Abstract
A multivariate morphometric study of the Balkan taxa from the diploid–polyploid complex of Alyssum montanum-A. repens (Brassicaceae) was performed. The western European species A. montanum and central European A. gmelinii were also included in the study for comparison. A total of 1969 individuals from 89 populations were studied to explore morphological differences among taxa or genetic groups revealed in a parallel study by a combination of molecular and cytometric evidence. According to our results, several Balkan taxa are clearly morphologically differentiated, namely A. handelii, A. moellendorfianum, A. pirinicum, A. rostratum and A. wierzbickii. Other species—A. bosniacum, A. montenegrinum, A. reiseri and A. vernale—exhibit overlaps in values of the most differentiating characters, but can all be steadily distinguished. Alyssum repens, which is not genetically compact, is still morphologically recognizable from other Balkan taxa. Two species, A. austrodalmaticum and A. gmelinii, despite having clear genetic differences and an allopatric distribution, only have minor morphological differences. The tentatively accepted genetically heterogeneous species A. spruneri, which includes a major portion of the Greek and central Balkan populations, is also extraordinarily variable in morphology. An identification key of the studied taxa and their synonymy are provided. The taxonomic treatments of the recognized species and their geographic distribution are discussed.
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References
Ančev ME (1978) [Reports]. In: Löve Á (ed) IOPB chromosome number reports LXII. Taxon 27:532–533. https://www.jstor.org/stable/1219912
Ančev M (2007) Catalogue of the family Brassicaceae (Cruciferae) in the flora of Bulgaria. Phytol Balcan 13:153–178
Anchev ME (1991) Rod Alyssum L. v bulgarskata flora. In: Kozhukharov SI, Kuzmanov BA (eds) Evolyutsiya na tsvetnite rasteniya i florogenezis. 2. Slozhnotsvetni, krustotsvetni, zhitni rasteniya i ostritsovi. Izdatelstvo na Bulgarskata akademia na naukite, Sofiya, pp 85–117
Baldacci A (1891) Nel Montenegro. Una parte delle mie raccolte. Malpighia 5:62–82
Ball PW, Dudley TR (1993) Alyssum L. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora europaea 1. Ed. 2. Cambridge University Press, Cambridge, pp 359–369
Baumgartner J (1907) Die ausdauernden Arten der Sectio Eualyssum aus der Gattung Alyssum. Jahresber Nieder-Österr Landes-Lehrersem Wiener-Neustadt 34:1–35
Baumgartner J (1908) Die ausdauernden Arten der Sectio Eualyssum aus der Gattung Alyssum. Jahresber Nieder-Österr Landes-Lehrersem Wiener-Neustadt 35:1–58
Beck von Mannagetta G (1916) Flora Bosne, Hercegovine i novopazarskog Sandžaka. Glasn Zemaljsk Muz Bosni Hercegovini 28:47–468
JACQ Consortium (2004 onwards) Virtual Platform for Botanical Specimens. Available at: http://herbarium.univie.ac.at/database/search.php
Dihoru G, Negrean G (2009) Cartea roşie a plantelor vasculare din România. Editura Academiei Române, Bucureşti
Diklić N (1972) 24. Rod Alyssum L. In: Josifović M, Stjepanović L, Janković MM, Gajić M, Kojić M, Diklić N (eds) Flora SR Srbije 3. Srpska akademija nauka i umetnosti, Beograd, pp 286–311
Dorofeyev VI (2002) Krestotsvetnye (Cruciferae Juss.) Evropeiskoi Rossii/Cruciferae of European Russia. Turczaninowia 5(3):5–114
Dorofeyev VI (2003) Krestotsvetnye (Cruciferae Juss.) Rossiiskogo Kavkaza/Cruciferae of Russian Caucasus. Krestotsvetnye. Turczaninowia 6(3):5–137
