Amaryllidoideae

The Amarilidoideae (Amaryllidoideae) are a subfamily of monocotyledonous, herbaceous, perennial plants, provided with bulbs or rhizomes belonging to the Amaryllidaceae family and the Asparagales order. It comprises 59 genera and approximately 800 species native to mostly temperate and warm regions, from all continents. They were first classified by Jean Henri Jaume Saint-Hilaire in his work published in 1805.

Amarilidoids are usually bulbous plants that can be easily recognized by their rather fleshy leaves, their umbel-shaped inflorescence at the end of a scape, and by their flowers, usually large and showy, with six stamens and a inferior ovary. Members of the garlic and onion subfamily (Allioideae) are quite similar to the amaryllidoids, but differ from them by the position of the ovary and by not presenting allyl sulfide, a sulfur compound that gives garlic its characteristic odor. From another closely related group, the agapanthus (Agapanthoideae subfamily), they are also distinguished by the position of the ovary and by the absence of steroidal saponins, which are typical of the latter.

Many of the Amaryllid species are popular as ornamental plants in parks and gardens, and are also grown as cut flowers throughout the world.

Description

Perigonio (cream) and paraperigonio (yellow) in Narcissus.

Triphyte stigma Hippeastrum.

Umbela in Scadoxus.

Loculic capsule in Hippeastrum.

Amaryllidoids are terrestrial, rarely aquatic or epiphytic, herbaceous or succulent and perennial plants. They present bulbs or, more rarely, rhizomes (for example in Clivia and Scadoxus). The bulbs are covered by the membranous bases of the leaves, forming a structure called a "tunica". The primary root is well developed and have contractile roots.

The leaves are simple, parallel-lined, with an entire edge, linear, oblong, elliptic, lanceolate or filiform, sessile or petiolate, generally rosette, spiral or distichous. The leaves present a persistent basal meristem and basipetal development.

The flowers are hermaphroditic, actinomorphic (that is, radially symmetric) or slightly zygomorphic, pedicelate or sessile, showy, each one associated with a filiform bract. The perigonium is composed of six tepals arranged in two whorls of 3 pieces each, which have approximately the same shape and size. The tepals are free from each other or may be welded at the base, forming a perigonial tube or hypanthus, which is often prolonged into a crown (paraperigonium or false corolla, for example in Narcissus), sometimes reduced to unremarkable scales or teeth. Tepals can be green or green and white, pure white, or some combination of cream, yellow, red, pink, purple, or brown, very rarely blue.

The androecium has six stamens in two whorls of three pieces each (rarely 3 stamens, as in Zephyra, or in some cases up to 9-18, as in Gethyllis), opposite the tepals, inserted on the perigonium tube or the base of the tepals. The filaments are thin, filiform or widened at the base, they can be free (Hippeastrum) or be joined together by a membrane that surrounds the entire ovary called " staminal cup", as for example in Hymenocallis. The anthers are oblong or linear. The stamens sometimes have appendages that form a staminal crown (for example in Hymenocallis).

The gynoecium is ovarian and inferous, formed by three carpels joined together and delimiting three cavities or locules, which contain from two to three to many anatropous ovules with axillary placentation. The ovary is continuous with a style and with a minute stigma, capitate to deeply trifid. They usually present floral nectaries and nectar secretion comes from the perigonium or gynoecium, usually in the ovary septa.

The flowers are arranged in determined cymose inflorescences at the end of a scape, sometimes compacted and similar to umbels (for which they are called "pseudoumbelas"), rarely reduced to solitary flowers. Involucral bracts, those that enclose the flower buds, may be present or absent.

The fruit is an indehiscent capsule or a loculicidal capsule, occasionally it can be a berry. The seeds are dry to fleshy, flattened to globose, winged or wingless, and have an endosperm that does not reserve starch but rather oils. The testa is usually encrusted with phytomelanins (with a few exceptions, such as Amaryllis or Hymenocallis). The color of the seeds is usually black, or also green or red. Chromosomes in amaryllids are generally long, from 3 to 28 µm. The basic chromosome numbers are x = 6, 8, 9, 10, 11 and 26; and differ between tribes.

Ecology

Widely distributed, from tropical to temperate regions, and especially diverse in South Africa, Andean South America, and the Mediterranean region.

