A refined concept of the Critoniopsis bogotana species group in Colombia with two new species (Vernonieae, Asteraceae)

Abstract Critoniopsis bogotana is more precisely delimited, and two related Colombian species are described as new. The form of trichomes on the abaxial surfaces of the leaves is found to be of major importance. A short key to the Critoniopsis bogotana group is provided.


Introduction
Collections of Critoniopsis Sch.-Bip. (1863) made during fi eld work by the second author in 1984 have proven that the group of mostly 5-fl owered species including Vernonia bogotana Cuatrec. (1956) is more complex than previously believed. Th e two new species described here are based on the collections of the second author in 1984 and material collected by Ramirez and Cuayal in 1991. Both the collections of Keeley, and Ramirez and Cuayal had presented some problems when fi rst studied, mostly because features of leaf shape, seemed unreliable, the prominence of the veins on abaxial surface of the leaves diff ered but was rather subtle, and geography alone showed a near continuum. In at least one Ecuadorian species, Critoniopsis fl oribunda (Kunth in HBK) H. Rob., even the number of fl orets in the heads had proved unreliable (Haro-Carrión and Robinson 2008). Th e question arose as to what characteristics could be trusted, or whether there was only one highly variable species.
Th e most important treatment of Critoniopsis in the northern Andes was by Cuatrecasas (1956) at which time the group was treated as a Section of Vernonia Schreb. It was in the Cuatrecasas treatment that many of the Colombian species were described as new, including V. bogotana and V. killippii Cuatrec. Since then, Critoniopsis has been restored to separate generic status (Robinson 1980) and has been recognized as a closer relative of the genus Piptocarpha R. Br. (Robinson, Bohlmann andKing 1980, Keeley et al. 2007;Robinson 2007;Keeley and Robinson 2009). Th e most recent treatment of species of Critoniopsis with a key was that of Haro-Carrión and Robinson (2008) dealing with genus in Ecuador.
Th e present study arose from an attempt to fi nally resolve the identity of the series of collections made by the second author which had been put aside because they seemed closely related to Critoniopsis bogotana but did not exactly fi t that concept in the appearance of the leaf undersurfaces. Th is extensive set of Keeley collections from Cundinamarca in Colombia seemed to lack the prominent abaxial tertiary and quaternary leaf venation that is characteristic of C. bogotana. More careful study of the group has shown some major variation in leaf shape within the group as well as some close approximations of venation patterns in a few of the specimens in both typical C. bogotana and the Keeley collections. In the process, additional Keeley collections initially determined as C. bogotana from Cauca and Caldas were studied along with a few puzzling collections by Rameriz and Cuayal from Nariño that had been previously left unidentifi ed. At the same time, it has seemed appropriate to restate the diff erences between C. bogotana and C. killippii, the latter often incorrectly distinguished from C. bogotana.

Methods
Materials studied were all deposited in the U.S. National Herbarium, Department of Botany, National Museum of Natural History or in Bogota (COL) or Pasto (PSO). Examination included study with a light microscope and the USNM Leica 440, Scanning Electron Microscope (SEM), equipped with a lanthanum hexaboride (LaB) electron source.

Conclusions
Two species are recognized that have some diff erences in appearance of the abaxial leaf surfaces, but which are most reliably distinguished by the form of the trichomes on those leaf surfaces. Other features such as length of the outer pappus series, shape of the involucral bracts, broadenings of the tips of the inner segments of the pappus, and leaf shape are found unreliable.
In contrast to the confusion derived from other characteristics, the diff erences in the trichomes are striking. Th e trichomes in C. bogotana are elongate and sparsely irregularly branched, the trichomes of the new Cundinamarca species are strictly stellate with stiffl y spreading arms, and the trichomes of the Nariño species are fl attened and thin-walled. Th e species of the C. bogotana group can be distinguished by the following key based on features of the leaf bases and abaxial surfaces. Th e species ranges from near Bogotá southwestward to Nariño near the border of Ecuador.