Dorofeyev VI (2012) Fam. 70 Brassicaceae Burnett, nom. cons., nom. alt. In: Takhtajan AL (ed) Konspekt flory Kavkaza/Conspectus florae Caucasi. Tovarishchestvo nauchnykh izdanii KMK, Moskva, Sankt-Peterburg, pp 371–469
Dudley TR (1962) Some new Alyssa from the near east. Notes Roy Bot Gard Edinburgh 24:157–165
Dudley TR (1965) Alyssum L. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands 1. Edinburgh University Press, Edinburgh, pp 362–409
Dudley TR (1966) A new Greek endemic: Alyssum vourinonense and a note regarding Bornmuellera. Oesterr Bot Z 113:265–270
Geideman TS (1954) Opredelitel’ rastenii Moldavskoi SSR. Izdatel’stvo Akademii Nauk SSSR, Moskva, Leningrad
Güntsch A, Hyam R, Hagedorn G, Chagnoux S, Röpert D, Casino A, Droege G, Glöckler F, Gödderz K, Groom Q, Hoffmann J, Holleman A, Kempa M, Koivula H, Marhold K, Nicolson N, Smith VS, Triebel D (2017) Actionable, long-term stable and semantic web compatible identifiers for access to biological collection objects. Database 2017: bax003
Hartvig P (1986) Alyssum L. In: Strid A (ed) Mountain flora of Greece 1. Cambridge University Press, Cambridge, pp 281–303
Hartvig P (2002) Alyssum L. In: Strid A, Tan K (eds) Flora Hellenica 2. A.R.G. Gantner Verlag K. G, Ruggell, pp 199–227
Hayek A (1925) Prodromus florae peninsulae Balcanicae. 1. Band: Pteridophyta, Gymnospermae, Dicotyledoneae (Apetalae et Choripetalae). Repert Spec Nov Regni Veg Beih 30/1(3):353–672
Heuffel MD (1835) Plantarum Hungariae novarum vel non rite cognitarum Decas II. Flora (Regensburg) 18:241–256
Holub J (1984) Subspecies names in Jávorka, Magyar Flóra (1924–1925). Preslia 56:303–318
Hornemann JW (1815) Hortus regius botanicus Hafniensis 2. Hauniae
Jalas J, Suominen J, Lampinen R (1996) Atlas florae europaeae 11. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, Helsinki
Jordan A, Fourreau J (1868) Breviarum plantarum novarum 2. F. Savy, Paris
Klecka WR (1980) Discriminant analysis. Sage University Papers, Series: Quantitative Applications in the Social Sciences, no. 19, Beverly Hills
Klokov MV, Visjulina OD (eds) (1953) Flora USSR, vol 5. Vydavnytstvo Akademii Nauk Ukrains’koi RSR, Kyiv
Kotov MI (1979) Brassicaceae. In: Fedorov AA (ed) Flora evropeiskoi chasti SSSR IV. Nauka, Leningrad, pp 30–148
Magauer M, Schönswetter P, Jang T-S, Frajman B (2014) Disentangling relationships within disjunctly distributed Alyssum ovirense/A. wulfenianum group (Brassicaceae), including description of a novel species from the north-eastern Alps. Bot J Linn Soc 176:486–505. https://doi.org/10.1111/boj.12214
Marhold K (2011) Multivariate morphometrics and its application to monography at specific and infraspecific levels. In: Stuessy TF, Lack HW (eds) Monographic plant systematics: Fundamental assessment of plant biodiversity. Gantner, Ruggel, pp 73–99
Markgraf F (1960) Alyssum L. In: Hegi G, Illustrierte Flora von Mitteleuropa 4/1 (4. Lieferung). Carl Hanser, München, pp 277–290
McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme van Reine WF, Smith GF, Wiersema JH, Turland NJ (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code): adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Koeltz Scientific Books, Königstein [Regnum Veg 154:1–208]
Nyárády EI (1955) Cruciferae. In: Săvulescu T (ed) Flora Republicii Populare Romîne 3. Editura Academiei Republicii Populare Romîne, Bucharest, pp 102–501
Oprea A (2005) Lista critică a plantelor vasculare din România. Edit. Univ. „Al. I. Cuza”, Iaşi