Biology of reproduction

Vegetative multiplication in amaryllid species is ensured through the bulbs and rhizomes that these species present. As in other bulbous plants, a single individual, even in isolation, can multiply indefinitely over time in an asexual way thanks to these structures. Likewise, several species of amaryllidoids are sterile, so vegetative reproduction is the only reproductive alternative they have. An example is Hippeastrum petiolatum native to Uruguay. This species is a sexually sterile triploid that produces an abundant number of bulbils around the mother bulb. These bulbils are able to float in the water, so in the rainy season they are dragged by surface currents and travel to sites far from the original bulb, which ensures not only the propagation but also the distribution of this species.

All the species of the subfamily are hermaphrodites, so the possibility of producing seeds by self-pollination is high. This mode of reproduction, although it does not guarantee a high genetic diversity in natural populations, allows multiplication through seeds even in isolation, which is why it is a strategy used by many colonizing species. Hippeastrum reticulatum is an example of an autogamous species. In the same way, apomixis (asexual reproduction through seeds) is another of the reproductive strategies that numerous species of amaryllids put into play to produce descendants identical to the mother plant, even in conditions of isolation from other individuals of the same species. Examples of genera that have species with apomictic reproduction are Habranthus, Zephyranthes and Crinum.

Vegetative multiplication, autogamy and apomixis are highly effective reproductive alternatives in colonizing or sterile species. However, the continuous evolution in these species also requires the generation of new genetic variability through crossing between different individuals of the same species, a mechanism called outcrossing. Amaryllidoids present several strategies to prevent self-pollination and therefore favor outcrossing. Thus, there are self-incompatible species, that is, they can only produce seeds if they receive pollen from individuals that are not genetically related, as occurs in many species of Hippeastrum.

Dichogamy (protandry or protogyny) is also a mechanism that promotes allogamy in numerous species of amaryllidoids. In this case, the time of maturity of the pollen or the stigma are different, so it is not possible that the pollen could pollinate the pistils of the same flower. In Hippeastrum, for example, pollen is released approximately two days before the stigma of the same flower is receptive, so self-pollination in this species is highly unlikely.

Finally, heterostyly is another mechanism that promotes allogamy present in various species of amaryllidoids. In this case, there are two types of flowers (rarely three): flowers with a long style and short stamens, and flowers with a short style and long stamens. The only legitimate pollinations (that is, those that can give rise to seeds) are those that take place among the pollen produced by anthers of the same size as the pistils, for which, again, self-pollination is prevented. Heterostyly is common in Narcissus species.

Pollination

The butterflies of the Sphingidae family are pollinators of various species of amarilidoid.

Self-incompatibility, hercogamy, and heterostyly are reproductive strategies that favor outcrossing in amaryllids and require pollen to be transported between different plants. That transport is done through insects or birds.

The showy flowers of the Amaryllidaceae are pollinated by bees, wasps, butterflies, moths, and birds. Each species has developed different methods to ensure the visit of birds or insects and, therefore, the transport of pollen. For example, amaryllidoids adapted to pollination by moths (Sphingidae) have flowers with a long perigonial tube, light colors, a perigonium that fully expands at night, strong fragrance, and abundant nectar production. Species of the genera Crinum, Cyrtanthus and Pancratium from southern Africa display these characteristics.

Scatter

Seeds are usually dispersed by wind or water, but in some taxa, such as Eucharis subg. Eucharis, the blue seeds contrasting with the bright orange capsules, promote dispersal by birds. The large, fleshy seeds without phytomelanins have appeared numerous times within the family. Some are dispersed by water.

Phytochemistry and toxicity

Amarilidoids have a unique type of tyrosine-derived alkaloids called norbeladins. Such alkaloids are responsible for the poisonous properties of a large number of species of the subfamily. More than 200 different structures are known, of which 79 were identified in the genus Narcissus alone. The amaryllidoids do not present allyl sulfide (characteristic of the Alliaceae), anthocyanidins, ellagic acid, saponins or inulin. Flavonols may or may not be present.

