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Ficaria verna

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Lesser celandine
Scientific classification Edit this classification
Kingdom: Plantae
Clade: Tracheophytes
Clade: Angiosperms
Clade: Eudicots
Order: Ranunculales
Family: Ranunculaceae
Genus: Ficaria
Species:
F. verna
Binomial name
Ficaria verna
Synonyms[1]
Synonyms
  • Caltha hiranoi Tamura
  • Chelidonium minus Garsault [Invalid]
  • Ficaria ambigua Boreau
  • Ficaria aperta Schur
  • Ficaria boryi Heldr. ex Nyman
  • Ficaria bulbifera (Á.Löve & D.Löve) Holub
  • Ficaria communis Dum.Cours.
  • Ficaria degenii Harv.
  • Ficaria ficaria (L.) H.Karst. [Invalid]
  • Ficaria holubyi Schur
  • Ficaria intermedia Schur
  • Ficaria peloponnesiaca Nyman
  • Ficaria polypetala Gilib. [Invalid]
  • Ficaria pumila Velen. ex Bornm.
  • Ficaria ranunculiflora Moench ex St.-Lag.
  • Ficaria ranunculoides Roth [Illegitimate]
  • Ficaria robertii F.W.Schultz
  • Ficaria rotundifolia Schur
  • Ficaria stepporum P.A.Smirn.
  • Ficaria transsilvanica Schur
  • Ficaria varia Otsch.
  • Ficaria vulgaris J.St.-Hil.
  • Ranunculus ficaria L.

Ficaria verna (formerly Ranunculus ficaria L.), commonly known as lesser celandine or pilewort,[3] is a low-growing, hairless perennial flowering plant in the buttercup family Ranunculaceae. It has fleshy dark green, heart-shaped leaves and distinctive flowers with bright yellow, glossy petals.[4][5] Native to Europe and Western Asia, it is now introduced in North America, where it is known by the common name fig buttercup and considered an invasive species.[6][7][8][9] The plant is poisonous if ingested raw and potentially fatal to grazing animals and livestock such as horses, cattle, and sheep.[10] For these reasons, several US states have banned the plant or listed it as a noxious weed.[7][11] It prefers bare, damp ground and is considered by horticulturalists in the United Kingdom as a persistent garden weed;[12][13] nevertheless, many specialist plantsmen, nursery owners and discerning gardeners in the UK and Europe collect selected cultivars of the plant, including bronze-leaved and double-flowered ones. Emerging in late winter with flowers appearing late February through May in the UK, its appearance across the landscape is regarded by many as a harbinger of spring.[12]

Description

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Lesser celandine is a hairless perennial plant to about 25 cm (9.8 in) high, growing in clumps of 4-10 short stems, on which the leaves are spirally-arranged or all basal. The leaf stalks have sheathing bases, no stipules, a groove along their upper surface, and two hollows within. The leaves are cordate, 1–4 cm (0.39–1.57 in) across, dark-green above with a distinctive variegated or mottled pattern, and pale green below. Purple-leaved varieties are common. The margins of the leaves are sometimes entire (rounded) but more often angled or weakly lobed, with hydathodes at the tips. There are two types of roots: dense clusters of thick, pale-coloured elongated tubers surrounded by patches of short, fibrous roots. Some clumps give rise to long stolons to 10 cm (3.9 in) or more, allowing vegetative spread to produce extensive carpets of plants.[14]

Closed-up flowerhead of lesser celandine, showing the sepals and outside of the petals.

It produces large actinomorphic (radially symmetrical) flowers with a diameter of up to 3–5 cm (1.2–2.0 in), on long stalks arising individually from the leaf axils or in loose cymes at the top of the stem. There are no bracts. The flowers have a whorl of 3 sepaloid tepals and 7 to 12 glossy[4] yellow petaloid tepals, which are sometimes tinged purple or grey on the back. Double flowered varieties also occur. The stamens and carpels are numerous, and the fruit is a single-seeded, shortly hairy achene with a very short style. In several subspecies, tubers are formed in the leaf axils after flowering.[15]: 118  It blooms between March and May in the UK.[16]

Distribution

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Ficaria verna sensu lato is native to central Europe, north Africa and the Caucasus. It has been introduced into Iceland and North America.[17]

