Journal of the Cycad Society of South Africa EENCEPHALARTOSNCEPHALARTOS Tydskrif van die Broodboom Vereniging van Suid-Afrika

No. 115 March 2014 ISSN 1012-9987

www.cycadsociety.org PRELIMINARY RESULTS ON THE CLASSIFICATION OF THE ENCEPHALARTOS NATALENSIS COMPLEX 1* 2 1 Philip Rousseau , Piet Vorster & Braam van Wyk

INTRODUCTION

Most Encephalartos species are characterised by very localised distributions often to the extreme of a sin- gle colony (e.g. E. dyerianus). However there are some species that have larger distribution ranges e.g. E. sep- tentrionalis, E. hildebrandtii, E. manikensis, E. ferox, E. laevifolius and E. natalensis (Goode 2001). Character- istic of these widely distributed species is the amount of morphological variation attributed to them (e.g. see Capela 2006). This is sharply in contrast with the split- ting that is characteristic of the taxonomy in most of the genus and indicative of the incomplete taxonomic work on these “species complexes”. In part this is also due to a lack of infraspecific ranks (i.e. ranks below species level e.g. subspecies, variety or form) employed in the classification of the genus (Vorster 2004). Thus though the variation is informally known, perhaps most famous- ly in E. natalensis, it has not formally been investigated to determine its taxonomic ranking. As part of a grant by Figure 1.—Maps as constructed by John Kloppers. the Cycad Society of South Africa a two part project has been launched to investigate E. natalensis populations in terms of (1) pollination and scent chemistry (By Dr. Ter- rence Suinyuy, UKZN) and (2) morphological variation, population genetics/phylogeny and classification. This article will focus on the preliminary results of the latter investigations.

As mentioned previously much of the diversity cur- rently classified under E. natalensis is known from col- lections, often with locality names attributed to them, e.g. Hilton E. natalensis. The species as first described by Robert Allen Dyer & Inez Verdoorn in 1951 was known from only three localities: the type at “the valley of a thousand hills”; below Howick falls; and Krantzkop. The description thus encompasses very little of the cur- rently known diversity (as it was done from three indi- viduals and a dried male cone) as is usual in botany once Figure 2.— Type locality leaf top detail. Photo: Steele & Human IN imperfectly known species are studied further (perhaps Nel 2006. as a side note it is important to remember that describ- ing a species is easy while circumscribing a species of- ten takes a lot more work). By 1965 Dyer had expanded our knowledge to include the full distribution range of the species, however little mention was made on the vegetative diversity found at these new localities. It was Cynthia Giddy (Giddy 1980) whom with significant field work first made mention (though without illustrations) of the diversity, concluding under: “Geographic forms: Several geographical differences exists within the con- cept of Encephalartos natalensis... e.g. the broad leaved form from the Kranskop area, and the woolly crowned form from Vryheid. The cones however do not show any

