Niebla and Vermilacinia of Baja California

©The World Botanical Associates Web Page
Prepared by Richard W. Spjut
April 2003, updated Jan. 2004, revised Nov. 2005
Comments and Distribution Maps added under species pages, Nov. 2005
Expanded with reference to molecular studies, Sep 2012.

Niebla and Vermilacinia (Ramalinaceae) from California and Baja California.  
Spjut, R.W., 1996. ISSN 0833-1475, 208 pp.  
Sida, Botanical Miscellany: 14. Botanical Research Institute of Texas, Inc.
Review at www.botany.org/bsa/psb/1997/rev25-97.html 

 

Introduction

Species Identification and Concept in the Genus Niebla

  Divaricatic-acid species
  Salazinic-acid and related species
  Sekikaic-acid species

Morphological key: Species in Baja California

Outline of Key Characters by Chemotype for all species of Niebla

Corrections

References

 

Introduction

     Niebla and Vermilacinia are fruticose lichens that occur along the Pacific Coastal fog region of North America from southeastern Alaska to southern Baja California. Vermilacinia also occurs in South America from Peru to Chile. The above publication describes 70 species, 42 in Niebla and 28 in Vermilacinia; 27 are endemic to North America; two are endemic to South America (V. ceruchis, V. flaccescens).  Vermilacinia is divided into two subgenera, Vermilacinia and Cylindricaria.  Subgenus Vermilacinia includes V. ceruchis in South America, and 16 species in North America.  Subgenus Cylindricaria includes 10 species, three of which occur in both North America and South America (V. cerebra, V. leonis, V. leopardina).  Additional published and unpublished species are recognized in both genera on this website. 

     Vermilacinia was segregated from Niebla (Spjut 1995) by its secondary metabolites, predominantly terpenes, specifically the triterpene zeorin and the diterpene [-] -16 α-hydroxykaurane, and by the thallus morphology of the medulla lacking chondroid strands (longitudinal sclero-proso-plectenchymatous hyphae) The specified terpenes do not occur in Niebla. The medulla of Niebla has numerous chondroid (string-like) strands within a more freely branched network of periclinal hyphae. 

     The two genera (Niebla, Vermilacinia) and two subgenera of Vermilacinia (Cylindricaria, Vermilacinia) are recognizable by external morphology in addition to anatomical and chemical differences just mentioned.  Niebla has longitudinally oriented rib-like cortical ridges that support the upright habit ('backbone'), especially along branch margins where they unite, separate, and interconnect by cross ribs (transverse cortical ridges), and pycnidia confined to cortical ridges.  Vermilacinia subgenus Vermilacinia occasionally has well-defined  margins (V. johncassadyi, laevigata, V. rigida) but cortical ridges, which seem related to densely compacted bundles of hyphae in the outer medulla, do not always align with margins. The knot-like bundles of hyphae are evident in species of Vermilacinia with cylindrical branches by the cortex appearing bumpy (e.g., V. combeoides), or recessed between a reticulate network of ridges (e.g., V. paleoderma).  The branches of subgenus Vermilacinia, which lack chondroid strands, are further supported by a triangular (Hasse) lattice of medulla hyphae.  In North American subgenus Cylindricaria, stellar knots of hyphae develop throughout the medulla interconnected by much longer longitudinal fascicles of intertwining hyphae, similar to patterns created in “hand string games.”  This type of construction allows for collapse of the cortex and medulla during desiccation and expansion during hydration; the cortex of the dehydrated thallus of V. corrugata, for example, can appear like a honeycomb.  Pycnidia in Vermilacinia often develop in recessed areas (areoles) between cortical ridges as well as along cortical ridges.

     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 laevigata] appears to correspond to any of the seven substances in its congener, N. homalea.”  Each genus exhibits different evolutionary patterns in speciation (adaptive radiation).

    Niebla has also been interpreted to occur in the Mediterranean where it has been segregated from Ramalina by the  free medullary chondroid strands (Rundel & Bowler 1978; Spjut 1995, 1996); however, the basis for three name combinations later made by Bowler and Marsh (2004) for the Mediterranean Niebla in the Greater Sonoran Desert Lichen Flora contradicts their taxonomy for the North American Niebla since these authors also feel that the character attribute of isolated medullary chondroid strands does not justify generic separation of Vermilacinia from Niebla (see Review).  The Mediterranean species also appear related to Vermilacinia (subgenus Cylindricaria) by their secondary chemical substances of fatty acids (bourgeanic acid), and various depsidones, instead of just having one depsidone; however, the diterpene  [-]-16 α–hydroxykaurane has not been reported in the Mediterranean species.  North America Niebla and Vermilacinia are usually distinguished by the black pycnidia, in contrast to pale pycnidia of Ramalina, except the Macaronesian Ramalina portosantana, which is similar to Niebla josecuervoi but has pseudocyphellae as in Ramalina, not Niebla (Spjut 1995).  

     The morphological distinction between Niebla and Ramalina is further blurred by molecular data in one study that showed the “bourgeana clade” derived from within Ramalina, in contrast to a separate (sister) Niebla and Vermilacinia clade (Sérusiaux, van den Boom & Ertz 2010); however,  the ~30 species of Ramalina in the study were collected largely from Europe and Atlantic islands (one from Rwanda), and of the six species collected in North American, five were in the genus Vermilacinia; the one “N. homalea” from California is questionable since it was indicated to have protocetraric acid and triterpenes, a chemo-profile not previously known for that species, or for the genus (sensu Spjut 1996). No American species of Ramalina and no South American species of Vermilacinia were included in this study.  It should be noted that in Bowler and Marsh (2004), there appears to be a 'word-processing error' in mentioning protocetraric acid and other depsidones in their description of N. homalea; the authors also stated that these chemotypes belong to N. josecuervoi, which does not occur in California. 

