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Niebla and Vermilacinia (Ramalinaceae) from California and Baja
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Introduction Species Identification and Concept in the Genus Niebla
Divaricatic-acid species Morphological key: Species in Baja California Outline of Key Characters by Chemotype for all species of Niebla
Introduction Niebla and Vermilacinia are fruticose lichens found along fog areas of the Pacific Coast from SE Alaska to southern Baja California. The above publication differentiates 71 species, 69 in North America and 2 in South America, 53 of which are recognized as new with one new variety. Niebla is recognized here to include 44 species in North America (42 published, 2 unpublished); Vermilacinia has 31 species, 28 in North America (26 published, 2 unpublished) and five in South America, two of which are endemic. Vermilacinia was segregated from Niebla (Spjut 1995) based on the lichen secondary metabolites that are primarily terpenes, particularly in the presence of the diterpene [-] -16 α-hydroxykaurane, and by the lack of isolated medullary chondroid strands. The relationships between the two genera in North America seem more eco-geographical than phylogenetic. Indeed, unpublished molecular (“rDNA”) data reported by Arizona State University indicate that the former “Niebla (sensu Rundel & Bowler, 1978; Bowler & Marsh 2004) is paraphyletic” in which molecular data correspond to the separation of the two genera (Nash III letter to Spjut dated Nov. 15, 1995, initially stating that there is “additional evidence to support” “Vermilacinia” and that “Janet Marsh has been re-examining the generic segregations ”within the Ramalinaceae from a phylogenetic perspective”). Moreover, there is very little in common between the two genera in that they share none of the triterpenes, none of the depsides, and differ significantly in cortical features; Darrell Wright, in A Simplified TLC Method, published in the Bull. Calif. Lichen Soc.2 (1995), noted that “perhaps the most remarkable thing about this trace is that not one of the eight substances found in N. laevigata [= Vermilacinia laeviagata] appears to correspond to any of the seven substances in its congener, N. homalea.” Each genus exhibits different evolutionary patterns in speciation (adaptive radiation). The ramalinoid complex centers mainly in the Mediterranean Region where species of Ramalina have character features of Niebla and Vermilacinia. The interpretation of Niebla to occur in the Mediterranean has been based on six species there having isolated chondroid strands in the medulla (Spjut 1995, 1996); however, the basis for three name combinations recently made by Bowler and Marsh (in the Greater Sonoran Desert Lichen Flora, Vol. 2, 2004; see Spjut Review) is unclear since these authors feel that the character attribute of chondroid strands does not justify use for generic separation of Niebla. These ramalinae also appear related to Vermilacinia (subgenus Cylindicaria) by their secondary chemical substances of triterpenes, bourgeanic acid, and various depsidones, instead of just having one depsidone compound. In North America, Niebla and Vermilacinia are more distinct by the black pycnidia, in contrast to pale pycnidia of Ramalina. Exceptions include the Macaronesian Ramalina portosantana that is similar to Niebla josecuervoi except for the presence of pseudocyphellae, which are generally found in Ramalina, and not in Niebla (Spjut 1995). Species delimitation in Niebla is more taxonomically difficult than in Vermilacinia. The North American Niebla are easily classified by their secondary metabolites into two groups and six subgroups, which could be recognized as subgenera: (1) terpenoid deficient group, either with depsidones (protocetraric acid or hypoprotocetraric acid or salazinic acid), or without depsidones (acid deficient N. homaleoides) and (2) a terpenoid group with depsides (with either divaricatic acid or sekikaic acid complex). The subgroups are then defined by the presence of the specific lichen acids as just indicated. These differences could define the limits of the North American species; however, morphological variation in Niebla is difficult to ignore. Therefore, species are further differentiated morphologically. Most are polymorphic as evident by a wide range of morphotypes. Two subgenera of Vermilacinia are distinguished by thallus morphology, corresponding to the substrate upon which they grow; subgenus Vermilacinia has 18+ species that are mostly saxicolous (terricolous in South America), whereas subgenus Cylindricaria has 10+ corticolous (terricolous in South America). Subgenus Vermilacinia shows greater diversity morphologically in the Channel Islands, and chemically in peninsular Baja California Norte (BCN). Cylindricaria is more variable in secondary metabolites, particularly in South American species. Niebla reaches its greatest diversity on peninsular Baja California Norte (BCN) between Punta San Carlos and Punta Rocosa. Six species of Niebla, and two species of Vermilacinia, are endemic to this region. Other species of Niebla reach their southern distribution limits here such as Niebla homalea, generally not found south of Punta Baja except on Isla Cedros. Mesas between Punta Canoas and Puerto Catarina (Mesa Camacho) are exceptionally rich in lichens, 21 species of Niebla were recorded from this region and include endemics such as Niebla tesselata, Vermilacinia vesiculosa, and two provisionally named (undescribed) species, N. angulata and N. sinuata; see also Niebla and Vermilacinia communities of Baja California. Other Niebla rich communities occur as far south as Punta Rocosa. The photo on the cover page shows a sandy ridge just south of Punta Negra where many type specimens were collected (Niebla flagelliforma, Niebla homaleoides, N. infundibula, N. juncosa, N. podetiaforma, N. sorocarpia, N. undulata, and Vermilacinia rigida). Among the flowering plants in this region is a geographically isolated variety of Ziziphus parryi (not in the Wiggins Flora), otherwise, known only from Isla Cedros with a disjunct occurrence of another variety near Morongo Valley, California. North of Punta San Carlos, along the west peninsula of Bahía de San Quintín, is another undescribed species of Vermilacinia that has hybrid features between V. procera and V. leopardina. The islands along the Pacific Coast are generally less diverse in Niebla, although are richly represented in species of Vermilacinia. This may be related to the more localized occurrences of inland (orographic) fog in regard to Niebla, in contrast to species of Vermilacinia that favor the immediate coastal (mist) environment. A checklist of lichens of Isla Guadalupe by J. A, Elix and P. M. McCarthy (March 2005, with reference to their Catalogue of the lichens of the smaller Pacific Islands, Bibliotheca Lichenologica 70, 1 - 361, 1998.) reported nine species of Niebla and seven species of Vermilacinia, which included the endemic, N. isidiosa (their N. ceruchoides was treated by Spjut (1996) under Vermilacinia). Isla Cedros has four species of Niebla (N. homalea, N. flabellata, N. rugosa, and N. spatulata) and nine species of Vermilacinia (V. cedrosensis, V. johncassadyi, V. ligulata, V. paleoderma, V. reptilioderma, V. rosei, V. varicosa, and one