Boraginaceae (Borage family)

Boraginaceae unite about 115 genera and up to 2,500 species. They occur on all continents of the globe, but are most abundant in tropical, subtropical and partly in the northern temperate regions of the Earth. Boraginaceae are especially numerous in the Mediterranean, in western and central Asia and in the Pacific North America, in particular California.

They are distinguished by great diversity. Among them are woody and shrubby forms as well as perennial and annual herbs. Leaves are usually alternate, sometimes alternate-opposite, simple and usually entire, without stipules. With few exceptions Boraginaceae are characterized by a special type of stiff, bristly pubescence. Bristly hairs, bristles or even small spines are usually borne on white, naked or stellate-pubescent tubercles that are multicellular outgrowths of the epidermis. Many family members, in addition to the bristly hairs, also bear softer hairs, which like the bristles are various unicellular outgrowths of the epidermis.

A particular type of inflorescence is also common in Boraginaceae. It is always terminal, in the form of half-umbels composing one-sided coils (scorpioid or helicoid cymes), usually coiled like a snail before flowering. At fruiting the inflorescence axis uncoils and elongates considerably. The coils occur singly or in pairs at the stem tips or form complex panicle-like, corymbiform, spike-like or even head-like compound inflorescences; rarely the flowers are solitary in the axils of the upper leaves, as in Omphalodes scorpioides. Flowers are mostly bisexual, actinomorphic, sometimes slightly zygomorphic (for example in Alkanna), or distinctly zygomorphic as in Echium, usually 5-parted, very rarely 4-parted or many-parted. The calyx is gamosepalous, five-lobed or five-toothed; in fruit the calyx often becomes enlarged, sometimes very irregularly (e.g., Asperugo procumbens), and persists on the fruit, sometimes falling with it. The corolla is sympetalous, five-toothed or five-lobed. Petals in the bud are imbricate or contorted. Corolla coloration varies, and sometimes corollas on the same plant are differently colored, and in some species the color changes during the flowering period (for example yellow or white becomes reddish, pink becomes blue or violet). The adaptive significance of this phenomenon is not fully clear, and as K. Fægri and L. van der Pijl (1979) note, despite numerous attempts, no entirely satisfactory explanation from the point of view of pollination biology has yet been given. Some authors suggest that this color change increases contrast. It has also been noted that the flower color often changes noticeably after visits by pollinators. In the corolla tube, at the base of the stamens, fringed scales or tufts of hairs are sometimes visible, and sometimes the entire tube is hairy internally. There are five stamens, alternating with the corolla lobes or teeth and attached to its tube. Anthers are sometimes sagittate at the base, more rarely fused along their length or only at the base, forming a continuous tube that surrounds the style. The gynoecium usually consists of two (rarely more) carpels. The ovary is superior, usually two-locular, but in most Boraginaceae each locule is divided by a false septum into two parts, so that the ovary is divided into four false locules (chambers), each with one ovule. At the base of the ovary there is a ring-like disc that secretes nectar and is usually protected from unwanted insects and rain by scales or other appendages present in the corolla throat; more rarely the nectar disc is absent. The style is short; in representatives of the subfamilies Cordioideae, Ehretioideae and Heliotropioideae it is apical, but in the large and most advanced subfamily Boraginoideae, as well as in the small subfamily Wellstedioideae, the style is more or less long and gynobasic, i.e. arises from the depression between the lobes of the ovary. The style is simple, with a small capitate or bilobed stigma, or at the apex shortly bifid (as in most Echium species), or with four branches (as in the genus Cordia - Cordia).

