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14 December 2015

Trifolium angustifolium (narrow-leaf clover)

Datasheet Types: Pest, Documented species, Host plant

Abstract

This datasheet on Trifolium angustifolium covers Identity, Overview, Distribution, Dispersal, Diagnosis, Biology & Ecology, Environmental Requirements, Impacts, Uses, Prevention/Control, Further Information.

Identity

Preferred Scientific Name
Trifolium angustifolium L.
Preferred Common Name
narrow-leaf clover
International Common Names
English
narrow clover
narrowleaf crimson clover
narrow-leaf crimson clover
narrow-leaved clover
narrow-leaved crimson clover
Local Common Names
Sweden
luddklöver

Pictures

Trifolium angustifolium (narrow-leaf clover); habit, showing flowers and leaves.
Habit
Trifolium angustifolium (narrow-leaf clover); habit, showing flowers and leaves.
©Dick Culbert-2008, Gibsons, British Colombia, Canada/via wikipedia - CC BY 2.0
Trifolium angustifolium (narrow-leaf clover); flowers and leaves. Keila, Estonia. August 2013.
Flowers
Trifolium angustifolium (narrow-leaf clover); flowers and leaves. Keila, Estonia. August 2013.
©Ivar Leidus-2013, Estonia/via wikipedia - CC BY-SA 3.0

Summary of Invasiveness

The narrow-leaf clover Trifolium angustifolium is an annual legume native to central, southern and eastern Europe, western Asia and North Africa. It has been introduced elsewhere and is valued for forage and pasture improvement. It has become an environmental weed in a few countries such as Australia, Japan and Chile but has not been reported as an aggressive invader. It is included in the IUCN Red List (Least Concern) for its value as a genetic resource for forage legumes.

Taxonomic Tree

This content is currently unavailable.

Notes on Taxonomy and Nomenclature

Trifolium angustifolium is one of about 300 species in this genus of the Fabaceae and is a wild relative of the cultivated crops crimson clover (T. incarnatum) and red clover (T. pratense) (Osborne, 2013). The following subspecies are included in The Plant List (2013): T. angustifolium subsp. intermedium  (Guss.) Ponert and subsp. pamphylicum (Boiss. & Heldr.) Ponert. It is commonly referred to as narrow-leaf clover or narrow-leaved crimson clover (EPPO, 2014). The common name ‘white clover’ is listed in the IUCN Red List (Lopez Poveda, 2012; Osborne, 2013), but T. angustifolium has pink flowers and the name ‘white clover’ is usually reserved for T. repens.

Plant Type

Annual
Herbaceous
Seed propagated

Description

T. angustifolium is an annual herb growing to about 0.1- 0.6 m high. Its inflorescence is a cylindrical spike of pale-pink flowers, 1-5 cm in height, each flower having a calyx of sepals that have long, needle-like lobes which harden into bristles when the plant dries. Its herbage is of a hairy texture with solid stems and alternate trifoliate leaves with linear to lance-shaped leaflets up to 4.5 cm long (Webb et al., 1988).  

Distribution

T. angustifolium is native to central, eastern and southern Europe and the Mediterranean regions of Africa and Asia (Harshberger, 1922; Blake, 1923; Zohary and Heller, 1984; Osborne, 2013). There is some uncertainty about its native/introduced status in Belarus, Ukraine, Switzerland, Madeira and the Canary Islands (Lopez Poveda, 2012; Osborne, 2013; USDA-ARS, 2016). It has naturalized in some countries and is noted as an environmental weed in Australia and Japan (Auld et al., 2003) and Chile (Marticorena and Quezada, 1985). This species has not been reported as an aggressive invader.

Distribution Map

This content is currently unavailable.

Distribution Table

This content is currently unavailable.

History of Introduction and Spread

T. angustifolium was recorded for the first time in California, USA, in 1922 (Blake (1923).

Means of Movement and Dispersal

T. angustifolium seeds are mainly dispersed by agricultural activities and, due to bristles on the seeds, adhesion to the fleece of sheep (Manzano and Malo, 2006; Fernández-Lugo et al., 2011, TERRAIN, 2015).

Pathway Causes

Pathway causeNotesLong distanceLocalReferences
Crop production (pathway cause)Used as a green manure Yes
Forage (pathway cause)Used in making hay as a protein source Yes

Pathway Vectors

Pathway vectorNotesLong distanceLocalReferences
Livestock (pathway vector)Seeds attach to the fleece of sheep during grazing Yes
Plants or parts of plants (pathway vector) YesYes 

Plant Trade

Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
True seeds (inc. grain)
weeds/seeds
 Yes 

Growth Stages

Vegetative growing stage

Similarities to Other Species/Conditions

T. angustifolium can be distinguished from other Trifolium species by its long pink flower heads and narrow leaflets. An identification key to the clovers of New Zealand was presented by Healy (1961).

