|
Niebla and Vermilacinia (Ramalinaceae) from California and Baja
California.
Evolutionary history of coastal species
of fog lichen genera
Spjut R, Simon A, Guissard M, Magain N, Sérusiaux E. The
fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes):
their diversity and evolutionary history.
MycoKeys. 2020 Oct
30;74:109-110].
|
||
|
Key to the
genera Niebla and Vermilacinia
Introduction Vermilacinia is a genus of fruticose lichens in the family Ramalinaceae in which it is characterized by a thallus divided into narrow cylindrical (worm-like) branches, either united by a holdfast with erect branches from the base when growing on rocks or on shrubs, or without a central basal attachment and the branches all intricately divided similar in habit to reindeer lichens (Cladonia-Cladina) whether growing on earth or rocks. Twenty-eight species initially were distinguished based on morphology and secondary metabolites. Five more were similarly described, all of which are supported by DNA except for a black-banded group of corticolous species (Spjut et al. 2020). Vermilacinia has had a long history of being included in Niebla, preceded by its classification in Ramalina. It has been shown to be phylogenetically distinct from these genera, and an additional newly recognized genus, Nambialina, endemic to southwestern Africa (Spjut et al. 2020). Vermilacinia differs from Niebla by the absence of twine-like medullary hyphae referred to as chrondroid strands. In Niebla, multiple chondroid strands develop like optical fibers oriented longitudinally within a network of flexuous single hyphal strands surrounded by a double-layered cortex. The strands are often visible to the naked eye in cross section. The overlying cortex of Niebla exhibits various patterns of reticulate ridging that with practice can be distinguished by a distinct pattern of development (e.g., in ladder-like in N. rugosa, N. siphonoloba) from irregular developmental patterns in saxicolous Vermilacinia, or in the corticolous Vermilacinia, a regular corrugated cortex can be distinguished in V. corrugata. The texture of the saxicolous species cortex appears more like a pie-like crust and its medulla appears much like tissue paper. The corticolous species generally have a more flexible thallus organization that relates to swelling and shrinking as moisture is taken from fog and lost from retreat of fog . Its cortex acts like a pliable membrane overlying an accordion-like network of medullary bundles of hyphae ± periclinally oriented and knotted together at frequent intervals. Vermilacinia further differs in its secondary metabolites by containing zeorin and/or the diterpenoid [-] -16 α-hydroxykaurane (ceruchinol), at least in all saxicolous species, but ceruchinol is absent in some corticolous species. Bourgeanic acid is often present while its taxonomic value has not been fully assessed. Several species within subgenus Vermilacinia have unique triterpenoid compounds endemic to the coastal Vizcaíno Desert. For example, V. ligulata occurs only along the eastern coast of Isla Cedros and directly across on the adjacent Baja peninsula and further north, that of V. rosei is known from three scattered collections ranging from Isla San Roque, near Bahía de Tortugas, and Isla Cedros, and that of V. reptilioderma is also endemic to the western Vizcaíno peninsula and nearby Isla Cedros. They may have evolved in isolation from a more widespread ancestral species complex. In Niebla, the depsidone species group may also have evolved on an island in the Vizcaíno Desert Region that—after connection to the mainland peninsula—later spread north to the California chaparral-desert ecotone and west to the Vizcaíno Desert area and from there to the southern part of Isla Cedros. The species taxonomy for saxicolous Vermilacinia described by Spjut (1996) is fully supported and four new species were named and described (Spjut et al. 2020). The higher level classification into two subgenera based on corticolous (Subgenus Cylindricaria) vs. saxicolous (Subgenus Vermilacinia) habit includes a third subclade of two saxicolous species within the corticolous clade (Spjut et al. 2020). Nevertheless, all the saxicolous species are included in an updated key to the species presented in Spjut et al, (2020). Since this key is open access publication, the key below remains as it was presented on this website in April 2003 with minor changes and updates to the identifications of the images. The new species include (1) V. breviloba, a relatively small ± tubular inflated thallus with few basal branches, restricted to a narrow canyon inland from Puerto San Andrés, (2) V. lacunosa, distinct for its crateriform surface and possessing tumidulin, previously known only from corticolous species in South America, discovered near Bahía Tortugas; (3) V. pustulata, similar to V. cedrosensis, except the cortex pustular instead of pitted, appearing infrequent but widely distributed in Baja California and Baja California Sur; and (4) Vermilacinia reticulata, distinguished by ± rectangular cortical depressions, appearing of localy occurrence near Punta Eugenia.