     Another  molecular study (unpublished, Seelemann) on “[t]he distribution of multiple group I introns in nuclear ribosomal RNA in species of the lichen genera Ramalina and Niebla,” the sequences of “N. homalea” and “N. laevigata” deposited online appear so similar, in sharp contrast to that of “N. ceruchis,” that the species identifications are also questionable. 

     Additionally, many images presented on the Internet and  identified according to the Bowler and Marsh (2004) taxonomy are not correct (according to their classification); examples include misidentifications for Niebla isidiaescens, Niebla homalea, and others. A truly objective molecular study should obtain DNA of a species from more than one location as well as from multiple species that includes more than one chemotype. Photographs should be presented of the voucher specimens not of unrelated images obtained by others that have nothing to do with the study (e.g., Stephen Sharnoff  in Sérusiaux, et al. 2010), and identifications should also be compared to Spjut (1996) taxonomy.

     Biogeographic relationships that are evident between the North American and Mediterranean species of the ramalinoid complex may relate to a time when the Mediterranean floras diversified in each region (Axelrod 1975).  This is in contrast to Vermilacinia with biogeographical ties to South American species (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 differentiated morphologically.  Most are polymorphic as evident by a wide range of morphotypes referred to as 'variants'.

     Two subgenera of Vermilacinia are distinguished by thallus morphology as explained above, corresponding to the substrate upon which they grow; subgenus Vermilacinia has 18+ species that are largely saxicolous (also terricolous in South America), whereas subgenus Cylindricaria has 10+ corticolous species (also terricolous in South America).  Subgenus Vermilacinia is more diverse morphologically in California and more diverse chemically in Baja California.  Cylindricaria is more chemically diverse in South American than in North America.

     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, 28 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 further south to ridges above 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

     California has seven endemic species, Niebla dactylifera, N. disrupta, N. dissecta, N. halei, N. ramosissima, Vermilacinia polymorpha (?), and V. tuberculata.  Additional endemic species might be recognized in future studies, especially south of Monterey County and in the Channel Islands.  Diverse assemblages of species in both Niebla and Vermilacinia occur in Point Lobos State Reserve.

     The islands along the Pacific Coast are generally less diverse in Niebla, although richly represented in species of Vermilacinia. This may relate to more localized occurrences of inland (orographic) fog in regard to Niebla, in contrast to Vermilacinia species 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, one undescribed).  Most species were found on the foggier northwest coastThe 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, Niebla and Vermilacinia species are more frequently found on mainland California than in Baja California, and include endemic Niebla dactylifera and N. ramosissima on 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, and N. marinii near Morro Santo Domingo California.

Species Concept and Identification in the Genus Niebla

     Species Concept. Spjut (1994) presented a paper titled: “What is a species of Niebla?  In the abstract (American J. Botany) he stated “a broad diversity of morphotypes is evident and best classified when segregated according to the different chemotypes; morphological classification
criteria include differences in development of isidia, soredia, holdfast, fragmentation branchlets, thallus size, cortical ridging, and uniformity in shape of branches. Because differences appear significantly greater according to chemical criteria, it is felt that taxonomic emphasis should be placed on chemical differences in defining species even though lichenologists traditionally consider morphology to have greater taxonomic significance.”

     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, he (Spjut 1996) was able to differentiate them morphologically.  He compared the morphological variation within a species to recognizing the painting style of an artist, or to that of a large genus of plants such as Eriogonum, which is well-known for its wide diversity of reproductive (inflorescence) branching patterns that define the species.  This is in contrast to Bowler and Marsh (2004) who were unable to differentiate or accept morphological species of Niebla (sensu Spjut 1995, 1996); they recognized two chemical species, N. homalea and N. josecuervoi, which in their reality represent super chemosyndrome species of depsidones and depsides (but wrongly assigned the acid-deficient species, N. homaleoides, to the depside group), and one isidiate species, N. isidiaescens.

     The delimitation of Niebla species in Spjut (1996) is also 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.

     Niebla appears to have evolved various types of thallus branches for dispersing spermatia, ascospores and asexual thallus parts.  For example, Niebla flagelliforma is recognized by flagelliform branchlets that are densely covered with pycnidia. A branchlet of this species has a thinner cortex than the lower primary branch, thus, dispersal of spermatia (from pycnidia) may occur more readily by fragmentation of the pycnidia branchlet. Niebla flagelliforma thalli with apothecia, on the other hand, have fewer flagelliform branchlets, perhaps  they are dimorphic in the dispersal and reception of spermatia. Unfortunately, lichenologists have yet to directly determine how lichen sexual reproduction occurs in the wild.  But the circumstantial evidence for sexual reproduction and hybridization in Niebla is evident for many species.

     Isidia and soredia, which are common in many lichen genera, are uncommon in Niebla, while most species have pycnidia and/or apothecia; however, similar types of asexual reproductive parts are evident.  Besides the flagelliform branchlet, isidia-like branchlets, referred to as acicular branchlets, terminate the thallus in species such as N. arenaria.  They are often tipped with black pycnidia, particularly in species that contain depsidones.  In other species, apothecia apparently abort development and become soralia-like along branch margins similar to the true soralia in species of Parmotrema.  Another example is N. sorocarpia that has dense aggregate isidioid (nodular) apothecia on terminal branchlets, and also terminal pycnidia branchlets that are spike-like without a cortex. These kinds of branchlets may function for asexual as well as for sexual reproduction.