undescribed). Most species were found on the foggier northwest coast. The biogeographical significance of the Isla Cedros lichens is evident by the limited geographical occurrences on the nearby peninsula for N. spatulata, N. rugosa, Vermilacinia cedrosensis, V. ligulata, V. johncassadyi, and V. reptilioderma. This might be contrasted to that of Isla Guadalupe that has more species found in California than in Baja California. In the Channel Islands of California, the species of Niebla and Vermilacinia, as might be expected, occur more frequently on mainland California than in Baja California, and include endemic species such as Niebla dactylifera (San Nicolas Island) and N. ramosissima (San Nicolas Island). Towards the periphery of the geographical range of Niebla, single species populations are sometimes encountered. Examples are the isidiate N. isidiaescens and N. usneoides south of the Vizcaíno Peninsula in Baja California Sur, N. contorta on Isla Santa Margarita and on the Vizcaíno Peninsula, N. marinii near Morro Santo Domingo, and N. homalea in Sonoma County, California. Species Concept and Identification in the Genus Niebla Species Concept. Spjut (1996) referred to species of Niebla as “protean” in regard to “Proteus, an ancient Greek god who had the ability to change his shape at will.” Niebla species do appear to be “shape-shifters” in that they often include many morphotypes. Nevertheless, Spjut (1996) was able to differentiate them morphologically in which he compared the morphological variation within a species to recognizing the painting style of an artist, or to that of a large genus of lichens or plants. This is in contrast to Bowler and Marsh (2004) who were unable to differentiate species of Niebla (sensu Spjut 1995, 1996) by morphology; they only recognized two chemical species, N. homalea and N. josecuervoi, which in their reality represent chemosyndromes of depsidones and depsides (but wrongly assigned the acid-deficient species, N. homaleoides, to the depside group). The delimitation of Niebla species in Spjut (1996) is taxonomic (“diagnostic species concept”) based on biogeographic relationships of chemical and morphological data (also “phylogenetic species concept”). For example, in Baja California, terricolous species, which form much of the ground cover along the Pacific Coast between San Antonio del Mar and Punta Baja, almost always contain depsidones, usually salazinic acid. Californian species, on the other hand, are rarely terricolous, and those that are known, occur in the Channel Islands (San Nicolas Island, N. ramosissima; Isla Coronado, N. palmeri) with depsides, usually divaricatic acid or sekikaic acid derivatives. This infers a phylogenetic relationship that supports the division of the genus into two broad chemical groups of species in which both groups appear monophyletic (See Outline of Key Characters by Chemotype for all species of Niebla). There are no exceptions known for the North American Niebla; triterpenes are always found with the depside species, and they are always absent in the depsidone group and one acid-deficient species. This is in contrast to Mediterranean-Macaronesian species of Niebla (Spjut 1995, 1996), which differ from the North American species, in that triterpenes occur with depsidones, and that any one individual contains more than one depsidone compound except for Ramalina portosantana as noted earlier. Species identification usually requires working with a [taxonomic] key, a process of elimination in choosing between the alternative choices of character features indicated, leading to a decision on a species name. Spjut (1996) provided two types of identification keys to Niebla species, one weighted on morphological characters, the other emphasized chemical characters. He also provided detailed descriptions, illustrations, and photos for each species. Most keys present two alternative choices, or dichotomy, for deciding on which character features apply to a given specimen in question; however, the key below includes three choices (trichotomies) for key efficiency. The steps in the key where trichotomies occur are highlighted in color to facilitate their separation from the dichotomies. In addition to using a key, it helps to consult authenticated specimens annotated by a specialist. Generally one looks for a match between the specimen under consideration among those identified by the expert. Authenticated (annotated) specimens by Spjut are to be found in institutional herbaria. The main herbarium cited by Spjut (1996) is the United States National Herbarium, Smithsonian Institution in Washington, DC (US). Most of Spjut's (1996) holotypes are at US (see also letter from Smithsonian Institution to Dr. Spjut, 1990). Additionally, Spjut sent representative specimens of most species of Niebla and Vermilacinia to selected lichenologists; these specimens may be found at B (Botanischer Garten und Botanisches Museum Berlin-Dahlem, Zentraleinrichtung der Freien Universität Berlin, Germany, 54 specimens), BCMEX (Universidad Autónoma de Baja California, ~ 100 specimens delivered by Richard Marin to a scientist in Ensenada, Mexico who was associated with the WBA collecting permit) and DUKE (Duke University, Durham, NC, 48 specimens). Isotypes for most species were also sent to LA (University of California, Los Angeles) and BCMEX. Other specimens studied by Spjut (1996), collected by other lichenologists, are at the Smithsonian Institution (US), the University of Colorado in Boulder (COLO), the Santa Barbara Botanic Garden (SBBG, collections by Charis Bratt), and at the WBA herbarium. Photos of representative specimens from these institutions are shown on WBA web pages, linked by species name in key below, and by name when first mentioned in the discussion that follows.. In consulting herbarium specimens for identifying a specimen in question, one may look at species variation within a genus as well as within a species in trying to find a match; additionally, in lichen taxonomy one also has to consider species that may differ only by secondary chemical metabolites. Niebla species are further complicated by having many morphotypes with the same chemotype (morphosyndromes). Spjut's (1996) classification key—based on chemical characters—reduces the number of key steps in having to deal with the more complex morphology. As one gains experience in identifying species of Niebla, he or she will prefer the chemical key over the morphological key. An outline of the chemotypes and species is also provided below. Before working with any of the keys, it might help to look at representative specimens of species to get a better understanding of the variation in the species morphotypes, and how the key features tie them together. Six examples are discussed below to help one appreciate, on one hand, the taxonomic complexity, and on the other, the character features that distinguish the species of Niebla. These are divaricatic-acid species with one comparison to a sekikaic-acid species. This is followed by a discussion of the salazinic-acid species and then by the sekikaic-acid species. Divaricatic-acid species of Niebla 1. Niebla podetiaforma. This species is perhaps the easiest to comprehend in the genus. It includes an obvious morph recognized by the inflated branches (center photo in top row, Spjut 