Loranthaceae

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Loranthaceae

Description

Perennial evergreen hemiparasites, usually aerial stem-parasitic shrubs, sometimes terrestrial root-parasitic shrubs or trees; attachment to the host (in aerial stem-parasites) by many haustoria produced on epicortical runners (especially in Malesia) or by a single complex woody primary haustorium. Leaves mostly opposite, less frequently alternate or verticillate, always simple; stipules absent. Inflorescences mostly axillary, less frequently terminal, internodal or borne on the epicortical runners; uniflorescence a simple dichasium (triad) or a single flower, these usually aggregated to racemose, umbellate or capitate compound inflorescences. Whilst the external form of the flowers does not appear exceptional, there are some very unusual features of ovary structure and embryology (Maheshwari et al. 1957; Johri & Bhatnagar 1960). There are no normal ovules. In many species there is a central mound or column, the mamelon, which occupies most of the ovarian cavity, and which may be homologous with an axile placenta. In some cases the base of the mamelon is lobed, and these lobes may be homologous with ovules. Bands of tissue radiating between the lobes to the ovary wall may form 3 or 4 obscure cells in the ovarian cavity, and are possibly homologous with septa. In other cases the mamelon is simple or completely absent, and the ovarian cavity is hardly more than a small dilation of the base of the stylar canal. The sporogenous tissue is massive, located either in 3 to 4 blocks in the mamelon lobes or in a single block at the base of the ovarian cavity. These structures may represent progressive reduction of a syncarpous ovary, and the extreme of the reduction sequence, for example in Amyema, is an almost completely undifferentiated ovary with a single group of sporogenous cells at the base of the stylar canal. There are several embryo sacs which elongate up the stylar canal to various levels, so that fertilization occurs in the style, sometimes close to the base of the stigma (Helixanthera, Den- drophthoe). Rapid development of a long suspensor pushes the proembryo down into the ovary before the style is shed. Normally only one embryo develops in the seed, and the viscous layer develops from a zone in the ovary wall outside the vascular bundles. These features of embryology are so exceptional in angiosperms that Van Tieghem (1896) treated loranths and related groups as a subclass of the angiosperms with rank equivalent to the monocotyledons and dicotyledons.
Flowers dichlamydeous, mostly hermaphrodite, when unisexual plants mostly dioecious. Stamens as many as and opposite the petals, epipetalous; anthers mostly basifixed, immobile and continuous with the filament, sometimes dorsifixed and then usually versatile, opening by longitudinal slits; pollen mostly trilobate, rarely triangular or spherical. Ovary ('calyx tube' of some authors) inferior; ovarian cavity with or without a central column (mamelon); ovules absent; sporogenous tissue massive, located in lobes of the mamelon or at the base of the ovarian cavity; style and stigma simple. Fruit mostly berry-like, with a single seed covered by a sticky layer which develops outside the vascular bundles.

Distribution

Asia-Tropical:, New Guineapresent; Philippines (Philippinespresent) northern Borneo: present northern temperate zone: present southern temperate regions: present tropical regions: present
About 65 genera and 950 species, predominantly tropical tropical regionsbut well represented also in southern temperate regions; occurrence in the northern temperate zone is limited. In Malesia 23 genera and 193 species, distributed throughout the region; major centres of species richness are the Philippines, New Guinea and northern Borneo. For biogeography see below.

Ecology

Loranthaceae exhibit a suite of remarkable adaptations associated with the hemiparasitic habit, especially in the majority of the species which occur as aerial stem parasitic shrubs; for additional details see under morphology below.

Effective seed dispersal is by fruit-eating birds, and demonstrates close mutualism involving fruit and embryo structure, germination, and bird anatomy and behaviour (Docters van Leeuwen 1954; Reid 1989; Barlow & Schodde 1993). The ovoid seed, 5-12 mm long, is covered by a viscous layer rich in carbohydrates. The seed is removed from the fruit and swallowed whole, and passes through the short alimentary canal of the bird rapidly, commonly in 10-20 minutes. Although nutrients have been absorbed from the viscous layer, it is intact when the seed is voided. The most specialized bird dispersers, for example Dicaeum spp., perform specific movements when defecating, such that the voided seed is placed on the branch on which the bird is perched. The viscous layer cements the seed in place, and it germinates spontaneously, probably because it has been removed from an inhibiting environment within the wall of the fruit. These adaptations together greatly increase the likelihood that the seed will be dispersed to a suitable habitat on a tree branch. Instead of normal roots, the embryo radicle produces an haustorium which penetrates to the cambial layer of the host to take up water and nutrients from the xylem. See .

Host preference and specificity vary widely within the family. Most loranths grow on dicotyledonous trees, but some utilize gymnosperms as occasional hosts, and a few species are specialized for growth on gymnosperms. In mixed forests with high tree species diversity the loranths tend to have very low host specificity, occurring on a broad range of host species; this is the common situation in Malesia. In open woodlands with low tree species diversity and one or two dominant tree species, the loranth flora tends to be more closely adapted for growth on the common host, and therefore to show high host specificity. This situation is common in Australian woodlands, and occurs to a limited extent in the Malesian monsoon belt, especially in the Lesser Sunda Islands.

