A taxonomic review of the dry-fruited species of Anemone (Ranunculaceae) in southern Africa

The three dry-fruited species of Anemone sect. Pulsatilloides subsect. Alchemillifoliae (Ranunculaceae) from southern Africa are reviewed, with full descriptions and nomenclature, including complete synonomy, taxonomic history with nomenclatural corrections, ecological notes, and distribution. A. tenuifolia (L.f.) DC. from the Cape Floristic Region is segregated as ser. Pinnatifoliae from the two summer rainfall species, A. caffra (Eckl. & Zeyh.) Harv. and A. fanninnii Harv. ex Masters, which remain in ser. Alchemillifoliae , emphasising the strong vegetative differences between the two series.


INTRODUCTION
Generic relationships of tribe Anemoneae DC. (Ranunculaceae-Ranunculoideae) have been the subject of intensive morphological and molecular investigations (Hoot et al. 1994;Ehrendorfer & Samuel 2001;Schuettpelz et al. 2002;Hoot et al. 2012), resulting in the recent expansion of the circumscription of Anemone L. to include the small segregates Barneoudia C.Gay (3 spp.), Hepatica Miller (7 spp.), Knowltonia Salisb. (8 spp.), Oreithales Schldl. (1 sp.) and Pulsatilla Miller (± 38 spp.) (Tamura 1993). Second largest genus of tribe Anemoneae after Clematis L., Anemone s. l. is diagnosed by the presence of one or more leafy, cauline involucres beneath the fl ower, and a perianth comprised of imbricate, petaloid sepals only. It includes ± 200 species distributed throughout the world, primarily in the Northern Hemisphere with only a modest representation on the southern continents, where ± 30 species are recorded mainly from montane regions with a temperate climate . The austral representatives are concentrated in South America (12 spp.) and southern Africa (11 spp.), with A. thomsonii Oliver endemic to east tropical Africa and a handful of additional species in Indonesia and Australasia (Hoot et al. 2012).
Anemone in southern Africa traditionally included just three species with dry fruits, but has since been enlarged to 11 spp. by the recent transfer of the eight fl eshy-fruited species of Knowltonia (Manning et al. 2009). Although previously treated in Anemone by some authors, this close-knit group of species was generally retained as a distinct genus on the basis of its compound infl orescences of relatively small fl owers and its baccate or berry-like fruits. Phylogenetic analysis of plastid and nuclear DNA sequence data has now confi rmed its intimate relationship to the southern African Anemone species with dry fruits, with which it shares apomorphic pantoporate pollen, and all of the southern African species are now associated as subsect. Alchemillifoliae (Ulbrich) Hoot of A. sect. Pulsatilloides DC. (Hoot et al. 2012). The fl eshy-fruited species, which constitute ser. Knowltonia (Salisb.) J.C.Manning & Goldblatt within subsect. Alchemillifoliae, have been well monographed by Rasmussen (1979) [as the genus Knowltonia]. This is not the case with the dry-fruited southern African species, which, as yet, have been treated only incompletely or superfi cially (De Candolle 1824;Pritzel 1841;Harvey 1860;Ulbrich 1906), most recently as part of a wideranging review of all austral species of Anemone . Although very valuable, this latter treatment is nomenclaturally incomplete and also perpetuates some errors, notably the incorrect name and authors for A. tenuifolia (L.f.) DC., as well as containing some mistakes in typifi cation. We provide a complete review of the taxonomy and nomenclature of the dry-fruited species of Anemone from southern Africa, including full synonomy, taxonomic history, ecological notes and distribution.