Key to Niebla
and Vermilacinia
Medulla with twine-like (chondroid) strands; cortex with reticulate
ridging.....................................................
Niebla Key to Subgenera of Vermilacinia
Cortex crustaceous
(like a pie crust), with minute cracks or large
Cortex membranous, 15-30 μm
thick; usually with a regular network Subgenus Vermilacinia |
||
|
Subgenus Vermilacinia can be divided into two species complexes that correspond to their disjunct geographical occurrences, a South American V. ceruchis complex with lateral to subterminal apothecia, or without apothecia, and a North American V. combeoides Group with mostly terminal apothecia. In South America, only one species in subgenus Vermilacinia has been recognized (V. ceruchis); however, additional species are evident, some of which may be extinct. They are further discussed below as variants within a V. ceruchis complex followed by a key proposing their species status.
Vermilacinia ceruchis is typically terricolous, “lying without adhesion on bare sand” as described by Darwin for a specimen he collected near Iquique, Chile (Peru during his time). His specimen compares favorably with those collected by Joseph Dombey near Lima in Peru and by Archibald Menzies possibly near Valparaiso in Chile (type collections). This may now be an extinct species (see Follmann 1994). It is characterized by a thallus consisting of a single (prostrate) cylindrical 'stem' that creeps along the ground with occasional ascending to erect branches, all of which have a relatively thick crusty cortex (75–125 µm). This is in contrast to a much more divided thallus of thread-like branches as represented by the type for Usnea tumidula from Coquimbo, Chile. Both variants lack apothecia. The 'tumidula variant' from Chile (Taylor Herb., FH) is similar to V. ceruchoides from North America that differs by a thallus of more rigid compact branches terminating in short bifurcate branchlets; however, intermediates in South America are evident, although they appear related to the South American species. Their close similarity was evident to Herre (1906) who stated that he saw the “typical form” (Ramalina ceruchis) “only once” as “sterile”, occurring sparingly on sandstone cliffs above the sea at Sutro Heights, San Francisco. This was probably what is now regarded as V. ceruchoides
|
||
|
V. ceruchis |
 |
V. ceruchis, typical.
|
 |
||
|
Several other variants of the Vermilacinia ceruchis complex in South America differ from their North American counterparts by lateral or subterminal apothecia, while also separated from the related South American species by the thallus branches united at base into a central attachment or holdfast, presumably as a result of growing on rocks. Subterminal apothecia are defined as those that develop ± solitarily on upper branches resulting in a change direction of growth from where they originate, or develop an appendage (spur) like branch (especially subgenus Cylindricaria). This in contrast to lateral multiple apothecia on a relatively straight branches as seen in the specimen from Callao. It is not known whether the Callao variant is extant, although it was reported by Gaudichaud to be abundant on rocks at Callao (Montagne 1834). The illustration immediately above is from Montagne (1834, as Usnea ceruchis). Except for the spine-like extension on apothecia, which it seems that Montagne may have added to make it appear more like Usnea, the center and left figures compare closely to the specimen above thought to be from Callao, Peru. The specimen on right that is more branched may have come from spines of cacti or branches of arborescent shrubs at Coquimbo, or possibly terricolous as it resembles V. tigrina from Chile, see image below from Follmann (1966). It is interesting to note that specimens in the Tuckerman Herbarium (Farlow Herbarium) shown above—mounted together on one sheet—correspond to Tuckerman's (1882) description and comments for Ramalina combeoides: “quite simple podetiiform thallus, and commonly terminal, now clustered apothecia, grows the the next species in California (Bolander [in reference to R. homalea, Nylander monograph]) but, though certainly marked, is inseparable from South American forms (Tierra del Fuego, Wilkes exp.).” Thus, Tuckerman (1882) regarded the North American V. combeoides to be the same as saxicolous variants of V. ceruchis, except for the terminal apothecia as he himself indicated. It should also be kept in mind that V. ceruchis and Niebla homalea were treated in separate genera by Acharius (1810), and that Montagne (1852) combined them into a single genus and species, only to be soon segregated (Trevisan 1861) and later classified into three groups (Bowler 1981, 'homalea', 'combeoides', and tigrina ['ceruchis' misapplied]), and two genera (Spjut 1995).
