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Trifolium subterraneum L.

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General Information
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Family :

Famille :

Fabaceae

Synonym(s) :

Synonyme(s) :

Common Name(s) :

Nom(s) commun(s) :

Subterranean clover

(English) (USDA-ARS 2024)
Trèfle souterrain (French) (USDA-ARS 2024)
Erdklee (German) (USDA-ARS 2024)
Trifoglio sotteraneo (Italian) (USDA-ARS 2024)
Jimoguri-tsumekusa (Japanese) (USDA-ARS 2024)
Trevo-subterrâneo (Portuguese) (USDA-ARS 2024)
Grävklöver (Swedish) (USDA-ARS 2024)

Trifolium subterraneum seeds

  • Trifolium subterraneum seeds

  • Trifolium subterraneum seeds

  • Trifolium subterraneum seeds

  • Trifolium subterraneum seed

  • Trifolium subterraneum burr

  • Trifolium subterraneum legumes

  • Trifolium subterraneum  legume

  • Trifolium subterraneum seed surface, close-up

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Overview

Aperçu

Regulation :

Remarques Réglementation:

    Regulation Notes:

    Distribution :

    Répartition :

    Trifolium subterraneum is native to countries in the Mediterranean region, western Asia and north Africa, as well as the Atlantic coast of western Europe (Morley 1961; Nichols et al. 2009). It has been introduced and successfully grown in Australia, New Zealand, South Africa, southern South America, Spain, Portugal, Russia, the United States and Canada (Morley 1961; McGuire 1985).

    In the United States, T. subterraneum is cultivated in the Pacific coast states, Texas, the southeastern states, and along the east coast (Friddle 2018; USDA-NCRS 2024). The species has been introduced into the province of British Columbia in Canada (Brouillet et al 2010+).

    Habitat and Crop Association :

    Habitat et Cultures Associées :

    Trifolium subterraneum can become naturalized and spread beyond the areas where it has been planted, generally by animals or contaminated seed (Morley 1961; Gladstones 1966; Friddle 2018). This species has been found on roadsides, vernal pool habitats and along coastal bluffs (GOERT 2003). The species could outcompete native species and become a problematic weed in annual vegetable crops (Friddle 2018).

    In British Columbia, Canada, T. subterraneum is considered invasive in southeastern Vancouver Island, and is increasing in the local endangered Quercus garryana (Garry oak) ecosystem (GOERT 2003). The qualities that make it an excellent forage, such as nitrogen-fixing, a spreading habit and a persistent seedbank, also make it difficult to remove from natural areas (GOERT 2003; Friddle 2018).

    Economic Use, cultivation area, and Weed Association :

    Utilisation économique, zone de culture et association de mauvaises herbes :

    T. subterraneum plants can be grown and plowed into the field for nitrogen. This practice improved the yield of Sorghum sp. (grain sorghum) similar to an application of fertilizer (Friddle 2018). This species has been used as a living mulch to improve the yield of Zea mays L. subsp. mays (corn) and Secale cereale L. (rye) while suppressing weeds such as Panicum dichotomiflorum Michx. and Ipomoea hederacea (L.) Jacq. (Enache and Ilnicki 1990).

    T. subterraneum is a nutritious and palatable pasture plant and can tolerate heavy grazing (Nichols et al. 2009; Friddle 2018). Naturally occurring isoflavones may cause reproductive disorders and infertility in livestock; new varieties eliminate this effect (Morley 1961; McGuire 1983). Isoflavones in T. subterraneum may be useful as a source of hormones for human menopausal disorders and natural growth regulators for livestock (Nichols et al. 2013).

    T. subterraneum prefers regions with wet winters and dry summers and can grow in a wide range of elevations (Morley 1961). The species grows best on slightly to moderately acidic soils, although some varieties can tolerate neutral or alkaline soils (Morley 1961; McGuire 1985). Problematic weed species in T. subterraneum pastures are generally winter annual grasses and broadleaf weeds (Steiner and Grabe 1982). In Australia, Hordeum murinum L. subsp. leporinum (Link) Arcang. and Arctotheca calendula (L.) Levyns are common weed species (Morley 1961). In the United States, Bromus diandrus Roth., Avena fatua L., Festuca myuros L., Erodium species, Stellaria media (L.) Vill., Galium species and Medicago lupulina L. were reported field weeds (Steiner and Grabe 1982).