Life cycle

[edit]
Flowers appear in early spring

Lesser celandine grows on land that is seasonally wet or flooded, especially in sandy soils, but is not found in permanently waterlogged sites.[18] In both shaded woodlands and open areas, Ficaria verna begins growth in the winter when temperatures are low and days are short.[19] The plants mostly propagate and spread vegetatively,[20] although some subspecies are capable of producing up to 73 seeds per flower.[12] Germination of seeds begins in the spring, and continues into summer.[12] Seedlings remain small for their first year, producing only one or two leaves until the second year.[12]

Growth and reproduction is poor in dry or acidic conditions, though the plants can handle drought well once dormant.[12] By emerging before the forest canopy leafs out, Ficaria verna is able to take advantage of the higher levels of sunlight reaching the forest floor during late winter and early spring.[21] By late spring, second year plants quickly age as daylight hours lengthen and temperatures rise.[12] By the end of May, foliage has died back and plants enter a six month dormancy phase.[20]

If disturbed, separation of the plant's numerous basal tubers is an efficient means of vegetative propagation.[19] The plants are easily spread if the prolific tubers are unearthed and scattered by digging activities of some animals and humans.[21][12] Erosion and flood events are particularly effective means of spread, as the plants are very successful at colonizing low-lying floodplains once deposited.[19][22]

Typical root tubers: these structures separate easily and can become new plants, allowing the plant to colonize new areas rapidly
Bulbils form in the leaf axils of some subspecies after flowering

Ficaria verna exists in both diploid (2n=16) and tetraploid (2n=32) forms which are very similar in appearance.[12] However, the tetraploid types prefer more shady locations and can develop up to 24 bulbils at the base of the stalk.[12][20] Subspecies F. verna ssp. verna, and F. verna ssp. ficariiformis are tetraploid and capable of colonizing new areas much faster because they produce bulbils in their leaf axils[23]: 126 [20] in addition to root tubers. Subspecies F. verna calthifolia and F. verna verna are diploid[10][24] and hybrids between subspecies often create sterile triploid forms.[10]

Ecology

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Lesser celandine is pollinated by bees, small beetles, and flies, including Apis mellifera, Bibio johannis, Phora, and Meligethes. The larvae of Olindia schumacherana feed on the leaves.[25]

It associates with arbuscular mycorrhizal fungi.[25]

Fungal and oomycetous pathogens

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The leaves are parasitised by the chytrid fungus Synchytrium anomalum; the rust fungi Schroeteriaster alpinus, Uromyces ficariae, U. poae, and U. rumicis; the smut fungi Entyloma ficariae and Urocystis ficariae; the leaf spot fungi Septoria ficariae and Colletotrichum dematium; the grey mould Botrytis ficariarum; and the downy mildew Peronospora ficariae.[25][26]

The roots are parasitised by the fungi Botryotinia ficariarum (the anamorph of which is Botrytis ficariarum) and Dumontinia tuberosa.[26]

As an invasive species

[edit]
As an invasive species it forms a dense carpet in a floodplain forest in Fox Chapel, Pennsylvania

In many parts of the Eastern and Northwestern United States and Canada, lesser celandine is cited as an invasive species.[18] It poses a threat to native wildflowers, especially those ephemeral flowers with a spring-flowering lifecycle.[19] Since Ficaria verna emerges well before most native species, it has a developmental advantage which allows it to establish and dominate natural areas rapidly.[21] It is mainly a problem in forested floodplains, where it forms extensive mats, but can occur on upland sites as well.[21] Once established, native plants are displaced and ground is left barren and susceptible to erosion, from June to February, during the plant's six-month dormancy phase.[27]

In the United States, where lesser celandine is considered a plant pest to gardens, lawns, and natural areas, many governmental agencies have attempted to slow the spread of this species with limited success.[9] As of 2014, the species was reported to be invasive and established in 25 states.[28] USDA APHIS considers Ficaria verna to be a high-risk weed that could spread across 79% of the United States, anticipating possible impacts to threatened and endangered riparian species.[9] The U.S. National Park Service's Plant Conservation Alliance recommends avoiding planting lesser celandine, and instead planting native ephemeral wildflowers such as Asarum canadense, bloodroot, the native twinleaf (Jeffersonia diphylla), and various species of Trillium as alternatives.[21]

As a garden plant

[edit]

Christopher Lloyd is one of several horticulturists who have recommended one of the double-flowered Flore Pleno Group for planting at the base of a hedge next to a lawn.[29] The Daily Telegraph has even given advice on how to plant them, provided by the Royal Horticultural Society.[30] Double-flowered plants were noted as long ago as 1625 when one was found by John Ray.[31] The RHS specialist quarterly publication The Plantsman published a lengthy, well-illustrated article on double-flowered lesser celandine cultivars by Belgian gardener and alpine plant specialist Wim Boens in December 2017.[32] "RHS Plant Finder" online lists around 220 named cultivars (many of these may well be very similar; nevertheless, this indicates the interest in the species among gardeners).

