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A Guide to Identifying the Stem Fragments of Six South African Medicinal Encephalartos Species

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A Guide to Identifying the Stem Fragments of Six South African Medicinal Encephalartos Species South African Journal of Botany 84 (2013) 115–123 Contents lists available at SciVerse ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Sifting through cycads: A guide to identifying the stem fragments of six South African medicinal Encephalartos species S.R. Cousins ⁎, V.L. Williams, E.T.F. Witkowski School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits 2050, Johannesburg, South Africa article info abstract Article history: Sixty-three percent of the world's cycad taxa are threatened with extinction. In South Africa, 25 of the 38 in- Received 2 February 2012 digenous species are categorised as Threatened on the IUCN Red List, primarily due to illegal collecting. Three Received in revised form 5 October 2012 of the country's Encephalartos species are already Extinct in the Wild, while 10 Critically Endangered endemic Accepted 10 October 2012 Encephalartos species are undergoing rapid local extirpations across their ranges. Nearly two-thirds of South Available online 7 December 2012 Africa's Encephalartos species are used for traditional medicine, some of which are sold in traditional medi- fl Edited by JS Boatwright cine markets in the form of bark strips and stem fragments. The lea ess Encephalartos stems encountered in the medicinal and horticultural trades are generally difficult to identify to species and, since species iden- Keywords: tification of South African Encephalartos using DNA barcoding is not yet feasible, alternative methods of iden- Cycad tification are required. To determine the identity of the species sold in South Africa's two largest traditional Encephalartos medicine markets in KwaZulu-Natal (KZN) and Gauteng, surveys were conducted in the Warwick and Faraday mar- Harvesting kets respectively. Stem fragment samples purchased from the vendors in the markets were identified to species fi Identi cation using stem and leaf base morphological characters in tandem with harvesting locality records. Six KZN Encephalartos Leaf bases species were successfully identified viz. E. ferox, E. ghellinckii, E. natalensis, E. ngoynaus, E. senticusos and E. villosus. Markets Photographs of stem fragments and leaf bases of each species are presented here with supplementary quantitative Stem fi Traditional medicine trade and descriptive stem anatomical data. This paper therefore presents an identi cation guide to assist researchers and fi fi Wildlife forensics law enforcement of cers in the identi cation of Encephalartos species unlawfully harvested for the traditional med- icine and horticultural trades. The guide is thus also useful in the emerging discipline of wildlife forensics, and offers a unique approach to determining difficult-to-identify Encephalartos stem material. © 2012 SAAB. Published by Elsevier B.V. All rights reserved. 1. Introduction species (Encephalartos brevifoliolatus Vorster, Encephalartos nubimontanus P.J.H.Hurter and Encephalartos woodii Sander) are Extinct in the Wild Cycads are the world's most threatened group of plants; 63% of the (EW) (Raimondo et al., 2009). Ongoing dramatic declines and local 303 extant cycad species assessed in 2010 are threatened with extinc- extirpations are pervasive across the wild populations of South African tion (Hoffman et al., 2010; IUCN, 2010). Comparative analysis of the cycads (Donaldson and Bösenberg, 1999), largely due to illicit collecting Red List Index (RLI) for the world's cycad taxa shows that from of wild plants that enter the poorly-regulated horticultural trade 1997 to 2009, Africa has consistently been the region with the (Donaldson, 2003, 2008, 2011). Consequently, the situation has re- greatest threats to wild cycad populations (Donaldson, 2011). Over cently been termed the “South African cycad extinction crisis”,and half of Africa's cycad species are found in a critical centre of cycad the country is at risk of losing approximately 50% of its cycad species diversity in South Africa (Donaldson, 2008), where the two African in the immediate to near future (M.F. Pfab, SANBI Scientific Authori- cycad families represented – the Zamiaceae and Stangeriaceae – are ty, pers. comm.). the most threatened plant families in the country (Raimondo et al., One of the major obstacles to effective cycad monitoring in South 2009). Africa is the difficulty associated with determining the correct identity There are 38 cycad species indigenous to South Africa (37 of the Encephalartos spp. in the horticultural and traditional medi- Encephalartos spp. and Stangeria eriopus T. Moore), 29 of which are cine (TM) trades, more specifically stems that are illegally trafficked. endemic (Donaldson, 