thumb|[[Floral diagram of Fritillaria flower]]

Fritillaria (fritillaries) is a genus of spring flowering herbaceous bulbous perennial plants in the lily family (Liliaceae). The type species, Fritillaria meleagris, was first described in Europe in 1571, while other species from the Middle East and Asia were also introduced to Europe at that time. The genus has about 130–140 species divided among eight subgenera. The flowers are usually solitary, nodding and bell-shaped with bulbs that have fleshy scales, resembling those of lilies. They are known for their large genome size and genetically are very closely related to lilies. They are native to the temperate regions of the Northern Hemisphere, from the Mediterranean and North Africa through Eurasia and southwest Asia to western North America. Many are endangered due to enthusiastic picking.

The name Fritillaria is thought to refer to the checkered pattern of F. meleagris, resembling a box in which dice were carried. Fritillaries are commercially important in horticulture as ornamental garden plants and also in traditional Chinese medicine, which is also endangering some species. Fritillaria flowers have been popular subjects for artists to depict and as emblems of regions and organizations.

Description

General

Fritillaria is a genus of perennial herbaceous bulbiferous geophytes, dying back after flowering to an underground storage bulb from which they regrow in the following year. It is characterised by nodding (pendant) flowers, perianths campanulate (bell- or cup-shaped) with erect segments in upper part, a nectarial pit, groove or pouch at the base of the tepal, anthers usually pseudobasifixed, rarely versatile, fruit sometimes winged, embryo minute.

Specific

Vegetative

; Bulbs

The bulbs are typically tunicate, consisting of a few tightly packed fleshy scales with a translucent tunic that disappears with further growth of the bulb. However, some species (F. imperialis, F. persica) have naked bulbs with many scales and loosely attached bulbils, resembling those of the closely related Lilium, although F. persica has only a single scale.

; Stems and leaves

The stems have few or many cauline leaves (arising from the stem) that are opposite on the stem or verticillate (arranged in whorls), sometimes with a cirrhose apex (ending in a tendril).

Reproductive

; Inflorescence and flowers

The inflorescence bears flowers that are often solitary and nodding, but some form umbels or have racemes with many flowers. The flowers are usually actinomorphic (radially symmetric), but weakly zygomorphic (single plane of symmetry) in F. gibbosa and F. ariana. The campanulate perianth has six tepals, in two free whorls of three (trimerous), that can be white, yellow, green, purple or reddish. The erect segments are usually tesselated with squares of alternating light and dark colours. While the tepals are usually the same size in both whorls, in F. pallidiflora, the outer tepals are wider. The tepals have nectarial pits, grooves (F. sewerzowii) or pouches at their base. In F. persica the nectarial pouch is developed into a short spur. The perigonal nectaries are large and well developed, and in most species (with the exception of subgenus Rhinopetalum), are linear to lanceolate or ovate and weakly impressed upon the tepals. Extrafloral nectaries are present at least the northwest American species according to Mizell 2004.

; Gynoecium

The flowers are bisexual, containing both male (androecium) and female (gynoecium) characteristics. The pistil has three carpels (tricarpellary). The ovaries are hypogynous (superior, that is attached above the other floral parts). The ovule is anatropous in orientation and has two integuments (bitegmic), the micropyle (opening) being formed from the inner integument, while the nucellus is small. The embryo sac or megagametophyte is tetrasporic, in which all four megaspores survive. The style is trilobate to trifid (in 3 parts) and the surface of the stigma is wet.

; Androecium

Stamens are six, in two trimerous whorls of three, and diplostemonous (outer whorl of stamens opposite outer tepals and the inner whorl opposite inner tepals). Filaments filiform or slightly flattened, but sometimes papillose and rarely hairy (F. karelinii). Anthers are linear to ellipsoid, but rarely subglobose (F. persica) in shape, and their attachment to the filament is usually pseudobasifixed (connective tissue extends in a tube around the filament tip), rarely attached at the centre and free (dorsifixed versatile; F. fusca and some Liliorhiza species). In contrast, pseudobasifixed anthers can not move freely. The pollen grains are spheroidal and reticulate (net like pattern), with individual brochi (lumina within reticulations) of 4–5 μm.