11301) that are characterized by a medulla loosely filled with hyphae surrounded by a relatively thin cortex (< 75µm thick). This morph is frequently found on the Pacific coastal mountain slopes of southern Baja California Norte (BCN). Despite its obvious characteristic of inflated branches, it was not given separate species or varietal status because it is clearly associated with other morphs with a less inflated medulla, examples of which are also shown. This is reminiscent of a perennial herb, Eriogonum inflatum, of the Mojave Desert, distinguished from others in a very large genus by its inflated stems, but includes a variety known as var. deflatum, while there is also a related species E. trichopes, which produces both normal and inflated stems. Most of the variation shown for Niebla podetiaforma occurs throughout the range of the species in Baja California. A nice photo of N. podetiaforma by F. Bungartz is also presented in the Lichen Flora of the Greater Sonoran Desert Region, Vol. 2, which Bungartz identified as N. homalea. This species, N. podetiaforma, can often be recognized without the aid of TLC data. 2. Niebla undulata and N. rugosa. In order to fully appreciate the variation in Niebla podetiaforma, one needs to compare this species to other shape-shifter Nieblas. Good examples are divaricatic-acid species, Niebla undulata and N. rugosa. Open an internet browser for each species. Look closely at the apical branches. Observe that the cortical ridges of N. undulata near apex of branchlets are oriented more longitudinally to diagonally with the apical part of the branch twisting, also appearing undulate along margins. Cortical ridging in Niebla podetiaforma, in contrast, is more transversely oriented near apex with the branch remaining mostly straight. In N. rugosa the transverse ridges are more conspicuous in the upper half of the branches, often complete between branch margins, and the branches fold slightly like an accordion, a character attribute that is distinctive for this species. The cortical ridging in Niebla, or internal hyphal ribbing in its 2-layered cortex, makes-up the “backbone” of the Niebla thallus. Just like vertebrates that are classified by differences in bone structure and how bones are connected, species of Niebla are differentiated by their hyphal framework—as seen by the hyphal ribbing in the cortex—that provides much of the “backbone” support to the thallus branches to rise above the surface. The main structural support is the medulla with its numerous longitudinal cord-like, sclero-proso-plectenchymatous, hyphae, which are isolated from the cortex, generally referred to as chondroid strands, visible in many specimen photos where thallus branches have broken off. The epithets were chosen to emphasize structural features of the cortical ribbing, undulata for the undulate branches, podetiaforma for the resemblance of a branch to a podetium of Cladonia spp. (in some morphotypes), and rugosa for the wrinkled (accordion-like) branches. Observe also the variation in the thallus habit and in the shape of the branches for Niebla undulata. The branches are generally ribbon-like in that they are rather broad-linear, or oblong, undulate and thickened along margins, but appear distinctly bladelike in one variant (13023). Basal branches of some thalli are very much compacted (or caespitose). These may spread outwards or rise upwards (9784, 13022), or they appear nearly prostrate in that they spread close to the ground (13022, 13023, 13048). In other specimens, the branches are loosely tufted, more upright and notably contorted (10321, 12739). Except for the morph with the blade-like branches, much of the variation may be related to environmental differences. Niebla undulata is not only differentiated by the apical diagonal to longitudinal cortical ridges, but can be recognized by the cortex appearing more deeply recessed between the ridges in comparison to that of N. podetiaforma. Niebla rugosa shows considerable variation in width, thickness, and length of branches. The specimen from Isla Cedros is quite small, in contrast to specimens from mainland BCN. Yet, they are all remarkably similar in the marginal folding and transverse ridging. 3. Niebla siphonoloba. In this example, a comparison is made between a sekikaic acid species N. siphonoloba and a divaricatic-acid species, N. rugosa. Some lichenologists might treat these as chemical variants or races of one species; however, the arrangement of the cortical ridges, which are similar in the two species, are not exactly the same. A main difference is that some of the transverse ridges of N. rugosa are complete between margins, whereas those of N. siphonoloba are often interconnected between margins. This difference may partly explain why branches of Niebla siphonoloba do not fold like an accordion. Instead, the branches of N. siphonoloba are like old knotted or broken tree stumps. Just as one might recognize different stumps in a forest, the basal tubular (siphon or pipe-like) branches of N. siphonoloba will exhibit different shapes at different locations. Niebla siphonoloba can be further distinguished from related species by the predominantly monopodial branches, occasionally dividing into secondary branches that show little differentiation from primary branches. This is in contrast to fragmentation branchlets in a related sekikaic-acid species, N. fimbriata. Nevertheless, one must not forget that an important taxonomic feature for distinguishing N. siphonoloba from N. rugosa is their lichen metabolites, sekikaic acid (N. siphonoloba) instead of divaricatic acid (N. rugosa). Another less obvious difference is the concentration of yellow pigmentation at the base of the thallus, which causes a blackish discoloration to extend above the base. This pigmentation is stronger in N. rugosa than in N. siphonoloba. Another morphotype shown under N. siphonoloba, and also under N. suffnessii, referred to by an unpublished name, N. sinuata, is distinct for the sinuous cortical ridges. Similar sinuate ridging is seen in sekikaic-acid species in the Channel Islands, one of which is also shown under N. suffnessii, known as N. disrupta. These examples are intended to show that more study is needed in the genus, particularly for sekikaic-acid species in the Channel Islands. Molecular studies, which many lichenologists regard as necessary, will be complicated by need for fresh material in which sampling would have to be done throughout the range of the genus in order to obtain a good representation of the chemotypes and morphotypes. It should also be realized that Spjut's (1996) treatise provides the foundation upon which molecular studies can refine the taxonomy of the genus, especially since Bowler and Marsh (2004) could not distinguish any species by morphological characters even though they also recognized the genus to be exceedingly rich in morphotypes and chemotypes. 