Habitat

T. angustifolium has been observed colonizing disturbed areas like roadsides, pastures, paddocks and coastal areas, generally on course-textured soils low in nutrients (Fletcher, 2007; Hackney et al., 2007).

Habitat List

CategorySub categoryHabitatPresenceStatus
Terrestrial    
TerrestrialTerrestrial – ManagedManaged grasslands (grazing systems)Present, no further detailsHarmful (pest or invasive)
TerrestrialTerrestrial – ManagedManaged grasslands (grazing systems)Present, no further detailsProductive/non-natural
TerrestrialTerrestrial – ManagedDisturbed areasPresent, no further detailsHarmful (pest or invasive)
TerrestrialTerrestrial – ManagedDisturbed areasPresent, no further detailsProductive/non-natural
TerrestrialTerrestrial – ManagedRail / roadsidesPresent, no further detailsHarmful (pest or invasive)
TerrestrialTerrestrial – ManagedRail / roadsidesPresent, no further detailsProductive/non-natural
TerrestrialTerrestrial ‑ Natural / Semi-naturalNatural forestsPresent, no further detailsNatural
TerrestrialTerrestrial ‑ Natural / Semi-naturalNatural grasslandsPresent, no further detailsNatural
TerrestrialTerrestrial ‑ Natural / Semi-naturalRocky areas / lava flowsPresent, no further detailsHarmful (pest or invasive)
TerrestrialTerrestrial ‑ Natural / Semi-naturalRocky areas / lava flowsPresent, no further detailsProductive/non-natural
Littoral Coastal areasPresent, no further detailsHarmful (pest or invasive)
Littoral Coastal areasPresent, no further detailsProductive/non-natural

Biology and Ecology

Genetics

The chromosome number is 2n=16 (Löve, 1980; CCDB, 2015).

Reproductive Biology

T. angustifolium reproduces sexually through seed. The seed size is relatively small compared with other annual clovers and is associated with high fecundity (Norman et al., 2005).

Physiology and Phenology

The germination rate of T. angustifolium seed is low in unsuitable environments with growth being directly related to availability of water (Western Australian Herbarium, 2015). This species has long-term hardseededness which allows risk of failure to spread across seasons (Norman et al., 2005) as the hard coat makes this plant very tolerant of abiotic factors. Seeds of T. angustifolium have been found to persist in the soil of forests despite being absent above ground (Erfanzadeh et al., 2013). Studies on germination have shown that smoke and charred wood solutions enhance seed germination but this is negatively affected by exogenous applications of nitrogenous compounds and/or salts (Pérez-Fernández and Rodríquez-Echeverría, 2003).

Associations

T. angustifolium has a symbiotic association with nitrogen-fixing Rhizobium bacteria in the soil which makes it possible for this plant to colonize disturbed areas and nutrient-poor soils (Driouech et al., 2008).

Environmental Requirements

T. angustifolium prefers dry, usually nutrient-poor, disturbed, acid soils (Fletcher, 2007). There is little information on tolerance of frost and drought, however, the closely related crimson clover T. incarnatum is considered sensitive to these abiotic factors (Frame, 2015).

Climate

Climate typeDescriptionPreferred or toleratedRemarks
BS - Steppe climate> 430mm and < 860mm annual precipitationPreferred 
Cs - Warm temperate climate with dry summerWarm average temp. > 10°C, Cold average temp. > 0°C, dry summersPreferred 
Cw - Warm temperate climate with dry winterWarm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)Preferred 

Latitude/Altitude Ranges

Latitude North (°N)Latitude South (°S)Altitude lower (m)Altitude upper (m)
3045  

Air Temperature

ParameterLower limit (°C)Upper limit (°C)
Absolute minimum temperature-3 
Mean annual temperature1516
Mean maximum temperature of hottest month2235
Mean minimum temperature of coldest month018

Rainfall

ParameterLower limitUpper limitDescription
Dry season duration  number of consecutive months with <40 mm rainfall
Mean annual rainfall400900mm; lower/upper limits

Soil Tolerances

Soil texture > light
Soil reaction > acid
Soil reaction > alkaline
Special soil tolerances > infertile

List of Pests

This content is currently unavailable.

Impact Summary

CategoryImpact
Environment (generally)Positive and negative

Impact: Economic

The positive economic impact of T. angustifolium relates to its forage value and use as a nitrogen-fixing green manure. No information has been found on economic impact when it is present as a weed.