Amarilidoids are endowed with various chemical defenses against herbivory (insects, mammals). Among such defense mechanisms are alkaloids and lectins. Although the presence of these substances provides plants with an effective defense mechanism against herbivorous animals, they make them highly toxic to humans. In fact, the vernacular names of some species allude to this characteristic. Thus, Boophone disticha is known in South Africa as "gifbol" (poison bulb) due to its legendary toxicity. This property was used by the aborigines of Southern Africa to poison their arrowheads when hunting. Most, if not all, amaryllids are toxic to humans. As an example, Amaryllis belladonna has an alkaloid in the bulb called lycorine, which affects the heart and if the bulbs are ingested in large quantities, they can be fatal. The genera Ammocharis, Boophone, Brunsvigia, Clivia, Crinum, Cyrtanthus, Galanthus, Haemanthus, Hymenocallis, Narcissus, Nerine, Scadoxus and Zephyranthes have been cited as toxic to humans due to the presence of alkaloids in the bulbs or other parts of the plant.

Systematics

Phylogeny

Combined analysis of three chloroplast DNA sequences for 50 genera of amaryllids jointly analyzed with members of the Allioids subfamily and the families Behniaceae, Convallariaceae, Hyacinthaceae, Themidaceae, and Hemerocallidaceae resolved the Amaryllids as a monophyletic group and the agapantoids as its most closely related clade. In turn, he arranged the Agapantoidea-Amarilidoidea clade as the sister clade to the Allioideae.

Tribal characterizations within the family were provided by Alan W. Meerow (1995), Meerow et al. (1999a, b, 2000a, b), and Meerow and Snijman (1998, 2006).

Amaryllideae (Amaryllis, Nerine, Crinum and related) is sister to the other genera, Amaryllideae is easily recognizable by the apomorphies of the presence of a sclerenchyma sheath on the scape, bisulcated pollen with a spiny exine, ovules with a single integument, non-dormant seeds, rich in water that do not have phytomelanins and have a chlorophyll embryo.

Among the other genera, Haemantheae (containing for example Haemanthus, Clivia) are diagnosed by their fruits being berries, and are present in Africa, while the rest of the genera are American and Eurasians and form a clade.

A large group of American genera (Hymenocallis, Eucharis, Habranthus, Zephyranthes, Hippeastrum, andGriffinia) probably form a monophyletic group. They could be recognized by their obvolute spataceous bracts (ie two bracts that overlap at the bud so that one half of each is external and the other half is internal). Eurasian genera, such as Lycoris, Narcissus, Leucojum, and Galanthus, also form a clade, which apparently has no morphological support.

The cladogram that synthesizes the phylogenetic relationships between the tribes and subtribes of the Amaryllids is provided below:

The tribes of Amaryllidoideae

The subfamily, according to phylogenetic analyses, originated in western Gondwana (Africa) and then migrated to the rest of the world. The 800 species of the subfamily can be arranged into 13 tribes which, in turn, can be grouped into clades as suggested by their phylogenetic analysis based on plastid DNA sequences. Such clades are consistent with the geographic distribution of the tribes. A first clade, made up of the tribe Amaryllideae, is sister to the rest of the family. The two remaining African tribes (Haemantheae and Cyrtantheae) and the Australasian tribe (Calostemmataceae) make up a second clade. Finally, the American and Eurasian elements of the family form two separate, monophyletic, sister clades. The Amaryllidaceae tribes, the number of genera that make up each one, their basic chromosome number and some characteristics of each one, are listed below:

• Amaryllideae (11 genera, x=10 and 11): this tribe is characterized by the presence of cartylaginous fibers in the leaves, escapos with sclerénquima, bisulcated pollen with spinulous exine (the pollen grains are monosulcated and with reticulated exine in the remaining genera of the family) and by the unitégmic eggs. The seeds of the members of this tribe are green and fleshy and do not present a period of sleep or latency, so they germinate quickly, even on the same mother plant. Several popular genres in gardening belong to this tribe, entirely African, such as Amaryllis, Crinum and Nerine.

• Cyrtantheae (1 genus, x=8): consists of a single endemic gender in Africa, Cyrtanthus, which has been separated from the remaining members of Haemantheae to dispose of in their own tribe. It shares with some Haemantheae genres the same chromosomal number (x=8) and the strictly African distribution, but is distinguished by its locculic capsules. The chat, winged and phytomelanine seeds distinguish Cyrtantheae from all other African tribes. It is, on the other hand, the most diverse tribe in terms of floral morphology.