Plazibat M (1997) Brassicaceae (=Cruciferae). In: Nikolić T (ed) Flora Croatica. Index Florae Croaticae, Pars 2. Nat Croat 6 (Suppl.): 21–39
Plazibat M (2009) A short synopsis of the tribe Alysseae (Brassicaceae) in Croatia with some taxonomic novelties. Nat Croat 18:401–426
Rešetnik I, Satovic Z, Schneeweiss GM, Liber Z (2013) Phylogenetic relationships in Brassicaceae tribe Alysseae inferred from nuclear ribosomal and chloroplast DNA sequence data. Molec Phylogen Evol 69:772–785. https://doi.org/10.1016/j.ympev.2013.06.026
Ruprecht FJ (1869) Flora Caucasi 1. Mém Acad Imp Sci Saint-Pétersbourg, sér. 7, 15(2):1–302
SAS Institute Inc. (2009) SAS/STAT® 9.2 user’s guide, 2nd edn. SAS Institute, Cary
Schols P, Dessein S, Dhondt C, Huysmans S, Smets E (2002) Carnoy: a new digital measurements tool for palynology. Grana 41:124–126
Smejkal M (1992) Alyssum L. In: Hejný S, Slavík B, Kirschner J, Křísa B (eds) Květena České republiky 3. Academia, Praha, pp 144–149
Španiel S, Marhold K, Filová B, Zozomová-Lihová J (2011a) Genetic and morphological variation in the diploid-polyploid Alyssum montanum in Central Europe: taxonomic and evolutionary considerations. Pl Syst Evol 294:1–25. https://doi.org/10.1007/s00606-011-0438-y
Španiel S, Marhold K, Passalacqua NG, Zozomová-Lihová J (2011b) Intricate variation patterns in the diploid-polyploid complex of Alyssum montanum-A. repens (Brassicaceae) in the Apennine peninsula: evidence for long-term persistence and diversification. Amer J Bot 98:1887–1904. https://doi.org/10.3732/ajb.1100147
Španiel S, Marhold K, Thiv M, Zozomová-Lihová J (2012a) A new circumscription of Alyssum montanum ssp. montanum and A. montanum ssp. gmelinii (Brassicaceae) in Central Europe: molecular and morphological evidence. Bot J Linn Soc 169:378–402. https://doi.org/10.1111/j.1095-8339.2012.01225.x
Španiel S, Zozomová-Lihová J, Passalacqua NG, Marhold K (2012b) Infraspecific classification of Alyssum diffusum (Brassicaceae) in Italy. Willdenowia 42:37–56. https://doi.org/10.3372/wi.42.42104
Španiel S, Kempa M, Salmerón-Sánchez E, Fuertes-Aguilar J, Mota JF, Al-Shehbaz IA, German DA, Olšavská K, Šingliarová B, Zozomová-Lihová J, Marhold K (2015) AlyBase: database of names, chromosome numbers, and ploidy levels of Alysseae (Brassicaceae), with a new generic concept of the tribe. Pl Syst Evol 301:2463–2491. https://doi.org/10.1007/s00606-015-1257-3
Španiel S, Marhold K, Zozomová-Lihová J (2017) The polyploid Alyssum montanum-A. repens complex in the Balkans: a hotspot of species and genetic diversity. Pl Syst Evol. doi: https://doi.org/10.1007/s00606-017-1470-3
Stafleu FA, Cowan RS (1983) Taxonomic literature, vol. 4.: P-Sak, 2nd edn. Regnum Veg. 110. Bohn, Scheltema & Holkema, Utrecht
Stojanov N (1970) Alyssum L. In: Jordanov D (ed) Flora na narodna republika Bulgarija 4. Izdatelstvo na Bulgarskata Akademija na Naukite, Sofija, pp 489–512
Stojanov N, Achtarov B (1939) Neues Material zur Kenntnis der Flora des Pirin-Gebirges. Izv Carsk Prir Inst Sofija 12:181–187
Strid A, Franzén R (1982) New Floristic Records from the Mountains of Northern Greece (Materials for the Mountain Flora of Greece, 12). Willdenowia 12:9–28
Thiers B (2014) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, New York. Available at: http://sciweb.nybg.org/science2/IndexHerbariorum.asp. Accessed 22 Aug 2017
Thorpe RS (1976) Biometric analysis of geographic variation and racial affinities. Biol Rev Cambridge Philos Soc 51:407–452. https://doi.org/10.1111/j.1469-185X.1976.tb01063.x