1 H.G.W.J. Schweickerdt Herbarium, Department of Plant 2Science, University of Pretoria. Department of Botany & Zoology, University of Stellen- bosch. Figure 3.—Type locality leaf bottom detail. Photo: Steele & Human *Contact: [email protected] IN Nel 2006. ARTICLES 28 Encephalartos March 2014 No. 115 Figure 4.—Common habitat of E. natalensis. marked differences and the separation of these ecotypes OVERALL IMPRESSION as varietal forms or even species, does not appear to be justified”. The next significant contributions are those of As the research is incomplete at this stage, the dis- Douglas Goode (1998, 2001, Cooper & Goode 2004) cussion of specific populations will be conducted on the who illustrated some of the different leaf forms from basis of overall impression gathered from a few standout natural populations. The greatest published diversity is characters. This approach is commonly known as using recorded in Prof. Nat Grobbelaar’s (2002) work, though the Gestalt of an organism, a German word meaning the this is from cultivation. By far however, the most thor- general Shape/Form/Build/Character. In biology it can be oughly and systematic cataloguing the diversity found defined as a technique for identifying organisms without in the species are two unpublished works by Avis Nel being able to explain one’s ability to do so, i.e. simply and colleagues and John Kloppers. John Kloppers’ work by a combination of traits given a certain overall form. consists of a thorough synthesis of all other literature Some people are better with this than others, owning to and his own photographs from gardens, systematically various personal aptitudes, but this serves as an often presented per geographic locality. In this he recognises very natural way to not only distinguish taxa (the collec- 48 geographic “forms” many very closely distributed tive term for diversity at any taxonomic rank) but also to together but with seeming consistent vegetative iden- delimit natural ones. tities. This was then mapped (Figure 1) on a detailed map to the closest city of each “geographic form name” given to cultivated material. Avis Nel’s work is based on All the localities visited so far seem to support E. na- a cycad summit held in Durban in 2006 and consists talensis on similar habitat types: inland on mountainous of detailed photographs of the basal, middle and top forest edges with steep slopes often between boulders portions (both top and undersides) of 61 forms (Figures or on cliffs, or less commonly inside deep forest (Figure

2–3), though this includes some E. woodii and mutated 4). There is however a large variation in the elevations ARTIKELS individuals e.g. Ramshorn. Their final tally amounted to at which populations occur (confirmed by Donaldson 55, with herbarium vouchers housed at my home insti- 2010), so far classifiable into three ranges ~120, ~500 tution (PRU). These works are very important as they and 900–1100 meters above sea level. The growth are arranged the same way as the research is aimed habit and certain vegetative characteristics such as to be conducted, i.e. each populations is considered an cataphylls and crown indumentum (hairiness) (Figure 5) unordered entity and only after a fine scale range or cline are also consistent throughout its range. However there of variation has been investigated for the species as a seems to be an identity of consistent leaf characters in whole, will decisions be made on the ranks (if any) at some populations, though this is shared among many which this diversity should be recognised. of the nearby populations. Contrary to this the cones

No. 115 March 2014 Encephalartos 29 Figure 5.—Cataphylls and crown indumentum typical of all E. na- Figure 7.—Atypical flat male sporophyll shape from ‘Jolivet’. talensis.

Figure 8.—Atypical rounded male sporophylls from ‘Jolivet’ popula- Figure 6.—Typical beaked male cone from ‘Jolivet’. tion.

of both sexes display larger variation within populations TYPE DESCRIPTION (Figure 6–10) than between them, even onto the geo- graphical extremes of the species. This current situation Firstly let us start with the type description (Dyer & then seem to be indicative of an incomplete speciation Verdoorn 1951, amended by Dyer 1965 with Red List in- with less pressure on the vegetative identity to remain formation by Donaldson 2010) as this is where the same constant. Rather the vegetative identity seems adaptive E. natalensis is applied to: Stems suckering from the to specific micro-environments with the morphology ow- base, length 3–4m occasionally up to 6.5m (Figure 11) ing to the specific founding stock of the population. Be- and 30–40mm in diameter. Crown deciduously golden fore delving into the specifics a disclaimer on geographic woolly with the production of cones or new leaves (Fig- information is necessary. All “geographic” names given ure 5). Leaf bases 50mm long, 30–40mm wide. Leaves herein do not refer to actual geographic localities visited 1.3–3.2m long, 400mm broad, glossy dark green and (these will be kept confidential) but refers to the closest glabrous. Rachis straight sometimes slightly curving to- “geographic form” as given in the Kloppers Map. wards the tip, hairy at first become smooth, clear peti- ARTICLES 30 Encephalartos March 2014 No. 115 Figure 9.—Brown haired female cone from ‘Jolivet’. Figure 11.—E. natalensis habit.