Almost all Boraginaceae are entomophilous, pollinated mainly by bees and other Hymenoptera, while ornithophily has been observed in Cordia. Adaptations for cross-pollination are very diverse. Some species are protandrous, i.e. the stamens mature before the stigmas; others are heterostylous (presence of flowers with short or long styles). In Symphytum and Anchusa cross-pollination is aided by a prominently protruding style. Self-pollination can occur in the absence of insects, but in such cases seeds may fail to develop. Cleistogamous flowers are rare. In the relatively more primitive groups of Boraginaceae the fruit is a drupe with a fleshy or spongy epicarp and a hard stone containing 1–4 seeds (subfamilies Cordioideae and Ehretioideae and part of Heliotropioideae), but in most family members the fruit is dry and schizocarpic, splitting at maturity into four indehiscent nutlet-like lobes (mericarps). Sometimes only two carpels develop and accordingly two one-seeded nutlet-like lobes are formed (Rochelia), or the fruit divides into two two-locular halves, each containing a two-loculed nutlet-like portion (Cerinthe). The nutlet-like fruit lobes occur in a great variety of forms — elongate, nearly globose, sometimes dorsiventrally flattened, glabrous or hairy, smooth or tuberculate, longitudinally or reticulate-wrinkled or covered with hooked spines and other structures that aid their dispersal. Rarely the fruit is a capsule (the genus Wellstedia). With respect to dispersal methods, Boraginaceae are mainly epizoochorous; sometimes ballistic, anemochorous, myrmecochorous, or hydrochorous modes occur. All this depends on fruit size and structural formations — exocarpical outgrowths on the nutlet-like lobes. The nutlet-like lobes are attached to a flat or raised, pyramid-shaped four-angled gynobase which may be elevated above the nutlets or not exceed them. Based on differences in the structure of the gynoecium, androecium and other features, Boraginaceae are divided into five subfamilies.

Subfamily Cordioideae (Cordioideae) is characterized by an entire, unlobed ovary and an apical, twice two-cleft style. The fruit is a drupe with a 1–4-seeded stone. Cotyledons are folded. Endosperm is absent. Trees (sometimes fairly tall) and shrubs of subtropical and tropical regions. The main genus Cordia contains over 250 species, distributed mainly in the Americas. Some Cordia species provide valuable timber. The fruits of many species of this genus are quite edible, and some of them, for example the Mexican Cordia dodecandra (С. dodecandra), are cultivated as fruit trees.

Members of the subfamily Ehretioideae (Ehretioideae) also have an entire, unlobed, four-grooved ovary. The style is apical, bifid or entire, more rarely there are two styles. The fruit is a drupe with two two-seeded or four one-seeded stones. Cotyledons are flat. Endosperm may be present or absent. Almost all Ehretioideae are trees and shrubs. The only herbaceous representative of this pantropical subfamily is the genus Coldenia, characterized by having two styles sitting at the apex of the ovary; 20 species of this genus occur in tropical America, and one — Coldenia procumbens (С. procumbens) — in the tropics of the Old World. Ehretia (Ehretia), counting about 50 species and distributed in the tropics and subtropics mainly of the Old World, is characterized by having a single style with two grooves.

In members of the subfamily Heliotropioideae (Heliotropioideae) the ovary is entire or more or less lobed. The style is apical, with a ring of hairs beneath a conical or awl-shaped stigma. The fruit may be a drupe with two two-seeded or four one-seeded stones, or the fruit may be dry and schizocarpic (the genus Heliotropium). Seeds have poorly developed endosperm. Trees and shrubs occur in the tropics and subtropics, or more often herbs. The large pantropical and subtropical genus Tournefortia, with about 150 species, includes trees and shrubs. Very close to Tournefortia is the genus Argusia, containing 4 species, of which one — Argusia sibirica (A. sibirica) — is a perennial herb distributed from Japan across Siberia and the European part of Russia to Romania, growing on slightly saline seashores, lake shores and other water bodies; the second — Argusia sogdiana (A. sogdiana) — is also perennial, growing in the sandy deserts of Central Asia; the third — Argusia argentea (A. argentea) — is a small tree growing along seacoasts from Australia to Madagascar, and Argusia gnaphalodes (A. gnaphalodes) is a shrub occurring on the coast of West India. The genus Heliotropium (about 250 species) is the most widely distributed and species-rich. In the tropics and subtropics it is mainly shrubs; in temperate climates — herbs. The commonest in the Mediterranean to Iran and north to the Rhine region is Heliotropium europaeum (H. europaeum). In North and South America Heliotropium curassavicum (H. curassavicum) grows widely. Heliotropium peruvianum (H. peruvianum), native to Peru and Ecuador, has long been cultivated in many countries as a popular ornamental plant whose flowers have a vanilla-like scent.

