Amaryllidaceae

The Amaryllidaceae (amaryllids) are a family of herbaceous, mainly perennial and bulbous (rarely rhizomatous) flowering plants included in the monocot order Asparagales. The family takes its name from the genus Amaryllis, hence the common name of the amaryllis family. The leaves are usually linear, the flowers usually bisexual and symmetrical, arranged in umbels on the stem. The petals and sepals are undifferentiated as tepals, which may be fused at the base into a floral tube. Some also display a corona. Allyl sulfide compounds produce the characteristic odour of the onion subfamily (Allioideae).

The family, which was originally created in 1805, now contains about 1600 species, divided into about 75 genera, 17 tribes and three subfamilies, the Agapanthoideae (agapanthus), Allioideae (onions and chives) and Amaryllidoideae (amaryllis, daffodils, snowdrops). Over time it has seen much reorganisation and at various times was combined together with the related Liliaceae. Since 2009 a very broad view has prevailed based on phylogenetics, and including a number of other former families.

The family are found in tropical to subtropical areas of the world and include many ornamental garden plants and vegetables.

Description

The Amaryllidaceae are mainly terrestrial (rarely aquatic) flowering plants that are herbaceous or succulent geophytes (occasionally epiphytes) that are perennial, with the exception of four species. Most genera grow from bulbs, but a few such as Agapanthus, Clivia and Scadoxus develop from rhizomes (underground stems).^[3]

The leaves are simple rather fleshy and two-ranked with parallel veins. Leaf shape may be linear, strap like, oblong, elliptic, lanceolate (lance shaped) or filiform (threadlike). The leaves which are either grouped at the base or arranged alternatively on the stem may be sessile or petiolate and possess a meristem.

The flowers, which are hermaphroditic (bisexual), are actinomorphic (radially symmetrical), rarely zygomorphic, pedicellate or sessile, and are typically arranged in umbels at the apex of leafless flowering stems, or scapes and associated with a filiform (thread like) bract. The perianth (perigonium) consists of six undifferentiated tepals arranged in two whorls of three. The tepals are similar in shape and size, and may be free from each other or fused at the base (connate) to form a floral tube (hypanthium). In some genera, such as Narcissus, this may be surmounted by cup or trumpet shaped projection, the corona (paraperigonium or false corolla). This may be reduced to a mere disc in some species.

The position of the ovary varies by subfamily, the Agapanthoideae and Allioideae have superior ovaries, as do the while the Amaryllidoideae have inferior ovaries. There are six stamens arranged in two whorls of three, occasionally more as in Gethyllis (Amaryllidoideae, 9–18).

The fruit is dry and capsule-shaped, or fleshy and berrylike.

The Allioideae produce allyl sulfide compounds which give them their characteristic smell.^[4][5]

Taxonomy

History

Early

The name Amaryllis had been applied to a number of plants over the course of history. When Linnaeus formerly described the type genus Amaryllis, from which the family derives its name, in his Species Plantarum in 1753,^[6] there were nine species with this name. He placed Amaryllis in a grouping he referred to as Hexandria monogynia (i.e. six stamens and one pistil)^[7] containing 51 genera in all^[8] in his sexual classification scheme.

The Hexandria monogynia have come to be treated as either liliaceous or amaryllidaceaous (see Taxonomy of Liliaceae) over time.^[9] From 1763, when Adanson conceived of these genera as 'Liliaceae'^[10] they were included in this family, placing Amaryllis in Section VII, Narcissi.^[11] of his scheme, in which the Liliaceae had eight sections.

With de Jussieu's came the formal establishment of organising genera into families (ordo) in 1789.^[12] De Jussieu established the hierarchical system of taxonomy (phylogeny), placing Amaryllis and related 15 related genera within a division of Monocotyledons, a class (III) of Stamina Perigynia^[13] and 'order' Narcisse, divided into three subfamilies.^[14] This system also formally described the Liliaceae, which were a separate order within the Stamina perigynia (Lilia). The use of the term Ordo (order) at that time was closer to what we now understand as Family, rather than Order.^[15][16] In creating his scheme he used a modified form of Linnaeus' sexual classification but using the respective topography of stamens to carpels rather than just their numbers.

The Amaryllidaceae family was formally named as 'Amaryllidées' (Amaryllideae) in 1805, by Jean Henri Jaume Saint-Hilaire.^[17] In 1810 Brown proposed that a subgroup of Liliaceae be distinguished on the basis of the position of the ovaries and be referred to as Amaryllideae^[18] and in 1813 de Candolle described Liliacées Juss. and Amaryllidées Brown as two quite separate families.^[19] The literature on the organisation of genera into families and higher ranks became available in the English language with Samuel Frederick Gray's A natural arrangement of British plants (1821).^[20] Gray used a combination of Linnaeus' sexual classification and Jussieu's natural classification to group together a number of families having in common six equal stamens, a single style and a perianth that was simple and petaloid, but did not use formal names for these higher ranks. Within the grouping he separated families by the characteristics of their fruit and seed. He treated groups of genera with these characteristics as separate families, such as Amaryllideae, Liliaceae, Asphodeleae and Asparageae.^[21]

