Campanula cichoracea (Campanulaceae), a neglected species from the Balkan-Carpathian C. lingulata complex as inferred from molecular and morphological characters

Siniša Škondrić; Jelena M. Aleksić; Dmitar Lakušić

doi:10.3372/wi.44.44111

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19 March 2014 Campanula cichoracea (Campanulaceae), a neglected species from the Balkan-Carpathian C. lingulata complex as inferred from molecular and morphological characters

Siniša Škondrić, Jelena M. Aleksić, Dmitar Lakušić

Author Affiliations +

Willdenowia, 44(1):77-96 (2014). https://doi.org/10.3372/wi.44.44111

Abstract

The taxonomically intricate Campanula lingulata complex confined to the Balkan Peninsula is reviewed using molecular and morphological data. An extensive sample of 62 individuals for phylogenetic analyses and 402 individuals for morphometric analysis from 17 populations across the species range was used. The phylogenetic analyses based on two chloroplast intergenic spacers (trnG^UCC-trnS^GCU and psbA-trnH) and morphological analysis based on 50 characters revealed two allopatrically distributed lineages of the C. lingulata complex that comprise individuals from the C and S Balkans, respectively. Both molecular and morphological data allowed us to re-establish C. cichoracea Sm., a species endemic to Thessaly in Greece. This species can easily be distinguished from C. lingulata s.str. by its calyx appendages hairy on the margins and adaxial side, and ovary continuously downwards hairy all over the surface. Molecular characters that can be used to distinguish these two species comprise four parsimony-informative substitutions within trnG^UCC-trnS^GCU, and a microsatellite with a dinucleotide (AT) motif present only within the psbA-trnH region in C. lingulata. Further studies are required for resolving the taxonomic status of the remaining Macedonian and Rhodopean sub-lineages from the S Balkans.

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References

1.

J. M. Aleksić , D. Stojanović , B. Banović & R. Jančić 2012: A simple and efficient DNA isolation method for Salvia officinalis. — Biochem. Genet. 50: 881–892. Google Scholar

2.

T. Borsch , N. Korotkova , T. Raus , W. Lobin & C. Löhne 2009: The petD group II intron as a species level marker: utility for tree inference and species identification in the diverse genus Campanula (Campanulaceae). — Willdenowia 39: 7–33. Google Scholar

3.

A. L. P. P. de Candolle 1830: Monographie des Campanulacées. — Paris: Desray. Google Scholar

4.

CBOL Plant Working Group 2009: A DNA barcode for land plants. — Proc. Natl. Acad. Sci. U.S.A. 106: 12794–12797. Google Scholar

5.

N. Cellinese , S. A. Smith , E. J. Edwards , S.-T. Kim , R. C. Haberle , M. Avramakis & M. J. Donoghue 2009: Historical biogeography of the endemic Campanulaceae of Crete. — J. Biogeogr. 36: 1253–1269. Google Scholar

6.

M. W. Chase & M. F. Fay 2009: Barcoding of plants and fungi. — Science 325: 682–683. Google Scholar

7.

F. Conti , G. Abbate , A. Alessandrini & C. Blasi 2005: An annotated checklist of the Italian vascular flora. — Roma: Palombi. Google Scholar

8.

J. Damboldt 1978: Campanula L. — Pp. 2–64 in: P. H. Davis (ed.), Flora of Turkey and the East Aegean Islands 6. — Edinburgh: University Press. Google Scholar

9.

A. Degen 1938: Flora velebitica 3. — Budapest: Verlag der Ungar. Akademie der Wissenschaften. Google Scholar

10.

J. J. Doyle & J. L. Doyle 1987: A rapid isolation procedure for small quantities of fresh leaf tissue. — Phytochem. Bull. Bot. Soc. Amer. 19: 11–15. Google Scholar

11.

A. J. Drummond , M. A. Suchard , D. Xie & A. Rambaut 2012: Bayesian phylogenetics with BEAUti and the BEAST 1.7. — Molec. Biol. Evol. 29: 1969–1973. Google Scholar

12.

W. M. M. Eddie & M. J. Ingrouille 1999: Polymorphism in the Aegean “five-loculed” species of the genus Campanula, section Quinqueloculares (Campanulaceae). — Nordic J. Bot. 19: 153–169. Google Scholar

13.

