Conservatoire et Jardin botaniques de la Ville de Genève
Monographia Aquifoliacearum - Loizeau Pierre-André & Gabrielle Barriera
Trees or shrubs, rarely climbers; base of trunk straight, rarely with small butresses; stem without latex or resin. Leaves usually evergreen, rarely deciduous, spirally arranged, rarely opposite or subopposite, simple, coriaceous to chartaceous, stipulate. Plants dioecious. Flowers small, hypogynous, regular, unisexual by abortion, without disk, often 4-6-merous or up to 23-merous, in axillary cymose inflorescences, sometimes reduced to one flower. Sepals small, more or less connate at the base or free (I. mucronata). Petals imbricate, mostly connate at the base, rarely free (e.g. Ilex collina and I. mucronata). Stamens usually isomerous, alternating with the petals, and connate at the base. Carpels isomerous, united to form a superior ovary, with as many locules as carpels, each generally containing one ovule. The fruit is a drupe red, black, yellow, white, orange or purple but mostly variation of red, containing 1--6 (--23) pyrenes, seed small with abundant oily and proteinaceous endosperm, without starch. A family of irregular cosmopolitan distribution; comprising one genus and more than 500 species.
Vegetative morphology and anatomy. The stem is straight and up to 30 m high, and rarely has small buttresses. The leaves are simple, evergreen or rarely deciduous, spirally arranged (2/5 for the leaves, bracts and cymes), rarely opposite or subopposite, orbiculate, oblanceolate, elliptic, ovate or lanceolate. Their length is approximately 2-15 cm, with a maximum of 35 cm in I. megaphylla from Sarawak and a minimum of 4 mm in I. microphylla. The base of the lamina is acute to obtuse, the apex truncate to acute, often acuminate, and the margin can be serrate, crenate, or entire, rarely spinose. Heterophylly with leaves spiny or entire can be present in the same species (e.g. I. dipyrena and I. dimorphophylla), or on the same plant (e.g. I. aquifolium). Stipules present, often caducous, small. The leaves are coriaceous, rarely chartaceous, rarely pubescent, and punctate or not. Hairs simple and unicellular. The cortex is grey or ochre; the sub-epiderm is green. The wood is yellow and its sap oxidizes rapidly after damage and becomes black. This provides important field characters. Wood anatomy has been extensively studied by Baas (1974). Based on the observation of 81 species of Ilex, he concluded that the wood is characterized by conspicuous growth rings, numerous narrow but relatively short vessel elements with few bars per perforation plate. Thickenings on vessel and fibre walls are spiral, and the fibre-tracheids frequently have numerous conspicuously bordered tangential wall pits (Baas 1974).
Inflorescence structure. The flowering unit is the cyme, which can be reduced to one flower, or amplified up to 1531 flowers. They are then solitary dichasium, or arranged in thyrses, fascicles or thyrsoids. Most of the species contains thyrses, which are mostly borne at the axillary meristems, rarely terminals. Thyrses could be either non-proliferating, or proliferating when the post-flowering growth is vegetative. In the case of the former, the axis of the thyrse can be contracted, so that it appears like a fascicle. A determinate thyrse is defined as a thyrsoid inflorescence. Solitary dichasium takes place when the bracts of proliferating thyrses are developed in leaves, thus only dichasia occur, appearing to be axillary. The evolution and classification of the genus Ilex can be based on the structure of the inflorescences. Loesener (1901, 1908) classified his sub-genera and lower ranks on the basis of the inflorescence type (e.g. solitary cymes, fascicles, racemes, or panicles). Hu (1949-1950) in her work on the Ilex of China used the cyme as the flowering unit, while Loizeau and Spichiger proposed a phylogenetic classification (Loizeau 1994).