Taxonomic relationships among the dry-fruited southern African species of Anemone were fi rst formalised by Ulbrich (1906), who segregated A. tenuifolia [as A. capensis] in the monotypic ser. Pinnatifoliae; retaining A. caffra and A. fanninii, the two rosulate species with unlignifi ed caudices and palmate leaves, in ser. Alchemillifoliae. This treatment, with an emphasis on morphology, was followed by subsequent authors until recently when Hoot et al. (2012) weighted phylogenetic considerations by including all three species in an expanded ser. Alchemillifoliae within subsect. Alchemillifoliae, arguing that the two leaf morphs of A. tenuifolia differed more from one another in DNA base sequences than did A. caffra from A. fanninii. There is no compelling morphological basis for this treatment, since A. tenuifolia is intermediate between ser. Knowltonia and ser. Alchemillifoliae in having the compound foliage of the former but the sericeous, fusiform achenes of the latter. The molecular topology retrieves ser. Knowltonia as sister to a clade in which A. tenuifolia is in turn sister to A. caffra + A. fanninii and is thus consistent with either classifi cation. Signifi cantly, however, the cladistic Bothalia 43,1: 1-13 (2013) branches subtending A. caffra / A. fanninii, the two leaf morphs of A. tenuifolia, and the members of ser. Knowltonia in the molecular phylogram presented by Hoot et al. (2012) are all of similar length, indicating comparable levels of sequence divergence of the three lineages from their last common ancestor. This observation, coupled with the clear morphological and ecological differences among the lineages, prompts us to revert to the segregation of the dry-fruited species in two series, with the fl eshy-fruited species comprising a third series. This classifi cation, which incorporates both phenetic and phylogenetic information, seems more appropriate to us than the alternative that stresses the slightly closer phylogenetic relationship between the dry-fruited species over their obvious morphological diversity. We do not consider ser. Knowltonia further here, and readers are referred to the taxonomic revision by Rasmussen (1979) and the revised generic placement by Manning et al. (2009) for further details.

MATERIALS AND METHODS
All relevant types were examined, as well as all specimens from BOL, MO, NBG, PRE and SAM (acronyms after Holmgren et al. 1990), the herbaria housing the most comprehensive collections of southern African species. All species were also studied in the fi eld. TAXONOMY Anemone L., Species plantarum: 538 (1753). Type: A. coronaria L.
There is no specimen under the name Atragene tenuis in Thunberg's herbarium nor is the species included in his Flora capensis (Thunberg 1823), but the name was treated as a synonym of At. tenuifolia L.f. by both Poiret (Lamarck 1812) andDe Candolle (1818), and the concordance between the description of At. tenuis and that of At. tenuifolia in Thunberg's Flora capensis is consistent with this interpretation. There is no reason to doubt that the two names apply to the same taxon and it is likely that both were in fact based on the same Thunberg collection. We therefore designate the specimen in the Thunberg herbarium as a neotype to fi x this application. Although the specimen itself is not precisely localised, the collecting locality is cited as the Groot Winterhoek Mtns behind Tulbagh by Thunberg (1823)
Distribution and ecology: Anemone tenuifolia is largely restricted to the coastal slopes of the Cape Fold mountains, from the Bokkeveld Escarpment south to the Cape Peninsula and thence east to the Baviaankloof Mtns, extending inland along the southern coast onto the Kammanassie Mtns and the upper southern reaches of the Swartberg (Figure 2). It favours cooler, moister situations on south-facing slopes, typically in sheltered gulleys or in the lee of rocks, generally at moderate to high altitudes, 500-1 200 m but well above 1 500 m on the Swartberg and down to 300 m along the coast. Plants grow in moist, loamy soils, mostly on sandstone but also on granite, shale and limestone. Flowering has been recorded from autumn though summer but takes place mainly in winter and spring, and is strongly stimulated by a summer fi re.
Diagnosis and relationships: the only dry-fruited winter-rainfall species of Anemone in South Africa, A. tenuifolia is a sclerophyllous, semi-shrub, with a distinctive, ± caulescent habit and glabrescent, bi-to triternate leaves. The infl orescence is invariably 1-fl owered and usually simple but occasionally compound, with one or two secondary, 1-fl owered infl orescences developing within the primary involucre, each with a secondary involucre.
The species is highly variable in the degree of dissection of the leaves, which vary from biternate with cuneate, toothed or pinnatifi d leafl ets to triternate with pinnate leafl ets divided into needle-like segments. The two extremes were, understandably enough, treated for some time as distinct species under the names Atragene/ Anemone tenuifolia and At./A. capensis respectively, but with further collecting it is now clear that they represent part of the variation within a single species. The more highly dissected foliage morph is the most common and is found throughout the range of the species whereas forms with less-divided, biternate leaves are largely restricted to the extreme southwest, occurring on Table  Mountain and adjacent mountain ranges, from Franschhoek to the Kogelberg. We have seen only one early collection of the less dissected leaf morph from outside of the southwestern Cape, from near Uitenhage (Ecklon & Zeyher 679).
