Verbascum salicifolium Zograf., Ioannidis, Liveri & Dimop., 2022

Zografidis, Aris, Liveri, Eleni, Ioannidis, Vasilis & Dimopoulos, Panayotis, 2022, Verbascum salicifolium (Scrophulariaceae) a new species from Central Macedonia, Greece, Phytotaxa 552 (3), pp. 182-190 : 183-188

Verbascum salicifolium Zograf., Ioannidis, Liveri & Dimop. , sp. nov. ( Figs 1 & 2 )

Diagnosis: a species morphologically close to V. adenanthum but distinguished by its oblanceolate to narrowly elliptic, ±acute basal leaves, its leaf-like bracts subtending the lower branches of the inflorescence, and by its corollas with obovate lower lobes.

Type :— GREECE. Nomos and Eparchia Kilkis: sandy flats just E of lake Doirani, 155 m elev., 41°12’N, 22°47’E, 17 May 2021, Zografidis 677 (holotype UPA!, isotype ATH!) ( Fig. 2 ) .

Biennial, eglandular-hairy herb producing a taproot and a basal-leaf rosette in the first year of growth and an erect, terete, finely striate, leafy flowering stem 0.4–1 m high in the second year. Indumentum light grayish, thin, soft, ±persistent (but inflorescence axes more sparsely pubescent), composed of appressed stellate hairs. Rosette and lower cauline leaves oblanceolate to narrowly elliptic, petiolate, long attenuate at base, subacute or acute at apex (rarely acuminate), the largest ones 10–25 × 1–3 cm, with petioles 0.5–5.5 cm. Margins of leaf lamina subentire, crenulate, crenate or crenate-dentate, frequently somewhat undulate/incurved. Middle and upper cauline leaves progressively smaller, sessile, lanceolate or narrowly oblong, subacute to acuminate (upper). Inflorescence freely branched, frequently branched from well below middle, ovoid-ellipsoid, lax. Branches growing at (20–)30–70 degrees angle, ±arcuate ascending. Internodes of upper inflorescence branches 1–2.5(–3) cm. Lower bracts (subtending lower branches of inflorescence) leaf-like,> 1 cm. Glomerules 2–5(–7) flowered. Bracts linear-lanceolate/subulate to linear, 2.5–4.5 mm in length; bracteoles smaller, linear-lanceolate to linear. The longest pedicels 2–6 mm, thickened in fruit. Calyx 2.5–3.5 mm with oblong-lanceolate/ subulate segments divided almost to the base. Corolla rotate, yellow, 2–3 cm in diameter, with obovate lobes; outer surface of corolla with stellate hairs, inner surface glabrous. Pellucid glands on corolla present, numerous, scattered. Stamens 5 with reniform, medifixed anthers c. 1 mm long. Stamen hairs white. Three posterior stamens 5.5–7 mm, hairy up to the connective. Anterior stamens 6.5–8 mm with filaments glabrous for c. 2 mm below the connective. Ovary pubescent, c. 1 mm; style glabrous, 5–7 mm; stigma obovoid-clavate. Capsules ovoid- to ellipsoid-cylindrical 4.6–8 × 2–3.3 mm, shortly beaked (beak c. 0.5 mm). Seeds numerous, prismatic to oblong-prismatic, blackish, 0.6–0.9 × 0.4–0.5 mm, with 5–7 longitudinal rows of alveoli.

Etymology:— The specific epithet refers to the long, narrowly elliptic/oblanceolate basal leaves of the new species reminiscent of a willow ( Salix ) leaf shape.

Phenology:— The first flowers are observed in late April to early May with the peak of flowering in mid-May to early June. Capsules mature in June and July.

Karyology:— Several plants from the locus classicus of Verbascum salicifolium were studied karyologically. The results showed the chromosome number 2 n = 36 for the new species and a symmetrical karyotype consisting of chromosomes varying in size from 0.75 to 1.77 μm ( Fig. 3 ). Due to their small size no detailed karyological analysis was carried out. Two spherical satellites are observed in most karyotypes ( Fig. 3 ).