      The wide diversity of morphotypes in Niebla is suggested to be a product of frequent genetic exchange within local communities of Niebla species followed by geographical fragmentation into separate communities as climate changed perhaps since the Paleogene.  Coastal fog, for example, might develop or become blocked by continental uplifting, and fog has likely shifted northwards and southwards during glacial cycles since the Pliocene.   Niebla communities are not continuous along the Pacific Coast; rather, they are of localized but frequent occurrence.  Niebla communities that become isolated may also reconnect, leading to perhaps hybridization between formerly disjunct species.  Indeed, each Niebla community is unique in terms of its total characterization of morphotypes and chemotypes. 

    As exemplified under Niebla testudinaria, the more widely distributed species of Niebla are viewed as plesiomorphic character traits from which variants possibly further evolved, but are not formally named because they also appear in some cases to be 'hybrids' (e.g., see N. homaleoides).  In the angiosperm genus Eriogonum, varieties are recognized for many of its ~250 species, E. umbellatum, for instance, has 41 varieties (Reveal, Flora North America 5. 2005).  But for the variable species of Niebla it does not seem useful at this time to formally name "variants"  (or 'morphs') with the exception of N. juncosa var. spinulifera.

     Species of Niebla that are more restricted geographically are viewed as ancestral or derived types with unique character traits.  An example of an ancestral type is the development of numerous conspicuous pycnidia along the entire branch of N. tesselata rather than on specialized fragmentation branchlets; it is known from the type locality near Mesa Camacho and nearby Mesa San Carlos in northern Baja California.  Its monopodial branches are similar to the widely distributed N. siphonoloba, which produces pycnidia in the upper third of its branches, in addition to subterminal and terminal apothecia.  Endemic to San Nicolas Island is N. dactylifera that appears to be an evolutionary derived (apomorph) species in a 'tesselata' lineage, characterized by a thallus that is increasingly branched towards apex, without apothecia and with pycnidia only near the tips of the branchlets. Intermediate to these species is N. dissecta, a species found in the Channel Islands and along the California coast mainland; it has scattered pycnidia on primary and upper branches.  These species all have sekikaic acid and similar cortical features, further evidence of being more closely related to each other than to other monopodial branch species such as Niebla homalea, which contains divaricatic acid.

    Clinal relationships are also evident within species such as Niebla limicola that appears to exhibit wider branches going from north to south in Baja California. This is viewed as another example of evolutionary change, not random plasticity or hybridization.

     Other rare species such as Niebla ramosissima on San Nicolas Island and N. versiforma near San Antionio del Mar (BCN) were recognized for their unusual combination of character traits.  Both are terricolous and contain divaricatic acid. Niebla ramosissima differs in having a flaccid thallus divided into numerous filamentous branches with few apothecia and few pycnidia just below the branch tips. Niebla versiforma, in contrast, has stiff ribbon branches with abundant apothecia and pycnidia. They appear related to another rare terricolous species, N. palmeri, found on Isla Coronado and the Baja peninsula north of Punta Baja, characterized by the lichen substance sekikaic  acid and by rigid ribbon-like branches with pycnidia only at branch tips.  These species are perhaps relicts of former depside terricolous Niebla communities that were once common in California coastal chaparral desert transition vegetation. 

    Putative hybrids are evident in one Niebla community that included N. homaleoides, N. infundibula, and N. josecuervoi on a ridge south of Punta Negra in Baja California.  As shown on the N. homaleoides page, they are remarkably similar in their smooth glossy cortex and branching, while the only clear differences were in their chemistry, N. homaleoides with no major lichen substances, N. infundibula with divaricatic acid, and N. josecuervoi with salazinic acid.  Because twelve of the thirteen thalli shown for N. josecuervoi  from other locations all have a dull reticulated cortex, the circumstantial evidence is strong that gene exchange has occurred among these species. 

     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.

     Six examples are discussed below to help one grasp, on one hand, the taxonomic complexity, and on the other, the character features that distinguish the species of Niebla.   These are according to chemotypes; divaricatic-acid species with one comparison to a sekikaic-acid species, followed by a discussion of the salazinic-acid species and then by the sekikaic-acid species.

Divaricatic-acid species of Niebla

      Many divaricatic-acid species of Niebla are recognized by differences in cortical features.  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 in order to rise above the surface. 

             1. Niebla podetiaformaThis species is perhaps the easiest to comprehend in the genus and easiest to recognize without TLC data.  It includes an obvious morph ('variant') characterized by strongly inflated branches (center photo in top row, Spjut 11301) in which the medulla is loosely filled with hyphae within a relatively thin cortex (< 75µm thick). This variant (morph) frequently occurs on pebbles along the Pacific Coast of southern Baja California Norte (BCN).  Despite its obvious  distinctive 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 that is often distinguished from others in the genus by its inflated stems, but the species is also recognized with deflated (normal) stems.  A photo of N. podetiaforma by F. Bungartz  is shown in the Lichen Flora of the Greater Sonoran Desert Region, Vol. 2, identified as N. homalea. Most variation shown for Niebla podetiaforma occurs throughout the range of the species in Baja California.   

      2.  Niebla undulata and N. rugosa compared to N. podetiaforma.  Cortical ridges of N. undulata near apex of branchlets are oriented longitudinally to diagonally with the apical region of the branch twisting and with the branch margins undulate.  Transverse ridges are also evident along branch margins. Cortical ridging in Niebla podetiaforma, in contrast, is more strongly 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 and often complete between branch margins;  consequently, the branches fold slightly like an accordion, a distinct character attribute of this species. 

     Niebla undulata can also be recognized by the bluish green color and the cortical surface appearing more deeply recessed between ridges in comparison to yellowish green bulging (inflated) cortical surface of N. podetiaforma.

      Niebla undulata exhibits a wide range in variation in the thallus habit and in the shape of the branches.  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). Branches may be ribbon-like and channeled or tubular  near base  and ribbon-like above. The ribbon-like portion is usually undulate and thickened along margins.