Impact: Environmental

Impact on Habitats

T. angustifolium is adapted to nutrient-poor soils (a characteristic of Mediterranean environments) (Muensher, 1955; Webb et al., 2003). This attribute enables it to establish in areas which have low levels of vegetation providing the potential for moderate changes in the density or cover of the herbaceous layer.
Through the symbiotic association with nitrogen-fixing Rhizobium bacteria, there is also potential for T. angustifolium to alter the soil nutrient balance where introduced. It is able to fix between 131.7 and 146.7kg/ha/year (Driouech et al., 2008).

Impact on Biodiversity

T. angustifolium has a relatively large inflorescence, long flowering period and high nectar production which attracts bees. This may indirectly affect the pollination of domesticated crops and native plants.
The increased soil nitrogen resulting from an introduced legume may alter the plant community and aid the establishment of other alien plants that are more invasive. 
In California, USA, the threatened annual Halocarpha macradenia (Santa Cruz tarplant) is disadvantaged by overgrowth by non-native species including T. angustifolium (Holl and Hayes, 2005; US Fish and Wildlife Service, 2014).

Threatened Species

Threatened speciesWhere threatenedMechanismsReferencesNotes
Holocarpha macradenia (Santa Cruz tarplant)
California
Competition
 

Risk and Impact Factors

Invasiveness

Fast growing
Has high reproductive potential
Has propagules that can remain viable for more than one year

Impact outcomes

Increases vulnerability to invasions
Modification of nutrient regime
Threat to/ loss of endangered species
Threat to/ loss of native species

Impact mechanisms

Competition (unspecified)

Likelihood of entry/control

Highly likely to be transported internationally deliberately

Uses

Economic Value

T. angustifolium has long been utilized as self-seeding forage in making hay or direct grazing. Studies conducted by Kamalak and Canbolat (2010) on its nutritive value showed that it contains high levels of crude proteins. However with advancing maturity, its nutritive value decreases. Its low tannin levels enable it to be used as an alternative legume to reduce bloating risk in ruminants grazed on pastures.
Its rapid establishments and association with nitrogen-fixing bacteria make T. angustifolium suitable as a winter cover crop to produce green manure in organic or low-input vegetable production systems in Mediterranean regions (Driouech et al., 2008). It is also valued for honey production.
T. angustifolium is also recognized as a potential gene donor to other cultivated clovers (T. incarnatum and T. pratense) and it has been included in the IUCN Red List for this reason (Osborne, 2013).

Social Benefit

This plant is traditionally used to treat diarrhoea and relieve stomach aches (Rauter et al., 2002).

Uses List

Medicinal, pharmaceutical > Traditional/folklore
Human food and beverage > Honey/honey flora
Animal feed, fodder, forage > Forage
Genetic importance > Gene source

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control and Sanitary Measures

Normal cultivation practices effectively control clovers, including T. angustifolium, in crops. When carried out before flowering, the seed bank is reduced (UC IPM, 2014). Mulching of invaded areas using compost, wood chips or organic mulch helps reduce weed spread by limiting the amount of light available. Mulch also preserves moisture for the cultivated crops giving them a competitive edge over T. angustifolium. Changing the fertilizer programme, by increasing the rates of nitrogen and reducing phosphorous, helps control re-infestation by T. angustifolium and other leguminous weeds (UC IPM, 2014).
T. angustifolium has a hard seed coat which means that composting and soil solarization do not reduce seed viability (UC IPM, 2014).

Physical/Mechanical Control

Where T. angustifolium has spread to new areas, especially cultivated plots, hand pulling before flowering or seed set may reduce spread (UC IPM, 2014).

Movement Control

As grazing sheep are known to disperse seeds which adhere to their fleece, avoid livestock in areas colonized by T. angustifolium after flowering (DiTomaso and Healy, 2007).           

Biological Control

Grazing animals will feed on T. angustifolium, however, as mentioned above, there is a risk that they aid seed dispersal (Manzano and Malo, 2006). No biological control using arthropods or pathogens has been considered as this plant is often used for pasture or soil improvement.

Chemical Control

Pre-emergent and/or post-emergent herbicides such as glyphosate have been used against clovers. However, these weeds tend to regrow after chemical treatment (UC IPM, 2014). Western Australian Herbarium (2015) recommends glyphosate before flowering and spot spray with clopyralid up to the 6-leaf stage for control of T. angustifolium.

Links to Websites

NameURLComment
GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gatewayhttps://doi.org/10.5061/dryad.m93f6Data source for updated system data added to species habitat list.
Global register of Introduced and Invasive species (GRIIS)http://griis.org/Data source for updated system data added to species habitat list.