ole 100–160mm long. Leaflets (Figure 2–3) forming a broad V, broadly lanceolate curving towards the tip, with a rounded asymmetrical base, apical 100X15mm, medi- an 160–230X250–450mm, basally reduced to spines, pungent or with 1–5 sharp teeth on one or both margins. Cones 2–3 produced simultaneously, yellowish–green with grey, white/light red or brown hairs. Male cones 450mm long, 95mm in diameter (dry scales measured and not reported here), sporophylls beaked (Figure 6) central facet 80X70mm. Female cones ovoid, 500mm long, 250mm in diameter, central facet warty (Figure 10) elevated 50X40mm with lateral lobes 20mm long, Seeds red, 50mm long, 20mm in diameter. IUCN Red List status is Near Threatened unchanged from the 2003 assessment. This is due to the declined in certain parts of its range, with an overall population decline es- timated to be <30% over the past 60 years based on repeat photography and field work. The general popu- lation trend is decreasing with the species as a whole thought to be represented by between 8,300–12 000 mature individuals. Some subpopulations have been im- pacted by collecting and bark harvesting for medicinal

purposes. From personal observations natural regenera- ARTIKELS tion occurs in most populations even though populations are relatively small (less than 100 individuals).

POPULATIONS VISITED

Thus far nine populations of E. natalensis have been visited representing the northernmost (and beyond) up to the southernmost known distribution in the KwaZulu-Na- Figure 10.—Orange female cone from ‘Jolivet’. tal province. Characters that will be reported here to form

No. 115 March 2014 Encephalartos 31 Figure 12.—Ngoye forest.

Figure 13.—E. natalensis from ‘Emnyati Gluckstad’ showing persist- ent silvery hairs. Figure 14.—Overlapping nature of ‘Emnyati Gluckstad’.

an overall impression of populations include: Leaf length; 40X10–40mm, glossy bright green with persistent sil- petiole length; number of prickles; median leaflet dimen- very hairs, 2–4 teeth on both margins, pp 150°, pr 45– sions, teeth, texture, and arrangement. At two localities 75°, s 0°. Gestalt MEDIUM WIDTH, HEAVILY TOOTHED, E. natalensis were not found, those being “Ingwavuma” OVERLAPPING, PERSISTENT SILVERY HAIRY (Figure where species most resembling E. lebomboensis were 13–14). This compares well with Nel (2006). Unfortu- found, and Ngoye Forest. This is not surprising as in the nately no female individuals were reproducing and only first case, the northernmost known distribution of E. na- a single male plant (Figure 15) in cone could be found talensis is around Vryheid about 100 km south of “Ingwa- though natural recruitment does occur (Figure 16). vuma”, while in the second case Ngoye Forest does not seem to contain suitable habitat for E. natalensis (Figure Central 12), as there are no steep slopes or cliffs. Moving north to south then the following seven E. natalensis populations “Kloppers 25. Hilton”: Leaf length 1.6–2m, peti- will be divided as per the Kloppers map into Northern, ole clear 130–150mm, 2–4 prickles, median leaflets Central and Southern populations with each populations length/width/spacing 160X25–37X25–35mm, glossy given a specific gestalt in capital letters. [pp = pinna- dark green, 0–3 teeth, pp 135°, pr 45–75°, s 0°. Gestalt pinna angle, pr = pinna-rachis angle, s = swing angle]. MEDIUM WIDTH, FEW TEETH, SLIGHT OVERLAP (Fig- ure 17). This does not compare with “47. Hilton” as set Northern out by Nel (2006) as the leaf photographed therein (Fig- ure 18) is very narrow, consistently toothed and median “Kloppers 2. Emnyati/5. Gluckstad”: Leaf length leaflets slightly swung towards the leaf tip. Members of 1.2–2.5m, petiole clear 100–220mm, 3–5 prickles, both sexes were reproducing (Figure 19–20) with good median leaflets length/width/spacing 115–190X29– recruitment (Figure 21). ARTICLES 32 Encephalartos March 2014 No. 115 Figure 15.—Male cone from ‘Emnyati Gluckstad’. Figure 17.—Leaf from ‘Hilton’.