When host specificity is high the loranth species may sometimes show a visual resemblance to the preferred host (Barlow & Wiens 1977). By influencing the birds' search image, this may increase the likelihood of dispersal to the preferred host species. It may also confer some protection from herbivores. Because of the generally low host specificity of Malesian loranths this phenomenon is almost absent in Malesia, although the parasites of Eucalyptus, Melaleuca and Pittosporum in Timor and adjacent islands tend to resemble the host in leaf form. In rain forests any resemblance between the leaves of loranths and their hosts is probably convergence in response to habitat conditions rather than a genuine mimicry.

There are several pollination syndromes in the family. Bird pollination is most common and many genera, especially in Malesia, have tubular curved brightly coloured corollas with exserted stamens and nectar chambers at the base. In Malesia the pollinators are commonly sunbirds to the west of Charles's Line and honey eaters to the east. Beyond Malesia bird pollination may include explosive mechanisms, especially in Africa. Insect pollination also occurs, and is indicated in species with relatively small spreading choripetalous corollas or short bell-like tubular corollas which are often pale-coloured. Insect pollination is probably the primitive state for the family (see below), and in Malesia this may be represented in Cecarria. In other genera such as Amyema and Den- drophthoe insect pollination may be a secondary development. In some Malesian genera, notably Macrosolen and Trithecanthera, slender tubular corollas may reach 150 mm in length, and may be pollinated by moths. Beyond Malesia, corolla lengths up to 250 mm occur, notably in the South American genus Aetanthus.

Taxonomy

Until relatively recently the family Loranthaceae has been treated in a broader sense. It was traditionally divided into two subfamilies, Loranthoideae and Viscoideae, the latter including genera now placed in Viscaceae and Eremolepidaceae. There are substantial differences between Loranthaceae sens.str. and Viscaceae in flower and fruit development and structure, summarized by Barlow (1964). The brief diagnostic key to the two families presented at the end of this section covers all Malesian taxa. Loranthaceae and Viscaceae may not be directly related; the former is possibly derived from root parasitic Olacaceae, whilst the latter is probably close to and derived from aerial stem-parasitic Santalaceae (Kuijt 1969).

At generic level, the taxonomic history of Loranthaceae sens. str. (= Loranthoideae) has been turbulent. Originally hundreds of species were assigned to a single genus Loranthus, which was therefore cosmopolitan and very heterogeneous. Many segregate genera had been recognized early in the 19th century (but subsumed in Loranthus by other authors), and in this respect the work of Blume was notable for Malesia, as he recognized several genera now widely accepted (Dendrophthoe, Elytranthe, Lepeostegeres, Lox- anthera, Macrosolen). Engler (1889) recognized 10 genera, but still retained a very large and diverse genus Loranthus. Between 1894 and 1902 Van Tieghem revised the loranths, recognizing many new diagnostic characters, and distinguishing about 100 genera. However, Van Tieghem's approach was somewhat mechanical, and he used diagnostic characters of doubtful value as generic determinants repeatedly in different groups. Between 1929 and 1933 Danser reviewed and rationalized Van Tieghem's work, and recognized c. 65 genera, including a few he circumscribed himself. The generic classification of the family now generally accepted is little different from that of Danser (1929, 1933); for summary see the outline by Kuijt in Barlow et al. (1989). It is fortunate that Danser's special interest was in Malesian Loranthaceae and Viscaceae, as his work has provided a critical and substantial base for the present treatment.

At the species level loranths have presented much taxonomic difficulty. Many species show considerable variability, and there is evidence of introgression in many taxa. Numerous segregate taxa have been recognized where narrow species concepts have been applied, and have resulted in unsatisfactory treatments from both practical taxonomic and biogeographic viewpoints. For Malesia numerous names have been placed in synonymy, both by Danser (1931, 1935) and Barlow (1974, 1992, 1993). For further discussion see Barlow (1992: 297).

Phylogenetic analysis of Loranthaceae is aided by suites of character states in which polarity is clear and correlations strong. These include karyological and embryological data, morphological data from haustorial, inflorescence and floral structures, pollination syndromes and geographic relationships (see above). For details see Barlow (1983). The phylogeny of the family is strongly reflected in its biogeography (see below).

Subsequent to the recognition of Loranthaceae and Viscaceae as distinct families, there has been only limited attention to the classification of genera into infrafamilial groups. Kuijt, in Barlow et al. (1989), recognized a number of informal groups of genera in a provisional treatment not yet formalized. In this treatment the Malesian genera are grouped as follows.
  • Group "21-30": Amylotheca, Cyne, Decaisnina, Elytranthe, Lampas, Lepidaria, Lepeo- stegeres, Loxanthera, Macrosolen, Thaumasianthes (the last transferred from Group "31-39').
  • Group "31-39": Amyema, Cecarria, Dactyliophora, Distrianthes, Papuanthes, Sogerianthe.
  • Group "40-70": Barathranthus, Dendrophthoe, Helixanthera, Loranthus, Scurrula, Taxillus, Trithecanthera.