Key to the species of the Critoniopsis bogotana Group
At one time Vernonia calerana Cuatrec. was treated is a synonym of this species, (Robinson 1993) but diff ers by the much more numerous fl orets in the heads.
Th e much overused name V. pycnantha Benth [C. pynantha (Benth.) H. Rob.] has been applied to this species in the past, but the Bentham species is restricted to southern Ecuador and northern Peru (Haro Carrión & Robinson 2008). Careful examination of a photograph of the type of C. pycnantha at Kew shows a tendency for ultimate branches of the infl orescence to be scorpioid-or seriate-cymose, a trait seen only in members of the genus Critoniopsis from southern Ecuador and southward. Th e placement of the variety santandarensis in the species bogotana indicates the confusion that has existed between C. bogotana and C. killipii from the time of their description. Th is is surprising since C. killipii is distinct in both its leaf base and its geography. Th e base of the leaf blade has a strongly recurved margin and an abrupt decurrence ca. 1 cm long on the petiole. Th e specimens seen are from Depto Santander and Norte de Santander in Colombia and adjacent Tachira in Venezuela, both areas distinctly to the northeast of any known collections of C. bogotana.
Leaf bases similar to those of C. killipii, led to the misidentifi cation of a series of Keeley collections of C. glandulata (Cuatrec) H. Rob. as C. killipii. On closer examination, Critoniopsis glandulata is strikingly distinct in its more thyrsiform infl orescence branches, apiculate involucral bracts, and stalked T-shaped trichomes. Critoniopsis glandulata was originally described from Norte de Santander in Colombia. Th e 1983 Keeley collections,4464,4465,4466,4467,4468  Description. Shrubs or small trees up to 6 meters tall. Stems terete, dark brown, covered with grayish indument of short irregularly-shaped trichomes; internodes 0.5-1.0 cm long. Leaves alternate; petioles mostly 1.0-1.5 cm long; blades subcoriaceous, elliptical to broadly ovate-elliptical, 7-11 cm long, 2.7-4.3(-6.5) cm broad, base usually acute, without decurrence onto petiole, broad-leaved specimen (Keeley 4544) with obtuse to rounded base, margins mostly entire or with few teeth distally, broad-leaved specimen with margins distinctly serrate distally, apex acute, with little or no acumination, adaxial surface essentially glabrous, veinlets variously slightly incised to slightly prominulous, abaxial surface with prominent primary and secondary veins, tertiary veins prominulous and quaternary veinlets obscure to slightly prominulous, secondary veins ca. 8 on each half, mostly spreading at ca. 45°, arching, lower secondary veins more widely spreading in broad-leaved specimen (Keeley 4544), surface covered with dense appressed grayish pubescence, individual trichomes with short stem and stiff spreading stellate arms. Infl orescence terminal on leafy branches, densely pyramidally paniculate with corymbiform branches, mostly 9-12 cm high and wide. Branches grooved, covered with dense whitish tomentum, heads sessile or on short peduncles 1-3 mm long. Heads cylindrical, at anthesis ca. 12 mm long and 4 mm wide, with ca. 35 involucral bracts in ca. 7 series, ca. 4 rows of basal bracts densely imbricated, broadly ovate, ca. 0.5-3.5 mm long, 1.5-2.5 mm wide, with scarious lateral margins, persistent and widely spreading with age; inner bracts in ca. 3 series, oblong, 5-7 mm long, 1.5-2.2 mm wide, with narrowly recurved lower margins, with fl attened rounded, dark and membranous tips, highly deciduous with age, all but basalmost bracts glabrous on outer surface; receptacle glabrous, fl at. Florets 5 in a head; corollas white, funnelform, ca. 8 mm long, basal tube ca. 4 mm long, throat ca. 1.5 mm long, lobes ca. 2.6 mm long, linear-lanceolate; outer surface of upper tube, lower throat and lobes with minute monoseriate trichomes, a few glandular dots at tips of lobes; anther thecae purple, ca. 2.5 mm long, bases with short obtuse sterile margin, apical appendages ca. 0.5 mm long, oblong-ovate; style base broadened, shortly conical. Achenes light brown, ca. 4 mm long, without evident glands or setulae on surface, with longitudinal striae; Pappus white, ca. 5 mm long, inner pappus of ca. 40 capillary bristles, fl attened beyond middle and slightly broadened at tips, outer pappus a series of lanceolate squamae 0.5-1.7 mm long.