Figure 18.—Median leaflet detail from ‘Hilton’ Photo: Steele & Hu- Figure 16.—Seedling at ‘Emnyati Gluckstad’. man IN Nel 2006.

“Kloppers 28. Edendale”: Leaf length 1.5–2.3m, glossy dark green, 0–2 teeth, pp 90°, pr 75°, swing 0°. petiole clear 60–150mm, 3–5 prickles, median leaf- Gestalt NARROW, FEW TEETH, SLIGHT OVERLAP lets length/width/spacing 145–185X33–40X19–25mm, (Figure 26). This fits Nel (2006) well. This colony is glossy dark green, 2–3 teeth, pp 90°, pr 75°, s 0°. Ge- under serious threat from muthi collection with several ARTIKELS stalt BROAD, FEW TEETH, SLIGHT OVERLAP (Figure individuals already succumbing to overharvesting (Figure 22). Again this does not fit “23. Edendale” of Nel (2006) 27–29) and the populations very small (>50 individuals) who again presents (Figure 23) a leaf comparable to “Hilton”. Numerous individuals were seen reproducing with no natural regeneration witnessed. (Figure 24–25). Southern “Kloppers 31. Hopewell”: Leaf length1.5–1.8–2– 2.5m, petiole clear 60–130mm, 2–6 prickles, median “Kloppers 39. Jolivet”: Leaf length 1.8–2.5m, petiole leaflets length/width/spacing 175–200X32–36X24mm, clear 160–200mm, 2–4 prickles, median leaflets length/

No. 115 March 2014 Encephalartos 33 Figure 19.—Male cone from ‘Hilton’. Figure 21.—Numerous seedlings from ‘Hilton’.

Figure 22.—Leaf detail from ‘Edendal’.

width/spacing 150–215X28–50X30–42mm, glossy dark green, 3–5 teeth, pp 180–150°, pr 45–90°, s 30–90°. Gestalt NARROW, HEAVILY TOOTHED, LEAFLETS SWUNG FORWARD, SLIGHT OVERLAP (Figure 30–31). This fits “22. Highflats”, but not “19. High Flats” or “26. Jolivet Past Bizana” of Nel (2006) (Figure 32). Nume- rous individuals were reproducing (Figures 1–6) with good recruitment (Figure 33).

“Kloppers 42. Oribi Gorge”: Leaf length 1.6m, peti- ole clear ~100mm, 2–8 prickles, median leaflets length/ width/spacing 197–160X30–32X15–30mm, glossy bright–green, 0–2 teeth, pp 90–75°, pr 75–90°, s 0°. NARROW, TOOTHLESS, SLIGHT OVERLAP (Figure 34). Figure 20.—Female cone from ‘Hilton’. This fits Nel (2006) “38. Oribi Gorge” though leaflets ARTICLES 34 Encephalartos March 2014 No. 115 Figure 25.—Female cones from ‘Edendale’.

Figure 23.—Median leaflet detail from ‘Edendale’ Photo: Steele & Human IN Nel 2006. Figure 26.—Leaf detail from ‘Hopewell’. ARTIKELS

Figure 24.—Male cone from ‘Edendale’. Figure 27.—Mortality due to excessive bark harvesting.

No. 115 March 2014 Encephalartos 35 Figure 28.—Stem collaps due to medicinal harvesting.

Figure 31.—General form of ‘Jolivet’ individuals.

Figure 32.—Median leaflet detail for comparison with ‘Jolivet’ Photo: Steele & Human IN Nel 2006.

Figure 29.—Heavily harvested female individual with a separate stem already collapsed on the right.

Figure 33.—Poor dispersal but good germination. Whether many seedlings will survive under this sort of competition is question- Figure 30.—Leaf detail from ‘Jolivet’. able ARTICLES 36 Encephalartos March 2014 No. 115 Figure 34.—Leaf detail from ‘Oribi Gorge’. Figure 36.— E. natalensis at ‘Umtamvuna’ growing in deep shade next to a river.

