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Responses to Various Manipulations, and Storage Potential, of Seeds of the Unique Desert Gymnosperm, Welwitschia Mirabilis Hook

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Responses to Various Manipulations, and Storage Potential, of Seeds of the Unique Desert Gymnosperm, Welwitschia Mirabilis Hook South African Journal of Botany 2004, 70(4): 622–630 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY ISSN 0254–6299 Responses to various manipulations, and storage potential, of seeds of the unique desert gymnosperm, Welwitschia mirabilis Hook. fil. C Whitaker1, P Berjak1*, H Kolberg2 and NW Pammenter1 1 School of Biological and Conservation Sciences, University of KwaZulu-Natal, Howard College Campus, Durban 4041, South Africa 2 National Plant Genetic Resources Centre, National Botanical Research Institute, Private Bag 13184, Windhoek, Namibia * Corresponding author, e-mail: [email protected] Received 3 March 2004, accepted in revised form 26 May 2004 The tenacious, dry bracts constituting the coverings of Aspergillus niger var. phoenicis. Germination perform- seeds of the Namib desert gymnosperm, Welwitschia ance of the seeds was unaffected by their maintenance mirabilis, have been shown to impose a constraint on at 80°C for 48h, establishing both their highly orthodox germination rather than this being a case of physiologi- nature and possibility of ultra-dry storage, as well as a cal dormancy. Removal of these structures without any potential means of thermotherapy. Preliminary trials other treatment enabled rapid germination, whereas established that W. mirabilis seeds at the water content soaking the seeds either with the coverings intact or at which they are shed have the potential to be cryopre- removed, resulted in poor germination. After removal of served. Seeds from which the coverings had been the coverings, seed samples with a low proportion of removed not only survived immersion in liquid nitrogen, individuals infected by Penicillium crustosum respond- but also achieved undimished germination totality far ed well to treatment with a commercial fungicide more rapidly than did the equivalent, untreated sample. (Sporekill®), which eliminated the fungus, whereas sur- The present work has established the basis of guide- face-sterilisation with sodium hypochlorite was lines for the practical handling of W. mirabilis seeds and extremely damaging. This fungicide, however, was inef- hence conservation of this unique species. fective when the seed-associated fungus was Introduction The distribution of Welwitschia mirabilis Hook. fil. 1969). However, many characteristics of W. mirabilis are too (Welwitschiaceae), which is considered to be a taxonomical- specialised for this to have been the case, and the fact that ly-isolated gymnosperm endemic to the Kaokoveld Centre the plants are dioecious is one of the major factors eliminat- (Van Wyk and Smith 2001), extends from the Nicolau River ing them from the direct line of ancestry (Takhtajan 1969). in southern Angola to the Kuiseb River in Namibia (Kers The deep-rooted W. mirabilis plants retain their first- and 1967). This area is amongst the most arid world-wide, with only-formed leaves, the tissue of each being continually the coast recorded as having almost zero rainfall, while less regenerated from a deep-set meristem, throughout their than 100mm falls annually below the escarpment, mainly lifespan. There are only two of these leaves, although they from February to April, the late summer (Van Wyk and Smith become so longitudinally dissected by uneven growth of the 2001). While W. mirabilis is established in regions receiving truncated stem that the basal meristem becomes segment- less than 25mm rainfall, this is supplemented throughout the ed (Bornman et al. 1972), giving the plant the appearance of area by an equivalent of ~50mm provided by the coastal fog having many long, ribbon-like leaves, with micro- or mega- (Bornman et al. 1972). strobili appearing between the bases (Figures 1a, b). Welwitschia mirabilis is recorded as being ‘discovered’ by Individual simple microstrobili have six basally-fused Friedrich Welwitsch in 1859 — and the very plants he microsporangiophores, each bearing three fused sporangia described may still be extant, as some living specimens are (Bierhorst 1971) which have also been termed anthers, as estimated to be 1 500–2 000 years old (Bornman et al. they appear morphologically similar to these structures in 1972). Although a gymnosperm, W. mirabilis shows several angiosperm flowers. Each megastrobilis comprises 90–100 characters that are angiosperm-like, leading to the one-time megasporophylls, of which Bornman et al. (1972) found only opinion among botanists that the immediate ancestor of the 50–60% to be fertile. Ovules are bitegmented; the outer angiosperms had been discovered (reviewed by Takhtajan integument, formed from a pair of fused bracts, also gives South African Journal of Botany 2004, 70: 622–630 623 Figure 1: Individual Welwitschia mirabilis are shown established at considerable intervals from one another on the Welwitschia Flats in the Namib Naukluft Park, Namibia. (a) The plant in the foreground is a male, and the microstrobili are illustrated in the inset. (b) A female