4. Niebla caespitosa and N. dilatata (divaricatic acid). These are the tortilla chip Nieblas, which are also regarded as pebble lichens because they are often found on pebble-size rocks along beaches and slopes. Some lichenologists would refer to their habit has having flabellate types of branches. The thallus generally has flattened branches that fan out compared to prismatic strap-like branches in other species. The tortilla chip-like branches of N. caespitosa represent the sharply pointed type in contrast to the rounded type in N. dilatata, which also comes with the creamy dip along the edges in that the cortex is thickened along branch margins. Observe that some thalli have broad triangular chips (e.g., 10921) while others have much narrower well-defined branches with irregularly widened segments (11231) or apical lobes (type). Of course not all tortilla chips in a bag are exactly alike, and neither are the tortilla chip Nieblas. For two of the 11 specimens shown, hybrids are suggested, N caespitosa х N. undulata, and N. caespitosa х N. podetiaforma. This designation is not normally done in lichens. If this classification scheme were adopted for Niebla, it could lead to many such designations. Whether these are hybrids, remains to be proven. They may also prove to be N. undulata and N. podetiaforma. Such hybrid features were reported by Spjut (1996) among populations having mixed species, in contrast to single dominant Niebla communities. The possibility of “mechanical hybrids” (Bridge & Hawksworth 1998) from different thalli is a likely explanation (Spjut 1996) as suggested for Usnea (Grube & Kroken 2000), in view of Niebla growing abundantly in an open windy desert in which many of the morphological entities produce fragmentation branchlets. Assuming that they are hybrids, the question remains as to whether this justifies uniting the two species, or keeping them separate. If 85% of the thalli, for example, can be identified as belonging to N. caespitosa, does the 15% that form intermediates to other similarly distinct taxa justify a classification of the whole complex as one singles species, N. homalea, as done by Montagne (1852)? It should be kept in mind that the key was constructed to weigh the flattened feature of the branches so that the specimens in question would key out to N. caespitosa. 5. Niebla juncosa and N. turgida. In the preceding examples, the thallus consists of basal branches in small tufts, less than 6 cm high and usually less than 20 in number. In this example, the two species have many more basal branches, and/or branches that are generally longer than 6 cm in length. These are called bushy Nieblas. They usually produce many side branchlets (branches that develop from a primary branch and dead end along a main branch, especially N. juncosa. The main difference between these species is seen along the branch margins. Niebla juncosa has well defined straps because the branches do not twist as often, whereas the branches of N. turgida appear to have less defined margins because of more frequent twisting. Two distinct morphs are also shown for N. turgida, the type (1st specimen on third row, Spjut 10382) with narrow largely prismatic branches and another that resembles the tortilla chip N. caespitosa (Spjut 13088, 13100), but clearly associated with N. turgida by the larger size and upper branchlets that are acutely prismatic as also seen in the type. It is still possible that this flattened morph could prove to be a distinct species upon further study; however, as noted by Spjut (1996), it was treated under N. turgida because of its close association with the typical form. 6. Californian species, Niebla eburnea, N. homalea, and N. testudinaria. Lichenologists will probably have a much harder time accepting these species because their differences are less dramatic in comparison to the preceding examples, and they include a wider variation of morphotypes in which the species appear polymorphic. But the alternative of lumping them makes it harder to separate them from other species in the genus. The California species differ from the preceding (Baja California species) in having a much thicker cortex (> 75µm thick) and a solid medulla (hyphae densely compacted), which appears to be an adaptation to a cooler northern climate. As a result, the branches appear rigid and less crinkled or wrinkled on the cortical surface. Niebla testudinaria is recognized by its prismatic branches (x-section), which is obviously related to the protruding cortical ridges and frequent twisting of the branches. Like N. turgida, N. testudinaria includes morphs with short almost flattened branches as in the tortilla chip Nieblas (Moran 1055, Bratt 3212, Weber & Santesson), while others appear linear and straight (Howe 92, Herre 256), or linear and contorted as in N. flagelliforma (6431, 7202), and then there is the typical form that appears to be somewhat in between these. The main feature that holds these together is the conspicuous reticulate ridging; however, further studies might show that variants from the typical form could belong to other species such as N. caespitosa (Moran 1055, Bratt 3212 and Weber & Santesson) and N. flagelliforma (Bratt 6431, 7202). Justification for their reassignment seems stronger in view of redefining N. caespitosa as a result of recognizing N. dilatata to occur on the main peninsula of Baja California based on differences on rounded (N. dilatata) vs. acute branches (N. caespitosa) instead of on the thickness of cortex (Spjut 1996). However, these have been included under N. testudinaria because of the relatively thick cortex (> 75µm thick) and solid medulla. Molecular studies in this case might be used to determine whether thickness of the cortex is a more important than the shape of the branches as a taxonomic character. Niebla homalea is much like N. testudinaria except the reticulate ridging is mostly not evident, undoubtedly related to a thicker cortex, or “epicortex (Bowler 1981),” an additional epinecral layer beyond the melanized layer, which is normally the outer layer of a 2-layered cortex in Niebla (Bowler 1981). The “epicortex” forms a gloss over the surface of the branches; however, this feature is not always clearly absent in N. testudinaria so the development and lack of development of cortical ridging is given more weight. Niebla homalea has branches that appear more strap-like in shape, and this is also weighted in defining the circumscription of the species; i.e. the branches are always relatively narrow in N. homalea, whereas in the related N. testudinaria and N. eburnea, thallus branches can be narrow or broad. This leaves N. eburnea, that is identified by the ivory-like cortex appearing thicker along margins, and often by less twisted branches, twisting most near base and apex than in the mid region. For further discussion on the remaining divaricatic-acid species, consult the summaries provided on their respective pages by the links provided in the key below. Other species with unique attributes are rare. For example, Niebla halei, known only from San Bruno Mt. near San Francisco, has an intricately branched thallus that is much reduced in size, which may have been derived from N. dactylifera, whereas N. ramosissima from San Nicolas Island is distinct for its much dichotomously branched thallus of capillary branches. It should be obvious from the preceding discussion that cortical features of Niebla are given considerable weight for separating species. Among the other chemotypes to be discussed, salazinic acid and sekikaic acid species, differences are often based on habit and branching patterns. Thus, it also appears that the divaricatic-acid species form a monophyletic group from which at least the