Flower morphology. The flowers are hypogynous, regular, unisexual by abortion, often 4--6 or up to 23-merous in all whorls. The first flower of the cyme or the terminal flower of the thyrsoid can sometimes have one extra sepal and petal. The calyx is glabrous or pubescent, valvate, with small lobes and a more or less connate base. Calyx persistent, rarely caducous (I. mucronata), semipersistent in I. collina. The corolla is often white or cream, rarely green, yellow, pink, purple, red or chocolate-coloured, with imbricate petals, and 1--10 mm in length. The petals are mostly connate at the base to up to half of their length. Some species have free petals (I. collina, I. mucronata and I. vismiifolia). In the pistillate flowers, the stamens alternate with the petals, are usually glabrous, and have a white filament. The anthers are basifixed and introrse. The aborted ovary is conical. In the pistillate flowers, staminodes with sterile anthers are present, these are glabrous, rarely pubescent. The syncarpous ovary is globose, with as many locules as carpels. The style is terminal, very short, or absent, and has a distinct stigma, with lobes poorly developed. One ovule is found in each locule, but additional aborted ovules can occur. The ovules are generally apical-axile, pendulous, anatropous, apotropous, unitegmic, crassinucellar, and with a large funiculus. Because of the presence of staminodes in the pistillate flower and an aborted ovary in the staminate flower, some authors have considered Ilex to have bisexual flowers.
Embryology. Ives (1923) observed that embryo is in a very immature condition when the drupe falls from the tree. It continues growing, very slowly, for a long period of 8-12 months.
Pollen. The pollen morphology has been extensively studied by Lobreau (1969). The pollen is tricolporate, isopolar, clavate, the exo-apertures are furrows with granular membranes, and the endo-apertures are oval and small. Individual pollen grains are between 17-47 m X 18-48 m, being larger in species of higher latitude or altitude (Lobreau-Callen 1977).
Pollination. Pollination usually is accomplished by insects (ants, bees, flies, wasps) attracted by nectar produced at the base of the petals.
Fruit and seed dispersal. The seeds are dispersed by birds. They present a case of delayed germination. In nature it requires from one to three years, and the percentage of germination is about one in ten million (Ives 1923).
Kariology. Chromosome numbers of about 30 species of Ilex, mostly Asiatic, are known (Goldblatt 1981, 1984). Four different base numbers, x = 17, 18, 19, 20 are found. The majority of the species (21) are reported to be diploid and to have 2n= 40 chromosomes. Polyploidy occurs in some species: I. pedunculosa (2n = 120) is hexaploid, I. anomala (2n = 80) and I. verticillata (2n = 72) are tetraploid. Most Ilex species have 2n = 40 chromosomes.
Phytochemistry. The Aquifoliaceae are sometimes saponiferous or tanniferous, accumulate proanthocyanins and rarely cyanogenic compounds, but lack ellagic acid or iridoid compounds. Alikaridis (1987) studied the natural constituents of approximately 50 species worldwide; their stimulating and vomitive actions have to be related to the presence of purine bases in very high quantity (caffeine, theobromine, theophylline or adenine). Moreover, they contain vitamins (C, B1, B2), nicotinic acid, and carotene (Alikaridis 1987). According to Lewis et al. (1991), I. guayusa has the highest concentration of caffeine and methylxanthine known.
Affinities. Various hypotheses for the affinities of Aquifoliaceae have been published. For Cronquist (1981, 1988), Aquifoliaceae were considered to be included in Celastrales, near Celastraceae. This view is based on the morphology of the ovule with a dorsal raphe (Bentham and Hooker 1862) and the thick funiculus of the Aquifoliaceae which was considered by Loesener (1908) to be homologous to the aril in the Celastraceae. Hallier (1903) placed Aquifoliaceae in his "Umbellifloren" (Umbellifereae/Apiaceae and their relatives) because of the small embryo and their common unisexuality. Baillon (1891) put Aquifoliaceae between Ericaceae (because of the descendent placenta) and Ebenaceae (because of the drupaceous fruit). Tieghem (1898) placed Aquifoliaceae near Solanaceae because of the unitegmic ovule and the isomerous stamens alternating with the petals. Based on pollen, Lobreau (1969) bracketed Aquifoliaceae together with Gentianales and Campanulales. Finally, Dahlgren (1983) placed them in Cornales because of the unitegmic ovules, whereas Thorne (1992) placed Aquifoliaceae in Theales, as did Baas (1974, 1975) on the basis of wood anatomy. Based on several phylogenetic studies based on both molecular and non-molecular characters, Aquifoliaceae are now well placed within order Aquifoliales together with Helwingia Willd. and Phyllonoma Willd., two genera with epiphyllous inflorescences, at the basis of euasterids (Savolainen et al. 2000a, 2000b; Soltis et al. 2000; Bremer et al. 2001). This placement of Ilex into a clade containing mostly gamopetalous plants is confirmed as the petals are often connate at the base of the tube and because of the unitegmic ovules. Putative synapomorphies for the family may include the unisexual flowers and fleshy fruits (Bremer et al. 2001). Since Nemopanthus has been shown to be included with Ilex (Powell et al. 2000), Aquifoliaceae, Helwingiaceae and Phyllonomaceae are three monotypic families that may be better fused into a single family (Bremer et al. 2001; Powell et al. 2000; Savolainen et al. 2000a; 2000b; Soltis et al. 2000).