[edit]

Sources:[33][34][32]

(Double-flowered and semi-double cultivars are unlikely to be invasive as they either cannot set seed or do not often do so. Semi-doubles may occasionally cross with single cultivars, which is probably how some of the most desirable cultivars originally arose.)

  • Alba Group (cream to white flowers; foliage green or variously mottled with silver and occasional splashes of purple)
  • Brambling (unremarkable yellow flowers; grown for its small triangular or horseshoe-shaped leaves beautifully mottled with silver-grey and purple-brown)
  • Brazen Hussy (bright yellow flowers; glossy dark bronze foliage)
  • Collarette (golden yellow double flowers with neat, button-like centres, green in the middle, and a gappy ring of outer petals; silvery-green leaves often with a central streak or splash of purple-black)
  • Coppernob (bright orange, single flowers; glossy dark bronze foliage)
  • Double Bronze (syns. Bowles's Double, Wisley Double) (semi-double rich yellow flowers with reddish-bronze reverse; green foliage streaked with silver)
  • Double Mud (semi-double flowers, cream petals, muddy purple-brown on the reverse; green foliage mottled with silver)
  • Flore Pleno Group (fully double yellow flowers, green or greenish purple on the reverse making a neat rounded centre; foliage pale green or dappled with silver)
  • Green Petal (a curiosity with small double flowers resembling greenish-yellow roses; distinctive green foliage splashed silver, purple and bronze)
  • Ken Aslet Double (syn. Ken Aslet) (sterile, fully double white, cream at centre, dark purplish reverse to the petals; plain green or slightly mottled foliage)
  • Salmon's White (single flowers open cream, fading almost to white, purplish-blue on reverse; dark green foliage splashed silver and black)

Toxicity

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All plants of the buttercup family (Ranunculaceae) contain a compound known as protoanemonin.[35] When the plant is wounded, the unstable glucoside ranunculin turns into the toxin protoanemonin.[36] Contact with damaged or crushed Ficaria leaves can cause itching, rashes or blistering on the skin or mucosa.[37] Ingesting the toxin can cause nausea, vomiting, dizziness, spasms, or paralysis.[36] In one case, a patient experienced acute hepatitis and jaundice when taking untreated lesser celandine extracts internally as an herbal remedy for hemorrhoids.[38]

Treatment

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On drying of these plants, the protoanemonin toxin dimerizes to non-toxic anemonin, which is further hydrolyzed to non-toxic dicarboxylic acids.[39][40] Cooking of the plants also eliminates the toxicity of the plants and the plant has been incorporated in diets or herbal medicine after being dried, and ground for flour, or boiled and consumed as a vegetable.[18][40][41]

Historical herbal use

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The plant is known as pilewort by some herbalists because it has historically been used to treat piles (hemorrhoids).[42][43] Lesser celandine is still recommended in several "current" herbal guides for treatment of hemorrhoids by applying an ointment of raw leaves as a cream or lanolin to the affected area.[18][43][44] Supposedly, the knobby tubers of the plant resemble piles, and according to the doctrine of signatures this resemblance suggests that pilewort could be used to cure piles.[45]

Nicholas Culpepper (1616 – 1654), is claimed to have treated his daughter for 'scrofula' (or Kings evil) with the plant.[16]

The German vernacular skorbutkraut ("scurvy herb") derives from the use of young leaves, which are high in vitamin C, to prevent scurvy.[18][46] However, use of lesser celandine to prevent scurvy could be considered a misnomer, tied to its similar appearance to common scurvygrass (Cochlearia officinalis), which shares similarly shaped leaves as well as sharing the german name skorbutkraut.[47] The German Hager's Manual of pharmacy practice of 1900 states Ranunculus ficaria [sic] and C. officinalis both share this name and use,[47] though there was little documentation of the toxicity of untreated Ficaria species at the time.