sekikaic acid species may be derived. The evolution of metadepsides from paradepside precursors has been suggested for the Ramalina americana complex (C. Culberson et al. 1990). Salazinic-acid and Related Chemotype Species The salazinic-acid species are classified under a Terpenoid Deficient or Depsidone Species Group that includes one species (N. homaleoides) lacking in key metabolites (Spjut 1996). The key metabolites in the Depsidone Subgroup are salazinic acid, hypoprotocetraric acid, and protocetraric acid. In the Mediterranean Region, depsidone species of Niebla may include accessory triterpenes, bougeanic acid, and more than one depsidone; for example, Niebla webbii has both protocetraric acid and salazinic acid, but is without terpenes and bougeanic acid (Krog & Østhagen 1980; Spjut 1995). The biogeographic relationships between the North American and Mediterranean species may relate to a time when the Mediterranean floras diversified in each region (Axelrod 1975). This is in contrast to Vermilacinia, which also has biogeographical ties to South American species (Spjut 1995). Nevertheless, the North American Depsidone species of Niebla, which includes one acid deficient species, appear to constitute a monophyletic group. In Baja California, salazinic-acid species of Niebla occur from Isla Cedros and nearby Vizcaíno Peninsula north to near Colonet. These include Niebla josecuervoi, often identified by its convoluted basal branch that creeps partly along the ground with many erect spine-like branchlets that arise close together on the upper side (orientation of branching obviously induced by light) so as to appear comb-like (or pectinate), but other morphs with erect straighter branches are recognized. Niebla marini, which lacks fragmentation branchlets, has primary branches divided into similar secondary branches (isotomic branching), which are all narrow and whip-like. Niebla arenaria and N. limicola have a more intricately branched thallus with shorter antler-like, bifurcate (two-pointer) branchlets; the former has narrow basal branches, while the latter has a flabellate thallus. Niebla flabellata is similar to tortilla-chip Niebla caespitosa, but also exceedingly variable in that some thalli hardly resemble tortilla chips; these species are distinguished by chemistry. The other depsidone species, and one acid-deficient species, are relatively rare in occurrence, and largely allopatric or parapatric (N. homaleoides). For example, the hypoprotocetaric acid species include N. spatulata on Isla Cedros and at scattered locations from the Vizcaíno Peninsula north to near Rosarito and N. brachyura from near Punta Santa Rosalillita to Punta Canoas, and the one protocetraric acid species, N. pulchribarbara, is found further north in the chaparral region of Baja California, north of Punta Baja. The acid-deficient Niebla homaleoides lies mostly between the ranges of N. spatulata and N. pulchribarbara, from Punta Rocosa to just north of Punta Cono, overlapping in the southern range of N. brachyura. Although the cortical features of salazinic-acid species are more variable, compared to divaricatic-acid species, some exceptions may have taxonomic significance. Generally, the cortex of Niebla marinii is typically smooth and glazed, in contrast to prominent ridging in N. josecuervoi and N. flabellata in which the latter often differs by more transverse ridges. One notable exception is a morphotype shown under N. marinii, provisionally named N. angulata. It is distinct for the open branching and the sharp sinuous cortical ridges. This proposed species is known only from Mesa Camacho just north of Punta Canoas. Most lichenologists would expect this chemotype to be discussed in connection with the divaricatic acid species since their chemical structures are quite similar, and because morphotypes that differ only by these secondary metabolites are often viewed as replacement chemotypes or chemical races of a species as reported in a related genus, Ramalina (Krog & Østhagen 1980; Lumbsch 1998; Rundel 1978). However, the Niebla sekikaic-acid species also show differences in branch shape and branching patterns that parallel those of salazinic-acid species. The sekikaic-acid species are discussed here to emphasize their distinctiveness from the more closely related divaricatic-acid species. Niebla cornea (sekikaic acid) and N. eburnea (divaricatic acid). Specimens of N. cornea (sekikaic acid) from San Clemente Island (Murbarger 151, COLO), Santa Cruz Island (Schuster 151A, COLO), Morro Bay (Hale 33688, holotype US) and near Bahía de San Quintín (Spjut 9329, US), are all remarkably similar in apothecial features of shape, number and distribution on terminally dilated branchlets; a beautiful photo of Niebla cornea in Brodo et al. (2001) shows the apothecia features very clearly. They differ notably in thallus size in which the larger thalli in the Channel Islands could be considered a distinct variety. Apothecia in Niebla eburnea seem to develop more solitarily, and can occur well below the branch apex. This species also includes larger much-branched forms, which could be placed under N. versiforma (divaricatic acid), whereas Niebla cornea includes morphotypes that are much like the divaricatic-acid N. laminaria. While one may argue that morphotypes of sekikaic-acid species shown under Niebla cornea appear to have their divaricatic-acid counterparts in N. eburnea and N. laminaria, there are morphological patterns that suggest that sekikaic acid species have also separately diversified in which several or more related species may comprise sister groups (e.g., Grube and Krogen 2000, Figs. 3–5). The close similarity in apothecial features on one hand for N. cornea among specimens collected from mainland California, Channel Islands, and Baja California near San Quintín, in comparison, on the other hand, to larger thalli of N. cornea in the Channel Islands, suggests that N. cornea is not just a chemical variant of N. eburnea; the larger or smaller thalli may be a derived feature from an ancestral morphotype. These differences could be treated as varieties, but were referred to as different forms in Spjut (1996). Another case in point is the differences seen in thallus branching among other sekikaic-acid species that exhibit an evolutionary trend from less branched to very-much branched; for example, Niebla siphonoloba (Channel Islands and Baja California) is characterized by having mostly monopodial branches, compared to much-branched thalli for N. dissecta (California and Channel Islands), becoming more intricately divided in N. dactylifera (San Nicolas Island), and highly branched without a distinct holdfast as associated with a terricolous habit for N. palmeri (Isla Cornado and Baja California chaparral region). These morphological-biogeographical relationships seem to be a product of evolution, not morphological plasticity caused by environmental factors. These relationships are reinforced by other partially correlated character features. The cortex of sekikaic-acid species is often conspicuously sinuate along the ridges, in contrast to the usual plane reticulate patterns in divaricatic acid species, and in some sekikaic-acid species, distinct cortical ridging patterns are characteristic for a species as already exemplified for N. siphonoloba in case number 