John Lindley (1830, 1846) was the other important British taxonomist of the early nineteenth century. In his first taxonomic work, An Introduction to the Natural System of Botany (1830)^[22] he partly followed Jussieu by describing a subclass he called 'Endogenae, or Monocotyledonous Plants' (preserving de Candolle's Endogenæ phanerogamæ)^[23] divided into two tribes, the Petaloidea and Glumaceae. He divided the former, often referred to as petaloid monocots, into 32 orders, including the Amaryllideae.^[24] He defined the latter as "Hexapetaloideous bulbous hexandrous monocotyledons, with an inferior ovarium, a 6-parted perianthium with equitant sepals, and flat spongy seeds" and included Amaryllis, Phycella, Nerine, Vallota, and Calostemma.

By 1846, in his final scheme^[25] Lindley had greatly expanded and refined the treatment of the monocots, introducing both an intermediate ranking (Alliances) and tribes within families. Lindley placed the Liliaceae within the Liliales, but saw it as a paraphyletic ("catch-all") family, being all Liliales not included in the other orders, but hoped that the future would reveal some characteristic that would group them better. This kept the Liliaceae^[26] separate from the Amaryllidaceae^[27] (Narcissales Alliance). Of these Liliaceae^[26] was divided into eleven tribes (with 133 genera) and Amaryllidaceae^[27] into four tribes (with 68 genera), yet both contained many genera that would eventually segregate to each other's contemporary orders (Liliales and Asparagales respectively). The Liliaceae would be reduced to a small 'core' represented by the Tulipae tribe, while large groups such Scilleae and Asparagae would become part of Asparagales either as part of the Amaryllidaceae or as separate families. While of the four tribes of the Amaryllidaceae, the Amaryllideae and Narcissea would remain as core amaryllids while the Agaveae would be part of Asparagaceae but the Alstroemeriae would become a family within the Liliales.

Since then seven of Linnaeus' Hexandria monogynia genera have consistently been placed in a common taxonomic unit of amaryllids, based on the inferior position of the ovaries (whether this be as an order, suborder, family, subfamily, tribe or section).^[28] Thus much of what we now consider Amaryllidaceae remained in Liliaceae because the ovary was superior, till 1926 when John Hutchinson transferred them to Amaryllidaceae.^[29] This usage of the family entered the English language literature through the work of Samuel Frederick Gray (1821),^[30] William Herbert (1837)^[31] and John Lindley (1830,^[32] 1846^[33]). Meanwhile Lindley had described two Chilean genera which for which he created a new family, Gilliesieae.^[34]

The number of known genera within these families continued to grow, and by the time of the Bentham and Hooker classification (1883) the Amaryllidaceae (Amaryllideae) were divided into four tribes, of which only one (Amarylleae) is still included.^[35] The Liliaceae^[36] were becoming one of the largest families, and Bentham and Hooker divided it into 20 tribes, of which one was the Allieae,^[37] which as Allioideae would eventually become part of Amaryllidaceae as two of its three subfamilies. The Allieae included both Agapantheae,^[38] the third of the current subfamilies, and Lindley's Gilliesieae^[39] as two of its four subtribes.^[40]

The family were treated similarly in the German language literature, for instance Engler's classification. In Engler's system (1903) Allieae and Gilliesiae are both considered tribes of subfamily Allioideae, within Liliaceae.^[41]

Modern era

The early twentieth century was marked by increasing doubts about the placement of the alliaceous genera within Liliaceae. Lotsy was the first taxonomist to propose separating them, and in his system he describes Agapanthaceae, Alliaceae and Gilliesiaceae as new and separate families from Liliaceae.^[42] This approach was adopted by a number of other authorities, such as Dahlgren (1985)^[43] and Rahn (1998).^[44]

Another approach was that of John Hutchinson (1926), who performed the first major recircumscription of the family in over a century. He doubted that Brown's dictum that the position of the ovary was the distinguishing feature that separated Amaryllidaceae and Liliaceae. He believed that the characterising feature of the family was rather "an umbellate inflorescence subtended by an involucre of one or more spathaceous bracts".^[29] His work on this has been upheld by subsequent research and his definition remains valid today.^[45] Using this criterion, he removed a number of taxa (Agavaceae, Hypoxidaceae, Alstroemeriaceae) and transferred the Agapantheae, Allieae and Gilliesieae from Liliaceae to Amaryllidaceae.^[29]

Other writers proposed reuniting Amaryllidaceae with Liliaceae. Thorne (1976)^[46] and Cronquist (1988)^[47] both included Amaryllidaceae within a broad concept of Liliaceae^[28] (although Thorne would later separate them again, but keep Alliaceae as a third family).^[48] Thus 'Alliaceae' were variously included in either Liliaceae, Amaryllidaceae, or as a separate entity. This uncertainty of circumscription reflected a wider problem with the petaloid monocots in general. Over the course of time there have been widely differing views as to the limits of the family, and consequently much of the literature dealing with this family requires careful inspection to determine which sense of the Amaryllidaceae the work treats.