    Duration of Life Cycle :

    Durée du cycle vital:

    Annual

    Dispersal Unit Type :

    Type d’unité de dispersion :

    Seed

    General Information

    RENSEIGNEMENTS GÉNÉRAUX

    Trifolium subterraneum has developed from an accidental introduction by European settlers in the 19th century to the most widely sown annual legume in Australia and introduced worldwide (Morley 1961; Nichols et al. 2009). The ability to fix atmospheric nitrogen in the nutrient-poor soils of Australia led to significant improvements in crop yields and shaped Australian agriculture (Morley 1961; Moss et al. 2022).

    The species name of T. subterraneum refers to the below ground development of the seeds. The legumes are surrounded by a cluster of sterile flowers that form a fruiting head or bur (Moss et al. 2022). The hooked ends of the sterile calyces aid in burial of the structure, along with downward pressure from the stalk (peduncle) (Moss et al. 2022). This bur structure protects the seed from predation and aids in seed dispersal by catching on animal fur (Moss et al. 2022). In heavier soils, the bur matures at the soil surface which may result in a reduction in seed number, weight and viability (McGuire 1985).

    T. subterraneum seeds can naturally have both hard-seededness (prevents water absorption) and dormant embryos that require an after-ripening period (Morley 1961). Dormancy can be broken prematurely by cool temperatures, chemicals or removing the seed coat (Morley 1961).

    The flowers of this species are closed (cleistogamous) and self-fertilized, although a low amount (below 1%) of cross-fertilization can occur (Nichols et al. 2013). Three lines of locally adapted, natural genotypes have been classified as subspecies and developed into cultivars, generally distinguishable by morphology and environmental preferences (Piluzza et al. 2005). McGuire (1985) and Nichols et al. (2009; 2013) describe the three subspecies:

    • Trifolium subterraneum L. subsp. subterraneum, originally from southwestern Europe, has the widest native distribution, preferring well-drained neutral or acidic soils and grazed conditions. The fruiting heads (burs) are buried in the soil, and have dense sterile calyces.
    • T. subterraneum L. subsp. yanninicum Katzn. & Morley, native to Greece and the former Yugoslavia, adapted to poorly-drained acidic soils and grazed conditions. The burs are buried in the soil, and have sparse sterile calyces.
    • T. subterraneum L. subsp. brachycalycinum Katzn. & Morley, native to the Mediterranean region, adapted to neutral or alkaline, stony soils and lightly or ungrazed conditions. The burs remain at the soil surface, and the bur only partially covers the fertile calyces.
    .

    Identification

    Identification

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    • Fruiting head (bur)

      Size

      • Fruiting head (bur) length: 0.71-0.92 cm; width: 0.74-0.88 cm (Bouzaine et al. 2023)

      Shape

      • The fruiting head (bur) is round or oval shaped, terete in 3 dimensions

      Surface Texture

      • The fruiting head has a spiny texture, with many hooked calyx spines that are covered with stiff hairs

      Colour

      • The mature fruiting head is yellowish coloured

      Other Features

      • The fruiting head is composed of fertile flowers surrounded by several calyces (plural of calyx) that develop hooked ends to aid in burial or dispersal of the fruiting head
      • Each fruiting head may have up to 7 fertile flowers; 3 or 4 is the typical amount (Morley 1961; McGuire 1985).

      Trifolium subterraneum burr

    • Legume

      Size

      • Legume length*: 3.0-4.0 mm; width: 2.5-3.3 mm
      *Note: minimum and maximum based on 10 legumes in normal range of this species using specimen measurement protocol (ISMA 2020).

      Shape

      • Legumes are oval or egg-shaped, slightly compressed in 3 dimensions

      Surface Texture

      • Legumes are smooth with a network of raised veins
      • A ridge of thickened tissue is around the edge of the legume
      • Legumes have a papery or leathery consistency

      Colour

      • Mature legumes are yellowish coloured

      Other Features

      • Each legume contains 2 ovules, but only one seed generally develops (Morley 1961), but legumes with 2 seeds have been recorded (Bouzaine et al. 2023).
      • Legumes are indehiscent