     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.

     The epithets were often 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.

     3.  Niebla siphonoloba sekikaic acid compared to N. rugosa  divaricatic acid.  While some might treat these two species as chemical variants or races of one  species defined by mostly simple branches with prominent reticulate ridging, the cortical ridging is not the same. Transverse ridges of N. rugosa are often complete between the marginal or intermarginal longitudinal ridges, whereas they are more interconnected (reticulate) between margins of N. siphonoloba .  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.   Another 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 (skyrin) 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.  The upper branches of Niebla rugosa are sharply  3–4 angled, in contrast to appearing more uniformly prismatic 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.  

     4.  Niebla caespitosa and N. dilatata (divaricatic acid).  These are tortilla chip Nieblas, also regarded as pebble lichens because they are often found on pebble-size rocks along beaches and slopes.  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.  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.

     5.  Niebla juncosa and N. turgida.  In 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 because they usually produce many fragmentation branchlets along a primary branch. Niebla juncosa has well defined strap-like branches related to less twisting in contrast to N. turgida branches with less defined margins due to more frequent twisting.  Another difference is that the cortex is relatively smooth on upper branches of N. juncosa in contrast to sharply reticulate in N. turgida. 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, 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.  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 growing in a cooler northern climate.  As a result, the branches appear rigid and less crinkled or wrinkled on the cortical surface. These species include more variation than the preceding examples. The "variants" are classified in dendrograms for N. eburnea and N. testudinaria.  The alternative of lumping them only makes it harder to separate any species in the genus.  

     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 as seen in CalPhoto images of “Niebla homalea.”

     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. Another difference is that branches do not divide equally in N. homalea, or branches do not divide at all (monopodial branches).  Branches generally are ± of equal length in N. testudinaria, evident near apex where they shortly bifurcate.

      Niebla eburnea is identified by the ivory-like or creamy cortex appearing thicker along margins, and often by less twisted branches, half twisted near base and again near apex than in the mid region.  It shows a wide range in variation in branch shape and other cortical features such as having transverse cracks. Some thalli with relatively narrow branches that have transverse cracks at various intervals might be considered N. homalea; however, the branch margins often have nodular apothecia, whereas apothecia in N. homalea are usually solitary on the upper branches along a short wide branch-like extension.  Another variant with expanded lobes is similar to N. sorocarpia, which differs in its darker green cortex and lack of transverse cracks.  In identifying an individual specimen, it  helps to look at examples of species variation ('variants').

     Characteristics of other divaricatic-acid species are summarized in Spjut (1996) and on other web pages following presentation of images.  As noted above, 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. This might be compared to other rarities, N. dactylifera (sekikaic acid) and N. ramosissima (divaricatic acid) on San Nicolas Island.

    Cortical features in many divaricatic-acid species of Niebla are given more weight than in other chemical species subgroups.  Generally, salazinic acid and sekikaic acid species differ in habit and branching, whereas sekikaic acid species show further differences it apothecia position on the thallus (maturing more near base vs. apex) and shape (cupular vs. lenticular).  Evolution of metadepsides from paradepside precursors has been suggested for the Ramalina americana complex (C. Culberson et al. 1990).  This also seems evident in Niebla in which cortical differences appear pleisiomorphic to other derived features among divaricatic-acid species (e.g., see N. testudinaria), while also overlapping with seikikaic-acid species (e.g., N. homalea and N. disrupta; N. siphonoloba which may have given rise to N. dissecta and hybridized with N. testudinaria).

Salazinic-acid and Related Chemotype Species

     The salazinic-acid species of Niebla are classified under a Terpenoid Deficient or Depsidone Species Group that includes one species (N. homaleoides) lacking key metabolites (Spjut 1996).  The key metabolites in the Depsidone Subgroup are salazinic acid, hypoprotocetraric acid, and protocetraric acid.  Species differences in this group are seen mainly in the lichen substances, habit, branching patterns, and branch shape.

     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). These branchlets appear comb-like (or pectinate). Other variants with erect ± straight branches are recognized as N. josecuervoi Niebla marini, which lacks fragmentation branchlets, has primary branches divided into similar secondary branches (isotomic branching), which are all narrow and whip-like, and frequently bifurcate terminally into horseshoe like branchlets.  Niebla arenaria and N. limicola are more intricately branched terminating in short antler-like or bifurcate  (two-pointer) branchlets; N. arenaria has narrow basal branches in contrast to the flabellate thallus of N. limicola Niebla flabellata is similar to tortilla-chip Niebla caespitosa, but exceedingly variable in shape of branches, and  includes nearly linear branch forms similar to N. flagelliforma.  These are divaricatic-acid species; thus, identifying the lichen substances helps identify the species.

     The other depsidone species, and one acid-deficient species of Niebla, are relatively rare. They are 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.  Niebla brachyura occurs from near Punta Santa Rosalillita to Punta Canoas, and the only 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. One additional undescribed chemically deficient species is shown under N. homaleoides, but not included in the key.

     Although the cortical features of salazinic-acid species vary more, compared to divaricatic-acid species, exceptions, which may have taxonomic significance, include Niebla marinii that is typically smooth and glazed, in contrast to prominent ridging in N. josecuervoi, N. flabellata and provisional N. angulata.  The latter has sharp sinuous ridges often associated with sekikaic acid species, and it is interesting that it occurred with the unpublished sekikaic-acid species, N. sinuata; both endemic to Mesa Camacho.  These close associations of rare character features in chemically different species is also presented for a threesome involving N. homaleoides. What is remarkable is that while drastically different morphotypes can occur together with the same chemotype, one also finds two, three (or more) identical morphotypes belonging to different species occurring together represented by depsidone and depside chemotypes.

