Research Article |
Corresponding author: Chris J. Thorogood ( chris.thorogood@obg.ox.ac.uk ) Academic editor: Eberhard Fischer
© 2024 Majed Aldughayman, Chris J. Thorogood, Abdulridha A. A. Al-Mayah, Julie A. Hawkins.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Aldughayman M, Thorogood CJ, A. Al-Mayah AA, Hawkins JA (2024) An account of the genus Cistanche (Orobanchaceae) in Iraq and taxonomic considerations in the Middle East. PhytoKeys 238: 281-294. https://doi.org/10.3897/phytokeys.238.116470
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Species limits in the genus Cistanche are poorly understood, despite the plants’ long history of use in traditional herbal medicine and food across their range. Here we present a taxonomic account for the genus Cistanche in Iraq, where several taxa have been reported, most of them doubtfully. Using herbarium specimens, images of living material, and taxonomic literature, we found evidence of only one species occurring with certainty in Iraq: Cistanche tubulosa. We found no evidence for the occurrence of other Cistanche species in Iraq, including a putative new entity reported for the region. Our work highlights inconsistencies in the literature, and underscores the importance of examining multiple stable characters for delimiting species in the genus Cistanche.
Nomenclature, parasitic plant, speciation, taxonomy
Iraq has a rich flora with an estimated 3300 species owing to a convergence of phytogeographic regions and varied climate and topography (
The genus Cistanche Hoffmanns. & Link (family Orobanchaceae), was first identified officially in 1799 by Ventenat under the name Orobanchoideae. A decade later, the genus Cistanche was described by
Cistanche is a holoparasite that lacks vegetative traits traditionally used in taxonomy, including functional leaves and roots. The poor condition of herbarium specimens — particularly type specimens — has generated confusion in identification. Here we examine herbarium specimens, images of living material, and taxonomic literature to produce the first robust review of the genus Cistanche in Iraq, which will inform the treatment for the Flora, and other treatments for the genus in the Middle East.
We reviewed the names used for Cistanche in Iraq and neighbouring countries. The sources that were used to identify species of Cistanche putatively in Iraq, and the species in their accounts, were as follows:
Protologues for Cistanche eremodoxa, C. salsa, C. ridgewayana, C. fissa, C. laxiflora, C. flava, C. ambigua, C. lutea and C. phelypaea — the species identified as putatively in Iraq and adjacent regions of neighbouring countries — were examined as well the description of the unpublished putative species C. chabaharensis (
Google Earth was used to create coordinate assumptions for those specimens for which true coordinates were unavailable (Fig.
A literature review of Iraq and of adjacent countries, and of other relevant taxonomic studies, identified 10 published names and one unpublished name for species putatively in Iraq and adjacent countries. Species in adjacent countries, especially in Iran including, C. eremodoxa, C. ridgewayana, C. fissa, C. laxiflora and C. ambigua, were excluded from this investigation as their distributions and morphology suggest they are unlikely to exist in Iraq. Of the other species, two Atlantic/western European taxa were excluded on the basis that they are exceptionally unlikely to occur in the Middle East: C. lutea and C. phelypaea. Although C. lutea was cited in the Flora of Syria, Palestine and Sinai, the description does not provide adequate detail of morphological characters to discriminate between this and other species, including C. tubulosa. Cistanche phelypaea, as circumscribed currently, is a primarily Atlantic, coastal species, frequent from southwest Portugal south to Macaronesia and the coast of Morocco. We consider the inclusion of C. phelypaea in the Flora of Saudi Arabia to be equivocal, and cited with insufficient detail to merit further examination.
Finally, we considered C. chabaharensis, an as yet unpublished name referred to in the thesis of
A herbarium specimen of C. tubulosa collected in Iraq, mistakenly identified as C. flava B the holotype of putative species C. chabaharensis; note the woolly anther (inset) typical of C. tubulosa C herbarium specimen of C. tubulosa in (W) collected in lowland of Iraq, mistakenly identified as C. salsa.
Key morphological characters of Cistanche species putatively found in Iraq and adjacent territories.
