Trifolium

Trifolium L.

Trifolium is a genus of ca. 250-300 species native to Europe, Africa, Asia and North America. Its center of diversity surely is in the Mediterranean area. Several species are native in Belgium as well: Trifolium arvense L., T. aureum Pollich, T. campestre, T. dubium, T. fragiferum L., T. medium L., T. micranthum, T. montanum L., T. ochroleucon Huds., T. pratense L., T. repens L., T. scabrum L., T. striatum L. and T. subterraneum L. (Lambinon & Verloove 2012). Some of these are only locally native in Belgium and sometimes occur as aliens in other parts of the country, for instance Trifolium medium, T.  montanum and T. ochroleucon. Some others are native close to the Belgian frontiers and have been recorded in Belgium in the past but probably always as ephemeral introductions (Trifolium alpestre, T. rubens – see below). Trifolium spadiceum L. was probably indigenous in few localities in the eastern part of Belgium but is long extinct now. Similarly, Trifolium squamosum was formerly claimed as a rare native species in coastal habitats (Durand 1899). This is rather questionable and it now only occurs as an introduction. Therefore it is here accepted as a non-native species.

The monophyly of the genus was demonstrated by Elisson & al. (2006) and a Mediterranean origin was also suggested.

Trifolium is an economically important genus. Many species are widely cultivated as fodder plants, including some that are native in Belgium (mainly T. pratense and T. repens). The infraspecific variability of these species has not been thoroughly investigated in Belgium so far. Yet, it is obvious that an increasing number of records of these species surely represent non-native races. Plants of Trifolium pratense with larger flower heads and whitish corollas are sometimes seen on dumps or in newly sown roadsides. They probably belong with var. sativum Afzel. (syn.: T. sativum (Afzel.) Crome). Sell & Murrell (2009) provide a good overview of infraspecific taxa of these species.

Trifolium is a fairly complex genus. However, entire plants (including the subterranean parts, since life form is an important diagnostic feature!) with flowering and fruiting heads are usually readily identified. An accurate identification of plants without roots and fruiting calyces is often impossible. Flower colour is best noted in the field (colours often change after drying).

1       Calyx tube with 5 veins. Corolla yellow, turning brownish after anthesis (persistent). Annual (or biennial) (native) === Trifolium aureum, T. campestre, T. dubium and T. micranthum

         Calyx tube with more than 5 veins (usually 10 or 20; sometimes with 5 distinct and 5 obscure veins but then never a yellow-flowered annual). Perennial, biennial or annual  === 2

2       Each flower with a small bract at base. Pods 1-8-seeded === 3

         Flowers not subtended by bracts. Pods usually 1 seeded === 16

3       Calyx inflated and vesiculous at maturity, often distinctly reticulate-veined === 4

         Calyx not inflated at maturity, not reticulate-veined === 8

4       Calyx 20 or more veined, symmetric or asymmetric at base, glabrous. Calyx teeth subequal in fruit. Pod with 2-4 seeds === 5

         Calyx 10-veined, markedly asymmetric at base, pubescent. Calyx teeth very unequal in fruit. Pod 1-seeded === 6

5       Standard of corolla ca. 14-18 mm. Calyx symmetric at base, with tube 4-5 mm. Leaflets usually elliptical === T. vesiculosum

         Standard of corolla ca. 12-16 mm. Calyx asymmetric at base, with calyx tube 8,5-10 mm. Leaflets usually obovate === T. spumosum

6       Creeping perennial (native) === T. fragiferum

         Annual === 7

7       Inflorescence usually pedunculate (peduncle longer than the subtending leaf). Two upper calyx teeth distinct, divergent. Flower heads hairy but not woolly === T. resupinatum

         Inflorescence usually (sub-) sessile (peduncle shorter than the subtending leaf). Two upper calyx teeth indistinct, largely obscured by woolly hairs of the flower head === T. tomentosum

8       Stipules dentate-fimbriate, glandular-tipped. Glabrous annual. Corolla pink === T. strictum

         Stipules entire, never glandular-tipped === 9

9       Flower heads sessile or nearly so. Glabrous or glabrescent annual === 10

         At least some flower heads pedunculate (peduncle at least 5 mm long) === 11

10     Corolla pink, longer than the calyx. Stem usually erect or ascending, relatively long and always with distinct internodes === T. glomeratum

         Corolla white, shorter than the calyx. Stem often procumbent or decumbent, very short and usually with very short or no internodes === T. suffocatum