Distribution and habitat:— The known distribution of Verbascum salicifolium is restricted to a single location on the eastern shores of Doiran Lake in the administrative region of Central Macedonia ( Greece), where the species inhabits abandoned agricultural fields and roadsides with synanthropic vegetation (subnitrophilous annual grassland), along the road which surrounds the Greek part of the lake. The altitude is c. 150 m elevation and the substrate in the habitat is very sandy, calcareous and enriched with shell fragments. Accordingly, the new species is currently known only from a ruderal habitat. The level of the lake was lower 10 years ago when V. salicifolium could also be found in an open riparian forest just west of its extant population. Attempts to find the species at other sites, where a riverine forest still exists at the banks of Doiran Lake, were unsuccessful.

Conservation assessment:— Verbascum salicifolium is known from a single population consisting of c. 100 mature individuals (assessed in June 2021), whereas the estimated extent of occurrence (EOO) and area of occupancy (AOO) of the species are both less than 5 km 2. Today, the plants are found in a ruderal habitat composed of two neighboring abandoned fields and the adjacent roadsides, just east to the lake. Agricultural land use is dynamic in this region, and mainly concerns irrigated oilseed rape and maize production. The reestablishment of cultivation in the two fields, where most of the individuals of the new species reproduce, as well as the concomitant possible use of herbicides—that would also negatively affect the plants on the roadsides—would pose a major threat to it. Possible future reconstruction and widening of the motorway that surrounds the lake represents another threat. Water levels have significantly increased over the past 10 years, engulfing what was once a natural, open riparian forest. In 2012, the species could also be observed in a zone of at least 200 m west of its extant location in a natural habitat which stretched 450 m to the west of the present bank of the lake. Further rise of the level of the lake is considered unlikely, however, the species could not be detected at other sites with surviving riparian vegetation. According to the IUCN (2021) Red List criteria the species should be listed as Critically Endangered (CR) based on its very restricted EOO and AOO, the presence of only one location and the continuing decline in EOO, AOO, and quality of habitat: CR B1,2 ab(i,ii,iii). It is noteworthy that Doiran Lake is part of the NATURA 2000 network of protected sites (LIMNI DOIRANI, GR1230003 ) as well as of the Corine biotopes ( A00060009 ). Importantly, the northwestern, western and southwestern banks of the lake are part of the Republic of North Macedonia where efforts to locate the species should also be attempted.

Taxonomic comments:— Following the traditional classification based on morphology by Murbeck (1933), Verbascum salicifolium belongs to section Bothrosperma Murbeck (1933: 32) (alveolate seeds) and is further classified in subsection Fasciculata Murbeck (1933: 32) (flowers in dichasia) which comprises most of the species. Below the rank of subsection, the new species is classified in the successive groups of Isandra ( Franchet 1874: 177) Murbeck (1933: 32) (all anthers reniform and medifixed), Bracteolata Murbeck (1933: 33) (presence of bracteoles), Umbellulifera Murbeck (1933: 33) (dichasia sessile, alternatively known as glomerules) and Leianthera Murbeck (1933: 33) (glabrous connective of anthers). It is parenthetically noted that the infrageneric taxonomy of Verbascum needs revision, first and foremost because the most comprehensive accounts ( Murbeck 1933, 1939) have retained the genera Celsia and Verbascum , which, however, are better merged into one taxon ( Ferguson 1971 and references therein). The morphologically closest species to V. salicifolium is V. adenanthum , a Balkan endemic native to North Greece and Republic of North Macedonia. This species is also classified in Leianthera group and shares some additional characters with V. salicifolium , most noticeably a freely branched inflorescence and comparable sizes of calyxes and corollas. For distinguishing the two species, the most obvious diagnostic characteristic is the shape of the leaves, which is more elongated, and ±acute in V. salicifolium . Due to its longer leaves and ±shorter internodes, the mature plants of the new species appear leafier, too. Furthermore, V. salicifolium is frequently branched well below the middle, where the first branches of the inflorescence are subtended by leaf-like bracts; a trait not observed in V. adenanthum . Additional differences between V. salicifolium and V. adenanthum are provided in Table 3 . Verbascum adenanthum grows from 450–1800 m elevation and is mostly reported from rocky mountain slopes and roadsides that cross its natural habitat. Accordingly, the ecological preferences of the two species are apparently distinct. More morphologically distant to V. salicifolium is V. biledschikianum Bornmüller (1930: 355) an Anatolian endemic which approaches more V. adenanthum in habit; however, this species belongs to the group Adenanthera Murbeck (1933: 33) (hairy connective of anthers) and it is further distinguished from both V. salicifolium and V. adenanthum by its smaller calyxes and corollas, its lack of pellucid glands on the corolla and by its dense indumentum on the outer surface of the corolla.