A full range of leaf dissection can be found within a single population in the southwest, sometimes even within a single plant, with juvenile leaves tending to be less deeply dissected than those produced later (e.g. Manning 3361). This variation in leaf dissection among or even within individuals was fi rst noted by Harvey (1860) on Table Mountain.
History: the fi rst of the African anemones known to science, Anemone tenuifolia has a long history that has been vexed by nomenclatural confusion until today. Its fi rst modern entry, in the Species plantarum under the name Atragene capensis (Linnaeus 1753), derives from a description and engraving ['Pulsatilla foliis trifi dis, dentatis, fl ore incarnato, pleno'] published in Johannes Burman's Rariorum africanarum plantarum (Burman 1738). The name was lectotypifi ed against the Burman engraving by Oliver (1969) (Wilson et al. 2002), is perplexing as we fi nd no reference to the species there. Paul Hermann (1646-1695), professor of Botany at Leiden, sailed for India in 1682 and called in at the Cape en route, where he made the fi rst known herbarium collection of the local fl ora. A. tenuifolia is thus among the earliest elements of the Cape fl ora to become known to science. Lamarck (1783) was the fi rst to treat the species in the genus Anemone, under the name A. capensis, with an amplifi ed description based on a specimen in De Jussieu's herbarium (now in P). Although it is possible that Lamarck merely intended transferring Linnaeus's name to Anemone, he refers in the protologue only to Hermann's polynomial and his name must therefore be treated as the new species A. capensis Lam., as was done by Pritzel (1841), with the De Jussieu specimen as the type (Oliver 1969). Ziman et al. ( 2006) Killick (1977), although again with the incorrect reference to De Candolle (1824).
Distribution and ecology: Anemone caffra is distributed throughout the mountains of the Eastern Cape from Grahamstown to Kokstad and inland on the Winterberg into southern Lesotho, with scattered collections further north along the foothills of the KwaZulu-Natal Drakensberg as far as Nkandla (Figure 4). Plants favour cooler, grassy or scrubby slopes, sometimes along watercourses, from 300-2 000 m but mostly below 1 500 m. Flowering is stimulated by burning of the veld the preceding winter.
The fl owers are mostly moderately sized, with tepals 20-40 × 3-8 mm, but plants from Nsikeni Mtn near Kokstad (Abbott 7051) are especially handsome, with unusually large, white to pale pink fl owers, the tepals 50-55 × 10-18 mm. The species is also variable in fl ower colour. Usually white or sometimes pale pink, or the outer tepals fl ushed pink beneath, individuals with bright cyclamen pink fl owers, sometimes with a white centre, occur in some populations. These striking colour morphs are relativelty rare but have been recorded in the Eastern Cape from the Amatola Mtns and between eNgcobo and Kokstad, and in KwaZulu-Natal from Nkandla.

Diagnosis and relationships: distinguished from
Anemone fanninii by its smaller stature, with smaller, mostly sparsely hairy leaves, the blades (40-)60-100(-180) mm diam. and lobed less than halfway, thinly pubescent above and glabrescent or thinly pubescent (rarely densely villous) beneath, mainly along the nerves, and mostly solitary-fl owered scapes up to 200 mm long. The sepals are ± monomorphic, the outer typically only thinly sericeous beneath. A. fanninii is a much more robust species with larger, densely velvety leaves 150-350 mm diam., and mostly 2 or 3-fl owered infl orescences on stout scapes 200-800 mm long. The sepals are always distinctly dimorphic with the outer series broader than the inner and ± densely sericeous or villous beneath.
Specimens of A. caffra from the Eastern Cape Drakensberg and southern Lesotho (viz. Nienaber 1014, Schmitz 8848, Strever 1234, Victor 1591 have the younger leaves (especially the lower surface) more densely pubescent than usual and have been confused with A. fanninii, especially individuals with two fl owers per stem, but are readily distinguished from that species by their much smaller, shallowly lobed leaves with relatively fewer (<10), proportionally larger primary teeth along each side of the lobes, and their generally shorter stature. The mature leaves in these populations are also not nearly as densely villous beneath as A. fanninii. We have not noticed any differences between the two species in the fi laments (purportedly strongly expanded basally in A. caffra) nor carpel vestiture (basal hairs not distinctly shorter in A. fanninii) reported by Ziman et al. (2006).
The two species are essentially parapatric, with A. caffra distributed mainly south and east of A. fanninii, often at lower altitudes, but both occur around Polela, Qachas Nek and Mt Ayliffe, although they have never been recorded growing together.