In members of the subfamily Boraginoideae (Boraginoideae) the ovary is 2–4-locular, mostly 4-lobed. The style is basal, gynobasic, located at the base of the ovary between its lobes, simple or shortly bifid at the tip. The fruit is dry, schizocarpic, splitting into four one-seeded nutlet-like lobes. Seeds lack endosperm. The plants are predominantly herbs, less often subshrubs and shrubs (in the tropics). This subfamily mainly includes species of the Mediterranean and temperate regions. The subfamily is divided into 12 tribes, but we will touch on only some of them.

Members of the tribe Lithospermeae (Lithospermeae) typically have actinomorphic flowers. The style has a simple or two-lobed stigma or is split at the apex into two short or four longer branches. The receptacle is flat or lowly pyramidal. One of the relatively large genera of this tribe is Lithospermum (about 60 species), distributed almost worldwide (except Australia), but with the greatest number and diversity in North and partly South America, as well as in the Mediterranean. Many species of this genus are shrubs and subshrubs, others are herbs. Cross-pollination in Lithospermum is facilitated by a considerable narrowing of the corolla throat, so that an insect can touch stigmas and anthers with different parts of its proboscis. The most widespread species of this genus is Lithospermum officinale (L. officinale) with smooth glossy fruits. Its range extends from Europe to western China. The roots contain the coloring substance lithospermine, and the seeds contain fatty oil valued by the paint and varnish industry. The genus Onosma, much richer in species, contains at least 150 species distributed mainly in the dry regions of the Mediterranean and western and central Asia to western China. Its representatives are characterized by a tubular corolla with an open throat. Anthers are deeply divided at the base, with membranous appendages at the apex. Roots of almost all species contain alkanin. The greatest amount of alkanin is found in the roots of members of the Mediterranean genus Alkanna, which includes up to 30 species. Alkanna tinctoria (A. tinctoria), native throughout the Mediterranean countries, is cultivated in several European countries as a valuable dye plant and tolerates cold winters reasonably well. Many other genera belong to this tribe, including Arnebia (25 species distributed from the Mediterranean to the Himalayas and in tropical Africa), the small genus Moltkia (7 species from Italy to Iran), and the large boreal genus Mertensia (Mertensia), comprising over 50 mesophilous species growing in meadows and forests of Eurasia and North America. Some Mertensia species are the northernmost representatives of the Boraginaceae.

The tribe Cerintheae is characterized by a tubular corolla without folds in the throat, the presence of two 2-loculed parts of the fruit attached to a flat receptacle, and anthers with apices produced into a lanceolate-acuminate appendage. The tribe includes only one genus, Cerinthe, with about 10 species distributed in the temperate zone of Europe, Mediterranean countries and western Asia. They differ from other Boraginaceae by the near absence of long bristle-like hairs and by broader, stem-clasping leaves at the base.

The tribe Echieae is characterized by a slightly irregular calyx almost dissected to the base and a tubular corolla of various colors with a distinctly zygomorphic limb. The style in this tribe is long, filiform, and usually forked at the tip. The genus Echium, belonging to this tribe, includes over 50 species distributed in the western part of the Mediterranean. Among them are herbaceous perennials and shrubs. The eastern boundary of the genus runs through the Caucasus, the Caspian Sea region and southern Ukraine. Echium species are protandrous plants.