Most guides today point out that medicines should be made from the dried herb or by heat extraction as the untreated plants and extracts will contain protoanemonin, a mild toxin.[42][43] The plant has been widely used in Russia and is sold in most pharmacies as a dried herb.[48] The protoanemonin found in fresh leaves is an irritant and mildly toxic but is suggested to have antibacterial properties if used externally.[42] The process of heating or drying turns the Ranunculaceae toxin to anemonin which is non-toxic and may have antispasmodic and analgesic properties.[42]

Killynether wood, Northern Ireland

Mesolithic Hunter gatherers in Europe consumed the roots of the plant as a source of carbohydrates boiled, fried or roasted.[49]

References in literature

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The poet William Wordsworth was very fond of the flower, which inspired him to write three poems: "To the Small Celandine," "To the Same Flower," and "The Small Celandine." The third poem begins thus:

There is a Flower, the lesser Celandine,
That shrinks, like many more, from cold and rain;
And, the first moment that the sun may shine,
Bright as the sun himself, 'tis out again![50]

Near České Budějovice, Czech Republic

Upon Wordsworth's death it was proposed that a celandine be carved on his memorial plaque inside St Oswald's Church, Grasmere, but unfortunately the greater celandine Chelidonium majus was mistakenly used.[51]

Edward Thomas wrote a poem entitled "Celandine".[52] Encountering the flowers in a field, the narrator is reminded of a past love, now dead. He also remarked on banks of celandines in his early prose work "In Pursuit of Spring" (1913).[53]

C. S. Lewis mentions celandines in a key passage of The Lion, the Witch and the Wardrobe, when Aslan comes to Narnia and the whole wood passes "in a few hours or so from January to May". The children notice "wonderful things happening. Coming suddenly round a corner into a glade of silver birch trees Edmund saw the ground covered in all directions with little yellow flowers - celandines".[54]

D. H. Lawrence mentions celandines frequently in Sons and Lovers. They appear to be a favorite of the protagonist, Paul Morel:

...going down the hedgeside with the girl, he noticed the celandines, scalloped splashes of gold, on the side of the ditch.

'I like them,' he said, 'when their petals go flat back with the sunshine. They seem to be pressing themselves at the sun.'

And then the celandines ever after drew her with a little spell.[55]

