Clivia mirabilis ( Amaryllidaceae : Haemantheae ) a new species from Northern Cape , South Africa

Clivia m irabilis Rourke is a new pendulous tubular-flowered species from Oorlogskloof Nature Reserve in Northern Cape. Its distribution area is some 800 km outside the previously accepted range of the genus Clivia. This sun-tolerant species is adapted to an arid Mediterranean climate, producing vegetative growth in winter and maturing its seeds rapidly in late summer/early autumn to synchronize with the arrival o f winter rains.


INTRODUCTION
The genus Clivia Lindl., consisting of four currently recognized species, C. nobilis Lindl.(1828), C. miniata (Lindl.)Regel, C. gardenii Hook.(1856) and C. caulescens R.A. Dyer (1943), is presently considered to be endemic to southern Africa (Vorster & Smith 1994: Snijman 2000).These species occur in coastal and inland Afromontane forest from Eastern Cape through K w aZulu-Natal, Swaziland and Mpumalanga to the Soutpansberg in Northern Province.Rumours o f the occurrence of Clivia in Mozambique have not yet been confirmed by accu rately localized herbarium collections.
Clivia is an evergreen, rhizomatous genus in the A m aryllidaceae, characterized by distichous strap shaped leaves, umbellate solid scapes and red subglobose berries containing one to few cartilaginous, pearly-white seeds embedded in soft yellow pulp.
In February 2001 material of a further species was submitted to the Compton Herbarium for identification in a batch of herbarium specimens from the Oorlogskloof Nature Reserve near Nieuwoudtville, in Northern Cape, collected by the nature conservation officer in charge.Mr Wessel Pretorius.The author confirmed this astonishing discovery during a site visit to Oorlogskloof on 22 February 2001 when two fruiting populations were examined.The new species is here described as Clivia mirabilis.Rarely can such an extravagant epithet as mirabilis be confidently applied, yet in the case of this extraordinary Clivia.so unusual in its distribution and characters, its usage seems entirely appropriate.

Diagnostic < haracters
Clivia mirabilis is distinguished by its straight, actinomorphic, bicolored (orange/yellow) tubular corolla, long drooping pedicels, 25-40 mm long, that are orangered at anthesis and green when fruiting; the distinctive single median white striation on the upper surface of the leaves with smooth cartilaginous margins; and irregular ly shaped glebulose-gongyloid berries.The basal part of the leaves forming the leaf sheath is flushed a deep carm ine m aroon, unlike any other Clivia except C. n o bilis, which occasionally produces sim ilarly coloured leaf bases.The orange-red coloration of the pedicels in this species during anthesis is a unique char acter in the genus Clivia.

Distribution and habitat
Apparently confined to the Oorlogskloof Nature Reserve in Northern Cape (Figure 2), Clivia mirabilis is restricted to a small area on the eastern margin of the Oorlogskloof Canyon.Populations are known to occur just north of Eland se Kliphuis adjacent to Agterstevlei Farm and a little further south around the Driefontein Waterfall.The distance between these sites is ± 5 km.The species also occurs at a few sites between these two localities.
The margins of the Oorlogskloof Canyon are capped with 30 m cliffs of Peninsula Formation Sandstone.This has eroded to form coarse sandstone talus screes below the cliffs that are partly covered in a light woodland of relictual Afromontane evergreen forest elements, princi pally Olea europaea subsp.africana, Maytenus acum i nata, M. oleoides, Cassine schinoides, Halleria lucida and Podocarpus elongatus with additional shade provid ed by outsize.(4 m tall) specimens of Phylica oleaefolia.Small groups of C. mirabilis grow rooted in humus between cracks in the sandstone talus of the rock scree, either as solitary individuals or in small groups.Occasionally some clumps occur in full sun but these tend to have shorter leaves and often show signs of water stress (dried leaf tips).However, the remaining leaves show no signs of sunburn, despite the intense insolation experienced for several months each year.The main pop ulation extends over several hectares and probably con sists of well over 1 000 individuals.Due to the position of these two sites under the eastern cliffs of Oorlogskloof Canyon, most plants experience shade until about midmorning after which they are in direct sun.
The area is characterized by a semi-arid Mediter ranean climate with a strictly winter rainfall regimeexactly the opposite climatic conditions experienced by the other four species in this genus.The mean annual rainfall for Oorlogskloof is 414 mm, falling mainly between May and September.Vegetative growth is thus restricted to a brief winter growing period.Situated at 850-900 m, some 100 km inland from the coast, these populations are subject to brief but light frost in winter.

