A preliminary assessment of the conservation status of Cypripedium species in the wild

BotunicalJoumal ofthe Linnean Socieb (1998), 126: 183-190. With 2 figures Orchid population biology: conservation and challenges. Edited by S. Waite A preliminary assessment of the conservation status of Cypripedium species in the wild PHLLP CRBB AND MARANNE SYRYLAK SANDSON Rval Botanic Gardens, Kew, Richmond, Suvy TW9 3AB The conservation of few plants produces such an emotive response as that of hardy slipper orchids of the genus Cypripedium. The genus, comprising 45 species and two varieties, is holarctic in distribution with the centre of diversity in. Much is known about the status of some species and their populations in Europe and North America, hut little information is available on the Asiatic and Mexican species. Most cypripediums are showy orchids and are well represented in herbaria, allowing an estimate of the present distribution, frequency and conservation status of the known species to be made. The authors conclude that having considered the number of herbarium specimens, nearly half of the genus may be considered threatened and in need of some legal protection if the plants are to survive in the wild. They identlfy a need to examine the conservation status of the taxa in this genus more closely, and outline two important conservation tools that may help efforts to this end: the UCN Red List Categories and Criteria for the Amendment of the Appendices of CTES (Convention on nternational Trade in Endangered Species of Wild Fauna and Flora). 0 1998 The Linnean Societv of London CONTENTS ntroduction................... Material, methods and conservation criteria........... Herbarium specimens................. UCN Red List categories and criteria for the amendment of the CTES appendices.................... The CTES Criteria................. Results....................... Results of the application of the UCN Red List categories and the CTES Criteria.................. Conclusions...................... References....................... 183. 185. 185. 186. 187. 187. 188. 190. 190 NTRODUCTON The genus Cjpripedium, comprising 45 species and two varieties, has a holarctic distribution, ranging from the Arctic Circle in Alaska and Scandinavia, south to Correspondence to Dr M. Sandison. Email: m.sandison@rbgkew.org.uk 0024-4074/98/010183 + 08 $25.00/0/bt970153 183 0 1998 The Linnean Society of London

18+ P. CRBB.\1\D ~1. S. SA:'\'DSON TABLE 1. List of C)pripedium species and their distribution Taxon (Total=+7) C. subtropicum S. C. Chen & K. Y. Lang C. u ardii Rolfe C. irapeanum La Llave & Lex. C. molle Lind. C. dicl... insonianum Hagsater C. ralifomitum A. Gray C. flavum P. F. Hunt & Summerh. C. reginae Walter C. pmserinum Richardson C. ra/reolus L. C. hem:ri Rolfe C. segmmi ~asam. C. shnnxirose S. C. Chen C..fasciolatum Franc h. C.jarreri \\'. \\'. Sm. C. r01digerum D. Don C. parvijlorum var. parvijlorum E. Salish. C. pan:ijlorum var. pubescens (Willd.) Knight C. kmtuckienre C. F. Reed C. montamun Douglas ex Lind. C. candidum Muhl. e-x Willd. C. macranthos Sw. C. }'unnanense Franch. C. 'tudlou ii P. J. Cribb C. tibeticum King ex Hems. C. smithii Schltr. C. franchetti Rolfe C. himalaicum Rolfe ex Hems. C.fasciculatum Kellog ex S. Watson C. arietinum R. Br. C. plectrorhilum Franch. C. japonirum Thunb. C. formosanum Hayata C. acaule Aiton C. guttatum Sw. C. )'ntabeanum ~fakino C. elegans Rchb. f. C. palangshanense T. Tang & F.T. Wang C. dehile Rchb.f. C. micranthum Franch. C. bardolphianum var. bardolj1hianum \\'.\\'.Sm. & Farrer C. bardolphianum \'ar. ;:hongdianen.1e S. C. Chen C. margaritaceum Franch. C. lichiangense P J. Cribb & S. C. Chen C. forrestii P. J. Cribb C. jargesii Franch. C. u umen,gense S. C. Chen ~lexico, ~lexico Distribution Guatemala, Honduras ~lexico C.S.. \. C.S.A. C.S.A. Canada Europe, Russia, Korea, Taiwan. Korea, E. Russia ndia. ~cpa, Bhutan C.S.A., Canada C.S.A.. Canada C.S.A C.S.A, Canada C.S.A.. Canada Europe, Russia, Korea,,] a pan, Taiwan ~epal, Bhutan, l\. ndia, 1\epal, Bhutan, C.S.A C.S.A., Canada.Japan, Taiwan C.S.. \.. Canada Europe, Russia, Korea,, \ epa, X ndia. Bhutan, Alaska.Japan, E. Russia, Alaska 1\epal, \. ndia, Bhutan,, Taiwan..Japan Known from> 15 herb. specimens Key:, indicates taxa known from 15 herbarium specimens or fewer (see also Table 2). Honduras in Central America and the Himalayas (Cribb, 1997). Table 1 gives distributions for each taxon. These hardy slipper orchids are readily recognized by their plicate leaves, and flowers that have a unilocular ovary, a slipper-shaped lip and a column with two fertile anthers and a sterile apical staminode. Cypripediums