2008). Twenty-five of the taxa occurring in Many Encephalartos spp. are morphologically similar and closely re- South Africa are classified nationally as threatened (Donaldson, lated species are often difficult to distinguish from one another, even 2009), 10 of which are Critically Endangered (CR). Three endemic when leaves and/or cones are present (Golding and Hurter, 2003; Grobbelaar, 2004). Differentiating southern African Encephalartos spp. is complicated further by the existence of several ‘species complexes’ ⁎ Corresponding author. Tel.: +27 735021425(mobile). E-mail addresses: [email protected] (S.R. Cousins), [email protected] that comprise one or more closely related and morphologically similar (V.L. Williams), [email protected] (E.T.F. Witkowski). species (e.g. the Encephalartos cycadifolius (Jacq.) Lehm. complex sensu 0254-6299/$ – see front matter © 2012 SAAB. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.sajb.2012.10.004 116 S.R. Cousins et al. / South African Journal of Botany 84 (2013) 115–123 Oberprieler, 1995; Vorster, 2004). Another layer of complexity is added In terms of South African Encephalartos identification, pilot studies at the species level where cycad aficionados distinguish various ‘forms’ on the development of Amplified Fragment Length Polymorphism or ‘variants’ within species (Grobbelaar, 2004). These ‘forms’ are usually (ALFP) techniques have shown potential, but the technology has from subpopulations of subtly dissimilar entities of a single species oc- not yet been developed to a stage where it can be implemented curring at separate localities (e.g. the 11 variants of E. nubimontanus (Donaldson, 2008). Results from a recent DNA barcoding study on 60 sensu De Klerk, 2004). of the 65 African Encephalartos spp. showed that 12 species were re- The Encephalartos specimens encountered in the horticultural solved using a three-gene barcode (matK+rbcLa+nrITS; Rousseau, trade are often uprooted stems with neither leaves nor cones 2010, 2011). Ten of the 12 resolved species were South African en- (Fig. 1a). In TM markets, however, cycads are sold as chopped-up demics. While the study revealed that genetic variation in the genus is stems and/or ‘bark’ strips (Donaldson, 2008; Cousins, 2012; Cousins very low, the Encephalartos phylogeny is at least somewhat resolved, et al., 2011, 2012)(Figs. 1b&2a). Hence, the physical state of the and specimens can be assigned to taxon groups usually comprising Encephalartos material in both trades renders determining the actual less than six species (Rousseau, 2011). However, until species identifi- species sold exceptionally challenging (Cousins et al., 2012). This dif- cation of South African Encephalartos using DNA barcoding becomes ficulty is of particular concern in the horticultural trade, where nu- feasible, and in cases where monetary resources are limited, other merous illegally-collected Encephalartos taxa change hands on a means of identifying the cycads in the TM and horticultural trades are regular basis (Donaldson, 2008). Unlawfully-harvested rare species required. are often purposefully misidentified as more common species that The aim of this paper is to present a photographic guide with accom- are unlikely to raise suspicions among law enforcement officers panying morphological descriptions as a forensic identification tool, (Donaldson, 2008). Such misidentifications may have dire conse- primarily for use by researchers and law enforcement officers encoun- quences for the wild populations from which the cycads are collected, tering illegally harvested South African Encephalartos species. The especially since many highly sought-after species and variants thereof guide focuses specifically on the stem fragments of six KwaZulu-Natal naturally occur in low abundance and have extremely restricted geo- (KZN) Encephalartos spp. harvested for TM, but the methods described graphical ranges (Donaldson, 2003). Hence, an improved forensic ap- can be applied to Encephalartos species. in other South African prov- proach to rapid routine cycad identification is required in order to inces, and potentially other African countries as well. circumvent these problems. While the illegal collection of South African cycads for the horticul- tural trade is by far the greatest threat to their survival in the wild, 2. Methods they are also impacted by harvesting for TM (see Fig. 1b), which affects at least 23 Encephalartos spp. and S. eriopus (Cousins et al., 2012). The 2.1. Market surveys correct identification of the Encephalartos spp. present in both trades is therefore crucial for monitoring and their in situ conservation. The Surveys were conducted in South Africa's two largest TM markets, most accurate way to identify cycads to species without diagnostic mor- Warwick in Durban, KZN and Faraday in Johannesburg, Gauteng Prov-
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