Root system
On excavating several plants in the habitat for culti vation at Kirstenbosch.the enormous root system char acteristic of this species was revealed.Large adult plants have a mass of fleshy, succulent roots radiating between V2-V 4 m from the base of the rhizome, each root ± 20 mm in diameter.This disproportionally large volume of sub terranean biomass gives mature plants an extensive water storage capacity, allowing them to survive the prolonged rainless summers of the Oorlogskloof environment.

Flower colour, development and pollination
The general impression o f a fully open scape is of bicoloured perianths, orange-red at the base, yellow towards the mouth and with orange-red pedicels.During the development of the flower, both perianth and ovary progress through a series of well-marked colour changes.The unopened bud is yellowish, but prominently greentipped, and the ovary is also pale green.At anthesis the green coloration slowly disappears from the tips of the tepals which take on the same yellow tones as the basal half of the perianth.The pedicels and upper half of the perianth are deep orange-red at this stage.After pollina tion the yellow coloration disappears and the whole peri anth and ovary take on a uniform orange/red colour.As the perianth begins to wither, the ovary swells and under goes an abrupt colour change from orange to bright green, as do the pedicels.No other Clivia has pedicels the same colour as the perianth when the flower is fully open.The pedicels abruptly change to green as the peri anth abscisses and the ovary swells in the post-pollina tion phase.
The purpose of these colour changes is not yet under stood, but is probably related to pollinator cues.Pollination appears to be by sunbirds.A single sighting of a malachite sunbird probing the perianths was made at Oorlogskloof on 18 October 2001 suggesting that sun birds could be involved in pollen transfer.However, like the other three tubular-flowered species, C. mirabilis may also be a selfer as between 80 and 90% of the flow ers in each umbel are pollinated and produce viable berries.Flowering tim e: ± six weeks, from October to mid-November.

Fruiting
The berries mature more rapidly than in the other Clivia species.By the end of February, four months after flowering, the fully developed berries turn from yellow and orange to pinkish and later red by the end of March and are shed shortly thereafter prior to the onset of the first winter rains in April/May.This rapid autumn matu ration of berries is in sharp contrast to the summer rain fall area clivias which mature slowly, usually 12 months for C. miniata and C. gardenii, about nine months for C. caulescens and C. nobilis (Duncan 1999) to coincide with the commencement of October/November summer rains.

Seed dispersal and germination
Berries commence falling from late February to early April.Germination appears to be rapid in response to the onset of autumn/early winter rains.At Kirstenbosch seeds sowed on 18 March 2001 had already developed a 10 mm radicle by 10 April 2001.
On germinating, the primary root develops into a swollen, white, succulent cylinder up to 50 x 5 -6 mm.During the moist winter months (M ay-September), it swells, accumulating water in its succulent tissue.By October, two short (5-10 mm long) leaves have been produced, whereafter further vegetative growth of the seedling slows or largely ceases with the onset of sum mer dormancy (Novem ber-April).During the rainless phase of ± six months the seedling survives on water reserves stored in the greatly enlarged primary root.Vegetative growth commences again in autumn.Thus the biology of a C. mirabilis seedling in its first year is much akin to a winter rainfall area geophyte with the swollen primary root being functionally equivalent to a corm or bulb.
The phenology of the germinating seed described above is clearly an adaptation to a semi-arid Mediter ranean climatic regime-exactly the reverse of the sum mer rainfall region Clivia species.
Within a few months of germinating, the plumular bud (cotyledon plus first true leaf) (Boyd 1932), becomes densely pigmented with anthocyanins (Plate IF).This prominent development of anthocyanins at the base of the leaves is later evident in the leaf sheaths of adult plants which are heavily suffused with purplecarmine pigments.Why the seedlings of C. mirabilis are so densely pigmented with anthocyanins is not clear, but it may be a response to the intense levels of sunlight experienced in the natural habitat, thereby providing effective screening during the seedlings' critical estab lishment phase.

