Rahchamani, Ranjbar & Rahchamani, 2018

Ranjbar, Massoud & Rahchamani, Narges, 2018, The species of Scrophularia L. (Scrophulariaceae) with white margined leaves in Flora Iranica, Adansonia (3) 40 (6), pp. 67-87 : 75-83

2. Scrophularia marginata Boiss. ( Figs 5 ; 6 )

In Diagnoses Plantarum Orientalium novarum, ser. 1, 4: 72 (1844) . — Typus: Iran. Hamedan, Alvand (Elwend) mountain, Aucher-Eloy 2898, lectotype and isolectotype here designated (lecto-, G-DC[G00673693]!; isolecto-, G-BOIS[G00334025]!).

PHENOLOGY. — Flowering and fruiting from April to July.

CONSERVATION STATUS. — Based on GeoCAT tool (Bachman et al. 2011), the extent of occurrence (EOO) of Scrophularia marginata is estimated to 1 113.575 km 2. This species is known from about 20 disjunctive populations, representing about nine different localities. The relatively limited taxon could be categorized as Endangered (EN) according to IUCN Red List criteria ( IUCN 2012).

OTHER SPECIMENS EXAMINED. — Iran. Hamedan: Alvand mountain , s.d., Ranjbar et al. 757 ( BASU!) ; Alvand mountain , s.d., Ranjbar 758 ( BASU!) ; Alvand mountain, Heydareh , 28.V.2013, Ranjbar 33745 ( BASU!) ; Tuyserkan , 6.V.2016, Ranjbar & Rahchamani 59063 ( BASU!) ; Malayer, Lolohar village , 21.V.1998, Kulivand 655 ( BASU!) ; Hamedan to Asad Abad, 20 km before Asad Abad , 1979 m, 20.VI.2011, Ranjbar 29242 ( BASU!) . 20 km to Songhor from Asad Abad , 1904 m, 29.V.2012, Ranjbar 29608 ( BASU!) ; Darreh Morad Beyg , 34°75’20’’N, 48°50’74’’E, 2130 m, 29.III.2014, Ranjbar 36940 ( BASU!) ; Sarkan , 21.V.1988, Cheraghali 962 ( BASU!) ; Varkaneh , 2230 m, 34°40’34’’N, 48°37’10’’E, Nuri 59227 ( BASU!) . Kurdistan. In montibus calcareis Avroman et Schahu , VI-VII.1867, Haussknecht s.n. ( P03553852 !, P03553853 !) .

Asie occidentale. 1837, Aucher-Eloy s.n. (P03553854!).

DESCRIPTION

Perennial herb, 30-45 cm tall, ascending to erect, at the base woody. Stems numerous, light green to light brown, whitish at the base, approximately quadrangular, glabrous or with very sparsely short glandular hairs. Basal leaves whorled, light green, brown to purple when dry, thick, coriaceous, white margined, glabrous or with very sparsely short glandular hairs on both surfaces, orbiculate to ovate to elliptic, obtuse, 5-20 × 5-15 mm, sessile to petiolate, petiole to 10 mm long, venation pinnate, prominent and light green to white in base, undulate, crenate to dentate, with 7-9 teeth in one side; to 1 mm long, angle of teeth 50-80º, obtuse, apical side of tooth convex, basal side of tooth convex. Cauline leaves opposite with lateral branches, light green, thick, coriaceous, white margined, glabrous with very sparsely short glandular hairs on both surfaces, ovate to elliptic to lanceolate, obtuse to acute, 10-30 × 5-10 mm, sessile to petiolate, petiole to 15 mm long, venation pinnate, prominent and green to approximately purple in base, undulate, crenate to dentate, with 6-11 teeth in one side; to 1 mm long, angle of teeth 50-80º, obtuse to acute, apical side of tooth convex, basal side of tooth convex to straight. Inflorescence 15-25 cm long, bracteate, paniculate, cymous dichasium, many-flowered. Bracts lanceolate, entire, acute, to 3 mm long, green, with white mucro, glabrous or with very sparsely short glandular hairs. Bracteoles linear to lanceolate, entire, acute, to 1 mm long, green, with white mucro, glabrous or with very sparsely short glandular hairs. Peduncle 5-10 mm long, pedicel 1-2 mm long, glabrous or with very sparsely short glandular hairs. Calyx 2-2.5 × 2-3 mm, sepals equal, broadly ovate, obtuse, 1/2 corolla length or shorter, green, with narrowly white margin to 0.2 mm, glabrous or with very sparsely short glandular hairs. Corolla 4-4.5 × 4.5-5 mm, ventricose, lobes unequal, upper lobe 1 mm larger, obtuse, purple when fresh, purple to red in dried status, glabrous. Stamens 4, fertile, exserted, 4-4.5 mm long, filaments white, with sparsely glandular points, anthers red to purple. Staminode orbiculate. Ovary globose to ovoid, 1.5-2 × 1.5-2 mm, glabrous. Style terminal, filiform, 4-5 mm long, glabrous. Capsule globose to ovoid, 4-5 × 4-5 mm, mucronate, mucro 0.5 mm long, light brown, glabrous. Seeds cylindrical to ovate to triangular, 1-1.8 × 0.5-1 mm, dark brown.