Sekikaic-acid Species

     Sekikaic and divaricatic acid  are similar chemical structures that  are often viewed as replacement chemotypes or chemical races of a species in a related genus Ramalina (Krog & Østhagen 1980; Lumbsch 1998; Rundel 1978) and suggested for Niebla (Bowler et al. 1994, N. isidiaescens in Baja California).   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.  An examples was discussed above for N. siphonoloba and N. rugosa.

     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 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 may develop solitarily, near branch apices or may develop further down the branch in aggregates.  This species also includes larger much-branched forms similar to N. versiforma (divaricatic acid), whereas Niebla cornea includes morphotypes that are much like the divaricatic-acid N. laminaria

     While morphotypes of  Niebla cornea appear to have their divaricatic-acid counterparts in N. eburnea and N. laminaria, there are morphological patterns within species that suggest lineage evolution 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 ridge patterns are characteristic for  a species as already exemplified for N. siphonoloba in case number 3 above.   Other sekikaic-acid species, however, appear variable in their cortical features (N. cornea, N. disrupta, N. dissecta) but further studies may sharpen the species parameters.

     In addition to 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 (V. tigrina) 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.  

     Nevertheless, sibling species appear evident between Niebla spatulata (hypoprotocetaric acid) and N. flabellata (salazinic acid) and in the genus Vermilacinia subgenus Vermilacinia  between V. paleoderma and V. reptilioderma, and between V. rosei and V. varicosa. 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 (Spjut 1994, 1996).  Niebla thalli are not always picky about who they share their chemistry or their physical attributes with in their promiscuous life style.  In questionable cases of identification, the lichen substance is the more reliable taxonomic character.

    Finally, the significance of the Niebla species concept is further evident by observation that many species morphotypes appear to have disjunct occurrences, while much of the problematic variation is 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 emphasizes the Baja California species where most of 42 North American species are found. Additional species (unpublished) are further recognized with links to images of specimens. Positive species identification requires identification of the secondary metabolites, usually by TLC (thin-layer chromatography) or HPLC.  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

        

Key

 

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
1.  Medulla PD-; pycnidia inconspicuous or absent at apex of most branches, although often prominent 
        along branch margins............................................................................................................... 10

Depsidone Species Group

2.  Branchlets antler-like near apex; apothecia usually absent or rarely fully developed........................................ 3
2.  Branchlets fringed, whip-like, ribbon-like, torn or with rounded lobes near apex; apothecia present or absent........ 4

3.  Branches mostly linear, or dilated more near apex than base; branchlets geniculate; salazinic acid; 
        common
.................................................................................................................. N. arenaria
3.  Branches with flattened and dilated parts from near base, terminating in crispate bifurcate branchlets; 
        salazinic acid; common
................................................................................................. N. limicola
3.  Branches with either of the preceding key features but with hypoprotocetraric acid; rare................ N. brachyura

4.  Branches and branchlets regularly divided dichotomously, whip-like and flaccid, terminal branchlets wide 
        spreading, horseshoe like; salazinic acid....................................................................................... 5a
4.  Branches irregularly divided or lacerated; branchlets in a pectinate arrangement, stick-like, often
        abruptly bent (geniculate), usually spreading less than 90°................................................................... 5b

       5a. Branchlets teretiform; cortex mostly smooth; southern half of Vizcaíno Desert...............................N. marinii
      
5a. Branchlets angular; cortex prominently ridged; endemic to Mesa Camacho................................. N. angulata

5b.  Branches irregularly widened and lacerated from near base to apex, or entirely flabellate................................ 6
5b.  Branchlets mostly linear, or dilated near apex.................................................................................... 8b

6.  Thallus brittle, usually saxicolous; branches strongly compressed—more flattened than tubular prismatic,
       irregularly widened in part from near base to apex, dilated parts often lacerated.............................. ............7
6.  Thallus rigid, often terricolous; branches more tubular-prismatic than flattened, with well-defined  
       branchlets, linear throughout or dilated just below apical branchlets, or often ±digitately
       divided near apex.....................................................................................................................8a 

7.  Salazinic acid; common, Vizcaíno Desert, peninsular BCN and Isla Cedros........................................ N flabellata
7.  Hypoprotocetraric acid; rare, southern half of Vizcaíno Desert, peninsular BCN and Isla Cedros............. N. spatulata

8a.  Branches ±linear throughout, basal branches with many long side branchlets—more than 2 mm long,
        often comb-like; salazinic acid; common, BCN................................................................... N. josecuervoi
8a.  Branches dilated and/or appearing digitately branched (fringed) near apex, branchlets usually 
        less frequent towards base, less than 2 mm long...............................................................................  8b

8b.  Pycnidia conspicuous; key lichens substances absent (PD-); rare, Punta Cono S to ridges 
         above Punta Rocosa.
............................................................................................... N. homaleoides
8b.  Pycnidia obscure; lichen substances present (PD+)................................................................................ 9

9.  Salazinic acid; common terricolous lichen of desert and chaparral regions of BCN.................................. N. effusa
9.  Protocetraric acid; rare, chaparral desert transition...........................................................N. pulchribarbara
9.  Hypoprotocetraric acid; rare, desert, southern peninsular BCN.................................................... N. brachyura

Depside Species Group

10. Thallus with a distinct holdfast........................................................................................................... 11
10. Holdfast not evident....................................................................................................................... 43

11. Branchlets mostly linear or whip-like, or thallus with many spine-like branchlets, dilated parts,
        if evident, widest below mid region.................................................................................................. 12
11. Branchlets irregularly widened without any regular shape............................................................. .............. 22