; Fruit and seeds

The capsule is obovoid to globose, loculicidal and six-angled, sometimes with wings. The seeds are flattened with a marginal wing, the seed coat made out of both integuments, but the testa is thin and the endosperm lacks starch. The embryo is small.

Phytochemistry

Fritillaria, like other members of the family Liliaceae, contain flavonol glycosides and tri- and diferulic-acid sucrose esters, steroidal alkaloids, saponins and terpenoids that have formed the active ingredients in traditional medicine (see Traditional medicine). Certain species have flowers that emit disagreeable odors that have been referred to as phenolic, putrid, sulfurous, sweaty and skunky. The scent of Fritillaria imperialis has been called "rather nasty", while that of F. agrestis, known commonly as stink bells, is reminiscent of canine feces. On the other hand, F. striata has a sweet fragrance. The "foxy" odor of F. imperialis has been identified as 3-methyl-2-butene-1-thiol (dimethylallyl mercaptan), an alkylthiol.

Genome

Fritillaria represents one of the most extreme cases of genome size expansion in angiosperms. Polyploidy is rare, with nearly all species being diploid and only occasional reports of triploidy. Reported genome size in Fritillaria vary from 1Cx (DNA content of unreplicated haploid chromosome complement) values of 30.15 to 85.38 Gb (Giga base pairs), that is > 190 times that of Arabidopsis thaliana, which has been called the "model plant" and > 860 times that of Genlisea aurea, which represents the smallest land plant genome sequenced to date. Giant genome size is generally defined as >35 pg (34 Gb). The largest genomes in diploid Fritillaria are found in subgenus Japonica, exceeding 85 Gb. At least one species, tetraploid F. assyriaca, has a very large genome. With approximately 127 pg (130 Gb), it was for a long time the largest known genome, exceeding the largest vertebrate animal genome known to date, that of the marbled lungfish (Protopterus aethiopicus), in size. Heterochromatin levels vary by biogeographic region, with very little in Old World and abundant levels in New World species. Most species have a basic chromosome number of x=12, but x=9, 11 and 13 have been reported.

Taxonomy

History

Pre-Linnaean

Gerard (1597) states that Fritillaria was unknown to the ancients, but certainly it was appearing in the writings of sixteenth century European botanists, including Dodoens (1574, 1583), Lobelius (1576, 1581), and Clusius (1583) in addition to Gerard, and was mentioned by Shakespeare and other authors of the period (see Culture). Species of Fritillaria were known in Persia (Iran) in the sixteenth century, from where they were taken to Turkey. European travelers then brought back specimens together with many other exotic eastern plants to the developing botanical gardens of Europe. discovered F. meleagris growing in the Loire meadows in 1570, he wrote to Carolus Clusius, describing it, and saying that it was known locally as fritillaria, supposedly because the checkered pattern on the flower resembled the board on which checkers was played. Clusius believed this to be an error, in that is actually the Latin name for the box in which the dice used in the game were kept, not the board itself.

Some North American species are called "mission bells".

Distribution and habitat

thumb|upright=1.5|Distribution map of ten Fritillaria species in Europe and western and central Asia|alt=Map showing the distribution of ten species of Fritillaria in Europe and Asia

alt=Fritillaria Imperialis in Dena, Iran|thumb|[[Fritillaria imperialis|Fritillaria Imperialis in Dena, Iran]]

Fritillaria are distributed in most temperate zone of the Northern Hemisphere, from western North America, through Europe, the Mediterranean, Middle East and Central Asia to China and Japan. Centres of diversity include Turkey (39 species) and the Zagros Mountains of Iran (14–15 species). Iran is also the centre of diversity of species such as F. imperialis and F. persica. There are five areas of particularly active evolution and clustering of species - California, Mediterranean Greece and Turkey, Anatolia and the Zagros mountains, central Asia from Uzbekistan to western Xinjiang and the eastern Himalayas in southwestern China. Fritillaria species are found in a wide variety of climatic regions and habitats, but about half of them show a preference for full sun in open habitats.

