in lichens. Introduced in 1965, schizidia were described as flattened diaspores formed when the upper layers of the lichen thallus split, often resembling scale-like, rounded segments, as seen in Baeomyces rufus. In 1986, thlasidia were defined as cylindrical, easily detached structures in Gyalideopsis anastomosans, resembling isidia and likely function likely functioning as diaspores.[4]

In Heiomasia sipmanii, Aptroot et al. (2009) labeled disc-shaped isidioid structures as schizidia, differing from the definition given by Frisch and Kalb (2006) for Stegobolus in the family Graphidaceae. These structures in H. sipmanii and H. seaveyorum resembles thallus outgrowths more than true isidia, which have an upper cortex and photobiont layer.[21] Terms like "pseudisidia" (isidioid structures without a cortex) and "pseudoisidia" (isidia-like formations devoid of photobiont cells) can cause confusion.[22][21] The former refers to isidioid structures without a cortex, while the latter signifies isidia-like formations devoid of photobiont cells.[21] Nelsen and colleagues suggest referring to these Heiomasia structures as isidia, as their lack of cortex is due to the thallus being ecorticate.[23]

The debate over these terminologies persists, especially for ecorticate isidia-like outgrowths in lichens like Heiomasia seaveyorum. "Pseudisidia" and "pseudoisidia" are used interchangeably employed by different authors, adding to the confusion.[24]

An isidioid soredium appears as a secondary corticate protuberance in soralia-like clusters. Polyisidia, clustered isidia formed on thalline outgrowths, are unique to the genus Pyxine.[21] Thlasidia resemble pseudoisidia at their ends but contain photobiont cells in soredia-like patches at their bases. They originate from the thlasidium and are found only in the crustose, epiphytic lichen Gyalideopsis anastomosans.[21]

Another unique structure is the Phyllophiale-type isidium, also called scutelliform isidia.[25] This disc-shaped propagule, associated with the foliicolous lichen fungus Phyllophiale (now Porina), has a small Phycopeltis alga thallus surrounded by fungal hyphae. It grows via its hyphal fringe and algal filaments, forming a fungal network over adjoining algal thalli, eventually producing similar disc-like propagules elevated from the main thallus.[25]

Taxonomic value[edit]

Erik Acharius first defined a genus (Isidium) based on the presence of isidia. William Nylander classified manyParmelia species by their presence or absence of isidia. In 1924, Du Rietz's ascribed taxonomic value to isidia and introduced the concept of species pairs, which are morphologically and chemically identical but differ in the presence of vegetative diaspores.[12] In some genera, isidia serve as important taxonomic markers. For example, Leptogium lichens can be differentiated by their isidium development and morphology, with two primary types: hirsutum-type and saturninum-type. Mature isidia in certain Leptogium species help distinguish superficially similar species due to their unique characteristics.[26]

The value of isidial features in taxonomy is debated. Poelt noted that isidia formation in Collema, used by Gunnar Degelius to delineate varieties and forms, was "little stabilized morphologically or systematically".[12] Kalb and Hafellner described Porina isidiata as the isidiate counterpart of specimens resembling P. atlantica, but regional observations suggest P. isidiata might be a variant of P. atlantica. In Porina, distinguishing genuine isidia from abnormal photobiont outgrowths is challenging. McCarthy (1993) and Harris (1995) suggested some structures result from aggressive photobiont growth. Certain species, like P. ocoteae, display isidioid outgrowths under stress. These observations indicate that "isidia" presence should not always be a defining taxonomic criterions, as their structure can be influenced by environmental factors.[27]

Distribution and habitat[edit]

  • General habitats where lichens with isidia are commonly found.
  • e.g. this, from the 2023 paper: “It seems that, in groups of perithecioid lichens, isidia are much rarer than in apothecioid lichens (e.g. Diederich and Ertz (2020); Orange and Chhetri (2022))”
  • Factors influencing the distribution of isidia-bearing lichens.

Lichens that produce vegetative propagules commonly occur without apothecia, or, if they do occur, they are often sparse or immature.[28] It has been estimated that 25–30% of foliose or fruticose lichens form isidia.[1]

Eponyms[edit]

Niebla isidiascens is one of many lichens named for the taxonomic uniqueness of their isidia.