show- ing the crown of the plant and developing megastrobili. The longitudinally-dissected leaves can be seen in both specimens, and the refuge for animals provided by the downwardly deflected leaves in the otherwise hostile environment can be appreciated (a) 624 Whitaker, Berjak, Kolberg and Pammernter rise to the wings of the seed, while the inner originates as a ities. Seed-associated fungi could pose a serious problem in complete ring of tissue, extending apically as the micropylar terms of propagation of the species in its natural habitat, as tube in the mature ovule (Chamberlain 1966, Bierhorst well as via planting programmes, as quiescent inoculum is 1971). Seed development is recorded as being complete in likely to survive with the dry seeds, but will proliferate when less than four months (Chamberlain 1966). While the seeds water is provided. This could either preclude seed germina- may be wind-blown along the surface of the sand (Bornman tion or, if germination does occur, overcome the developing 1978), they are considered to be too heavy to become air- seedlings (Kolberg, pers. obs.). Thus survival of this unique borne, but during episodic heavy rains (Pearson 1906) the species could become jeopardised by lack of seedling wings may function for buoyancy in run-off water, thus facil- recruitment in the field, as well as by the inability to provide itating seed dispersal. The dry seed (c. 7 x 5 x 2–3mm; aver- vigorous young plants for regeneration programmes. age mass 120mg) contains a centrally located embryo, often Aside from its intrinsic value as an endemic species, W. separated by a narrow space from the surrounding gameto- mirabilis plants provide refuge, shade, food and water (from phyte tissue (Figure 3) as previously described (Butler et al. intercepted fog) for a variety of desert animals. As an exam- 1973, Bornman et al. 1979). The seeds contain ~35% oil ple, large numbers of the heteropteran, Probergrothius sex- (Bornman 1978), making them attractive as food for various punctatis, can be found associated with most female W. desert animals. mirabilis plants, where they feed on the sap (Lovegrove When separated from the megasporophyll, each seed is 1999). High frequencies of A. niger spores associated with enveloped by tenacious dry bracts, thus constituting a ‘seed the megastrobili, have been associated with the presence of unit’. Although the term, ‘perianth’ has been used to describe these insects (Cooper-Driver et al. 2000), which exhibit a the structures enclosing the W. mirabilis seed (Pearson preference for female over male cones (Bornman et al. 1906, Bornman et al. 1972), these are termed seed cover- 1972). The spatial distribution of plants with which fungal ings in the present work. From earlier investigations, it has spores are associated, supports the hypothesis that the vec- been proposed that some component of the seed unit con- tor is a non-flying insect — such as P. sexpunctatis (Cooper- tains an inhibitor, which has to be leached before germina- Driver et al. 2000). tion proceeds (Bornman et al. 1972). This led to the propos- The present investigation details responses of W. mirabilis al by those authors that seeds would germinate naturally seeds to various pre-germination treatments; reports on fun- only if there had been sufficient rainfall to leach out the puta- gal status of, and some preliminary trials to eliminate fungi tive inhibitor and facilitate its diffusion away from the devel- from, the seeds; comments on desiccation tolerance and oping root. hence seed categorisation; and considers the potential of Bornman et al. (1972) record that under laboratory condi- cryostorage as a means to conserve high-quality planting tions germination will occur within 48h after seeds have material. been supplied with the equivalent of 25mm rain, and that root growth is extremely rapid — up to 1.5mm per hour. The Materials and Methods shoot apex with its paired cotyledons appears to be with- drawn from the seed as the hypocotyl elongates (Bierhorst The seeds of W. mirabilis for most of the present investiga- 1971). The attenuated cotyledons, which are photosynthet- tions (accessions HK 1249 and HK 1250) were collected by ic, persist for a matter of two to three years (Chamberlain Kolberg et al (H Kolberg, S Loots, R Moses: NPGRC, 1966), even when the two later-developing true leaves have National Botanical Research Institute, Private Bag 13184, become considerably longer than they are (Bornman et al. Windhoek, Namibia) in May 2002 in the vicinity of the 1972). According to Chamberlain (1966), a continuous plate Messum River (21°20’48”S, 14°09’12”E, altitude 400m asl) that covers and arrests development of the stem apex, is and on the western side of the Messum Crater (21°24’18”S, formed from two laterally-expanded buds, each arising in the 14°08’27”E, altitude 340m asl). In particular experiments (as axil of one of the cotyledons. indicated), seeds used were from accession HK 1322, col- Although there are many mature W. mirabilis plants, the lected by Kolberg and Tholkes (H Kolberg, T Tholkes: long-recorded scarcity of young plants (Pearson 1906) has NPGRC, National Botanical Research Institute, Private Bag now become a matter of concern (Cooper-Driver et al.
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