CONSERVATON STATUS OF CYPRZPELZLM SPECES 185 have been cultivated in Europe for over four centuries (Dodoens, 1568; Parkinson, 1640) and, although difficult to maintain in cultivation, their popularity has never waned. They are the showiest and most sought after hardy orchids, collected and increasingly grown by orchid and alpine plant enthusiasts alike. Cypripediums have been widely used in North America and the Far East for their medicinal properties (Rafinesque, 1828; Zhu, 1989). The species that have been used in North America include C. pam$lorum, C. acaule, C. reginae and C. candidum, while in both C. guttatum and C. macranthos are stiu used. Wild populations are the major source of material for horticulture and medicine. As a result, the more accessible populations of many species have declined through over-collection. Habitat destruction, particularly logging, agricultural improvement and drainage of habitats, especially in Europe and North America, has also led to the decline of many species. The current conservation status of the European, Japanese and North American species is relatively well known, but that of Asiatic and Mexican species is still rather poorly understood. Concern over the conservation status of hardy slipper orchids is not a recent phenomenon, Farrer (1 9 19) commented critically on the over-collection of C. calceolus in northern England that had, even then, brought it to the verge of extinction as a native species. Concern in continental Europe is frequently expressed over the future of this attractive orchid, many populations now being protected in nature reserves. The European Union (EU) has placed C. calceolus on the EC Habitats Directive, as a species whose conservation requires the designation of special areas of conservation giving the species strict protection (N. McGough, pers. comm.). The genus is also included in Appendix 1 of the Convention on nternational Trade in Endangered Species of Wild Fauna and Flora (CTES). The European Union, however, takes stricter measures than the Convention by including certain orchids in Annex A of Council Regulation (EC) No 338/97 implementing CTES in the EU. This means that the 15 EU Member States treat C. calceolus as if it were on Appendix of CTES. Outside Europe, nearly every recent article written about the native slipper orchids in North America mentions their decline in accessible habitats through overcollection or habitat modification. However, most concern has been expressed about local populations of widespread species. We are considering the global status of Cypripedium species and whether any useful information can be gleaned from the examination of herbarium specimens and the field work undertaken for this study. MATERAL, METHODS AND CONSERVATON CRTERA Herbarium specimens For information on relative rarity, we have counted the number of herbarium species of each of the 47 taxa covered in a recently completed monograph of the genus (Cribb, 1997). Field observations on hardy slipper orchids, including C. lichiangeme and C. bardolphianum listed here, in Yunnan and Sichuan (), and in Mexico, suggest that the method can be useful in determining relative rarity. Table 2 shows the taxa known from 15 or fewer herbarium specimens.

186 P. CRBB kyd hf. S. SkXDSON TABLE 2. Herbarium collections of Cjpripedium species showing taxa known from 15 or fewer specimens. *in cultivation. Underlined species are Chinese No. of herbarium 1 2 3 4 <5 specimens Species rubtropicurn dickinronianum wardii niicranthum molle baniolphianwn var. *-' bardolphianum var. showdianense bardolfihianum uwmmgense farrm *calfomicum ludlouii @langshanerue fasciolatum *i * katuckiase smithii fasciculatum jormo.ranum *ya,ntabeanum *maparitaceue *lichian~qense fargeslz Extinct Extinct in the,evaluatedl Adequate data 1 - Lower risk - Datadeficient f Notevaluated 1 Near threatened /Leastconcern Figure 1. Structure of the UCN Red list categories. Source UCN (1994). Shading indicates 'threatened' category. KTGV Red List categories and cn'h'afor the amendment of the CTES appendices The UCN Red List Categories and CTES are widely recognized, internationally respected and understood conservation tools. The UCN Red List Categories have been in use for almost 30 years and have become widely recognized as an easily understood method of highlighting species most in need of conservation. Ficgure 1