The karyological data for the genus Verbascum are quite rare; chromosome numbers have been reported only for approximately 14% of the species [based on Chromosome Counts Database – Rice et al. (2015)]. The chromosome number for V. salicifolium is determined here as 2 n = 36 ( Fig. 3 ), while the chromosome count for its morphologically related V. adenanthum is still unknown. Regarding the other species of the “ V. salicifolium clade” ( Fig. 4 ), karyological data are found only for V. densiflorum , which indicate several chromosome numbers: 2 n = 30, 32, 34, 36 in material from central Europe, Russia and European Turkey ( Rice et al. 2015). Scarce karyological data are also found for the more distant species of V. salicifolium . For example, V. blattaria and V. graecum show the chromosome numbers 2 n = 30, 32 ( Rice et al. 2015). It is well evident that further karyological studies must be conducted to form a hypothesis for the origin of the variable chromosome numbers in Verbascum species.

Preliminary results on the molecular phylogenetic study of Verbascum in the Balkan subcenter of its diversification (work in progress) have indicated that Verbascum salicifolium does not group with V. adenanthum but forms a sister clade along with species much more distant from a morphological standpoint. Here, we focus on the analysis specifically for V. salicifolium clade and several sympatric species including V. adenanthum collected from three distinct populations ( Fig. 4 ). The strongly supported clustering of V. salicifolium with V. macrurum , V. densiflorum and V. eriophorum appears to be interesting and somewhat unexpected. All three species differ from V. salicifolium in various respects; most interestingly in having long decurrent anthers of anterior stamens, a trait which places them in the group of Heterandra ( Franchet 1874: 175) Murbeck (1933: 32) . However, Murbeck (1933) had already pointed out that there are several cases where morphologically closely allied species differ in this trait and thus these groups based on the insertion of anthers are artificial and polyphyletic. In addition to the different morphology of the anthers, V. macrurum , V. densiflorum and V. eriophorum are much more robust plants than V. salicifolium , with basal leaves that may reach 50 × 30 cm, calyxes 5–15 mm, corollas 3–5 cm and distinctly different inflorescences (unbranched, rarely with a few short branches in V. densiflorum and V. macrurum ; and unbranched or with a few elongated branches in V. eriophorum ). Verbascum densiflorum and V. macrurum are furthermore distinguished by their long decurrent cauline leaves, whereas V. eriophorum has a floccose-glabrescent and densely glandular hairy inflorescent and purple stamen hairs (vs. eglandular not floccose inflorescence, and white stamen hairs in V. salicifolium ). It is noted that the relationships of V. salicifolium with the three other species in its group are not resolved. The new species may be perhaps more genetically related to V. densiflorum and V. macrurum (64% bootstrap support considered weak), two species which are clearly morphologically more related to each other than to V. eriophorum . The hypothesis of an ancient hybridization event of a maternal ancestor in V. salicifolium group with the ancestor of V. adenanthum could provide a possible explanation for the inclusion of the new species in a group of phenetically quite different species in the chloroplast tree. Lastly, as preliminary data suggest (work in progress), there are additional cases in which morphologically dissimilar but sympatric species are closely genetically linked, and, conversely, instances where similar but allopatric species may not be as closely genetically related as would have been expected, pointing to possible character reversals and convergent evolution in Verbascum .

Figures

FIGURE 1. Verbascum salicifolium, A, plants in habitat; B, basal leaf rosette with developing stem; C, corolla; D, capsules; E, seeds, scale bar = 1 mm.

FIGURE 2. Holotype of Verbascum salicifolium.

FIGURE 3. Microphotograph of mitotic metaphase place of Verbascum salicifolium, 2n = 36. Arrows indicate satellites; Scale bar = 10 μm.

FIGURE 4. Bootstrap consensus trees of the plastid dataset (atpH-atpI + rps16-trnQ + psbA-trnH + ndhF-trnL) inferred using the Maximum Likelihood method showing bootstrap values above the branches. Branches corresponding to partitions reproduced in less than 50% bootstrap replicates are collapsed.