TYPIFICATION NOTES

Boissier (1844: 72) introduced S. marginata from collected specimens by Aucher-Eloy from Iran, Alvand [Elwend] mountain with number 2898. But it was considered as synonym for S. deserti by Grau (1981: 264). Based on the morphological studies, these species should be considered as two separated species because they differ in terms of plant color and leaf shape and margin. So S. marginata is resurrected as a valid species and needed to be typified. This species is tracked in G and P herbaria. There are one specimen in G-BOIS and another specimen in G-DC herbarium with the label information matching with the original description. Since this species is introduced by Boissier, the lectotype specimen should be selected from G-BOIS (G00334025), but this specimen is an incomplete sheet and the important characters, such as shape and margin in basal and cauline leaves, are not clear. It seems that G-BOIS specimens is really a branch detached from the G-DC specimen. Boissier probably didn’t have this collection in his herbarium and asked his friend De Candolle for permission to remove a fragment from the specimen or alternatively, may be sent him a fragment. It is possible that Boissier has never seen De Candolle’s specimen, but it is unlikely that the handwriting on the G-BOIS fragment is related to Boissier. So if De Candolle would have sent him a fragment, it would be DC’s handwriting. However, we can never be sure about what happened and we have to take a pragmatic approach here ( Fig. 7 ). Since the G-DC specimen (G00673693) is much better, so the specimen is designed as lectotype for S. marginata . Also, this opinion has been confirmed by G herbarium. “Generally, if a species has been described by Boissier, so its specimen in his herbarium should be as holotype. If there is another specimen, e.g. in G or G-DC, they should be considered as isotypes. However, this is a general rule and there may be some exceptions. I think you pointed out one of these exceptions. I would follow your suggestion and advise in this case to consider both specimen as syntypes and to designate the G-DC as lectotype, explaining clearly that you did not chose the G-BOIS as holotype because there is evidence that it was detached from the G-DC specimen and that you suspect that Boissier saw the specimen that was in the De Candolle herbarium, not only his fragment” (Dr Laurent Gautier pers. comm.).

MORPHOLOGY

The examination of herbarium material clearly allowed to separate Scrophularia deserti from S. marginata as a distinct species. Results from morphological studies on about 60 populations of S. deserti and 20 populations of S. marginata indicated that although the white margined leaf is a character indicating the close relationship of these species, some characters such as stem color, leaves size, shape and margin, petiole length and staminode shape distinguish them well. In both species, basal leaves are approximately similar in term of size, shape and margin, but cauline leaves are clearly dentate to lobed or parted in S. deserti and crenate to dentate in S. marginata . Grau (1981: 266) believes that S. deserti has polymorphic leaves, forming usually undivided rosette which are strongly divergent from the cauline leaves. During fast growth in the first year, undivided leaves can be probably present also on the stem and old stems can build new shoots of leaf rosettes, which resemble to the basal leaves. So, S. marginata separated by Boissier, was synonymized for S. deserti . But, resulting from detailed studies on the numerous populations of both species, it seems that this hypothesis can be partly correct. In fact, in examining the type specimens and numerous collections from other herbaria, S. deserti reveals a wide variety of leaf size, shape and margin in its distribution range from Egypt to Pakistan. Leaf polymorphism is clearly seen in different populations of the species and even in an individual of a population. But S. marginata , with unique cauline leaves, appears in limited range in Hamedan and Kurdestan provinces, Iran. Thus, the two mentioned species should be considered clearly as distinct taxa at the specific rank. About the species S. moniliformis , not found in Iran, final decision is difficult and needs further stud - ies. However, it is apparently a correct synonym for S. deserti and it should remain in same situation. Scrophularia sinaica represented the symmetrical characters with S. deserti such as stem color, leaves size, shape and margin, white margined leaf, staminode shape, indumentum type, so despite cited as a separated species in Flora Iranica ( Grau 1981), it is resynonymized for S. deserti . Additionally, S. kotschyi Boiss. is an unpublished name which is only written on some herbarium specimens of S. deserti . If these specimens are S. deserti , so this name should be considered as a new synonym for S. deserti . Table 1 provides the comparison of morphological characters between these species. Differences in leaf variation and flower structure are also illustrated in Figures 8 and 9 , respectively.

ANATOMY

Anatomical studies showed Scrophularia deserti and S. marginata are similar in term of indumentum, stomata type and blade features. In available references, these species are introduced by glabrous character. But more examination of many populations from the species indicated that stems and leaves are glabrous to sparsely covered with short glandular hairs (23.91-28.26 µm long), which have a sack-shaped head and short 1-cell base.