Characters | C. tubulosa | C. salsa | C. flava |
---|---|---|---|
Scales | ovate- lanceolate, obtuse, glabrous, sinuate | ovate- lanceolate, obtuse, pilose on the outer side, scarious | long-lanceolate, obtuse, glabrous, scarious |
Bract | ovate-lanceolate, glabrous, sinuate, equal or slightly longer than calyx | oblong-lanceolate, pilose on the outer side, longer than the calyx, entire | oblong-linear, glabrous, scarious, sinuate, twice long as the calyx or even as long as corolla |
Bracteole | oblong- lanceolate, glabrous, sinuate, equal or shorter than calyx | linear-oblong, pilose on the outer side, entire, equal or slightly longer than calyx | oblong-linear, glabrous, sinuate, slightly shorter than calyx |
Calyx | tubular, up to 1⁄2 total corolla length, 5 lobes, oblong to oblong-ovate, glabrous, sinuate | tubular, ca. 1/3 corolla length, 5 lobes, oblong, pilose on the outer side and at the margins, entire | tubular-campanulate, 5 lobes, oblong to oblong-ovate, glabrous, sinuate |
Corolla | tubular-campanulate, 5 lobes, orbicular, glabrous, yellowish throughout or with violet limb (especially in bud) | campanulate, 5 lobes, orbicular, sparsely ciliate at the lobes, mauve and white | tubular-campanulate, 5 lobes, orbicular, glabrous, yellow to blue-violet |
Anther | ovate, obtuse at ends, densely pilose | ovate, obtuse at base and slightly aristate at apex, densely pilose | ovate, obtuse at ends, densely pilose |
Stigma | bilobate | bilobate | bilobate |
Here we consider the three taxa identified to potentially co-occur in the region. Cistanche salsa can be readily differentiated from C. flava and C. tubulosa by its hairiness; the latter two species are glabrous (see key). Cistanche flava is differentiated from C. tubulosa by its scarious, conspicuously long bracts which are twice as long as the calyx or even longer (Table
Cistanche species putatively found in Iraq and adjacent territories A, B C. tubulosa (photographed in Iran) C, D C. flava (photographed in Kazakhstan) E, F C. tubulosa (photographed in Iraq; note excavated stem bases in E). Used with permission: photographs A, B by Sajad Alipour; photograph C by Lina Valdschmit; photograph D by Bobur Karimov.
The name Cistanche tubulosa s.l. is used from Africa and the Middle East to South and Central Asia and China, however as currently applied, the name refers to a widely distributed, polyphyletic group of plants (
All material we examined from four Governorates: Karbala, Basrah, Muthanna and Wasit correspond to C. tubulosa (in its current, most widely-accepted circumscription). None of the material we examined pertained to either C. salsa or C. flava, based on our careful consideration of the traits emphasized above. Similarly, none of the specimens tentatively labelled C. salsa corresponded with that species either (Fig.
Our extensive investigation based on herbarium specimens revealed that C. tubulosa occurs in every Governorate of Iraq except for the Kurdistan Autonomous Region. This could be due to the wide distribution of potential hosts across three of four main ecological regions, namely the deserts west of the Euphrates River, Upper Mesopotamia and Lower Mesopotamia (
It is of note that the corolla colour of C. tubulosa varies with age and population, from pale lemon yellow, to deep orange-yellow, with varying levels of pink to violet pigmentation. Similarly, the height and stature vary from 15 cm to 130 cm depending on rainfall and, potentially, host species. The key below is based on our observations of multiple populations across the region.
1 | Plants lanate to glabrescent; whitish, with purple pigmentation | C. salsa |
– | Plants glabrous; cream to yellow with or without purple pigmentation | 2 |
2 | Bracts short: ovate-lanceolate, sinuate, equal to or scarcely exceeding the calyx | C. tubulosa |
– | Bracts long and slender: oblong-linear, glabrous, scarious, sinuate, 2 x the calyx | C. flava |
Phelypaea tubulosa
A robust, thick, glabrous plant, (15)20–50(130) cm tall. Lower scales sinuate, imbricate, broadly lanceolate, up to 3 cm long. Upper scales sinuate, ovate-lanceolate, grey, 4–10 m long. Bracts deeply sinuate, ovate-lanceolate, equal or slightly exceeding the calyx, grey, 14–22 mm long. Bracteoles sinuate, oblong-lanceolate, equalling or shorter than calyx, grey, 2–3 mm long. Calyx tubular, pentamerous, usually 1/2 the corolla length, with lobes subequal or one slightly shorter, oblong, obtuse. Corolla tubular-campanulate, pentamerous, lemon yellow to deep yellow, often with violet limb, 34–52 mm long, lobes equal, rounded. Stamens didynamous, epipetalous, densely woolly at the base. Anthers cordate, rounded at the base and acute at the apex, densely woolly. Ovary ovate. Style cylindrical, oblique. Stigma bilobate. Fruit a splitting capsule. Seeds small, black and numerous.