Th e specimens of the species were initially left unidentifi ed because of the comparative lack of prominence of the tertiary and quaternary veins and the comparatively even surface of the pubescence on the abaxial surfaces of the leaves. In C. bogotana, the venation of the abaxial leaf surfaces is distinctly reticulated, and the tomentum is mealy in appearance. Examination of the trichomes under the light microscope is suffi cient to show the profound diff erence in the trichome shape, shown here in SEM photos. Th e stellate form is consistent in every specimen sampled from what are evidently members of at least two separate populations.
A problem that seemed of importance when the specimens were fi rst studied, was the striking diff erence in the leaf shape of one of the collections (Keeley 4544). Th is broad-leaved form had more obtuse to rounded bases of the leaf blades, more broadly ovate blades, and distinctly multiple serrate distal margins on the leaves. Th is is seen here as a diff erence within the species. It is reminiscent of the leaves that often arise on sprouts or sucker shoots from stumps of felled trees, and is not regarded here as worthy of any taxonomic distinction. Description. Large shrub or small tree. Stem terete, brownish, with appressed pubescence; internodes scarcely defl ected, ca. 0.7 cm long. Leaves alternate; petioles 2.0-2.5 cm long; blades narrowly ovate-elliptic, 10-14.5 cm long, 3.5-6.3 cm wide, base obtuse to rounded, ending abruptly at petiole, margins entire, apex scarcely acuminate, with 9 or 10 secondary veins on each half, spreading at ca. 60° at base, somewhat arching, upper surface glabrous, slightly roughened with scarcely prominulous veinlets, abaxial surface with prominent primary and secondary veins, with obvious reticulum of prominulous brownish pubescent tertiary and quaternary veins, areoles fi lled with minute, pale, thin-walled, fl attened trichomes (Fig. 3E). Infl orescence terminal on   leafy branches, rounded to somewhat pyramidal, with loosely corymbiform branches; heads clustered on short branchlets and ultimately sessile in clusters of 3 or 4. Heads short-cylindrical, ca. 9 mm long, 3-4 mm wide; involucral bracts ca. 35 in ca. 7 series, basal bracts ca. 16, in 3-4 rows, persistent, weakly spreading in fruit, broadly ovate to ovate-oblong, 1.5-3.9 mm long, 1.0-1.7 mm wide, with scarious lateral margins, inner bracts mostly fallen in specimen, estimated in 3 series, 4-8 mm long, ca. 1.2 mm wide, oblong to oblanceolate, narrowed to base, with narrowly recurved basal margins, apices darkened, rounded, outer surfaces mostly glabrous; receptacle slightly convex, glabrous. Florets ca. 5 in a head; corolla color not stated, probably white, funnelform, 6.5 mm long basal tube ca. 3.5 mm long, throat ca, 0.7 mm long, lobes ca. 1. 8 mm long, lanceolate, traces of few minute monoseriate hairs seen on outer surfaces of upper tube, throat and lobes; anther thecae ca. 1.3 mm long, bases with acute hyaline edge; apical appendages ca. 0.3 mm long; style not observed. Achene body brownish, 3.5-4.0 mm long, with 3 or 4 angles, mostly glabrous with some small glandular dots near base; pappus white, ca. 5 mm long, with ca. 40 inner capillary bristles not or scarcely broadened at tips, outer series of short narrow squamae ca. 0.5 mm long.

Critoniopsis narinoensis
Th e species is known only from the type collection. Vegetatively the specimen is in excellent condition, and fortunately species of the genus Critoniopsis can usually be distinguished by leaves and number of fl orets in the head. Th e present new species might have been placed in either C. lindenii Sch.Bip. or C. popayanensis (Cuatrec.) H. Rob. on superfi cial examination, but the former diff ers obviously by the smoother abaxial surface of the leaves covered with goblet-shaped trichomes. Th e latter diff ers by the decurrence of the leaf blade onto the upper petiole.