Also these species represented the anomocytic and anisocytic types of stomata on both leaf surfaces. However, the anomocytic type has the highest density (87.23%) and anisocytic type shows lower density (12.76%). In the species, shape of the guard cells is reniform and the subsidiary cells have irregular margin. The stomata are surrounded by 3, 4 and 5 subsidiary cells, which are equal or unequal in size. In leaves of S. deserti , the quartet subsidiary cells show the highest density (50.22%) and triplet cells (36.17%) and quintet cells (13.61%) have lower density. Likewise in leaves of S. marginata , the quartet subsidiary cells show the highest density (48.31%) and triplet cells (39.27%) and quintet cells (12.42%) have lower density.

In two mentioned species, blade structure is also similar. Some characters such as blade thickness, thickness of upper and lower epidermis, midrib thickness, mesophyll type and idioblast size were measured. In S. deserti , the blade thickness was 347.61-637.51 µm, epidermis thickness in both surfaces was 31.25-52.38 µm and midrib thickness was 261.91-338.09 µm. Mesophyll tissues were asymmetric, in which numerous and large idioblasts in forms elliptic to ovate and in size 104.76- 214.28 × 71.42-95.23 µm were observed. In S. marginata , the blade thickness was 320.83-404.16 µm, epidermis thickness in both surfaces was 29.16-41.66 µm and midrib thickness was 213.54-325.78 µm. Mesophyll tissues were asymmetric, in which numerous and large idioblasts in forms elliptic to orbicular and in size 83.35-129.16 × 70.83-104.16 µm were observed. Details of anatomical study of stem indumentum, leaf stomata and blade structure of the studied species are illustrated in Figures 10 and 11 , respectively.

DISTRIBUTION

The species belonging to this section are the Irano-Turanian and Saharo-Arabian elements and grow in gravelly

stone habitats and sub-mountainous regions at elevation to 2500 m. The most numerous populations of the studied species are present in Asia. Scrophularia deserti is distributed in Afghanistan, Africa, Egypt, Iraq, Iran, Kuwait, Oman, Palestine, Pakistan, Qatar and Saudi Arabia. In Iran, it is widely collected from center, west, south and east, in Fars, Hormozgan, Kerman, Kermanshah, Khorasan-e Jonubi, Khorasan-e Razavi, Khuzestan, Kordestan, Lorestan, Markazi and Sistan and Baluchestan provinces, at elevations from 50 to 2500 m. Scrophularia marginata has limited distribution in Iran and is collected from west, in Hamedan and Kurdestan provinces, at elevations from 1000 to 2250 m. The distribution map of these species along with leaf variation is drawn in Figure 12.

AMENDED COMMENT

The studies on herbarium material and protologue information showed that S. cabulica cannot be a correct synonym for S. deserti and resurrected as a valid species. This species distributed in Afghanistan and Pakistan, differs in leaf size, shape and margin, calyx shape, staminode shape. In addition, the white margined leaf is not seen in this species. So, the species should be removed from the section and its complete description is presented below.

Figures

FIG. 5. — Scrophularia marginata Boiss.: A, habit; B, flower; C, inflorescence; D, leaf (Hamedan: Tuyserkan,6.V.2016, Ranjbar & Rahchamani 59063, BASU, Photographed by Rahchamani). Scale bars: A, 2 cm; B, 1 mm; C, 4 mm; D, 4 cm.

FIG. 6. — Lectotype of Scrophularia marginata Boiss. (Aucher-Eloy 2898, G-DC[G00673693]).

FIG. 7. — The base of Scrophularia marginata Boiss. specimens (Aucher-Eloy 2898): A, G-DC (lecto-, [G00673693]); B, G-BOIS (isolecto-, [G00334025]) (Photo- graphed by Dr Gautier).

FIG. 8. — Variation of the leaf in: A, cauline leaves in Scrophularia deserti Delile; B, cauline leaves in S. marginata Boiss.; C, alike basal leaves in S. deserti and S. marginata (Drawn by Rahchamani). Scale bar: 1 cm.

FIG. 9. — Structure of the flower in: A, Scrophularia deserti Delile; B, S. marginata Boiss., left to right: calyx, ovary, style and calyx; corolla, stamens and stami- node; flower in side view (Drawn by Rahchamani). Scale bar: 5 mm.

FIG. 10. — Anatomical review of Scrophularia deserti Delile:A, stem indumentum;B, blade structure;C, leaf stomata,subsidiary cells hollowed out (Kermanshah:Tazeh Abad to Javanrud, 15 km to Javanrud, 1255 m, 6.V.2017, Ranjbar 41143, BASU). Scale bars: A (left), B (left), 200 µm; A (right), 50 µm; B (right), 100 µm; C, 20 µm.

FIG. 11. — Anatomical review of Scrophularia marginataBoiss.: A, stem indumentum;B, blade structure; C, leaf stomata, subsidiary cells hollowed out (Hamedan: Tuyserkan, 6.V.2016, Ranjbar & Rahchamani 59063, BASU). Scale bars: A (left), B (left), 200 µm; A (right), 50 µm; B (right), 100 µm; C, 20 µm.

FIG. 12. — Distribution map of Scrophularia deserti Delile (●) and S. marginata Boiss. (·) (designed by Pasban).