In lichens, specific features related to their isidia are often captured in their species epithet. For instance, the epithet of Porina coralloidea alludes to its isidial features,[29] while Aspicilia stalagmitica earned its name due to distinct isidia-like outgrowths.[30]

Many authors incorporate the term "isidia" (or its variations) directly in species epithets, emphasizing its taxonomic significance. Here, a range of these eponyms are listed, with each accompanied by its respective author citation and year of publication:

Astrothelium isidiatum, characterized as a new species in 2023, is the only species of the large family Trypetheliaceae that is known to produce isidia.[31]

Furthermore, some species names combine "isidia" with descriptive terms to portray specific characteristics:

Acanthotrema alboisidiatum is named for the white isidia that contrast with its light olive-green thallus.

In some cases, species are named for both their isidial attributes and geographical distribution, exemplified by epithets such as N. amerisidiata, N. australisidiata, N. brasilisidiata, and N. siamisidiata.[43]

History[edit]

Erik Acharius was the first to recognize the taxonomic value of coral-like outgrowths on lichen thalli.[44] In 1794, defined the genus Isidium as "branchlets produced on the surface, or coralloid, simple and branched".[45] The genus included densely isidioid species such as Isidium corallinum (now Lepra corallina) and I. westringii (now Pertusaria pseudocorallina). Genus Isidium has since been synonymized with Pertusaria.[46]

German botanist Friedrich Rosendahl described isidia development in several Parmelia species.[47] In P. papulosa, which has a cortical layer one cell thick, isidia begin as small swellings or warts on the upper thallus surface. The cortex cells lose their normal arrangement and show irregular division, further dividing as gonidia and hyphae push up. The mature isidia in this species are cylindrical or clavate, simple or branched, and they minute rhizoids, a unique feature. The inner tissue matches the normal thallus with a distinct cortex, gonidial zone, and pith. Similarly, in Parmelia proboscidea, isidia develop into dark-coloured cilia.[44]

In Parmelia scortea the cortex is several cells thick, with the outermost rows compressed and dead in older parts of the thallus. Isidia begin as minute warts, with lower layers of living cortical cells dividing actively. The protuberance formed pushes off the outer dead cortex and emerges as an isidium, which is stouter than those of P. papulosa and may be simple or branched. In this case, gonidia are scattered through the pith of the isidium rather than forming a definite zone.[44]

The coralloid branching isidia of Umbilicaria pustulata adorn the upper surface and margins of the thallus. They begin as small tufts of cylindrical bodies, sometimes broadening into leafy expansions with crisp edges. Typically situated on bulging pustules where intercalary growth is active, these isidia cause the tissue to become slack. The centre of the isidial tuft may fall out, leaving a hole that enlarges with thalline expansion. New isidia sprout from the wound edges, repeating the process. Bitter demonstrated that these structures form due to isidial growth weakening the thallus, not from injury.[44]

About 100 years ago, Du Rietz categorized isidia shapes as globose, cylindrical, claviform, or coralloid.[10] The term isidium was first used in its current sense by Georg Meyer (botanist) [de] in 1825, and adopted by Elias Fries in 1831.[48]

The term isidium derives from the New Latin isidium, which comes from the Ancient Greek isis, Classical Greek: Ἶσις, meaning "coral", with the diminutive suffix idium.[3] The adjectival form of isidia is isidiate,[3] and isidiiferous refers to a lichen thallus bearing isidia.[49]

A low-cost device was designed to trap microscopic from the air. Molecular techniques were developed to identify the captured propagules, capabile of detecting a single asexual propagule, such as an isidium. This combined approach of using mechanized traps with DNA diagnostics represents a pioneering effort to study lichen dispersal.[50]

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Cited literature[edit]

Tønsberg, T. (1992). The Sorediate and Isidiate, Corticolous, Crustose Lichens in Norway. Sommerfeltia. Vol. 14. p. 129. ISBN 82-7420-015-2.

Category:Lichenology Category:Fungal morphology and anatomy

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