Relationships
The distribution ranges of all four previously known Clivia species are contiguous or overlap, while at many localities different pairs of species occur sympatrically, C. nobilis with C. miniata, C. gardenii with C. miniata, and C. caulescens with C. miniata.Geographically, pop ulations of C. nobilis in Eastern Cape, though more than 800 km distant, are the closest spatially to C. mirabilis.C. nobilis also appears to be the closest relative to C. mirabilis on morphological grounds: tough stiffly erect coriaceous leaves with a median pale striation on the upper surface (some populations of C. nobilis occa sionally have a faint median striation), and the small seeds.

Phytogeographic implications
Palynological evidence indicates that in Western Cape and southern Namaqualand, subtropical forests were pre sent during Miocene and Pliocene times (± 5.3 million years BP) (Scott et al. 1997).Since then, apart from more recent cyclical changes in the Quaternary, there has been a progressive eastward retreat of these forest elements.Assuming that the genus Clivia has not changed its dependence on a forest environment significantly since pre-Q uatem ary tim es, it can be argued that the Nieuwoudtville species is relictual and that its survival in the Oorlogskloof Canyon is partly fortuitous and partly due to its adaptation to a different climate.The berry maturation period, seedling and germination biology are so perfectly in harmony with an arid Mediterranean cli matic regime that Clivia mirabilis is able to survive envi ronmental conditions inimical to all other Clivia species.
It is currently believed that the late Miocene also saw the development of a Mediterranean climate in the west ern part of the Cape (Axelrod & Raven 1978).This would have interrupted the further spread of an essen tially summer rainfall genus like Clivia into the forests of the southern and western part of the Cape.It would also have left the precursors of Clivia mirabilis to adapt to increasing aridification and the onset of a pronounced Mediterranean type climate.Thus if C. mirabilis evolved from forms with an essentially summer rainfall phenolo gy, the adaptation to an arid Mediterranean type climate is a derived condition dating from late Miocene times.
Long distance dispersal should also be considered as a possible explanation for this bizarre distribution pat tern, but this seems highly unlikely as no living vectors for the long-distance dispersal of Clivia seed have yet been identified nor has biotic dispersal been recorded for any other species of Amaryllidaceae (Meerow & Snijman 1998).Birds are probably the main seed dispersal vec tors.Clivia miniata, C. gardenii and C. caulescens have all been observed by the author growing epiphytically in forest trees, five or more metres above ground level.It is probable that frugivorous birds deposited seeds in these positions, leading one to postulate that forest dwelling birds are responsible for the dispersal of large scarlet Clivia berries.While the dispersal of Clivia seed by birds between closely adjacent forest patches is a strong possi bility, dispersal over distances of 800 km of arid country seems highly unlikely.

Conservation status
No populations are known outside the Oorlogskloof Nature Reserve where the species currently enjoys max imum protection.Yet there is no reason why C. mirabilis should not occur further down the Oorlogskloof Canyon, outside the reserve, as numerous suitable habitats occur there.If this proves to be the case, special efforts will have to be made to protect these populations as the species' horticultural potential will render it vulnerable to exploitation.

FIGURE
FIGURE 1.-Clivia m irabilis: A, mature inflorescence; B, fruiting head with irregularly shaped berries; C, longitudi nal section through flower; note filament bases adpressed to style forming nectar reservoir; D, detail of filament bases.Scale bars: 10 mm.Artist: John Manning.

FIGURE 2 .
FIGURE 2.-Distribution o f C. m irabilis, • , in relation to the distrib ution o f the remainder o f the genus Clivia (black shaded area).