W. M. M. Eddie , T. Shulkina , J. Gaskin , R. C. Haberle & R. K. Jansen 2003: Phylogeny of Campanulaceae s.str. inferred from ITS sequences of nuclear ribosomal DNA. — Ann. Missouri Bot. Gard. 90: 554–575. Google Scholar

14.

R. C. Edgar 2004: MUSCLE: multiple sequence alignment with high accuracy and high throughput. — Nucl. Acids Res. 32: 1792–1797. Google Scholar

15.

Euro+Med 2006+ [continuously updated]: Euro+Med PlantBase — the information resource for Euro-Mediterranean plant diversity. — Published at http://ww2.bgbm.org/EuroPlusMed [accessed 4 Aug 2013]. Google Scholar

16.

A. A. Fedorov 1957: Campanulaceae Juss. — Pp. 126–450, 459–475 in: B. K. Shishkin (ed.). Flora URSS 24. — Moscow: Akademia Nauk. Google Scholar

17.

A. A. Fedorov & M. Kovanda 1976: Campanula L. — Pp. 4–93 in: T. G. Tutin , N. A. Burges , A. O. Chater , J. R. Edmondson , V. H. Heywood , D. M. Moore , D. H. Valentine , S. M. Walters & D. A. Webb (ed.). Flora europaea 4. — Cambridge: University Press. Google Scholar

18.

N. Filipowicz , M. H. Nee & S. S: Renner 2012: Description and molecular diagnosis of a new species of Brunfelsia (Solanaceae) from the Bolivian and Argentinean Andes. — PhytoKeys 10: 83–94 [online at http://dx.doi.org/10.3897/phytokeys.10.2558 ]. Google Scholar

19.

B. Frajman & G. M. Schneeweiss 2009: A campanulaceous fate: the Albanian stenoendemic Asyneuma comosiforme in fact belongs to isophyllous Campanula. — Syst. Bot. 34: 595–601. Google Scholar

20.

P. A. González-Gutiérrez , E. Köhler & T. Borsch 2013: New species of Buxus (Buxaceae) from northeastern Cuba based on morphological and molecular characters, including some comments on molecular diagnosis. — Willdenowia 43: 125–137. Google Scholar

21.

W. Greuter , H. M. Burdet & G. Long (ed.) 1984: Med-Checklist 1. — Genève: Conservatoire et Jardin botaniques & Med-Checklist Trust of OPTIMA. Google Scholar

22.

H. I. Griffiths , B. Kryštufek & J. M. Reed (ed.) 2004: Balkan biodiversity: pattern and process in the European hotspot. — Dordrecht: Kluwer. Google Scholar

23.

A. Grisebach 1846: Spicilegium florae rumelicae et bithynicae 2. — Brunsvigae: F. Vieweg et filium. Google Scholar

24.

R. C. Haberle , A. Dang , T. Lee , C. Peñaflor , H. Cortes-Burns , A. Oestreich , L. Raubeson , N. Cellinese , E. J. Edwards , S.-T. Kim , W. M. M. Eddie & R. K. Jansen 2009: Taxonomic and biogeographic implications of a phylogenetic analysis of the Campanulaceae based on three chloroplast genes. — Taxon 58: 715–734. Google Scholar

25.

M. B. Hamilton 1999: Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. — Molec. Ecol. 8: 521–523. Google Scholar

26.

E. J. Jäger & E. Welk 2003: Pflanzengeographische Gliederung Europas. — Pp. 79–86 in: U. Bohn & R. Neuhäusl (ed.), Karte der natürlichen Vegetation Europas 1. — Münster: Landwirtschaftsverlag. Google Scholar

27.

N. Korotkova , T. Borsch , D. Quandt , N. P. Taylor , K. F. Müller & W. Barthlott 2011 : What does it take to resolve relationships and to identify species with molecular markers? An example from the epiphytic Rhipsalideae (Cactaceae). — Amer. J. Bot. 98: 1549–1572. Google Scholar

28.