CONCLUSIONS

As mentioned these are preliminary results as only a single population from the northern area was sam- pled and only a single individual from the southernmost population in KZN. Also more populations across the border into the Eastern Cape province need to analysed to determine their affinity to either the taxon in ques- tion or E. altensteinii. However from the current results it does seem that there may be three different meta- populations, with populations in the north at higher al- titudes and colder climates with relatively broad leaflets overlapping relatively strongly covered in persistent hairs and are heavily toothed. Those in the center with inter- Figure 35.—Seedling from ‘Oribi Gorge’. mediate to broad leaflets overlapping slightly, with few teeth (which conform to the type description which is seems a bit narrow in the photograph. No individuals also from this area). Lastly in the south leaflets tend were found reproducing in the colony, though there is to become narrower and even less toothed being well evidence of natural recruitment (Figure 35). spaced. Whether or not this is a continuous cline will only be known by finer grained field work as populations “Kloppers 44 & 45. Umtamvuna”: Leaf length 2.8m, assessed currently are distributed very far from each petiole clear ~66.25mm, 4–6 prickles, median leaf- other. In addition to this there are standout populations lets length/width/spacing 275X24.5X42.3mm, glossy in between these conforming metapopulations, such as ARTIKELS dark green, few spines always on the upper margin, pp the “Jolivet” plants which have a very consequent identi- angle 180°, pr 90°, swing 0°. Gestalt VERY NARROW, ty very different from its closest conspecifics. Thus far it FEW TEETH, WELL SPACED (Figure 36). Confirms Nel would seem that we are dealing with a very vegetatively (2006) “41. Umtamvuna” though the female cone of the variable taxon with the three main types that could be only individual located is very atypical (Figure 37). But given varietal status, other standout populations need to as the individual was growing in atypical conditions, and be investigated as these, e.g. “Jolivet”, seems rather to it was the only one sampled, more variation needs to be conform to our preliminary idea of a subspecies in the incorporated before any real conclusions can be made genus. However before any formal effort towards clas- on this population. sification is made a fine cline needs to investigated.

No. 115 March 2014 Encephalartos 37 ACKNOWLEDGEMENTS

A big thank you goes to the Cycad Society for the funding that was used to conduct this research. Also to John Kloppers who instigated the research and provided invaluable information including his map. Avis Nel and co-authors (Steele & Human) for their previous work on the group and for the use of photographs in presenta- tions and as cited here. Lastly for financial support the NRF and the University of Pretoria is thanked.

REFERENCES

CAPELA, P. 2006. Speculations on the Encephalartos species of Mozambique. Released by the author, Chimoio, Manica, Mo- zambique. COOPER, M.R. & GOODE, D. 2004. The cycads & cycads moths of KZN. Peroniceras Press, 7 Ridge Road, 3610 New Germany. DONALDSON, J.S. 2010. Encephalartos natalensis. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. www. iucnredlist.org. DYER, R.A. 1965. The cycads of southern Africa. Bothalia 8: 405– 515. DYER, R.A. & VERDOORN I. 1951. Encephalartos natalensis. Bo- thalia 6: 205–211. GIDDY, C. 1980. Cycads of South Africa. 2nd edition, 3rd impres- sion. Purnell, Cape Town. GOODE, D. 1989. Cycads of Africa. Struik, Cape Town. GOODE, D. 2001. Cycads of Africa Volume I. D.E. Cycads of Africa Publishers, Gallo-manor, South Africa. GROBBELAAR, N. 2002. Cycads—with special reference to the southern African species. Published by the author, Pretoria, Gauteng, South Africa. VORSTER, P. 2004. Chapter 6: Classification concepts in Encepha- lartos (Zamiaceae). In T. Walters, & R. Osborne (eds), Cycad classification: concepts and recommendations. CABI Publish- ing, Wallingford. Figure 37.—Very atypical female cone at ‘Umtumvuna’. ARTICLES 38 Encephalartos March 2014 No. 115