12. Cortex mostly smooth, the surface appearing creamy, glazed or glossy, occasionally with 
       transverse cracks.......................................................................................................................... 13
12. Cortex prominently transversely and/or reticulately ridged.......................................................................... 17

13. Basal branches with numerous short to long side branchlets that often break off, the main branches appearing 
        lobulate where branchlets have fallen off............................................................................................. 14
13. Basal branches mostly dichotomously divided with or without occasional to frequent shorter side branchlets, the
        ultimate branchlets usually remaining attached....................................................................................... 16

14. Branches irregularly prismatic, branchlets often long, flagelliform or hair-like, remaining attached, or
        breaking off above junction with main branch; cortex pale yellowish-green, smooth or pruinose
        or with reticulate ridges, sekikaic acid................................................................................... N. suffnessii
14. Branches with well defined margins, branchlets often shorter, spine-like, often breaking off
        near junction with main branch; cortex dark green, irregularly creased.......................................................... 15

15. Upper branchlets with one or two subterminal apothecia, or mature apothecia more near base of thallus,
       or apothecia lacking; cortex smooth on upper branches; divaricatic acid...............................N. juncosa var. juncosa
15. Upper branchlets with many alternate apothecia, or with terminal solitary apothecia; 
       sekikaic acid; cortex with prominent ridges on upper branches.......................,,,,,,,,,,,,,,,,,,,,,,........... N. fimbriata

16. Cortex glossy with frequent transverse cracks; branches closely fastigiate, long linear, 1-3 mm wide, 
        with entire margins, frequently twisting..............................................................................................16a
             16a Branches dividing unequally; apothecia maturing on upper branches; divaricatic acid; BCN & CA........ N. homalea
             16a Branches dividing equally; apothecia maturing near base of thallus; sekikaic acid; CA......................N. disrupta
16. Cortex glazed, like frosting on a pastry, transverse cracks sometimes frequent but then the branches not regularly
       twisting; branches spreading from base, 3–5 mm wide on narrower parts, usually dilated and fringed near
       apex like fingers or claws spreading from the palm of a hand, the margins of the expanded regions either thickened
       from aborted apothecia or with many short lobulate branchlets, or if branches linear, the margins densely
       lobulate from broken off branchlets; basal branches often half twisted near base and apex......................... N. eburnea

         Note: N. cornea (sekikaic acid) from California has more flattened ribbon-like branches with small clusters of nearly terminal apothecia.

17. Branches prismatic in x-section, geniculate, terminally short bifurcate, or not differentiated terminally...................... 18
17. Branches
± lenticular (elliptical) in x-section, terminally whip-like or flagelliform................................................. 19

18. Cortical ridges more curved to straight than sinuous; terminal branching shortly bifurcate, ± equally divided, the
       branchlets often like bunny ears, or occasionally antler-like; divaricatic acid...................................... N. testudinaria
18. Cortical ridges more sinuous that straight; branches simple or terminally whip-like; sekikaic acid.............................. 26a

19. Isidia conspicuous, short cylindrical, usually densely covering the thallus.............................................................. 20
19. Isidia absent..................................................................................................................................... 21

20. Sekikaic acid; pycnidia sparse, 1 or 2 to a branch........................................................................... N. usneoides
20. Divaricatic acid; pycnidia sparse to frequent.............................................................................. N. isidiaescens

21. Pycnidia abundant from near base to apex; sekikaic acid; rare, endemic to Mesa Camacho area...................... N. tesselata
21. Pycnidia mostly on flagelliform branchlets or not evident; divaricatic acid; frequent.............................. N. flagelliforma

22. Cortex prominently transversely and/or reticulately ridged.............................................................................. 23
22. Cortex mostly smooth, the surface appearing creamy, glazed or glossy, occasionally with 
       transverse cracks.............................................................................................................................. 36 

23. Thallus with small tufts of basal branches, usually less than 20, these occasionally divided.......................................... 24
23. Thallus divided into numerous branchlets, these sometimes arising from less than 20
       basal branches.................................................................................................................................. 29

24. Branches tubular near base, tubular to strap-like above................................................................................... 25
24. Branches strongly flattened, strap-like to flabellate at base, often lacerated above.................................................. 30

25. Upper half of branches sharply angled with complete transverse cortical ridges between main longitudinal ridges;
         basal branches strongly pigmented near holdfast; divaricatic acid........................................................... N. rugosa
25. Transverse cortical ridges with a network of interconnected ridges between margins; basal pigmentation variable,
          lacking in N. siphonoloba (sekikaic acid), N. lobulata (sekikaic acid), N. sinuata (sekikaic acid), and N. contorta 
         (divaricatic acid) or prominent in divaricatic acid species (N. laminaria, N. undulata, N. podetiaforma)...................... 26

26. Cortex with prominent sinuous reticulate ridges, the transverse ridges between branch margins joining a main
         longitudinal ridge (branches thus tubular prismatic); thallus primarily of erect simple fastigiate branches,  
         not undulate or contorted.............................................................................................. N. siphonoloba- 26a
26. Cortical ridges generally reticulate, lacking a main longitudinal ridge, straight to curved, sinuous
         in N. lobulata; basal branches often spreading, simple or much-branched, often undulate or 
         contorted in upper half or to near base.................................................................................................... 27

    26a. Cortex with longitudinal oriented sinuous ridges; branches sharply angled; apothecia laminal; basal branches
              with occasional to frequent short side branchlets, tapering acutely to apex; ; rare, endemic to
              Mesa Camacho .................................................................................................................. N. sinuata
    26a. Sinuous cortical ridges mostly transversely oriented; branches not sharply angled; apothecia
               terminal or subterminal; basal branches mostly simple or occasionally dichotomously branched,
               mostly obtuse to apex................................................................................................... N. siphonoloba