11       Pedicels of lowermost flowers at least as long as the calyx, often becoming deflexed after anthesis === 12

         Pedicels very short, not deflexed after anthesis === 15

12    Annual === 13

         Perennial === 14

13     Calyx teeth 2-4 times as long as tube, erect at maturity === T. michelianum

         Calyx teeth about equaling tube, slightly reflexed at maturity === T. nigrescens

14     Stem creeping and rooting at the nodes. Corolla usually white (native) === T. repens

         Stem not creeping and rooting. Corolla usually white suffused with red or pink === T. hybridum

15     Annual. Corolla pink === T. isthmocarpum

         Perennial. Corolla white or yellowish (native) === T. montanum

16     Fertile flowers 2-12-flowered, surrounding several sterile flowers (native) === T. subterraneum

         Fertile flowers numerous, sterile flowers absent === 17

17     Calyx 20-veined (veins sometimes obscured by dense hairs) === 18

         Calyx 10-veined === 20

18     Perennial. Calyx teeth unequal, the longest at least twice as long as the shortest. Inflorescence much longer than broad. Leaflets linear-lanceolate, at least twice as long as wide === T. rubens

         Annual. Calyx teeth subequal to slightly unequal (the longest less than twice as long as the shortest). Inflorescence about as long as wide. Leaflets obovate to oblanceolate, less than twice as long as wide === 19

19     Flower heads subtended by a distinct involucre (in fact the upper stipule). Calyx tube densely hairy === T. hirtum

         Flower heads not involucrate. Calyx tube readily glabrescent === T. lappaceum

20     Perennial === 21 

         Annual === 23

21     Corolla purplish or pinkish (if cream or white, then stipules abruptly contracted into a setaceous point) (native) === T. medium and T. pratense

         Corolla yellowish-white. Stipules linear-lanceolate, never abruptly contracted at apex === 22

22     Peduncle 3-16 cm long. Corolla 20-26 mm long. Lowest calyx teeth 7,5-10,5 mm long === T. pannonicum

         Peduncle absent or up to 2,5 cm long. Corolla 15-20 mm long. Lowest calyx teeth 3-8,2 mm long (native) === T. ochroleucon

23     All leaves alternate === 24

         At least uppermost leaves (usually those subtending the inflorescence) opposite === 30

24     Lateral veins of leaflets distinctly recurved and very prominent at margins (native) === T. scabrum

         Lateral veins straight or only very weakly curved, not very prominent at margins === 25

25     Leaflets of upper leaves lanceolate, linear or linear-oblong, at least twice as long as wide (often much longer) === 26

         Leaflets of upper leaves obovate, less than twice as long as wide === 27

26     Corolla ca. 4 mm long. Calyx throat open after anthesis. Flower heads 10-25 mm long (native) === T. arvense

         Corolla 10-12 mm long. Calyx throat closed by bilabiate callosity after anthesis. Flower heads 20-80 mm long === T. angustifolium

27     Flower heads sessile and involucrate (native) === T. striatum

         Flower heads on distinct peduncles === 28

28     Calyx teeth subulate, about as long as to slightly longer than tube, with tubercle-based hairs. Standard 5-9 mm long. Seeds tuberculate === T. sylvaticum

         Calyx teeth narrowly triangular to lanceolate, markedly longer than tube, without tubercle-based hairs. Standard 9-18 mm long. Seeds smooth === 29

29     Corolla not exceeding calyx. Flower heads globose or obovoid. Calyx throat after anthesis more or less closed by dense hairs === T. stellatum

         Corolla longer than calyx. Flower heads oblong-ovoid to cylindrical, up to 60 mm long. Calyx throat open === T. incarnatum

30     Calyx throat closed by bilabiate callosity after anthesis === 31

         Calyx throat open (but sometimes obscured by hairs) === 34

31     Calyx tube campanulate, not constricted at throat === 32

         Calyx tube urceolate, constricted at throat === 33

32     Calyx teeth unequal (the lowest much longer), 1-veined (or sometimes 3-veined at base) === T. echinatum

         Calyx teeth nearly equal (the lowest slightly longer), very distinctly 3-veined at least to the middle === T. squamosum

33     Corolla much longer than calyx. Calyx teeth 1-3-veined. Calyx tube not tuberculate. Fruiting heads usually not wider than 10 mm === T. constantinopolitanum

         Corolla slightly longer than calyx. Calyx teeth 3-5 veined. Calyx tube often covered with tubercles. Fruiting heads up to 20 mm wide === T. squarrosum