See also

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References

[edit]
  1. ^ a b "Ficaria verna". World Checklist of Selected Plant Families. Royal Botanic Gardens, Kew – via The Plant List. Note that this website has been superseded by World Flora Online
  2. ^ "Ficaria verna". Germplasm Resources Information Network. Agricultural Research Service, United States Department of Agriculture.
  3. ^ BSBI List 2007 (xls). Botanical Society of Britain and Ireland. Archived from the original (xls) on 2015-06-26. Retrieved 2014-10-17.
  4. ^ a b Functional optics of glossy buttercup flowers Journal of the Royal Society Interface 14:20160933
  5. ^ Buttercups focus light to heat their flowers and attract insects New Scientist 25 February 2017
  6. ^ "Weed of the Week - Lesser Celandine". University of Maryland Extension. Archived from the original on 2016-03-02. Retrieved 2016-02-12.
  7. ^ a b "Lesser celandine, Ficaria verna". Washington State Noxious Weed Control Board. Archived from the original on 24 March 2016. Retrieved 12 February 2016.
  8. ^ NRCS. "Ranunculus ficaria". PLANTS Database. United States Department of Agriculture (USDA). Retrieved 18 October 2015.
  9. ^ a b c "Weed Risk Assessment for Ficaria verna Huds (Ranunculaceae) – Fig buttercup" (PDF). Animal and Plant Health Inspection Service. United States Department of Agriculture. August 12, 2015. Archived from the original (PDF) on 16 February 2016. Retrieved 12 February 2016.
  10. ^ a b c Post, Angela R.; Krings, Alexander; Wall, Wade A.; Neal, Joseph C. (2009-01-01). "Introduced Lesser Celandine (Ranunculus Ficaria, Ranunculaceae) And Its Putative Subspecies In The United States: A Morphometric Analysis". Journal of the Botanical Research Institute of Texas. 3 (1): 193–209. JSTOR 41972152.
  11. ^ "6 NYCRR Part 575 Prohibited and Regulated Invasive Species Express Terms - NYS Dept. of Environmental Conservation". www.dec.ny.gov. Archived from the original on 2016-03-02. Revised pdf copy (updated 10 September 2014)
  12. ^ a b c d e f g h i j Bond, W; Davies, G; Turner, R (November 2007). "The biology and non-chemical control of Lesser Celandine (Ranunculus ficaria L.)" (PDF). Henry Doubleday Research Association. Ryton Organic Gardens. Archived from the original (PDF) on 2 February 2017. Retrieved 12 February 2016.
  13. ^ Don, Monty (2001-04-22). "Invasion of the soil snatchers". The Guardian. ISSN 0261-3077. Retrieved 2016-02-12.
  14. ^ Poland, John; Clement, Eric (2009). The Vegetative Key to the British Flora. Southampton: John Poland. ISBN 978-0-9560144-0-5.
  15. ^ Stace, C. A. (2010). New Flora of the British Isles (3rd ed.). Cambridge, U.K.: Cambridge University Press. ISBN 9780521707725.
  16. ^ a b Reader's Digest Field Guide to the Wild Flowers of Britain. Reader's Digest. 1981. p. 26. ISBN 9780276002175.
  17. ^ "Ranunculus ficaria L." Plants of the World Online. Royal Botanic Gardens, Kew. Retrieved 21 March 2023.
  18. ^ a b c d e Axtell, Annie E.; DiTommaso, Antonio; Post, Angela R. (2010-04-01). "Lesser Celandine (Ranunculus ficaria): A Threat to Woodland Habitats in the Northern United States and Southern Canada". Invasive Plant Science and Management. 3 (2): 190–196. doi:10.1614/IPSM-D-09-00044.1. ISSN 1939-7291. S2CID 925729.[permanent dead link]
  19. ^ a b c d "Ranunculus ficaria L." Global Invasive Species Database (GISD). Retrieved 11 February 2016.
  20. ^ a b c d Sohrabi Kertabad, S.; Rashed Mohassel, M. H.; Nasiri Mahalati, M.; Gherekhloo, J. (2013). "Some biological aspects of the weed Lesser celandine (Ranunculus ficaria)". Planta Daninha. 31 (3): 577–585. doi:10.1590/S0100-83582013000300010. ISSN 0100-8358.
  21. ^ a b c d e Swearingen, J.; K. Reshetiloff; B. Slattery & S. Zwicker (2002). "Lesser Celandine". Plant Invaders of Mid-Atlantic Natural Areas. National Park Service and U.S. Fish & Wildlife Service, Washington, D.C.
  22. ^ "Lesser Celandine" (PDF). Invasive Plants in Pennsylvania. Pennsylvania Department of Conservation and Natural Resources. Archived from the original (PDF) on March 3, 2015. Retrieved 12 February 2016.
  23. ^ Stace, C. A. (2019). New Flora of the British Isles (Fourth ed.). Middlewood Green, Suffolk, U.K.: C & M Floristics. ISBN 978-1-5272-2630-2.
  24. ^ "Ficaria verna Huds". www.tropicos.org. Retrieved 2016-02-12.