A number of Fritillaria are widely introduced. Cultivated fritillaries (F. meleagris) have been recorded in British gardens since 1578, but only in the wild since 1736, it is likely to be introduced, rather than be endemic. It is greatly diminished there due to loss of habitat, although persistent along the River Thames in Oxfordshire. F. imperialis was introduced into Europe around the 1570s, with Ulisse Aldrovandi sending a drawing to Francesco de' Medici in Florence, famed for his gardens at Villa di Pratolino in 1578. His friend Jacopo Ligozzi (1547–1627) was also including it in his paintings, as well as F. persica. In Britain, F. imperialis was first seen in the London garden of James Nasmyth, surgeon to King James I in April 1605.

Ecology

The majority of species are spring-flowering. Lily beetles (scarlet lily beetle, Lilioceris lilii and Lilioceris chodjaii) feed on fritillaries, and may become a pest where these plants are grown in gardens or commercially.

Fritillaria are entomophilous (insect pollinated). Those species with large nectaries (4–12 x 1–4 mm) and have more fructose than glucose in the nectar are most commonly pollinated by wasps, while those with smaller nectaries (2–10 x 1–2 mm) and a more balanced nectar composition are most commonly pollinated by bumblebees.

Conservation

A number of species of Fritillaria are endangered, from over-harvesting, habitat fragmentation, over-grazing and international demand for herbals. These include many species in Greece, and Fritillaria gentneri in the pacific Northwest of North America. In Japan, five of the eight endemic species (subgenus Japonica) are listed as endangered. In China, the collection of Fritillaria bulbs to make traditional medicine, particularly F. cirrhosa from southwest China and the eastern Himalayas of Bhutan and Nepal and one of the most intensively harvested of the alpine medicinal plants threatens extinction.

In Iran, F. imperialis and F. persica are endangered and F. imperialis is protected. The genus is threatened by irregular grazing, change in pasture usage, pest (primarily Lilioceris chodjaii) migration from pasture destruction, and harvesting by poor people for sale to florists.

One species, F. delavayi, has begun to grow brown, greyish flowers to better camouflage amongst the rock of its habitat. Scientists believe it is evolving to combat its biggest predator — humans. Over-picking has greatly decreased the availability of this species in China and even though there is no known difference between the flowers picked in the wild and those grown commercially, hunters continue to believe the wild flowers offer better medicinal benefit.

Toxicity

Most fritillaries contain poisonous steroidal alkaloids such as imperialin in the bulbs and some may even be deadly if ingested in quantity.

Uses

The bulbs of a few species, such as F. affinis, F. camschatcensis, and F. pudica, are edible if prepared carefully. They were commonly eaten by indigenous peoples of the Pacific Northwest coast of North America. The wild species flowering in areas such as Iran have become important for ecotourism, when in late May people come to the Valley of Roses, near Chelgerd, to see F. imperialis blooming. The area is also rich in F. reuteri and F. gibbosa.

Because of their large genome size, Fritillaria species are an important source for genomic studies of the processes involved in genome size diversity and evolution. They also have important commercial value both in horticulture and traditional medicine.

Horticulture

Species of Fritillaria are becoming increasingly popular as ornamental garden plants, and many species and cultivars are commercially available. They are usually grown from dormant bulbs planted in Autumn. As perennials they repeat flower every year, and some species will increase naturally. While Fritillaria is mainly harvested from the wild fields for commercial use, the growing price of the herbal product results in over-exploitation and puts the species at risk of depletion.