27. Sekikaic acid.......................................................................................................................... N. lobulata
27. Divaricatic acid................................................................................................................................. 28a

28a. Thallus rigid, the cortex relatively thick; divaricatic acid................................................................... N. laminaria
28a. Thallus brittle, branches often inflated near base, the cortex generally thin......................................................... 28b

   28b.  Basal branches tubular prismatic near base with prominent reticulate ridges, expanded to
             digitately divided above, usually < 3.5 cm high; mostly Vizcaíno Peninsula, Isla Santa Margarita;
             divaricatic acid................................................................................................................ N. contorta

  
28b.  Basal branches near base rounded with obscure cortical ridges except near margins, strap-like to
             tubular prismatic above, simple to irregularly divided above, >3.5 cm long; peninsular BCN................................. 28c
      
28c.  Basal branches mostly strap-like, strongly undulate in upper two-thirds; cortical surface recessed
                 and glaucous between ridges........................................................................................... N. undulata
      
28c.  Basal branches inflated or rounded tubular, becoming tubular prismatic above, 
                 irregularly divided and undulate to lacerated in upper half; cortical ridges generally raised 
                 from surface, scarcely recessed between ridges.............................................................. N. podetiaforma

29. Branches more gradually curved than abruptly bent; cortical surface recessed between sinuous ridges on 
                 upper branchlets; holdfast not pigmented; sekikaic acid.......................................................... N. suffnessii
29. Branches more abruptly bent than gradually curved; cortical surface plane between curved to straight ridges
                 (the ridges thus appear more sharply raised) on upper branchlets; holdfast and branches near base often
                 strongly pigmented, the medulla notably yellow, the cortex blackened; divaricatic acid....................... N. turgida

30. Sekikaic acid; thallus generally flattened and flabellate, with lobulate margins, the lobes usually rounded,
                 the branches often undulate and thinner along margins............................................................. N. lobulata
30. Divaricatic acid; thallus flattened or with blade-like branches, flattened thalli generally thicker at margins
                 except N. caespitosa, which is often but not always lacerated along margins.............................................. 31

31. Isidiate or sorediate; Isla Guadalupe
         31a Isidia globose................................................................................................................ N. isidiosa
        
31a Soredia fissural and/or from cylindrical isidia, or only isidia....................................................... N. sorediata
31. Without isidia or soredia..................................................................................................................... 32

32. Branches mostly strap-like, linear to oblong (mostly California)......................................................................... 33
32. Branches mostly flabellate, obovate to rotund............................................................................................. 35

33.  Branches with various marginal features extending from apex to below mid region, with short lobes 
        to spine-like branchlets, or margins undulate................................................................................ N. laminaria
33.  Branches with terminally deltoid lobes or ±digitately divided near apex into broad  
        acute branchlets or lobes.................................................................................................................... 34

34. Thallus brittle; branches becoming ±lacerated, irregularly divided terminally; cortex relatively thin with
         sharply defined ridges..........................................................................................................N. caespitosa
34. Thallus rigid; terminal branches without apothecia regularly bifurcate, like bunny ears; cortex relatively thick
         with rounded ridges (near Monterey, CA)................................................................................. N. testudinaria

35. Thallus with short rounded constricted lobes along margins of main branches; Isla Guadalupe, 
        peninsular BCN...................................................................................................................... N. dilatata
35. Thallus mostly lacerated, lobes broadly deltoid to spine-like................................................................N. caespitosa

36. Apothecia in dense terminal aggregates on well-developed tubular branches, often aborted in
         development, bead-like, the thallus often appearing like "broccoli"; divaricatic acid................................ N. sorocarpia
36. Apothecia solitary to many along branch margins, not numerous or touching, or apothecia absent.................................. 37

37. Cortex appearing glazed or creamy, branches twisting mostly near base and apex, straight or recurved 
        above the mid region......................................................................................................................... 38
37. Cortex appearing glossy or glaucous; branches often strongly contorted in the upper half 
        (except N. juncosa, N. infundibula)........................................................................................................ 40

38. Apothecia when present becoming more developed towards apex, in small subterminal to terminal 
        aggregates, cupular in shape; sekikaic acid...................................................................................... N. cornea
38. Apothecia when present solitary to aggregate, plane or aborted in development towards apex, more mature
        towards base; divaricatic acid.............................................................................................................. 39

39. Branches sharply twisted in mid region, fringed to lobulate along margins to below mid region........................ N. laminaria
39. Branches gradually twisted, more near base or apex, digitately expanded or branched above
        mid region, lobulate to fringed more notably towards apex, especially on dilated parts................................ N. eburnea

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
       
41. Thallus of erect to wide spreading branches, the branches breaking apart, especially near apex...N. juncosa var. juncosa

40. Thallus mostly of strap-like undulate branches 2–6 cm long................................................................................ 42

   42. Sekikaic acid....................................................................................................................... N. lobulata
   42. Divaricatic acid................................................................................................................... N. undulata

43. Sekikaic acid; apothecia mostly absent; pycnidia only near tips of branchlets.............................................. N. palmeri
43. Divaricatic acid; apothecia common; pycnidia occasional to abundant below branch tips........................................... 44

  44. Branches strongly dilated near base; pycnidia inconspicuous, occasional to frequent................................. N. versiforma
  44. Branches mostly narrow throughout; pycnidia conspicuous, often aggregate, especially along
              marginal ridges............................................................................................. N. juncosa var. spinulifera

 

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
      x-section; margins entire to nodular, thickened or rounded; cortex smooth, glazed,
      rarely cracked, often with longitudinal creases.  Related chemotype species: N. cornea.