34     Corolla reddish purple, not or hardly exceeding calyx. Calyx teeth blunt (with some long hairs at apex) === T. diffusum

         Corolla cream (rarely pink), much longer than calyx. Calyx teeth sharp or blunt at apex === 35

35     Calyx teeth equal, blunt at apex. Leaflets obovate-ovate, less than twice as long as wide. Corolla cream or pink === T. pallidum

         Calyx teeth unequal, sharp at apex. Leaflets at least twice as long as wide. Corolla cream === T. alexandrinum


Additional aliens: Trifolium alpestre L. (C and SE-Eur., SW-As., vector obscure), T. patens Schreb. (C and S-Eur., W-As., vector unknown), T. purpureum Loisel. (Medit., seed alien) and T. retusum L. (syn.: T. parviflorum Ehrh.) (C and S-Eur., SW-As., wool and grain alien). Trifolium alpestre is native in Luxemburg, close to the Belgian frontiers. Belgian records of Trifolium alpestre were rejected by Durand (1899) and ascribed to native T. medium. However, at least records from the surroundings of Bouillon and Spa (all from the 2nd half of the 19th century) surely belong with Trifolium alpestre. Lawalrée (1961) has also obviously intermixed Trifolium alpestre, T. medium and T. rubens.

Literature:


Coombe D.E. (1968) Trifolium. In: Tutin T.G. & al. (eds.), Flora Europaea, vol. 2. Cambridge University Press, Cambridge: 157-172.

Coulot P. & Rabaute P. (2013) Monographie des Leguminosae de France. Tome 3 Tribu des Trifolieae. Bull. Soc. Bot. Centre-Ouest N.S. 40: 760 p.

Durand T. (1899) Phanérogames. In: De Wildeman E. & Durand T., Prodrome de la flore belge. A. Castaigne Editeur, Bruxelles: 1112 p.

Elisson N.W., Liston A., Steiner J.J., Williams W.M. & Taylor N.L. (2006) Molecular phylogenetics of the clover genus (Trifolium--Leguminosae). Mol. Phylogenet. Evol. 39(3): 688-705. [available online at: http://www.science.oregonstate.edu/bpp/faculty/liston/ellison.etal.2006.pdf]

Haerinasab M. & Rahiminejad M.R. (2012) A Taxonomic Revision Of The Genus Trifolium L. Sect. Fragifera Koch (Fabaceae) In Iran. Iranian Journal of Botany 18(1): 22-30. [available online at: https://www.researchgate.net/publication/265844832_A_TAXONOMIC_REVISION_...

Hendrych R. (1989) Vierte Reihe der nomenklatorischen Ergänzungen zur Trifolium -Monographie von Zohary und Heller (Taxa specifica et intraspecifica). Acta Univ. Carol., Biol. 33(4): 257-314.

Hossain M. (1961) A revision of Trifolium in the nearer East. Notes Roy. Bot. Gard. Edinburgh 23: 387-481.

Lambinon J. & Verloove F. (avec coll. Delvosalle L., Toussaint B., Geerinck D., Hoste I., Van Rossum F., Cornier B., Schumacker R., Vanderpoorten A. & Vannerom H.) (2012) Nouvelle Flore de la Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des Régions voisines (Ptéridophytes et Spermatophytes). Sixième édition. Jardin botanique national de Belgique, Meise: CXXXIX + 1195 p.

Lawalrée A (1961) Papilionaceae. In: Robyns W. (ed.), Flore Générale de Belgique, vol. 4, fasc. 1. Jardin Botanique de l’Etat, Bruxelles: 9-134.

Munoz Rodriguez A.F. (1992) Revisión del género Trifolium sect. Trifolium en la Península Ibérica et Islas Baleares. Acta Bot. Malac. 17: 79-118.

Sell P. & Murrell G. (2009) Flora of Great Britain and Ireland. Vol. 3 Mimosaceae – Lentibulariaceae. Cambridge University Press, Cambridge: XXVIII + 595 p.

Verloove F. & Lambinon J. (2008) Neophytes in Belgium: corrections and adjustments. Syst. Geogr. Pl. 78: 63-79.

Zohary M. & Heller D. (1984) The genus Trifolium. Israel Academy of Sciences and Humanities, Jerusalem: 606 p.

Taxonomic name: 
Scratchpads developed and conceived by (alphabetical): Ed Baker, Katherine Bouton Alice Heaton Dimitris Koureas, Laurence Livermore, Dave Roberts, Simon Rycroft, Ben Scott, Vince Smith