The tribe Boragineae (Boragineae) unites genera whose corolla is always actinomorphic with scales in the throat; the style is simple, naked, the stigma capitate and entire. The receptacle is flat; nutlet-like fruit lobes have a distinct ring of attachment and a conspicuous white caruncle projecting from it. One of the best-known members of this tribe is the genus Symphytum (comfrey) — more than 25 species distributed in the Mediterranean, western Asia and in the temperate climate of Europe. They have a tubular corolla with a bell-shaped or inflated limb of blue or yellow color and villous scales in the throat converging into a cone. Because of the relatively long corolla tube, Symphytum flowers can only be pollinated by insects with sufficiently long proboscises and long legs, so that the head and proboscis reach the base while the curved abdomen reaches the apex of the cone formed by the anthers. In doing so, they catch with their claws a special toothed appendage on the filament and detach the stamen from its neighbors; at the same time floury pollen is ejected from the cone onto the abdomen of the visiting insect. Symphytum officinale has long been cultivated in gardens and vegetable plots as a crop with a pleasant cucumber-like scent. It easily becomes wild and now occurs as an escaped and weedy plant in many regions of Europe and Asia. It is a good honey plant.

Among other genera of this tribe should be mentioned the predominantly European Pulmonaria (about 70 species). These are early-flowering woodland herbs of central and partly eastern Europe, but Pulmonaria mollissima (P. mollissima) with a tomentose and even velvety indumentum is distributed to Asia Minor and eastern Siberia. Pulmonaria is characterized by dimorphic heterostylous flowers. Its nectar is protected from all unwanted visitors except bumblebees by the long corolla tube.

The tribe Myosotideae is characterized by a short tube and a rotate limb. Petals in the bud are contorted-imbricate. Scales in the corolla throat are mostly well developed. The genus Myosotis (forget-me-not) of about 80 species is distributed in Eurasia and also in the mountains of tropical South Africa, New Guinea, Australia and New Zealand (where there are 34 species, almost all endemic). These are mesophilous herbs with thin stems and delicate leaves lacking stiff pubescence, often glabrous or nearly so. They inhabit forests, meadows, bogs, steppes and alpine zones. As in Lithospermum, cross-pollination is ensured by a considerable narrowing of the throat. Some Myosotis species have good ornamental qualities, creating an excellent blue background and can be widely used in ornamental gardening. The European alpine forget-me-not (M. alpestris) has long been a favorite lawn plant.

The tribe Eritrichieae, close to the forget-me-nots, contains up to 30 genera. Members of the tribe are characterized by a forget-me-not-like (brachymorphic) corolla type, with a short tube and a rotate or campanulate (in annuals) limb and colored scales in the corolla throat. The nutlets grow upward by their apices, so that they overtop the style, which is usually hidden between them, less often exceeding it. Externally the nutlets may be winged, but more often bear anchoring spines by which they are easily dispersed by animals. The most typical representative of the tribe is the genus Eritrichium (about 30 species), distributed in cold regions of Asia, partly in Europe and in western North America. The type of the genus is the alpocarpathian mountain species Eritrichium nanum (E. nanum), close to the arctoalpine Eritrichium villosum (E. villosum), which grows on stony places and rocks in the Arctic and in the high mountain belt of Siberia, the Far East and Central Asia.

The tribe Cynoglosseae is distinguished by the presence, in fruit, of a tall pyramidal elevated receptacle to which the nutlet-like lobes are attached. The largest genus in the tribe, Cynoglossum, contains up to 70 species distributed in temperate and subtropical zones and in the mountains of the northern hemisphere. The most widespread of them is Cynoglossum officinale (C. officinale), whose roots contain alkanin used to dye fabrics red. Young leaves are eaten as salad and are also used in folk medicine.

The subfamily Wellstedioideae (Wellstedioideae) is characterized by a four-parted flower and a laterally compressed two-lobed ovary. The fruit is a capsule, with 1–2 seeds in each locule. The genus Wellstedia (Wellstedia) includes two species distributed in southwestern Africa (Somalia) and on the island of Socotra. These are low woody herbs or subshrubs with densely appressed-pubescent leaves. As for the useful properties of many Boraginaceae members, they have been known for a long time. Already in the first century AD Pliny the Elder in his "Natural History" mentions the use of the leaves of Asperugo in the treatment of gout. In the directive "Capitulare de villis" issued in 812 under Charlemagne a list of many plants to be cultivated in gardens is given, among them borage (Во-rago officinalis), of which it is said: "Let it be used cheerfully in food and drink," since the leaves of the plant have a pleasant cucumber-like scent. In later times many Boraginaceae species are also mentioned in lists of useful plants.