|
||
|
|
||
|
Subterminal
apothecia are seen more often in Subgenus Cylindricaria, usually
accompanied by a relatively short continuous branch that ascends sharply upwards
as shown above for V. leopardina.
This is in contrast to South American subgenus Vermilacinia
with
apothecial branches that bend abruptly (geniculate) as evident for the 'roccellaeformis
variant'.
The mildew-like appearance of the specimens is the result of efflorescence—a chemical change associated with the breakdown of the cortex from which the internal (medullary) hyphae erupt. The decorticating condition has been attributed to [-]-16 α-hydroxykaurane, a diterpene found in all species of subgenus Vermilacinia, most North American species of subgenus Cylindricaria, but not in Niebla (Spjut 1995, 1996). This diterpene is apparently rare in lichens, although known in mosses (Physcomitrium). The mold-like condition develops within a period of six months after a specimen has been collected; however, efflorescence can be prevented by storing specimens in a refrigerator below 40°F, although there may be a trade-off in that long term storage in a frost-free refrigerator causes the cortex to become brittle over time (gen. obs., ~9 yrs). Efflorescence is common in subgenus Vermilacinia and V. cephalota, V. cerebra, and V. tigrina in subgenus Cylindricaria, in which its occurrence seems closely associated with an unidentified triterpene (T3, Spjut 1996), and with bourgeanic acid, a distinct chemical class of aliphatic depsides (White & Johnson 1994). These compounds—and also the triterpene zeorin—occur in both subgenera but not in Niebla. Indeed, Niebla and Vermilacinia have little in common in their secondary metabolites except for occasional weak presence of accessory lichen depsidones in Vermilacinia. The distinction has been further sharpened by finding that species in the Old World 'Bourgeana clade'—also classified in Niebla (Rundel & Bowler 1978; Bowler & Marsh 2004)—are nested within the Old World Ramalina (Sérusiaux et al. 2010).
|
||
|
Summary: Key to South American species of Vermilacinia subgenus Vermilacinia
1. Basal branches solitary, or without a
central attachment point; apothecia lacking;
terricolous................................2
2. Thallus a
single cylindrical 'stem', 2–3 mm wide near base, sparingly branched;
Valparaiso and
3. Basal branches loosely united,
wide spreading, long attenuate; Coquimbo Chile,
extinct?.....................V. tumidula
4. Basal branches erect, inflated;
apothecia lateral; Callao Peru (see also V. vesiculosa, N
Am)..........Vermilacinia sp.