  25. ^ a b c Taylor, K., Markham, B. (1978). "Ranunculus Ficaria L. (Ficaria verna Huds.; F. Ranunculoides Moench)". Journal of Ecology. 66 (3). [Wiley, British Ecological Society]: 1011–1031. doi:10.2307/2259310. ISSN 0022-0477.
  26. ^ a b Ellis, W. N. (2024). "Ficaria verna". bladmineerders.nl. Retrieved 20 December 2024.
  27. ^ "Alien Plant Invader: Lesser celandine". The City of Portland, Oregon. Retrieved 2016-02-13.
  28. ^ "Lesser celandine - US States Distribution". Early Detection & Distribution Mapping System. The University of Georgia - Center for Invasive Species and Ecosystem Health. 20 June 2014. Retrieved 12 February 2016 – via EDDMapS.
  29. ^ Lloyd, Christopher. 1970,1985. The Well-Tempered Garden. London, Penguin Books. 81.
  30. ^ "Your garden this week: planting celandines and dividing perennials". www.telegraph.co.uk. The Telegraph. 25 March 2006. Retrieved 4 April 2019.
  31. ^ "February Celandines (Ficaria verna)". www.thewildflowersociety.com. The Wild Flower Society. Retrieved 4 April 2019.
  32. ^ a b Boens, Wim (December 2017). "Double -flowered celandines". The Plantsman. 16 (4). Royal Horticultural Society: 249–255. ISSN 1477-5298.
  33. ^ "Ficaria verna". www.johnjearrard.co.uk. John Jearrard. Retrieved 4 April 2019.
  34. ^ Boens, Wim (April 2017). "Ficaria verna, a weedy menace? The double flowered lesser celandine" (PDF). International Rock Gardener. 88. Scottish Rock Garden Club: 2–21. ISSN 2053-7557. Retrieved 4 April 2019.
  35. ^ List, PH; Hörhammer, L, eds. (1979). Hagers Handbuch der pharmazeutischen Praxis (in German) (4th ed.). Springer Verlag. ISBN 3-540-07738-3.
  36. ^ a b Lewis, Robert Alan (1998-03-23). Lewis' Dictionary of Toxicology. CRC Press. ISBN 9781566702232.
  37. ^ Frosch, Peter J.; Menne, Torkil; Lepoittevin, Jean-Pierre (2006-06-07). Contact Dermatitis. Springer Science & Business Media. p. 779. ISBN 9783540313014.
  38. ^ Yilmaz, Bulent; Yilmaz, Barış; Aktaş, Bora; Unlu, Ozan; Roach, Emir Charles (2015-02-27). "Lesser Celandine (Pilewort) Induced Acute Toxic Liver Injury: The First Case Report Worldwide". World Journal of Hepatology. 7 (2): 285–288. doi:10.4254/wjh.v7.i2.285. ISSN 1948-5182. PMC 4342611. PMID 25729484.
  39. ^ Berger, Artur; Wachter, Helmut, eds. (1998). Hunnius Pharmazeutisches Wörterbuch (in German) (8th ed.). Walter de Gruyter Verlag. ISBN 3-11-015793-4.
  40. ^ a b Mithen, S., N. Finlay, W. Carruthers, S. Carter, and P. Ashmore. 2001. Plant use in the Mesolithic: Staosnaig, Isle of Colonsay, Scotland. J. Archaeol. Sci 28:223–234.
  41. ^ North, P. 1967. Poisonous Plants and Fungi in Colour. London Blandford. 121.
  42. ^ a b c d Chevallier, A. 1996. The Encyclopedia of Medicinal Plants. New York DK. 258.
  43. ^ a b c Chillemi, S. and M. Chillemi . 2007. The Complete Herbal Guide: A Natural Approach to Healing the Body. Morrisville, NC Lulu. 231.
  44. ^ De BaÏracli Levy, J. 1991. The Illustrated Herbal Handbook for Everyone. London Faber and Faber. 51.
  45. ^ "THE DOCTRINE OF SIGNATURES". www.botgard.ucla.edu. Retrieved 2016-02-13.
  46. ^ "Lesser celandine". Nature's Calendar. Archived from the original on 2016-02-16. Retrieved 2016-02-13.
  47. ^ a b Hager, Hermann (1900-01-01). Hager's Handbuch der pharmaceutischen Praxis für Apotheker, Ärzte, Drogisten und Medicinalbeamte. ... (in German). J. Springer.
  48. ^ Grieve, Maud (1971-06-01). A Modern Herbal: The Medicinal, Culinary, Cosmetic and Economic Properties, Cultivation and Folk-lore of Herbs, Grasses, Fungi, Shrubs, & Trees with All Their Modern Scientific Uses. Dover Publications. ISBN 9780486227986.
  49. ^ Bishop, Rosie R. (2021-03-15). "Hunter-gatherer carbohydrate consumption: plant roots and rhizomes as staple foods in Mesolithic Europe". World Archaeology. 53 (2): 175–199. doi:10.1080/00438243.2021.2002715. ISSN 0043-8243. S2CID 247170423.
  50. ^ "The small Celandine" . Poems (Wordsworth, 1815) – via Wikisource.
  51. ^ Miranda Seymour (2002). A Brief History of Thyme and Other Herbs. page 18
  52. ^ Ed. Mohit K. Ray (Editor) The Atlantic Companion to Literature in English, p. 530, at Google Books
  53. ^ Oates, Matthew (28 March 2013). "Our pursuit of spring continues, 100 years after Edward Thomas's". The Guardian. Retrieved 31 October 2017.
  54. ^ C. S. Lewis (1950). The Lion, the Witch and the Wardrobe. End of chapter 11, beginning of chapter 12
  55. ^ D. H. Lawrence (1913). Sons and Lovers. Chapter 6: Death in the family
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