Dunes, gravel substrates, mudstone, or seasonally arid saline habitats.
Haloxylon salicornicum (Moq.) Bung, Capparis spinosa, Zygophyllum propinquum Decne (syn. Tetraena propinqua), Tamarix spp., Salsola spp.
Ephedra spp., Limonium spp., Anabasis spp.
Iraq: Diyala: Hamrin, near Shahraban, 34°16'06.8"N, 44°48'48.5"E, 8 May 1958, s. col. s,n. (E); Shahraban, 33°56'09.4"N, 44°55'10.8"E, 11 April 1957, Haines Wheeler 847 (E,K); Mandali, 33°42'48.9"N, 45°32'06.1"E, 26 March 1932, E.R. Guest 1742 (K, BAG); 30 km north east Mandali, 210 m, 33°48'35.5"N, 45°34'48.7"E, 26 April 1979, Al-kaisi & Khayat 50782 (K); Basrah: 77 km northwest of Zubair, 30°36'12.5"N, 47°00'36.7"E, 19 March 1964, Fred Barkley & Hikmat Abbas Al-ani 6499 (K,W); Near Jalibah, 30°27'57.0"N, 46°52'02.6"E, 8 April 1933, s. col. 5065 (K); 28 km south east by south of Zubair, 12 m, 30°16'33.4"N, 47°47'35.6"E, 23 March 1957, E. R. Guest, A. Rawi & K. H. Rechinger 16875 (K, BAG); 70 km east of Zubair, 30°17'35.3"N, 48°06'29.9"E, 13 February 1973, Turner 47457 (K); Between Zubair and Safwan, 30°15'41.7"N, 47°41'29.4"E, 23 March 1966, H. Alizzi 34341 (K); Rumaila, Toba railway station 20 km west of Ghubaishiyia, 30°32'56.0"N, 47°17'51.3"E, 27 March 1965, Sharif Y. Haddad 9535 (K); 30 km west of Jabal Sanam, 30°08'13.1"N, 47°27'36.6"E, 15 April 1963, Khalid Alizzi 32684 (K, BAG); Umm Qasr Port, 30°01'43.7"N, 47°56'05.3"E, 13 March 1973, Husain Al-ali 39929 (K); Jabal Sanam, 150 m, 30°07'43.5"N, 47°37'09.5"E, 6 March 1961, s. col. 29889 (BAG); Southern desert of Zubair, 30°20'00.0"N, 47°40'00.0"E, 23 March 1957, K. H. Rechinger 5247 (W); Shaib Al-batin, Jarishan, 30°04'06.1"N, 47°09'25.4"E, 24 March 1957, K. H. Rechinger (W); 6 km Southeast of Safwan, 30°05'08.2"N, 47°47'51.7"E, 23 March 1957, K. H. Rechinger 5245 (W); Anbar: 10 km N of Rutba, 33°09'48.3"N, 40°15'29.1"E, 28 February 1947, Rawi & Gillett 6326 (K); 10 km from Hit to Kubaysah, 33°38'19.9"N, 42°48'17.0"E, 85 m, 31 March 1976, S. Omar, Alkaisi, K. Hamad & H. Hamid 44354 (K); Ramadi east of Lake Tharthar, 33°29'28.6"N, 43°16'56.9"E, 3 April 1964, Fred A. Barkley & Ramdan Eljumaili 7263 (K); Shbaichan road 10 km north of Rawah, 34°34'24.8"N, 41°56'17.7"E, 260 m, 3 April 1962, Khatib & Hlizzi 31967 (K); 20 km north west Fallujah, 33°23'45.6"N, 43°48'58.9"E, 24 April 1982, Omar & Alkhayat 31967 (BAG); 10 km from Hit to Kubaysah, 33°38'19.9"N, 42°48'17.0"E, 85 m, 31 March 1976, S. Omar, Alkaisi, K. hamad & H. Hamid 44354 (BAG); Between Fallujah and Wadi Tharthar, 33°32'24.2"N, 43°37'13.0"E, 3 May 1957, K. H. Rechinger 11247 (W); Muthanna: 10 km south of Samawah, 31°15'03.0"N, 45°17'21.1"E, 20 m, 21 February 1947, Rawi & Gillett 6125 (K); 15 km west of Samawah, 31°18'44.5"N, 45°07'24.0"E, 20 m, 19 March 1955, Ali Rawi 14880 (K); 25 km to Busaiya