S. Kovačić 2006: Relationships and chorology of isophyllous and heterophyllous bluebells (Campanula L., Campanulaceae) in Adriatic Dinarids. — Doctoral Thesis, Department of Biology, Faculty of Science, University of Zagreb [original in Croatian available from Central Botanical Library, Faculty of Science, Zagreb]. Google Scholar

29.

S. Kovačić & T. Nikolić 2006: Relations of the western Balkan endemic Campanula L. (Campanulaceae) lineages based on comparative floral morphometry. — Pl. Biosyst. 140: 260–272. Google Scholar

30.

H. W. Lack with D. J. Mabberley 1999: The flora graeca story: Sibthorp, Bauer, and Hawkins in the Levant. — Oxford: University Press. Google Scholar

31.

D. Lakušić & F. Conti 2004: Asyneuma pichleri (Campanulaceae), a neglected species of the Balkan Peninsula. — Pl. Syst. Evol. 247: 23–36. Google Scholar

32.

D. Lakušić , Z. Liber , T. Nikolić , B. Surina , S. Kovačić , S. Bogdanović & S. Stefanović 2013: Molecular phylogeny of Campanula pyramidalis species complex (Campanulaceae) inferred from chloroplast and nuclear non-coding sequences and its taxonomic implications. — Taxon 62: 505–524. Google Scholar

33.

T. G. Lammers 2007: World checklist and bibliography of Campanulaceae. — Kew: Royal Botanic Gardens. Google Scholar

34.

K. Malý 1908: Beiträge zur Kenntnis der illyrischen Flora. — Magyar Bot. Lapok 7: 203–240. Google Scholar

35.

G. Mansion , G. Parolly , A. A. Crowl , E. Mavrodiev , N. Cellinese , M. Oganesian , K. Fraunhofer , G. Kamari , D. Phitos , R. Haberle , G. Akaydin , N. Ikinci , T. Raus & T. Borsch 2012: How to handle speciose clades? Mass taxon-sampling as a strategy towards illuminating the natural history of Campanula (Campanuloideae). — PloS ONE 7: e50076. — http://dx.doi. org/10.1371/journal.pone.0050076 Google Scholar

36.

J. McNeill , F. R. Barrie , W. R. Buck V. Demoulin , W. Greuter , D. L. Hawksworth , P. S. Herendeen , S. Knapp , K. Marhold , J. Prado , W. F. Prud'homme van Reine , G. F. Smith , J. H. Wiersema & N. J. Turland (ed.) 2012: International Code of Nomenclature for algae, fungi and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. — Königstein: Koeltz Scientific Books [ Regnum Veg. 154]. Google Scholar

37.

MedCalc Software 2005–2011: Digimizer Image Analysis Software Version 4.0.0.0. — Published at http://www.digimizer.com Google Scholar

38.

H. Meusel & E. J. Jäger 1992: Vergleichende Chorologie der Zentraleuropäischen Flora 3. — Jena: Fischer. Google Scholar

39.

N. Myers , R. A. Mittermeier , C. G. Mittermeier , G. A. B. da Fonseca & J. Kent 2000: Biodiversity hotspots for conservation priorities. — Nature 403: 853–858. Google Scholar

40.

C. F. Nyman 1879: Conspectus florae europaeae 2. — Örebro Sueciae: Typis officinae bohlinianae. Google Scholar

41.

M. Oganesian 1995: Synopsis of Caucasian Campanulaceae. — Candollea 50: 275–308. Google Scholar

42.

J. Pančić 1875: Elenchus plantarum vascularium quae eastate a. 1873. in Crna Gora legit Dr. J. Pančić. — Belgradi: Societas Erudita Serbica. Google Scholar

43.

J.-M. Park , S. Kovačić , Z. Liber , W. M. M. Eddie & G. M. Schneeweiss 2006: Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. — Syst. Bot. 31: 862–880. Google Scholar

44.

S. Pignatti 1982: Flora d'ltalia 2. — Bologna: Edagricole. Google Scholar

45.

P. Quézel 1953: Les Campanulacées d'Afrique du Nord. — Feddes Repert. Spec. Nov. Regni Veg. 56: 1–65. Google Scholar

46.

A. Rambaut 2006: FigTree v1.1.1: Tree figure drawing tool. — Published at http://tree.bio.ed.ac.uk/software/figtree/ Google Scholar

47.