      Trifolium subterraneum legumes

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    • Seed

      Size

      • Seed length: 3.2-3.8 mm; width: 2.4-2.8 mm (Bojňanský and Fargašová 2007)
      • Seed length: 2.2373 ± 0.088 mm; width: 1.8808 ± 0.0765 mm (Zoric et al. 2010)
      • Seed length: 2.2052 ± 0.1991 mm; width: 1.9245 ± 0.0752 mm (Baliousis et al. 2021)
      • Seed length: 2.68-3.35 mm; width: 1.69-2.16 mm (Bouzaine et al. 2023)

      Shape

      • Seed shape is oval or egg-shaped, with a protruding radicle tip ½ to 2/3 the length of the cotyledons, rarely the same length.
      • Seeds generally slightly compressed, biconvex in 3 dimensions
      • T. subterraneum L. subsp. brachycalycinum seeds are strongly compressed (Nichols et al. 2013)
      • Hilum is round

      Surface Texture

      • Surface appears smooth, is minutely stippled under 20x magnification and higher
      • Lens a slightly raised bump on the hilum end, largest in T. subterraneum L. subsp. brachycalycinum (Nichols et al. 2013)

      Colour

      • Seeds are generally dark purplish, reddish-brown at the hilum end
      • The lens is generally dark reddish-brown
      • Some seeds may be light yellow or brownish-yellow with a brownish lens
      • T. subterraneum L. subsp. yanninicum seeds are generally light yellow or brownish-yellow, rarely purplish.

      Other Features

      • Hilum is located in a shallow or V-shaped notch between the cotyledons and radicle tip

      Trifolium subterraneum seeds

    <
    >

    • Embryo

      Size

      • Embryo fills the seed

      Shape

      • Embryo is bent

      Endosperm

      • Nutritive tissue stored in cotyledons

    Identification Tips

    CONSEILS POUR L’IDENTIFICATION

    The seeds of T. subterraneum are generally larger than most species of Trifolium, but species such as T. incarnatum L. and T. alexandrinum L. have similar sized seeds (Zoric et al. 2010) and a similar oval shape with a protruding radicle. Most of the T. subterraneum cultivars can be readily distinguished by their dark purplish seeds, but yellowish-coloured varieties may look similar.

    Seed features that can generally distinguish T. subterraneum from similar species include:

    • Dark purplish colour of most cultivars
    • The radicle protrudes away from the cotyledons
    • Seed surface is stippled
    • The hilum is small relative to seed size
    • The lens is at the end of the cotyledon lobe on the hilum end

    Trifolium subterraneum seeds

    Additional Botany Information

    AUTRES RENSEIGNEMENTS BOTANIQUES

    Flowers/Inflorescence

    • Flowering clusters form near the ends of the prostrate stems, oval shaped and 10 mm long, peduncles 15-40 mm long (Steiner and Grabe 1982; Gallaher et al. 2020)
    • Each cluster generally has 3-4 fertile flowers, but can have up to 7 fertile flowers (Morley 1961; Steiner and Grabe 1982)
    • Flowers are 8-14 mm long, generally white or light yellow with pink or red stripes (Steiner and Grabe 1982; Gallaher et al. 2020)
    • The calyx is generally partially or fully reddish coloured, except in T. subterraneum L. subsp. brachycalycinum cultivars (Nichols et al. 2013)
    • Sterile flowers in the middle of the flowering head elongate and curve towards the flowering head after fertilization (Gallaher et al. 2020).
    • Fertile flowers have 10 stamens, 9 fused into a tube and one free (Gallaher et al. 2020)
    • The flowering stalk bends towards the ground as the sterile calyces develop (Morley 1961)
    • Burial of the fruiting head is through a combination of pressure from the elongating peduncle and the curving sterile calyces (McGuire 1985)

    Vegetative Features

    • T. subterraneum plants have stems that lay on the ground (prostrate), 2-3 dm long (Gallaher et al. 2020)
    • Plants may produce several runners (above ground stems) up to a meter in length depending on growing conditions and grazing pressure (McGuire 1985)
    • Leaves are compound, with 3 leaflets 8-20 mm long, egg- or heart-shaped with smooth or small-toothed edges (Gallaher et al. 2020).
    • Stems and leaves are generally hairy, are hairless in T. subterraneum L. subsp. brachycalycinum cultivars (Nichols et al. 2013)

    Similar Species

    ESPÈCES SEMBLABLES

    Similar species are based on a study of seed morphology of various species, and those with similar dispersal units are identified. The study is limited by physical specimen and literature availability at the time of examination, and possibly impacted by the subjectivity of the authors based on their knowledge and experience. Providing similar species information for seed identification is to make users aware of similarities that could possibly result in misidentification.