Niebla halei: Branches linear, 0.3–1 mm wide, prismatic in x-section, intricately divided;
     cortex smooth but with transverse cracks,  glossy. Related chemotype species: N. dactylifera.

Niebla homalea: Branches nearly linear, 1-3 mm wide, generally sub-elliptical in x-section;
    margins entire, acute to wing-like; cortex smooth but with transverse cracks, glossy.
    Related chemotype species: N. disrupta.

Niebla isidiosa: Branches flabellate with bladder-like swellings and papillar isidia.

Niebla testudinaria: Branches variable, 2-5 (-10+) mm wide, prismatic to somewhat
       flattened in x-section; margins entire, acute to rounded; cortex reticulately ridged,
       dull to glossy.  Related chemotype species: N. dissecta 

      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,
       thickened or rounded;  cortex smooth, glossy.

           Niebla laminaria: Branches variable; margins nodular to crenulate or incised, rounded;
       cortex dull, usually transversely cracked.  Related chemotype species: N. disrupta,
       N. cornea, N. dissecta.

     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:
        N. flabellata.

Niebla dilatata: lobes rounded; margins usually thickened
.  Related chemotype species:
        N. lobulata, N. flabellata.

       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
              often more than 20 in number, or with numerous spinuliferous
              branchlets.
 

                             Niebla sorocarpia: Apothecia in beadlike aggregates.

                 Niebla ramosissima:  Thallus flaccid, branches lying on the ground: Related
                               chemotype species: N. palmeri.

                            Niebla juncosa:  Branchlets mostly straight, spinuliferous, elliptic in x-section. 
                             Related chemotype species: N. fimbriata.

                            Niebla turgida: Branchlets geniculate, twisted, sharply prismatic. Related
                             chemotype species: N. suffnessii.

                            Niebla versiforma: Holdfast not evident, branchlets arising from a dilated branch
                              segment, appearing fringed. Related chemotype species: N. palmeri                

                       5.  Thallus not bushy, usually <6 cm high or broad; basal branches
               often <20, monopodial to dichotomously branched, or branchlets
               mostly persistent, not breaking off,
irregular, broadly lobed to
               lacerated, or linear in one species.

                         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
                                         between  N. podetiaforma and N. undulata.  Related chemotype
                                         species: N. lobulata.

                           Thallus > 3.5 cm high.

                                    Niebla undulata: Cortex with prominent  diagonal to longitudinal
                                                 ridges near apex, or cortex appearing mostly smooth, branchlets
                                                 usually twisted, notably undulate.  Related chemotype
                                                 species: N. lobulata.

                                   With prominent transverse cortical ridging on apical branches or lobes

                                               Niebla podetiaforma: Monopodial or irreguarly branched; branches or
                                                branchlets straight to geniculate (abruptly bent) or arcuate (curved
                                                like an arc), with entire margins.
                                                Related chemotype species: N. siphonoloba.

                                               Niebla rugosa:  Mostly monopodial, branches somewhat folded
                                                  like an accordion, conspicuously wavy (sinuous) along margins. 
                                                  Related  chemotype species: N. siphonoloba.

Sekikaic Acid

     Medulla solid; cortex firm, glazed to glossy

         Niebla cornea: Branches monopodial to digitately divided from dilated segments near apex,
                        elliptical to oblong or obovate, mostly flattened with rounded margins and short
                        prismatic segments. Related chemotype species: N. eburnea.

         Niebla disrupta: Branches regularly dichotomous or trichotomous, ultimately long flexuous
                       or geniculate, nearly long linear throughout, sub-teretiform in x-section, with acute
                       to obtuse margins; thallus taller than wide, similar to N. homalea.

         Niebla dissecta: Branches much divided dichotomously, sometimes digitately
                      divided near apex, nearly short linear to oblong throughout, or dilated
                      near apex, strongly prismatic, with ultimate branchlets long bifurcate
                      and divergent at wide angles; thallus usually broader than tall.
                      Related chemotype species: N. testudinaria.

         Niebla palmeri: Branches irregularly much divided without a holdfast, terricolous.
                      Related chemotype species: N. ramosissima.

     Medulla fistulose to subfistulose; cortex usually wrinkled or foveolate

         Niebla dactylifera: Branches much divided more near apex than base, short bifurcate
                        near apex.  Related chemotype species: N. halei.

         Niebla siphonoloba: Branches monopodial to occasionally divided near apex, usually
                        obtuse to truncate terminally, or with terminal apothecia.
                        Related chemotype species: N. rugosa.

         Niebla tesselata: Branches monopodial, tapered to apex; pycnidia densely covering
                        branches; apothecia unknown. Related chemotype species: N. flagelliforma
                         (morphotype from Isla San Martín).

          Niebla usneoides: With isidia.  Related chemotype species: N. isidiaescens.

          Niebla suffnessii: Branches dichotomously divided, terminally more divided into
                        long spinuliferous to long flagelliform branchlets. Related chemotype
                        species: N. turgida.

          Niebla fimbriata: Branches with spinuliferous branchlets arising from near
                        base along a main branch, branchlets often falling off, the margins appearing
                        lobulate. Related chemotype species: N. juncosa.

          Niebla lobulata: Branches flattened, incised to lobulate. Related chemotype species: N. undulata.

Terpenes Absent

Acid Deficient (No Depsidones)

     Niebla homaleoides

Depsidones

  Protocetraric acid

       Niebla pulchribarbara

  Hypoprotocetraric acid

     Niebla spatulata: Branches flabellate, lacerated; cortex thin.
 
        Niebla brachyura: Branches prismatic, spinuliferous; cortex thick.

  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

                         Niebla marinii: Branches mostly dichotomously divided, often terminally
                                 flagelliform

                 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)

Corrections

 

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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