• Haemantheae (6 genera, x= 6, 8, 9, 11 and 12): this African tribe consists of genera that have fruit in the form of fleshy berry and with seeds of short viability. In general, they have no bulb but fasciculated roots, for example Clivia, Scadoxus and Cryptostephanus

• Calostemmateae (2 genera, x= 10). This tribe consists of two genera, Proiphys and Calostemma, which constitute a component of Australasia isolated from the rest of the family.

• Lycoridae (2 genera, x= 11). It is the lineage of Central and Eastern Asia of the family. The two genres that make up it (Lycoris) and Ungernia) they are closely related philosophically to the Pancratiae tribe.

• Pancratieae (2 genera, x= 11). It is a tribe distributed in the Old World, with a very controversial phylogenetic position. Pancratium is the member of the tribe with a wider distribution.

• Narcisseae (2 genera, x=7, 10 and 11). Characterized by a solid escapo and spinal bracts merged into a tube. Narcissus presents paraperigonio, which is absent Sternbergia.

• Galantheae (5 genera, x=7, 8, 9, 11 and 12), is a tribe very related to the previous one and, in fact, for some taxonomes it should be considered a subtribu of Narcisseae. Galanthus and Leucojum are two popularly known genres in gardening.

Hipeastrum bicolor.

• Hippeastreae (ca 10 genera, x= 6, 8, 9, 10, 11 and 12). It's a neotropical tribe from America. It is characterized by a hollow escape and a certain development of paraperigonio. Hippeastrum, Griffinia, Habranthus, and Sprekelia are some of the genres of this tribe.

• Eucharideae (4 genera, x= 23). American tribe with representatives from the east of Los Andes. They present long, hairy leaves. The genders that make up this tribe are Eucharis, Caliphuria, Urceolina and Plagiolirion.

• Stenomesseae (8 genera, x=23). It is a Andean tribe, characterized by a chromosomal number 2n=46 and a paraperigonio well developed in most genres. Stenomesson is one of the representatives of the tribe.

• Hymenocallideae (3 genera, x=23). American tribe constituted by gender Ismene, Hymenocallis and Leptochiton, those with a very developed star crown.

• Eustephieae (3 genera, x=23). This tribe represents a clay of the central and southern Andes. Gender Eustephia, Hieronymiella and Chlidanthus have dry seeds, chats and discoids.

List of genres

The family has 59 genera and more than 800 species. The most represented genera are Crinum (130 species), Hippeastrum (70 species), Zephyranthes (60 species), Hymenocallis (50 species), Cyrtanthus (50 species), Haemanthus (40 species), and Narcissus (30 species).

The currently accepted genera of Amaryllidaceae are as follows (synonyms are listed in parentheses).