|
||
|
Subgenus Vermilacinia in North America
|
||
|
The North American species in the subgenus Vermilacinia are usually recognized by subterminal to terminal, often aggregate apothecia, in contrast to solitary to subterminal or lateral apothecia in the South American species. Included are species without apothecia found on rocks rather than on earth. One species, V. vesiculosa, is recognized for lateral large bladder-like (utricular) swellings and for the pycnidia that develop in tubercular lobes that form the thalline margin. Bladder-like or gall-like outgrowths ~ 1 mm—that are common on Vermilacinia and also Niebla—contain lichenicolous Heterobasidiomycetes Tremella nieblae (Diederich 2007); however, the development of lateral swellings in V. vesiculosa and the terminal swelling in the corticolous V. cerebra, appear related to an aborted development of apothecia. The utricular swellings in V. vesiculosa are exceptionally large, ~10 mm diam. Four species—Vermilacinia johncassadyi, V. ligulata, V. reptilioderma, and V. rosei—are recognized by triterpenes in RF Classes 1–2—than what characterizes most species in Subgenus Vermilacinia. The species occur in southern Baja California, Isla Cedros, and on the Vizcaíno Peninsula and nearby Isla San Roque. In TLC, these terpenes appear quite strong, and seem to replace terpenes in higher RF classes, but not zeorin and [-]-16 α-hydroxykaurane. Vermilacinia johncassadyi is morphologically similar to V. laevigata. Vermilacinia ligulata may be compared to V. polymorpha in the Channel Islands in having relatively short basal branches; the Baja California species is ± digitately divided into twisted lobes, whereas the California species has more cylindrical dichotomously divided branches. Vermilacinia reptilioderma, a relatively rare species, is closely related to V. paleoderma, a common species along the Pacific Coast south of Punta Baja. They are sympatric on the Vizcaíno Peninsula and on Isla Cedros and can only be distinguished with confidence by their lichen substances. Similarly, V. rosei strongly resembles V. varicosa, in which they are sympatric on Isla San Roque, and V. rosei has also been collected on Isla Cedros and recently on the Vizcaíno Peninsula. Except for V. ligulata, they may be regarded as sibling species. The following key defines the species in the North American Vermilacinia subgenus Vermilacinia. |
||
 |
||
|
Key to
Species of Subgenus Vermilacinia: North America
1 Cortical surface
with regular protruding ridges, creases, or crater-like depressions…........................................… 2
2 Thallus cushion-like, of short branches
tightly compacted, 1–2 (-4) cm high, rarely unbranched for more than
3(2) Thallus of mostly
undivided tubular branches
with terminal or subterminal apothecia, the branches arising from
3 Basal branches simple to shortly bifurcate near
apex, or densely branched below apex, often matted
4 (3) Thallus lacking terminal acicular branchlets, or abruptly with
narrow acicular isidia; basal branches
sparingly
5(3) Basal branches closely compacted, without isidia or soredia, mostly simple
and stubby, or shortly divided
7(2) Branches with bladder-like swellings; pycnidia elevated on pustular
lobes; rare, between
8(7) Primary branches 5–10˟ longer than wide, twisted, lobulate; triterpenes present in RF classes 1–2; Isla
9(8).
Branches flexuous, 0.5–1.5 mm wide; cortex on upper branches thinner,
eroded and pitted;
10(9).
Apothecia aggregate on expanded marginal and terminal lobes constricted below;
endemic to
11 Triterpenes present in RF Classes 1–2;
Vizcaíno Peninsula and Isla
Cedros (V. lacunosa if
12(1) Branches distinctly blade-like, two-edged.........................................................................................................
13
13(12) Triterpenes present in RF
classes G: 1–2; rare, Isla Cedros, southern half of
14(13) Branches uniformly blackened around base to slightly above,
usually less than 4 cm long,
1–4 mm
14(13) Branches
irregularly blackened near base and above, usually >3.5 cm long and 4–7
mm
wide;
15(13)
Branches uniformly cylindrical, irregularly blackened above base, often with
black transverse bands or cracks........
16
16(15)
Apothecia mostly terminal; Californian coastal chaparral region, San Francisco to San Quintín,
17(15)
Branches dilated, flattened and/or digitately divided;
Baja California.................................................................... 18
18(17) Triterpenes present in RF Classes 1–2; Isla San Roque
and Isla Cedros...................……..……... Vermilacinia rosei
19(17)
Branches inflated, ± round in x-section; Isla Guadalupe, Channel Islands, peninsular
BCN from
|
||
|
Additional images obtained from review of specimens collected for molecular
|
||