3 above. Also, N. dactylifera is more similar in cortical features to N. siphonoloba in the Channel Islands than to divaricatic-acid species. Related sekikaic-acid species, however, appear variable in their cortical features (N. cornea, N. disrupta, N. dissecta). Another chemical-biogeographical difference between sekikaic-acid and divaricatic-acid species is seen in the pigmentation at the base of the thallus, often lacking in sekikaic-acid species and conspicuously present in divaricatic acid species. This has been noted for mostly Baja California species with few exceptions (Spjut 1996), whereas in California both chemotypes exhibit strong pigmentation at the base of the thallus. Besides morphological differences, there are ecological differences. In Baja California, sekikaic-acid species occur more on reddish volcanic rocks, or further away from the coast, in contrast to divaricatic-acid species that are more coastal, or found more on calcareous rocks in association with salazinic-acid species (Spjut 1996). It has been suggested that the chemo-morphological relationships of Niebla species in California are comparable to the zonation of chemical species in the Ramalina siliquosa complex along the Atlantic Coast of western Europe (Bowler & Marsh 2004), but the comparison made by Spjut (1996) was to the chemosyndrome species of Vermilacinia, namely, V. cephalota, V. cerebra, V. leonis and V. tigrina. The latter was noted to include four chemotypes, hypoprotocetraric, psoromic, nortstictic, and salazinic acids; two of the chemotypes are endemic to South America, but no taxonomic status was accorded to any of them. Thus, a strong case has been made for recognizing sekikaic-acid species as distinct from their divaricatic relatives, however, one may still question such paired species as N. disrupta (sekikaic acid) and N. homalea (divaricatic acid), N. testudinaria (divaricatic acid) and N. dissecta (sekikaic acid), N. spatulata (hypoprotocetaric acid) and N. flabellata (salazinic acid), and the isidiate N. usneoides (sekikaic acid) and N. isidiaescens (divaricatic acid). The methodology Spjut (1996) adopted was to provide a consistent taxonomic treatment unless evidence to the contrary exists. Because species are protean in their morphology, and because the chemotypes are clearly distinct, chemistry was given the most weight for classifying species of Niebla. Finally, it might be noted that many species morphotypes appear to have disjunct occurrences, while much of the problematic variation is often of local occurrence. Lohtander et al. (1998)—in applying molecular techniques—discovered genotypic differences among local populations of another Pacific coast lichen—Dendrographa leucophaea in which the most closely related genotype was not necessarily the thallus growing nearby—in the same habitat, but one at a more remote location, e.g., Punta Banda in Baja California Norte and San Nicolas Island in California. It is interesting that genotypic differences in Dendrographa leucophaea parallel chemo-differences in isomorphs of species of Niebla, e.g., N. laminiaria (divaricatic acid) at Punta Banda and San Nicolas Island, or N. cornea (sekikaic acid) in the Channel Islands and at Morro Bay (Spjut 1996). The following key applies only to the Baja California species where most of the 42 North American species are found. Additional species (unpublished) are further recognized with links to images of specimens. The images of specimens can be enlarged twice (smaller monitors), look for a square symbol to appear on the lower right corner and click on it; the close-up view that follows is comparable to seeing the specimen under a dissecting scope. The images are intended exemplify the wide variation in branching and the shape of branches seen in many species. Positive species identification requires identification of the secondary metabolites, usually by TLC (thin-layer chromatography). Chemical reagents used in spot tests such as PD or K are not reliable for distinguishing all species of Niebla and Vermilacinia, especially for the depside species subgroups of Niebla, the acid-deficient N. homaleoides, and most species of Vermilacinia.
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| Medulla with string-like (chondroid) strands; cortex with reticulate
ridging................................................
Niebla Medulla lacking chondroid strands; cortex mostly a granular sheath or crust......................................... Vermilacinia Niebla 1. Medulla PD+ (except N.
homaleoides); pycnidia prominent at apex of most
branches...................................... 2 Depsidone Species Group 2. Branchlets regularly shortly bifurcate near apex; apothecia usually
absent or rarely fully developed.....................
3 3. Branches mostly linear, or dilated more near apex than base; branchlets
geniculate; salazinic acid; 4. Branches and branchlets regularly divided dichotomously, whip-like and flaccid,
terminal branchlets wide
5a. Branchlets
teretiform; cortex mostly smooth; southern
half of Vizcaíno Desert............................N. marinii 5b. Branches irregularly widened and lacerated
from near base to apex, or
entirely flabellate............................. 6
6. Thallus brittle, usually saxicolous; branches strongly
compressed—more flattened than tubular prismatic, 7. Salazinic acid; common, Vizcaíno Desert, peninsular BCN and
Isla Cedros....................................
N flabellata 8a. Branches ±linear throughout, basal branches with many long
side branchlets—more than 2 mm long, 8b. Pycnidia conspicuous; key lichens substances absent (PD-); rare,
Punta Cono S to ridges 9. Salazinic acid; common terricolous lichen of desert and chaparral regions of
BCN...............................
N.
effusa Depside Species Group 10. Thallus with a distinct holdfast...................................................................................................
11 11. Branchlets mostly linear or whip-like, or thallus with many
spine-like branchlets, dilated parts, 12. Cortex mostly smooth, the surface appearing creamy, glazed or
glossy, occasionally with 13. Basal branches with numerous short to long side branchlets
that often break off, the main branches appearing 14. Branches irregularly prismatic,
branchlets often long, flagelliform or hair-like, remaining attached, or
15. Upper branchlets with one or two subterminal apothecia, or mature
apothecia more near base of thallus, 16. Cortex glossy with frequent transverse cracks; branches closely
fastigiate, long
linear, 1-3 mm wide, 17. Branches tubular prismatic, geniculate...........................................................................................
18
18. Cortical ridges curved to straight, not
sinuous; divaricatic
acid............................................. N.
testudinaria 19. Isidia conspicuous, short cylindrical,
usually densely covering the thallus..................................................
20 20. Sekikaic
acid............................................................................................................
N. usneoides 21. Pycnidia abundant from near base to apex; sekikacid acid; rare,
endemic to Mesa Camacho area........ N. tesselata 22. Cortex prominently transversely and/or reticulately
ridged..................................................................