References

Auld B, Morita H, Nishida T, Ito M, Michael P, 2003. Shared exotica-plant invasions of Japan and south eastern Australia. Journal of Weed Science and Technology, 48(3):143-154.
AVH, 2015. Australia's Virtual Herbarium. Canberra, ACT, Australia: Council of Heads of Australasian Herbaria. http://avh.chah.org.au/
Blake SF, 1923. Two Mediterranean clovers new to the United States. Science, 57(1484):665-665.
CCDB, 2015. Chromosome Counts Database. http://ccdb.tau.ac.il/home/
Denison RF, 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist, 156(6):567-576.
DiTomaso JM, Healy AH, 2007. Weeds of California and other Western States, Volume 1. USA: University of California Press.
Driouech N, Fayad FA, Ghanem A, Al-Bitar L, 2008. Agronomic performance of annual self-reseeding legumes and their self-establishment potential in the Apulia region of Italy. In: Cultivating the future based on science. Volume 1: Organic Crop Production. Proceedings of the Second Scientific Conference of the International Society of Organic Agriculture Research (ISOFAR), held at the 16th IFOAM Organic World Conference in Cooperation with the International Federation of Organic Agriculture Movements (IFOAM) and the Consorzio ModenaBio in Modena, Italy, 18-20 June, 2008 [ed. by Neuhoff, D.\Halberg, N.\Alföldi, T.\Lockeretz, W.\Thommen, A.\Rasmussen, I. A.\Hermansen, J.\Vaarst, M.\Lueck, L.\Caporali, F.\Jensen, H. H.\Migliorini, P.\Willer, H.]. Bonn, Germany: International Society of Organic Agricultural Research (ISOFAR), 396-399.
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
Erfanzadeh R, Kahnuj SHH, Azarnivand H, Pétillon J, 2013. Comparison of soil seed banks of habitats distributed along an altitudinal gradient in northern Iran. Flora (Jena), 208(5/6):312-320. http://www.sciencedirect.com/science/journal/03672530
Fernández-Lugo S, Nascimento Lde, Mellado M, Arévalo JR, 2011. Grazing effects on species richness depends on scale: a 5-year study in Tenerife pastures (Canary Islands). Plant Ecology, 212(3):423-432. http://springerlink.metapress.com/link.asp?id=100328
Fletcher N, 2007. Mediterranean wildflowers. China: Sheck Wah Tong Printing Press.
Frame J, 2015. Trifolium incarnatum L. Grassland Species Profiles. Rome, Italy: FAO. http://www.fao.org/ag/agp/AGPC/doc/Gbase/data/pf000502.htm
Hackney B, Dear B, Crocker G, 2007. Naturalised pasture legumes. Primefacts No. 651. New South Wales, Australia: NSW Department of Primary Industries, 7 pp. http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0009/176688/Naturalised-pasture-legumes.pdf
Harshberger JW, 1922. Ecologic and morphologic study of the clovers (Trifolium). In: Proceedings of the American Philosophical Society, 61(2). 136-50.
Healy AJ, 1961. The identification of clovers in New Zealand. Proceedings of the 14th New Zealand Weed Control Conference 1961, pp. 22-39.
Holl DK, Hayes GF, 2005. Challenges to introducing and managing disturbance regimes for Holocarpha macradenia, an endangered annual grassland forb. Conservation Biology, 20(4):1121-1131.
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Kamalak A, Canbolat O, 2010. Determination of nutritive value of wild narrow-leaved clover (<i>Trifolium angustifolium</i>) hay harvested at three maturity stages using chemical composition and <i>in vitro</i> gas production. Tropical Grasslands, 44:128-133. http://www.tropicalgrasslands.asn.au/Tropical%20Grasslands%20Journal%20archive/PDFs/Vol_44%20(1_2_3_4)/Vol%2044%20(2)%20Adem%20et%20al%20128.pdf
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Löve Á, 1980. Chromosome number reports LXVIII. Taxon, 29(4):533-547.
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Norman HC, Cocks PS, Galwey NW, 2005. Annual clovers (<i>Trifolium</i> spp.) have different reproductive strategies to achieve persistence in Mediterranean-type climates. Australian Journal of Agricultural Research, 56(1):33-43.
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Pereira C, Barros L, Carvalho AM, Ferreira ICFR, 2013. Use of UFLC-PDA for the analysis of organic acids in thirty-five species of food and medicinal plants. Food Analytical Methods, 6(5):1337-1344. http://rd.springer.com/article/10.1007/s12161-012-9548-6
Pérez-Fernández MA, Rodríguez-Echeverría S, 2003. Effect of smoke, charred wood, and nitrogenous compounds on seed germination of ten species from woodland in Central-Western Spain. Journal of Chemical Ecology, 29(1):237-251.
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