    Trifolium incarnatum L.

    Seeds of T. incarnatum are a similar size or smaller (length*: 1.85-3.12 mm; width 1.56-2.21) than T. subterraneum. The radicle is more strongly appressed to the cotyledons, the surface is smooth and the lens is near the hilum end of the seed compared to the projecting radicle, stippled surface and lens at the hilum end on T. subterraneum seeds.

    *Note: minimum and maximum based on 10 seeds in normal range of this species using image measurement protocol (ISMA 2020).

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    Reference(s)

    Référence(s)

    Bojňanský, V. and Fargašová, A. 2007. Atlas of Seeds and Fruits of Central and East-European Flora: The Carpathian Mountains Region. Springer, Dordrecht, The Netherlands. 1046 pp.

    Brouillet, L., Coursol, F., Meades, S. J., Favreau, M., Anions, M., Bélisle, P. and Desmet, P. 2010+. VASCAN, the database of vascular plants of Canada. http://data.canadensys.net/vascan/ Accessed August 6, 2024.

    Friddle, M. 2018. Plant guide for subterranean clover (Trifolium subterraneum). USDA-Natural Resources Conservation Service, Corvallis Plant Materials Center, Corvallis, OR.

    Gallaher, T.J., Brock, K., Kennedy, B.H, Imada, C.T, Imada, K., Walvoord, N. 2020. Plants of Hawaiʻi. http://www.plantsofhawaii.org. Accessed August 8, 2024.

    Garry Oak Ecosystems Recovery Team (GOERT). 2003. Invasive Species in Garry Oak and Associated Ecosystems in British Columbia. Garry Oak Ecosystems Recovery Team, Victoria, BC.

    Gladstones, J. S. 1966. Naturalized subterranean clover (Trifolium subterraneum L.) in Western Australia; the strains, their distributions, characteristics and possible origins. Australian Journal of Botany 14: 329-354.

    International Seed Morphology Association (ISMA). 2020. Method for Seed Size Measurement. Version 1.0. ISMA Publication Guide.

    McGuire, W.S., 1985. Subterranean Clover. In: Taylor, N.L. (Ed.), Clover Science and Technology. Agronomy Monographs pp. 515–534.

    Morley, F.H.W. 1961. Subterranean clover. Advances in Agronomy 13: 57-123.

    Moss, W.M., Nichols, P.G.H., Foster K.J., Ryan M.H., Erskine, W. and Guzzomia, A.L. 2022. A century of subclover: Lessons for sustainable intensification from a historical review of innovations in subterranean clover seed production. Advances in Agronomy 171: 305-339.

    Nichols, P.G.H., Cocks, P.S. and Francis, C.M. 2009. Evolution over 16 years in a bulk-hybrid population of subterranean clover (Trifolium subterraneum L.) at two contrasting sites in south-western Australia. Euphytica 169: 31–48.

    Nichols, P.G.H., Foster, K.J., Piano, E., Pecetti, L., Kaur, P., Ghamkhar, K., and Collins, W.J. 2013. Genetic improvement of subterranean clover (Trifolium subterraneum L.): germplasm, traits and future prospects. Crop and Pasture Science 64:312‒346.

    Piluzza, G., Pecetti, L., Bullitta, S., and Piano, E. 2005. Discrimination among subterranean clover (Trifolium subterraneum L. complex) genotypes using RAPD markers. Genetic Resources and Crop Evolution 52: 193–199.

    Plants of the World Online (POWO). 2024. Facilitated by the Royal Botanic Gardens, Kew. Published at http://www.plantsoftheworldonline.org/ Accessed August 6, 2024.

    United States Department of Agriculture-Agricultural Research Services (USDA-ARS). 2024. Germplasm Resources Information Network (GRIN), https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysearch Accessed August 8, 2024.

    United States Department of Agriculture-Natural Resources Conservation Service (USDA-NRCS). 2024. The PLANTS Database. http://plants.usda.gov Accessed August 6, 2024.

    Author(s)

    AUTEUR(S)

    Jennifer Neudorf, Yimeng Wang, Janessa Emerson

    Canadian Food Inspection Agency, Canada  ssts@inspection.gc.ca

    contactus@idseed.org

    Last updated
    on 2023-03-27

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