23 23. Thallus with small tufts of basal branches, usually less than 20,
these occasionally divided........................... 24 24. Branches tubular near base, tubular to strap-like
above......................................................................
25 25. Upper half of branches with complete transverse cortical ridges
between margins; 26. Cortex with prominent sinuous reticulate ridges, the transverse
ridges between branch margins joining a main 26a. Cortex with longitudinal
oriented sinuous ridges; branches sharply angled; apothecia laminal; basal branches 27. Sekikaic
acid..............................................................................................................
N. lobulata 28a. Thallus rigid, the cortex relatively thick; divaricatic
acid....................................................... N. laminaria 28b. Basal branches tubular prismatic near
base with prominent reticulate ridges, expanded to
30. Sekikaic
acid.............................................................................................................
N. lobulata 31. Isidiate or sorediate; Isla
Guadalupe 32. Branches mostly strap-like, linear to oblong (mostly
California).............................................................
33 33. Branches with various marginal features
extending from apex to below mid region, with short lobes 34. Thallus brittle; cortex relatively thin with sharply
defined ridges.............................................N. caespitosa 35. Thallus with short, rounded, constricted, lobes along
margins of main branches; Isla Guadalupe, 36. Apothecia in dense terminal aggregates on well-developed
tubular branches, often aborted in 37. Cortex appearing glazed or creamy, branches twisting mostly near
base and apex, straight or recurved 38. Apothecia when present becoming more developed towards apex,
in small subterminal to terminal 39. Branches sharply twisted in mid region, fringed to
lobulate along margins to below mid region...........
N. laminaria 40. Thallus with well-developed tubular branches near base, 4–10 cm long; divaricatic acid............................... 41 41. Thallus of
erect rigid branches, the branches remaining intact to near
apex......................
N. infundibula 40. Thallus mostly of strap-like undulate branches 2–6 cm long.................................................................. 42
42. Sekikaic
acid..........................................................................
N. lob 43. Sekikaic
acid..............................................................................................
N. palmeri
44. Branches strongly dilated near
base.............................................................................
N. versiforma
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Outline of Key Characters by Chemotype Triterpenes with Depsides Divaricatic Acid 1. Cortex thick, > 75µm thick, and medulla solid to subfistulose. 2. Branching mostly regular; dichotomous, or somewhat digitate in some N. testudinaria.
Niebla eburnea: Branches variable, 2-5 (-10+) mm wide, generally
sub-elliptical in 2. Branching irregular, usually with fragmentation branchlets, or margins lobulate to nodular.
Niebla infundibula: Main branches somewhat oblong, 2-10 mm wide,
margins entire to nodular,
Niebla laminaria: Branches variable; margins nodular to crenulate or
incised, rounded; 1. Cortex thin, < 75µm thick, or medulla fistulose to subfistulose. 3. Branches flattened (more than twice as wide as high).
Niebla caespitosa: lobes deltoid to
spinuliferous; margins thin. Related chemotype species: 3. Branches prismatic to elliptical in x-section. 4. Soredia or isidia Niebla isidiaescens: Isidia only. Related chemotype species: N. usneoides. Niebla sorediata: With isidia and/or soredia. 4. Soredia or isidia lacking
5. Thallus
bushy, generally >6 cm high or broad, basal branches
Niebla sorocarpia: Apothecia in beadlike
aggregates.
Niebla juncosa:
Branchlets mostly straight, spinuliferous, elliptic in x-section.
Niebla turgida: Branchlets
geniculate, twisted, sharply prismatic. Related
Niebla versiforma:
Holdfast not evident, branchlets arising from a dilated branch
5. Thallus
not bushy, usually <6 cm high or broad; basal branches 6. Branchlets linear, arcuate or flagelliform Niebla flagelliforma: Related chemotype species: N. tesselata. 6. Branchlets ligulate or oblong, or irregularly widened
Niebla contorta:
Thallus < 3.5 cm high; cortex with features intermediate
Niebla podetiaforma: Monopodial or
irreguarly branched; branches or
Niebla rugosa:
Mostly monopodial, branches somewhat folded Sekikaic Acid Medulla solid; cortex firm, glazed to glossy
Niebla cornea:
Branches monopodial to digitately divided from dilated segments near apex,
Niebla disrupta: Branches regularly dichotomous or trichotomous,
ultimately long flexuous
Niebla dissecta:
Branches much divided dichotomously, sometimes digitately
Niebla palmeri:
Branches irregularly much divided without a holdfast, terricolous. Medulla fistulose to subfistulose; cortex usually wrinkled or foveolate
Niebla
dactylifera: Branches much divided more near apex than
base, short bifurcate
Niebla siphonoloba:
Branches monopodial to occasionally divided near apex, usually
Niebla tesselata:
Branches monopodial, tapered to apex; pycnidia densely covering Niebla usneoides: With isidia. Related chemotype species: N. isidiaescens.