History:Anemone caffra is one of many botanical novelties introduced to science by Christian Frederick Ecklon (1795Ecklon ( -1868 and Carl Ludwig Zeyher (1799-1858). Arriving independently but almost simultaneously in Cape Town, the two Germans turned to plant collecting as a profession, both separately and together. In October 1831 they undertook a joint expedition to the present Eastern Cape, reaching as far as Queenstown, on which they encountered Anemone caffra. On their return to Cape Town the following year, Ecklon left for Germany and the Hamburg Botanic Garden to set about sorting their vast collection of material and the preparation of a joint publication on it, the Enumeratio plantarum Africae australis extratropicae. It is here that Anemone caffra was formally described in the genus Pulsatilla. The species was collected more-or-less simultaneously by another German, Johann Franz Drège (1794-1881), a trained horticulturist and active plant collector who had arrived in Cape Town in 1826. Drège undertook an extensive expedition into the Eastern Cape at the end of 1831 in the company of his apothecary brother Carl, fi nally returning to Cape Town in January 1836 (Glen & Germishuizen 2010). The two brothers collected the species on the Katberg in November 1832, and it was subsequently collected by many of the botanically inclined travellers to the eastern districts of the erstwhile Cape Colony during the latter half of the nineteenth century.
Drège listed the species as Anemone alchemillifolia in his Zwei pfl anzengeographische Documente (Drège 1843). This was evidently a manuscript name given it by the Prussian Botanist Ernst Meyer, who wrote an introduction to the work. The species was subsquently published under Meyer's preferred but nomenclaturally illegitimate name by Pritzel (1841), who referred to both initial collections made by Ecklon & Zeyher and by Drège.
Minor variants among later collections from new localities in the Eastern Cape were seized upon as taxonomically signifi cant entities by the Frankfurt botanist Ernst Huth (1896), who recognised var. schlecteriana for plants with smaller tepals (± 20 mm long) collected in January 1896 on Mt Ntsizwa near Kokstad by the botanist Rudolf Schlechter , and var. grandifl ora for a collection with larger tepals (± 35 mm long) and laciniate involucral bracts made near Baziya, west of Umtata, by the missionary Leopold Richard Baur (1825-1889) sometime after 1873. It was during this year that Baur was visited at his mission station in Baziya by the Port Elizabeth businessman and amateur botanist, Russell Hallack (1824-1903, who enouraged him to botanise the area and to send his collections to Peter MacOwan (1830MacOwan ( -1909, principal of Shaw College in Grahamstown and expert on the regional fl ora. Another form with less deeply lobed leaves was described as var. pondoensis by the Berlin botanist Eberhard Ulrich from two unlocalised and undated collections from Pondoland (Eastern Cape) made respectively by the medical practictioner and naturalist Franz Bachmann (1856 to ±1916) and one C. Beyrich, about whom nothing is known. Bachman spent only a year in Pondoland, over the period November 1887-November 1888, and would have collected the species during this time.
Distribution and ecology: Anemone fanninii is largely restricted to the eastern foothills and scarp of the central and northern Drakensberg in KwaZulu-Natal as far north as Witzieshoek in northeastern Free State; but is also recorded further south from Qachasnek in the southern Drakensberg and from Mt Ayliffe south of Kokstad in Eastern Cape ( Figure 6). The species favours cooler, south-facing, grassy slopes, often along water courses or in seasonal seepages, from 600-3 000 m. Flowering is largely dependent on burning of the veld the preceding winter.
Diagnosis and relationships: closely allied to Anemone caffra but altogether more robust, with larger, thickly pubescent leaves, the blades 150-350 mm diam., velutinous above and densely villous or felted beneath, and mostly 2 or 3-fl owered infl orescences on stout scapes (200-)300-800 mm long. The whitish sepals, sometimes fl ushed maroon on the reverse, are always ± distinctly dimorphic with the outer series broader than the inner and densely sericeous or villous beneath. A. caffra is a smaller species with mostly thinly hairy leaves (rarely densely villous beneath, especially when young), 40-130 (-180) mm diam., and 1(2)-fl owered scapes up to 200 mm long, typically with ± monomor-phic sepals, the outer mostly similar in size and shape to the inner and only thinly, or at most moderately, densely sericeous beneath. The fl owers in both species vary signifi cantly in size. We are not able to corroborate any differences between the two species in the fi laments (purportedly strongly expanded basally in A. caffra) and in the carpel vestiture (basal hairs not markedly shorter than median in A. fanninii) reported by Ziman et al. (2006).