Phylogenetic era

The current phylogenetic era began with the work of Fay and Chase (1996) who developed the broader (sensu lato) concept of the family, utilising the plastid gene rubisco rbcL to demonstrate monophyly across three earlier families (Agapanthaceae, Alliaceae, Amaryllidaceae)^[49] and incorporating them into one large Amaryllidaceaefamily, the component families being reduced to subfamilies.^[50] The 2009 APG classification (APG III of 2009) formally adopted this broad view of the Amaryllidaceae. The Angiosperm Phylogeny Website (2013 onwards) lists 73 genera and 1605 species,^[51] while The Plant List (2013) gives 80 genera and 2,258 species.^[52]

Phylogeny of Amaryllidaceae

Cladogram

Family Amaryllidaceae

Subfamily Agapanthoideae (monogeneric, Agapanthus) Subfamily Allioideae Tribe Allieae (monogeneric, Allium) Tribe Tulbaghieae Tribes Gilliesieae, Leucocoryneae Subfamily Amaryllidoideae Tribe Amaryllideae Subtribe Amaryllidinae Subtribe Boophoninae Subtribe Strumariinae Subtribe Crininae Tribe Cyrtantheae Tribe Haemantheae Tribe Calostemmateae Eurasian clade Tribe Lycorideae European tribes Tribe Galantheae Tribe Pancratieae Tribe Narcisseae American clade Hippeastroid clade Tribe Griffineae Tribe Hippeastreae Subtribe Hippeastrineae Subtribe Zephyranthinea Andean clade Tribe Eustephieae Tribe Stenomesseae Tribe Eucharideae Tribe Clinantheae Tribe Hymenocallideae

Subdivision

A wide variety of suprageneric classifications existed within the Amaryllidaceae, for instance Hickey and King (1997) describe ten tribes by which the family were divided, such as the Zephyrantheae.^[53]

The Amaryllidaceae has three subfamilies;^[54]

• Agapanthoideae - previously the Agapanthaceae family with a single genus
• Allioideae - previously the Alliaceae family with around 20 genera
• Amaryllidoideae - previously the Amaryllidaceae family with about sixty genera.

These subfamilies are then further divided into tribes and genera as follows (see also Cladogram, below);

• Subfamily Agapanthoideae
•     Genus Agapanthus
• Subfamily Allioideae
•   Tribe Allieae
•     Genus Allium
•   Tribe Tulbaghieae
•     Genus Tulbaghia
•   Tribe Gilliesieae (18 genera)
• Subfamily Amaryllidoideae (15 tribes)
•   Amaryllideae Dumortier
•   Calostemmateae D. & U. Müller-Doblies
•   Clinantheae Meerow
•   Cyrtantheae Traub
•   Eucharidae Hutch.
•   Eustephieae Hutch.
•   Galantheae Parlatore
•   Griffineae Ravenna
•   Haemantheae Hutch.
•   Hippeastreae Sweet (Two subtribes)
•   Hymenocallideae Small
•   Lycoridae D. & U. Müller-Doblies
•   Narcisseae Lamarck & de Candolle
•   Pancratieae Dumortier
•   Stenomesseae Traub

Distribution

Tropical to subtropical areas of the world.

Cultivation and uses

The Amaryllidaceae include many ornamental garden plants such as daffodils, snowdrops and snowflake, pot plants such as amaryllis and Clivia, and vegetables, such as onions, chives, leeks and garlic. A number of tropical lily-like plants are also sold, such as the belladonna lily, tuberose (Polianthes), blood lily (Cape tulip), Cornish lily (Nerine), and the Eurasian winter daffodil, Sternbergia.

Their economic importance lies in floriculture for cut flowers and bulbs, and commercial vegetable production.

References

Bibliography

Wikispecies has information related to: Amaryllidaceae

Wikimedia Commons has media related to Amaryllidaceae.

External identifiers for Amaryllidaceae
Encyclopedia of Life	8187
GBIF	7682
ITIS	182703
NCBI	4668

Subdivisions of the Amaryllidaceae family, with type species Agapanthoideae Agapanthus Allioideae Allieae Allium Tulbaghieae Tulbaghia Gilliesieae Gilliesia Amaryllidoideae Amaryllideae Amaryllidinae Amaryllis Boophoninae Boophone Strumariinae Strumaria Crininae Crinum Cyrtantheae Cyrtanthus Haemantheae Haemanthus Calostemmateae Calostemma Lycorideae Lycoris Galantheae Galanthus Pancratieae Pancratium Narcisseae Narcissus Griffineae Griffinia Hippeastreae Hippeastrineae Hippeastrum Zephyranthinea Zephyranthes Eustephieae Eustephia Stenomesseae Stenomesson Eucharideae Eucharis Clinantheae Clinanthus Hymenocallideae Hymenocallis Subfamilies, Tribes, Subtribes, Genera