A. Rambaut & A. J. Drummond 2007: Tracer v1.4 — Published at http://beast.bio.ed.ac.uk/Tracer Google Scholar

48.

J. H. Ran , P. P. Wang , H. J. Zhao & X. Q. Wang 2010: A test of seven candidate barcode regions from the plastome in Picea (Pinaceae). — J. Integr. Pl. Biol. 52: 1109–1126. Google Scholar

49.

J. J. Roemer & J. A. Schultes 1819: Systema vegetabilium 5. — Stuttgardtiae: Sumtibus J. G. Cottae. Google Scholar

50.

C. Roquet , L. Sáez , J. J. Aldasoro , A. Susanna , M. L. Alarcón & N. Garcia-Jacas 2008: Natural delineation, molecular phylogeny and floral evolution in Campanula. — Syst. Bot. 33: 203–217. Google Scholar

51.

O. Seberg & G. Petersen 2009: How many loci does it take to DNA barcode a Crocus? — PLoS ONE 4: e4598 [online at http://dx.doi.org/10.1371/journal.pone.0004598 ]. Google Scholar

52.

J. Sibthorp & J. E. Smith 1806: Florae graecae prodromus 1. — Londini: Typis Richardi Taylor et socii, in vico Shoe Lane; Veneunt apud Johannem White, in vico Fleet street. Google Scholar

53.

J. Sibthorp & J. E. Smith 1819: Flora graeca 3. — Londini: Typis Richardi et Arthuri Taylor; Veneunt apud Payne et Foss, in vico Pal-Mal. Google Scholar

54.

D. Silvestro & I. Michalak 2011: raxmlGUI: a graphical front-end for RAxML. — Organisms Diversity Evol. 12: 335–337. Google Scholar

55.

J. Sims 1805: Campanula capitata. — Bot. Mag. 21: t. 811. Google Scholar

56.

A. Stamatakis 2006: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. — Bioinformatics 22: 2688–2690. Google Scholar

57.

StatSoft 1996: STATISTICA, Version 5.1 [data analysis software]. — Published at http://www.statsoft.com Google Scholar

58.

S. Stefanović & D. Lakušić 2009: Molecular reappraisal confirms that the Campanula trichocalycina-pichleri complex belongs to Asyneuma (Campanulaceae). — Bot. Serbica 33: 21–31. Google Scholar

59.

V. Stevanović , S. Vukojičić , J. Šinžar-Sekulić , M. Lazarević , G. Tomović & K. Tan 2009: Distribution and diversity of Arctic-Alpine species in the Balkans. — Pl. Syst. Evol. 283: 219–235. Google Scholar

60.

J. R. Stewart , A. M. Lister , I. Barnes & L. Dalén 2010: Refugia revisited: individualistic responses of species in space and time. — Proc. R. Soc. B 277: 661–671. Google Scholar

61.

K. Tamura , D. Peterson , N. Peterson , G. Stecher , M. Nei & S. Kumar 2011: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. — Molec. Biol. Evol. 28: 2731–2739. Google Scholar

62.

J. A. Tate & B. B. Simpson 2003: Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. — Syst. Bot. 28: 723–737. Google Scholar

63.

M. Tenore 1824–1829: Flora napolitana 3. — Napoli: Stamperia Francese. Google Scholar

64.

B. Thiers 2013+ [continuously updated]: Index herbariorum: a global directory of public herbaria and associated staff. — Published at http://sweetgum.nybg.org/ih/ [accessed 4 Mar 2014]. Google Scholar

65.

R. de Visiani 1847: Flora dalmatica 2. — Lipsiae: Apud Fridericum Hofmeister. Google Scholar

66.

F. P. A. Waldstein & P. Kitaibel 1801: Descriptiones et icones plantarum rariorum Hungariae 1. — Viennae: Schmidt. Google Scholar

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Siniša Škondrić, Jelena M. Aleksić, and Dmitar Lakušić "Campanula cichoracea (Campanulaceae), a neglected species from the Balkan-Carpathian C. lingulata complex as inferred from molecular and morphological characters," Willdenowia 44(1), 77-96, (19 March 2014). https://doi.org/10.3372/wi.44.44111

Published: 19 March 2014

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