Tretiyakov DI (1990) Novye i redkie vidy sosudistykh rastenii dlya flory Belorussii. Bot Zhurn 75:255–266
Trinajstić I (1982) Taxa nova et combinationes novae in Flora Jugoslaviae 8. Suppl Fl Anal Jugosl 8:3–11
Trinajstić I (1983) Analitička Flora Jugoslavije 2(3). Liber, Zagreb
Trpin D (1984) Alyssum montanum-kompleks v jugovzhodni Jugoslaviji. Razpr Slov Akad Znan Umetn, Razr Nar Vede 25:239–291
Velenovský J (1891) Flora Bulgarica. Descriptio et enumeratio systematica plantarum vascularium in principatu Bulgariae sponte nascentium. Fr. Řivnáč, Pragae
Zozomová-Lihová J, Marhold K, Španiel S (2014) Taxonomy and evolutionary history of Alyssum montanum (Brassicaceae) and related taxa in southwestern Europe and Morocco: diversification driven by polyploidy, geographic and ecological isolation. Taxon 63:562–591. https://doi.org/10.12705/633.18
Acknowledgements
We are grateful to all the colleagues who accompanied us in the field. We would like to thank to Directorate of Pirin National Park (Bansko) for permission to collect samples of Alyssum and to D. Lakušić (Belgrade) and M. Anchev (Sofia) for providing advice on the localities of Alyssum montanum s.l. in Serbia and Bulgaria, respectively. We also thank the curators of the herbaria for allowing us to access their collections. We thank Ihsan A. Al-Shehbaz and Dmitry A. German for helpful comments on typifications. This study was financially supported by the Slovak Research and Development Agency (APVV, Grant no. APVV-0139-12 to J.Z.-L. and K.M.), Grant Agency VEGA, Bratislava, Slovak Republic (Grant No. 2/0133/17 to S.Š.), the Czech Science Foundation (Grant No. 16-10809S to K.M.), the European Social Fund and the state budget of the Czech Republic (CZ.1.07/2.3.00/30.0022 to S.Š.). Part of the field expenses in Bulgaria and Romania was funded by the cooperation schemes of Slovak Academy of Sciences with Romanian Academy of Sciences and Bulgarian Academy of Sciences.
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Online Resource 1. Overview of the taxonomic treatment of the Alyssum montanum-A. repens complex in the Balkans based on the present study, and previous taxonomic treatments.
Online Resource 2. Results of classificatory discriminant analyses DA 1, DA 2, DA 3 and DA 4.
Online Resource 3. Results of canonical discriminant analyses (CDA 1–CDA 6) showing total canonical structure values that express correlations of morphological characters with canonical axes.
Online Resource 4. Descriptive statistics of the measured morphological characters of the 17 taxa/genetic groups of the Alyssum montanum-A. repens complex in the Balkans.
Online Resource 5. Canonical discriminant analysis of A. spruneri subgroup ‘graecum’ based on 20 morphological characters and individuals of two predefined groups: the population from Mt. Smolikas (185SMOm, 29 plants) and all the other poulations (336 plants).
Online Resource 6. Revised herbarium specimens of selected Alyssum species in herbaria BP, BUCA, GJO, LE, PRC, SOM, W, WU, and WU-Hal.
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Španiel, S., Zozomová-Lihová, J. & Marhold, K. Revised taxonomic treatment of the Alyssum montanum-A. repens complex in the Balkans: a multivariate morphometric analysis. Plant Syst Evol 303, 1413–1442 (2017). https://doi.org/10.1007/s00606-017-1468-x
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DOI: https://doi.org/10.1007/s00606-017-1468-x