Ecology and distribution. Ilex occurs in all tropical areas of the world and extends into temperate regions to up to 63° N (America, Eurasia) and 35° S (America, Africa) (Baas 1974) from lowland to montane forests and up to 4000 m altitude in the Andes (Loizeau 1994). However, its distribution is very irregular and most species occur in South America and Asia. Hu (1949-1950) estimated that there exist 120 species in China and up to 200 in South East Asia. Andrews (2002) assumes that there are some 120 species in South East Asia, and Loizeau (1994) estimated that up to 300 species are found in America. There exist only two to three species in Europe, I. aquifolium (also in N Africa), I. colchica and I. perado subsp. iberica; one in Australia, I. arnhemensis, and one in Africa south of the Sahara, I. mitis. 26 species are native to Eastern North America (Kartesz 1994).
Paleobotany. Pollen of a type attributed to Ilex is known from Turonian deposits in Australia and Coniacian deposits in Africa. The pollen is cosmopolitan in the Paleocene (Muller 1970).
Economic impostance and uses. Many species of Ilex are of horticultural importance and are widely grown in parks and gardens throughout the world for their foliage and decorative berries. These include (Andrews 1982, 1983a, 1983b, 1984a, 1984b, 1985, 1989, 1991, 1992) I. aquifolium, the common holly and its many cultivars, I. x altaclerensis (I. aquifolium x I. perado), I. opaca, the American holly (Eisenbeiss and Dudley 1973), I. cornuta, the horned holly, and I. crenata, the Japanese holly (Dudley and Eisenbeiss 1992). In China I. purpurea (I. chinensis is a misapplied name) is commonly planted as an ornamental tree, and the fruiting branches are used to decorate temple courts and halls from December to February. Large quantities of glossy- berried branches are sold at the Chinese New Year (Hu 1949-1950). The leaves of over 60 species of Ilex are used for beverages. The most widely known is a tea (tereré) made from I. paraguariensis, the Yerba Maté or Paraguay Tea (Loizeau 1988). This species is native to Argentina, Uruguay, Paraguay and Brazil and is drunk throughout South America. The Yaupon or I. vomitoria from Southeastern North America and Mexico has been used by certain North American Indians who brewed a tea called the Black Drink or Cassena. This was said to restore lost appetite, guarantee health and give courage and agility in war (Hudson 1979, Alikaridis 1987). Several species are known for their medicinal properties and the leaves of I. aquifolium were used as an infusion for smallpox, catarrh and pleurisy. The berries acted as an emetic and purgative and have been used for dropsy and to prevent bleeding (Coles 1657). Ilex guayusa (see phytochemistry) has been used for centuries as a medicine, an emetic and as a stimulant (Lewis et al. 1991). The roots of the widespread South East Asian I. cymosa are said to have medicinal properties, especially in the treatment of fevers (Andrews 2002). Ilex mitis, the only species to occur naturally south of the Sahara, has been used as an enema for colic in children, as a purgative and is used in witchcraft (Andrews 1994). The wood of I. aquifolium is hard and white and has been much prized for ornamental ware. The strong, straight shoots when stripped of their bark are made into whip handles and walking sticks (Dallimore 1908). The leaves were used as winter food crop for livestock in England, Wales and Northwest France from the Middle Ages onwards (Spray 1981). The wood of I. cissoidea from Sumatra, Sulawesi and Borneo has been used for firewood and possibly for making matches. The dried leaves were pounded into a powder and used as a soap (Andrews ined.), as were the leaves of I. mitis, while the wood is used for furniture, ceilings, brake blocks, railway sleepers or for firewood (Andrews 1994).
One genus in Aquifoliaceae: Ilex.