Group "21-30" corresponds with subtribe Elytranthinae Engl., recognized by Danser (1933), distinguished by cotyledons emerging from the seeds and expanding during germination, and by a basic chromosome number of x = 12. Groups "31-39" and "40- 70" together correspond with subtribe Hypheatinae Danser as accepted by Danser (1933). This subtribe is distinguished by cotyledons remaining embedded in endosperm in the seeds during germination, and by a basic chromosome number of x = 9. Groups "31- 39" and "40-70" differ in basic inflorescence structures (although obscured by inflorescence evolution in each Group), and generally in chromosome size. Group "31-39" is Australian/Papuasian in origin, whilst Group "40-70" is African/Asian. See also the discussion on plant geography below.

Cytology

Chromosomal characters have made a significant contribution to taxonomic and phylo- genetic knowledge of the family (Barlow & Wiens 1971; Martin & Barlow 1984). The primary basic chromosome number is x = 12, and the other basic numbers of x = 11, 10, 9 and 8 indicate progressive dysploid reduction. Polyploidy is virtually absent, but there is a general trend towards increase in chromosome size, and the largest chromosomes in the family are equal to any in the plant kingdom. There is considerable genomic stability, with particular chromosome numbers and sizes being constant for entire suites of related genera, and cytogeographic data are therefore phylogenetically useful. In Malesia there are lineages with x = 12 and x = 9, with different geographic histories; see discussion under biogeography below.

Uses

Mistletoes, including Loranthaceae, feature prominently in folk legend and medicine (Kanner 1939; Barlow 1987). Superstitions about mistletoe are widespread in many human cultures, and involve numerous species. In most cases mistletoes were regarded as a good omen, providing protection from misfortune, injury, crop failure or evil spirits, or good luck in finding wealth or fertility. They have been widely used medicinally, to treat a broad range of afflictions, through both internal and external application. In the related family Viscaceae some of these uses appear to be based on genuine medicinal properties (antispasmodic, diuretic, antihaemorrhagic, muscle toning, lowering blood pressure), but Loranthaceae do not appear to have these properties. The widespread prominence of mistletoe in legend and medicine is probably due to its growth habit. When growing on trees of ritual or utilitarian importance (see ), it may have been regarded as the 'heart' of the tree, important for its survival.

Phytochemo

Much of the phytochemical study of mistletoes has been undertaken at a time when Loranthaceae and Viscaceae were treated as a single family Loranthaceae sens. lat. Furthermore many of the studies have involved comparative work in several genera of both families, identifying similarities and differences between the groups then considered subfamilies. For this reason it is appropriate to consider the phytochemistry of the two families together, to identify the contribution of chemotaxonomy to the current treatment of the two families. Chemical data are not available for a third segregate family, Eremolepidaceaeand the status of this family is not considered further.

The chemical data presently available, although limited, allow some general observations on the taxonomic significance of metabolism and storage of primary and secondary plant products in stems, leaves, fruits and seeds of mistletoes, and their two major component groups, Loranthaceae and Viscaceae.

Apart from the considerable attention given to the traditional European mistletoe, Vis- cum album, phytochemical investigations of mistletoes are relatively few. The phyto- chemistry of Loranthaceae s.l. and its possible taxonomic implications were treated by Hegnauer (1966, 1989, where many additional phytochemical references are given). Many aspects of the biology of semiparasitic Santalales, especially of Loranthaceae and Viscaceae, were reviewed in a work edited by Calder & Bernhardt (1983). A series of International Symposia on Parasitic Flowering Plants (e.g., Weber & Forstreuter 1987) has also fostered contributions to phytochemical knowledge. Becker and Schmoll (1986) published a valuable ethnobotanical monograph of European Viscum album, and Kanner (1939) of mistletoes generally, of relevance for all students of mistletoes.

Citation

Kuijt - in Brittonia. 1969
P. Royen - in Alpine Fl. New Guinea. 1982: 2257
Backer & Bakh. f. - in Fl. Java. 1965: 67
Barlow et al. - in The Golden Bough. 1989
Danser - in Bull. Jard. Bot. Buitenzorg. 1929: 291
Barlow - in Proc. Linn. Soc. New S Wales. 1964: 269
Tiegh. - in Bull. Soc. Bot. France. 1894: 138
Agardh, Theoria Syst. PI. 1858: 117
Barlow - in Handb. Fl. Papua New Guinea. 1981: 206
Danser - in Verh. Akad. Wet. Amst. Afd. Natuurk. 1933
Tiegh. - in Bull. Soc. Bot. France. 1896: 247
Barlow - in Fl. Austral. 1984: 68
Miq. - in Fl. Ind. Bat. 1856: 807
Wiens - in Rev. Handb. Fl. Ceylon. 1987: 123