The following may be most commonly found in cultivation:-

  • Fritillaria acmopetala - pointed-petal fritillary
  • Fritillaria imperialis - crown imperial
  • Fritillaria meleagris - snake's head fritillary
  • Fritillaria pallidiflora - Siberian fritillary
  • Fritillaria persica - Persian fritillary
  • Fritillaria pyrenaica - Pyrenean fritillary

Traditional medicine

Species of Fritillaria have been used in traditional medicine in China for over 2,000 years, and are one of the most widely used medicines today. The production of medicines from F. cirrhosa is worth US$400 million per annum. Although some are cultivated for this purpose, most are gathered in the wild. In recent years demand has increased leading to over-harvesting of wild populations. In addition to China, Fritillaria products are used medicinally in the Himalayas, including India, Nepal and Pakistan, as well as Japan, Korea and Southeast Asia. To meet the demand additional countries such as Turkey and Burma are involved in the collection. The products are used mainly as antitussives, expectorants, and antihypertensives. The active ingredients are thought to be isosteroidal and steroidal alkaloid compounds. Chinese sources suggest 16 species as source material, but this may be an overestimate due to the large number of synonyms in Chinese. Of these, 15 are in subgenus Fritillaria (both subclades), but one (F. anhuiensis) is in subgenus Liliorhiza. F. imperialis also has a long history of medicinal usage in China and Iran.

thumb|Dried bulbs of [[fritillaria cirrhosa|F. cirrhosa|alt=Group of died bulbs of Fritillaria cirrhosa being prepared for making traditional medicine]]

Fritillaria extracts (fritillaria in English, bulbus fritillariae cirrhosae in Latin) are used in traditional Chinese medicine under the name (literally "Shell mother from Sichuan", or just ). Species such as F. cirrhosa, F. thunbergii and F. verticillata are used in cough remedies. They are listed as chuān bèi () or zhè bèi (Chinese: 浙貝/浙贝), respectively, and are often in formulations combined with extracts of loquat (Eriobotrya japonica). Fritillaria verticillata bulbs are also traded as bèi mǔ or, in Kampō, baimo (Chinese/Kanji: 貝母, Katakana: バイモ). In one study fritillaria reduced airway inflammation by suppressing cytokines, histamines, and other compounds of inflammatory response.

thumb|upright|[[Coat of arms of Großsteinbach, Austria|alt=Coat of arms of Großsteinbach in Austria, depicting a stylised flower of Fritillaria meleagris]]

Shakespeare, Matthew Arnold and George Herbert and more recently Vita Sackville-West (The Land 1927) wrote romantically about fritillaries. Fritillaries were also a favourite of the Dutch flower painters that emerged around 1600, such as Ambrosius Bosschaert and Jacob de Gheyn II, and appeared in Italian art, such as that of Jacopo Ligozzi in the late sixteenth century.

Fritillaries are commonly used as floral emblems. F. meleagris (snake's head fritillary) is the county flower of Oxfordshire, UK, and the provincial flower of Uppland, Sweden, where it is known as kungsängslilja ("Kungsängen lily"). In Germany, F. meleagris appears as a heraldic device in a number of municipalities, such as Hetlingen, Seestermühe and Winseldorf, and also in Austria (Großsteinbach).

In Croatia this species is known as kockavica (from , ), and the checkerboard pattern of its flowers may have inspired the checkerboard pattern on the nation's coat of arms. F. camschatcensis (Kamchatka fritillary) is the floral emblem of Ishikawa Prefecture and Obihiro City in Japan. Its Japanese name is kuroyuri (クロユリ), meaning "dark lily". Fritillaria montana is the floral emblem of Giardino Botanico Alpino di Pietra Corva, a botanical garden in Italy.

See also

  • Taxonomy of Liliaceae
  • History of botany

Notes

References

Bibliography

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Books and theses

  • , see also The Jepson Manual
  • see also Flora Europaea

Historical sources (chronological)

  • , trans. as
  • , see also Species Plantarum

Fritillaria in culture

Chapters

  • , in
  • , in
  • , in . additional excerpt

Articles

Regional

Traditional medicine and pharmacology

Subgenera

Species

Documents

Websites

  • see also

; Botanic gardens and herbaria

  • see also Giardino Botanico Alpino di Pietra Corva

; Databases

  • , see also Angiosperm Phylogeny Website

; Flora

; Organisations

; Posters