• Acis Salisb.
• Amaryllis L.
• Ammocharis Herb. (Incl.: Cybistetes Milne-Redh. & Schweick.)
• Apodolirion Baker.
• Boophone Herb.
• Brunsvigia Heist.
• Caliphruria Herb.
• Calostemma R.Br.
• Chlidanthus Herb. (incl.: Castellanoa Traub)
• Clinanthus Herb.: Callithauma Herb.; Crocopsis Pax; Anax Ravenna)
• Clivia Lindl.
• Crinum L.
• Crossyne Salisb.
• Cryptostephanus Welw. ex Baker.
• Cyrtanthus Aiton (without: Anoiganthus Baker; Vallota Salisb. ex Herb.)
• Eucharis Planch. " Linden
• Eucrosia Ker Gawl. Callipsyche Herb.)
• Eustephia Cav.
• Galanthus L.
• Gethyllis L. (no.: Klingia Schönl.)
• Griffinia Ker Gawl. Hyline Herb. as a subgender)
• Griffiniopsis Dutilh & Meerow.: Eithea Ravenna)
• Habranthus Herb.: Zephyranthella (Pax) Pax; Haylockia Herb.)
• Haemanthus L.
• Hannonia Braun-Blanq. & Maire
• Hessea Herb.: Kamiesbergia Snijman)
• Hieronymiella Pax.: Eustephiopsis R.E.Fr.)
• Hippeastrum Herb. (without: Moldenkea Traub)
• Hymenocallis Salisb.
• Ismene Salisb. ex Herb (incl. Elisena Herb. and Pseudostenomesson Velarde as subgeners)
• It's her. Lag.
• Leptochiton Sealy
• Leucojum L.
• Lycoris Herb.
• Mathieua Klotzsch
• Namaquanula D.Müll.-Doblies & U.Müll.-Doblies
• Narcissus L. (including Braxireon Raf. and Tapeinanthus Herb.)
• Nerine Herb.
• Pamianthe Stapf
• Pancratium L. (no.: Mizonia A.Chev.; Chapmanolirion Dinter)
• Paramongaia Velarde
• Phaedranassa Herb. (without: Neostrickland Rauschert; Strickland Baker)
• Phycella Lyndl. (incl.:Famatina Ravenna)
• Placea Miers
• Plagiolirion Baker.
• Proiphys Herb.: Eurycles Salisb. ex Schult. & Schult.)
• Pyrolirion Herb.
• Rauhia Traub
• Rhodophiala C.Presl (without: Rhodolirium Phil.; Rhodolirion Dalla Torre & Harms)
• Scadoxus Raf. Choananthus Rendle)
• Sprekelia Heist.
• Stenomesson Herb. (without: Pucara Ravenna)
• Sternbergia Waldst. " Kit.
• Strumaria Jacq. ex Willd. (No.: Bokkeveldia D.Müll.-Doblies & U.Müll.-Doblies; Carpolyza Salisb; * Gemmaria Salisb.; Carpolyza Salisb.; Tedingea D.Müll.-Doblies & U.Müll.-Doblies)
• Traubia Moldenke
• Ungernia Bunge
• Urceolina Rchb. Collania Schult. & Schult.f.; Pseudourceolina Vargas)
• Vagaria Herb.
• Worsleya (Watson ex Traub) Traub
• Zephyranthes Herb. (without: Cooperia Herb.)

The monotypic genus Pucara Ravenna has been included within Stenomesson Herb. according to phylogenetic studies carried out on nuclear and plastid DNA sequences. The genus Acis was reinstated in 2004 as a segregation of several species of Leucojum after Phylogenetic studies on DNA molecular data and morphology of Leucojum and Galanthus have been carried out. The study of the chromosomes of several species of the tribe Amaryllideae led some taxonomists to the conclusion creation of several genera, many of them monotypic, such as Bokkeveldia, Tedingea, Namaquanula, Kamiesbergia and to the re -installation of the old genus Gemmaria. However, later studies led to their reduction as synonyms of Hessea and Strumaria. Based on various morphological aspects, the genus Hyline was considered not to have enough differences to keep it separate from Griffinia and was transferred as a subgenus of the latter.

Intergeneric Hybrids

In the amaryllidoids several intergeneric hybrids have been obtained artificially, which propagate asexually. These hybrids of horticultural origin (notogenus) receive names that include the names of the two genera that gave rise to them. Some of the recognized notogena of amaryllidoids, with their corresponding synonyms, are:

• × Amarcrinum Coutts (no.: × Crindonna Ragion.; × Crinodonna Stapf; × Amarcrinaflora): is the result of the cross between species of the genus Amaryllis gender Crinum.

• × Amarine Sealy, it's the result of the cross between Amaryllis with copies of gender Nerine.

• × Hippeastrelia, is the result of the cross between a kind of Hippeastrum with a kind of Sprekelia.

Economic importance

Many of the Amaryllid species are popular as ornamental plants in parks and gardens. Thus, various species and varieties of the genera Crinum, Nerine, Amaryllis, Leucojum, and Hippeastrum have been cultivated for this purpose for centuries. A separate mention deserves the case of Narcissus, cultivated in various parts of the world as an ornamental in gardens and also for cut flowers.

Eucharis, Galanthus, Haemanthus, Hymenocallis, Lycoris and Cyrtanthus are also cultivated. Other genera, such as Habranthus and Zephyranthes, are not as well known, but their cultivation and breeding is already established in various parts of the world.

Many taxa are used by indigenous peoples for medicinal, flavoring, psychotropic, and other purposes.

The diversity of types of flowers in the Amaryllids

• 

  Zephyranthes citrine

• 

  Narcissus pseudonarcissus

• 

  Eucharis amazonica

• 

  Hippeastrum