Niebla suffnessii:
Branches dichotomously divided, terminally more divided into
Niebla fimbriata:
Branches with spinuliferous branchlets arising from near Niebla lobulata: Branches flattened, incised to lobulate. Related chemotype species: N. undulata. Terpenes Absent Acid Deficient (No Depsidones) Depsidones Protocetraric acid Hypoprotocetraric acid
Niebla spatulata: Branches
flabellate, lacerated; cortex thin. Salazinic acid Terminal branchlets shortly bifurcate Niebla arenaria: Branches mostly linear-prismatic Niebla limicola: Branches flabellate or irregularly dilated Terminal branchlets spinuliferous or of lacerated segments Branchlets mostly linear-prismatic throughout
Niebla
josecuervoi: Branches with spinuliferous branchlets Branchlets with dilated parts, or if linear, strongly flattened Niebla flabellata: Branches flattened, lacerated, variable in shape, saxicolous Niebla effusa: Branches prismatic and terminally dilated and fringed (digitate-like branching)
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Plate 3D and 3E. Niebla caespitosa. Re-identified here as N. dilatata. This was considered endemic to Isla Guadalupe, but I have since recognized this from thalli collected on the main peninsula of BCN. Pages 50, 59. Keys. Vermilacinia tuberculata. Riefner (1995) indicated this species was lacking in a key terpene, which Spjut interpreted to be the diterpene, [-]-16 α–hydroxykaurane, one that would be a significant chemical deficiency for the subgenus Vermilacinia; however, after publication, Spjut discovered the specimen by Gittens 4286, cited on page 159, had been determined by him, from TLC, to have this diterpene. Evidently, Riefner was referring to zeorin, a triterpene that was noted in the above publication by Spjut to sometimes occur in trace amounts in other saxicolous species, particularly V. combeoides. The distinction of V. tuberculata from earlier published V. ceruchoides is, therefore, based strictly on the morphology. Spjut had earlier included V. tuberculata under V. ceruchoides. Additionally, Spjut and Marsh also questioned whether V. tuberculata was distinct from V. ceruchoides in April 1996. Spjut did not have the opportunity to study the anatomical features of V. tuberculata. The main obvious morphological difference was noted to be thallus size; V. tuberculata being notably larger than V. ceruchoides. Page 138, photo 36.2. Niebla suffnessii. The collection number should be 9565, not 9965. Page 159. Vermilacinia ceruchoides, specimens cited, Riefner 86-30 (COLO: L-80765) from Morro Bay State Park. This was annotated by Spjut as V. tuberculata. Note: This specimen contains [-]-16 α–hydroxykaurane. Pages 163-164. Authority for Vermilacinia laevigata. The parenthetical authority should be Bowler & Rundel, not Rundel & Bowler. Pages 166-167. The type for Vermilacinia paleoderma was indicated on page 7 to include the holotype in US with isotypes sent to BCMEX and LA. Under citation of specimens. Moran 6852 (COLO: L-31117) from San Clemente Island was annotated by Spjut as V. robusta. Weber & Santesson (COLO: 42152) from Santa Catalina Island was annotated by Spjut as V. polymorpha. Gittens 4286 (COLO: L-58464) from Santa Barbara Island was annotated by Spjut as V. polymorpha. Note: Vermilacinia polymorpha is distinguished from V. paleoderma by its oblong contorted branches. Vermilacinia polymorpha has relatively small thalli with sharply folded lobes as opposed to the folds being more rounded in V. robusta. The above publication, while in press (with a copy to G. Follmann), had included V. cedrosensis and V. polymorpha under V. paleoderma, noting that some of the variants could be recognized as distinct species. Based on publications by Dr. Thomas Nash III and his associates, Spjut decided to recognize the variants, especially since Spjut had recognized V. cedrosensis in Dec. 1987 under another name (V. albicans Spjut ms ined.). He later included this under V. paleoderma as a result of Mason Hale's review of Spjut's first draft (Dec. 1987), a computer key generated from data coded in DELTA format. Dr. Hale questioned whether V. cedrosensis (as V. albicans ined.) was distinct from V. paleoderma. His review included the specimens, and he also commented that the distinction between the groups of Niebla were of major significance with regard to the presence and absence of chondroid strands. Spjut, being influenced by Dr. Hale's comment, decided to recognize a new genus, Vermilacinia, to which he attributed also to Hale as a coauthor (Spjut 1995). Pages 168-169. Authority for Vermilacinia procera. The parenthetical authority should be Rundel & Bowler, not Bowler & Rundel. |
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Axelrod, D. I. 1975. Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Ann. Missouri Bot. Gard. 62: 280–334.
Bowler, P.A. 1981. Cortical diversity in the
Ramalinaceae. Canad.
__________ & P. W. Rundel. 1978. Two new
lichens (Ramalina)
__________, R. E. Riefner, Jr., P. W.
Rundel, J. Marsh & T.H. _________ & J. Marsh. 2004. Niebla. Lichen Flora of the Greater Sonoran Desert 2: 368–380. Bridge, P. D. & D. L. Hawksworth. 1998. What molecular biology has to gell us at the species level in lichenized fungi. Lichenologist 30: 307–320 Brodo, I, S.D. Sharnoff & S. Sharnoff. 2001. Lichens of North America. Yale University Press, New Haven and London.
Culberson, C., W. L. Culberson & A. Johnson.
1990. The Ramalina
Follmann, G. 1976. Zur Nomenklatur der
Lichenen. III. Uber Grube, M. & S. Kroken. 2000. Molecular approaches and the concept of species in lichenized fungi. Mycol. Rev. 104: 1284–1294. Hale, M. E. & M. Cole. 1988. Lichens of
California. University
Howe, R.H., Jr. 1913. North American species of the genus
Krog, H. & H.
Østhagen.
1980. The genus Ramalina Lohtander, K., L. Myllys, R. Sundin, M. Kllersj, and A. Tehler. 1998. The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): Analyses based on ITS Sequences. Bryologist 101: 404–411. Lumbsch, H. T. 1998. The use of metabolic data in lichenology at the species and subspecific levels. Lichenologist 30: 357–367.
Marsh, J. & T.H. Nash, III. 1994. A
new lichen species, Niebla
Montagne, D.M.1852. Diagnoses
phycologicae. Ann. Sci. Nat. Nash, T. H. III, 1995. Arizona State University, Letter to Richard Spjut, Nov 15.
Nylander, W. 1870. Recognitio
monographica Ramalinarum. Bull.
Riefner Jr., R. E., P. A. Bowler, J. Marsh &
T. H. Nash III. 1995.
Rundel, P.W. 1978. Evolutionary
relationships in the Ramalina usnea complex. Lichenologist
10:141-156.
Rundel, P.W., P.A. Bowler & T.W.
Mulroy. 1972. A fog-induced
Rundel, P.W. and P.A. Bowler, 1978.
Niebla, a new generic name
Shreve, F. 1936. The transition from desert
to chaparral
_________. 1964. Vegetation of the
Sonoran Desert. Pp. 26-126 Smithsonian Institution. 1990 (Jan. 9). Letter from the Director of the Natural Museum of Natural History to Dr. Richard Spjut indicating renewal of his appointment as Associate and Collaborator, with particular emphasis on Dr. Spjut's study of the lichens of Baja California.
Spjut, R. W. 1995. Vermilacinia (Ramalinaceae,
Lecanorales), _________. 1996. Niebla and Vermilacinia (Ramalinaceae) from California and Baja California. Sida, Botanical Miscellany 14: 1–207, 11 plates.
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