Anemone fanniniii was deservedly described by Masters (1886) as a 'magnifi cent perennial' but despite his urgings it has not entered into general cultivation. Killick (1965) too recognised its promise as a garden subject but sadly observed that it had proven very diffi cult to cultivate away from its natural habitat. His hopes that horticulturists might soon discover its cultural requirements have so far remained unfulfi lled.
History: the largest of the African anemones, A. fanninii commemorates local farmer George Fannin (1832-1865), who collected it in September 1863, shortly before his death, at his farm The Dargle in the KwaZulu-Natal midlands. Renditions of the name in the feminine form 'fanniniae'are thus incorrect. Fannin took a great interest in the plants around his farm, sending many interesting specimens to botanist and fellow Dubliner, William Harvey (1811-1866 at Trinity College, who reciprocated by naming several of the novelties after Fannin. Duplicates of Fannin's herbarium specimens are housed at Kew, the KwaZulu-Natal Herbarium, and at Trinity College. Unfortunately, Harvey's publication of the name Anemone fanninii in the second edition of his Genera of South African Plants (Harvey 1868) lacks a description and the name was only formalised by the publication of the description of a later collection (Masters 1886). This collection, from Polela in the Drakensberg foothills, stems from material gathered in December 1885 by the English horticulturist Richard Adlam (1853Adlam ( -1903, then resident in Pietermaritzburg. Seed that Adlam sent to England was fl owered and the cultivated plant was described and illustrated in The Gardener's Chronicle Vol. 25 (Masters 1886). Maxwell Masters (1833-1907, editor of the magazine, provided the formal description and arranged for the fi ne engraving and is thus credited with the publication of the species. Masters sensibly lodged the fl owers and leaves of the Adlam material in the Kew herbarium, and they comprise the type of the name, not Fannin's collection as indicated by Ziman et al. (2006), who erroneously attribute the species to Harvey.
Adlam, a fl uent writer, contributed a popular article in the same issue of the Gardeners' Chronicle (Adlam 1886), vividly describing his rediscovery of the species. 'Next morning I started alone across country in search of a much talked-of plant', he writes, making it clear that his encounter was not a fortuitous one-news of this handsome anemone had clearly percolated among British horticulturists. 'The morning mists [after a heavy storm the previous night] still fl oat and sweep along the higher ground, alternately hiding and disclosing the cattle feeding on a thousand hills. My path led along a hill side, where Anemone Fanninii [sic] grew very strongly, fl ower stems 5 feet high, leaves 2 feet in diameter and fl owers 2 inches across. Twenty years ago Harvey noted it as a noble plant, yet I am not aware of its being in cultivation at home'. This was not quite true, for John Medley Wood (1827-1915, Curator of the Botanic Gardens in Durban, had sent living material of the species that he collected on the farm Ismont in 1883 to Kew. Received in June 1885, it was cultivated in a cool pit and fl owered two years later, in April 1887, when it was beautifully illustrated in colour by the Kew artist Walter Hood Fitch (Hooker 1887).
Another, undated herbarium collection with smaller fl owers collected by Adlam from the hills near Pietermaritzburg (possibly even from Fannin's original locality near The Dargle) and preserved in the South African Museum Herbarium (SAM), was described as var. parvifl ora by the Berlin botanist Eberhard Ulbrich (1906). A second variety, var. mafubuensis Beauv. (1914) is based on several beautifully pressed specimens collected at Mafube near Matatiele in the southern Drakensberg by Hélène Jacottet, sister of Dr Lautrè and the Rev. Edouard Jacottet. The unusually short fl owering stems of these plants that attracted the attention of Gustave Beauverd (1867Beauverd ( -1942, curator of the Boissier herbarium in Geneva, were artifi cially abbreviated by Mlle Jacottet in her pursuit of neatness and do not, as Beauverd thought, represent a naturally short genotype at all! Ethnobotany: the roots are used in traditional Zulu medicine, probably in the same way as A. caffra (Hutchings 1996). The sap is recorded as acrid-like many members of the family the species presumably contains the bitter glycoside ranunculin, which is enzymatically converted when the fresh plant is bruised to protoanemonin, a toxic oil with an acrid taste that causes blistering of human skin.