from Al-Khidr Al-mai, 30°12'23.7"N, 46°20'46.6"E, 200 m, 24 February 1978, Alkaisi, K. Hamad & H. Hamid 48514 (K); Al-Khidr Al-mai enclosure, 31°12'00.7"N, 45°33'11.5"E, 21 January 1978, F. Karim, A. Sharief, K. Hamad & H. Hamid 48066 (K); 50 km east of Busaiya to Al-khidr Al-mai, 30°39'58.4"N, 46°01'13.1"E, 21 January 1978, F. Karim, A. Sharief, K. Hamad & H. Hamid 48034 (K); 13 km west Samawah, 31°19'42.8"N, 45°12'30.5"E, 40 m, 26 March, Ibrahim Al-mahallal 15204 (K,BAG); Wasit: Kut, 32°39'07.9"N, 45°45'49.2"E, 19 April 1967, Alizzi & S. Omar 34893 (K); 55 km east of Kut, 32°26'50.8"N, 46°23'40.4"E, 6 March 1963, F. A. Barkley 33Ir4055 (K); 5 km from Badra to Kut, 32°33'17.2"N, 45°48'13.6"E, 90 m, 12 March 1977, Al-kaisi & H. Hamid 46525 (K,BAG); 51 km northeast of Kut between Jassan and Badrah, 33°01'52.0"N, 45°54'14.1"E, 5 April 1964, Hikmat Abbas & F. R. Bharucha 2613 (K,W); 80 km west of Shayk Sa’d, 32°35'05.8"N, 46°08'01.5"E, 30 m, 4 April 1958, Ali Rawi & S. Haddad 25520 (K); 10 km east of Zurbatiyah, 33°11'38.8"N, 46°04'38.3"E, 240 m, 13 March 1977, Al-kaisi & H. Hamid 46551 (BAG); Karbala: 8 km west of Karbala, 32°31'20.8"N, 44°00'59.8"E, 9 March 1947, Rawi & Gillett 6415 (K); Razazza, 32°37'59.4"N, 43°53'52.1"E, 38 m, 18 March 2019, A. Haloob, Ikhlas, R. Hamshkan & Riyadh 59879 (BAG); 2 km west of Ukhaidir, 32°26'25.5"N, 43°35'30.1"E, 60 m, 12 March 1980, s.col. 51219 (BAG); 18 km west of Karbala, 32°33'18.5"N, 43°53'14.1"E, 40 m, 4 May 1964, Martin L. Grant 18228 (W); Dhi Qar: Eridu, 30°49'49.9"N, 45°59'54.3"E, 1 February 1947, Seton Lloyd 6328 (K,BAG); Nineveh: Faidah Al-rbaswi, 36°37'09.7"N, 42°58'38.3"E, 7 April 1973, F. Karim, M. Noori, H. Hamid & H. Kadhim 40279 (K); 6 km from Rabia, 36°47'17.3"N, 42°06'55.9"E, 1 April 1973, F. Karim, H. Hamid & H. Kadhim 39944 (K); Najaf: Al-Hira, 31°53'18.1"N, 44°29'28.6"E, 8 m, 6 March 2018, Riyadh, Yasin, Dhya’a, Adel & Sinan 59291 (BAG). FPF, chelat-Amara, AL-Mayah and AL-Asady 16122 BSRA. FPF, wadi AL-Tib -Mayah and AL-Asady 15130 BSRA. DSD, Basrah-Nassiria road, 30km from Zubair towords Nassirya, AL-Mayah 1995 BSRA. DSD, Slop of jabal sanam, s.w. of Safwan, Basrah, I.A.AL-Mayah and J.Dehry 1597,BSRA. DSD, Zubair, AL-Mayah and AL-Asady 1404 BSRA. DSD,JARISHAN AL-Mayah and AL-Asady 1418 BSRA. DSD, Jabal Sanam AL-Mayah and AL-Asady 1419 BSRA.
The authors have declared that no competing interests exist.
No ethical statement was reported.
No funding was reported.
Majed Aldughayman conducted the research, Chris Thorogood and Julie Hawkins wrote the manuscript; Abdulridha A. A Al-Mayah contributed to the work.
Chris J. Thorogood https://orcid.org/0000-0002-2822-0182
Julie A. Hawkins https://orcid.org/0000-0002-9048-8016
All of the data that support the findings of this study are available in the main text.