CONSERVATON STATUS OF CYPRZPEDZUM SPECES 187 shows the structure of the revised Categories (UCN, 1994); three are known as the threat categories and can be described as follows: (1) Critically Endangered (CR): a taxon facing an extremely high risk of extinction in the wild in the near future; (2) Endangered (EN): a taxon, not CR, but facing a high risk of extinction in the wild in the near future; (3) Vulnerable (VU): a taxon, not CR or EN, but facing a high risk of extinction in the wild in the medium term. A range of criteria is used to evaluate a taxon against these categories. n2e CTES Critena CTES came into force in 1975 with the aim of controlling and monitoring the international trade in species threatened, or potentially threatened, with extinction as a result of such trade. The Convention has at its core two Appendices or lists of species. Of the orchid family, seven species and two genera are currently included in Appendix, which effectively bans the international trade in wild-taken specimens, but permits trade in artificially propagated species, subject to licence. The rest of the Orchidaceae family is included in Appendix 11, which includes the genus Cyprzpedium. The trade in both wild-collected and artificially propagated species included in Appendix 1 is allowed, subject to licence. The CTES Criteria (Anon, 1994) are a set of guidelines by which the merits of proposals to amend the Appendices can be judged. The criteria for the amendment of the CTES Appendices were, like the UCN Categories, recently revised. Again we can say, in summary, that the CTES Criteria also make use of two broad types of information on population and distribution. The CTES Criteria are, like the UCN Categories, structured so that even small amounts of information can be used effectively. We have made preliminary assessments of the conservation status of the 23 taxa known from 15 or fewer herbarium specimens being considered according to the most recently published UCN Red List Categories (UCN, 1994) and the new Criteria for the Amendment of the CTES Appendices (Anon, 1994). Our results are currently subject to peer review, and we hope to present and publish our findings in due course. RESULTS Twenty-three of the 47 taxa are known from 15 or fewer specimens. From Table 2, we can see that nine taxa are represented by only one or two specimens. Eleven taxa are known from four or fewer wild-collected specimens, while a further 12 taxa are represented by 15 or fewer wild-collected specimens. These figures are given with the proviso that the North American taxa are under-represented in the sample because we have not seen material from many of the smaller American Herbaria. The field status of the Asiatic species is also probably under-estimated because of the relative inaccessibility and under-collection of many of the localities, mostly in western and south-western. Nevertheless, these figures suggest that many taxa

188 P. CRBB,LYD M, S. SAYDSON are rather narrowly endemic. A number of species appear to be confined to a single mountain or mountain range. Whether any of the rarest nine taxa (<2 herbarium specimens) are restricted to a single locality is doubtful, although Cypripedium subtropicum, C. wumengense, C. segawai, C. ludlowii, C. bardolphianum var. zhongdianense, c. palangshanense and C. dickinsonianum are the best candidates. Of the 23 taxa listed (Table 2), 17 are Chinese (including Taiwan and Tibet), 3 North American and 2 Mexican. Only C. yatabeanum is found in both the Old and Sew Worlds, being recorded from Russia, Japan and Alaska. The narrow endemicity of many of the Chinese species is probably accurate and not merely an artefact of under-collecting. These regions are relatively poorly collected in comparison with North America and Europe, Japan and the Himalayas, but hardy slipper orchids are not easily overlooked and are indeed sought out by collectors because of their cxotic flowers and horticultural value. A comparison of the listed species with the phylogeny suggested by a cladogram based on morphological data (Fig. 2), and using the tropical American orchid Selanipedium palmijiolium as an outgroup, implies that most of the rare taxa are either basal species that might be considered to have a relictual distribution, or are among the most recently evolved species. Thus C. subtropicam and C. wardii, the two most basal species, both have very limited distributions in north-west Yunnan and adjacent south-east Tibet (Xizang); C. lichiangense, C. forrestii and C. wumengense are all restricted to south-west. Of the species occupying the middle of the phylogeny, C. regamai from Taiwan is a vicariant of the more widespread C. henryi, while C. dickinsonianum is an autogamous species closely related to C. molle and C. irapeanum. Few of the species in Table 1 are in cultivation. Of the rarest 11 taxa, only C. segawai is relatively frequently seen in collections. Qpripedium farreri has begun to appear in collections in Japan, Germany, the Netherlands and USA. Cypripedium dickinsonianum has been grown by Sterling Dickinson in Mexico (pers. comm.) in soil dug up around the plant but did not survive for long. We have no doubt that C. mbtropicum, C. wumengense and C. forrestii would be welcome additions to collections if they were available. Of the other 12 species listed, C. formosanum, C. yatabeanum and C. caltjbnicum are relatively frequent in cultivation, being desirable plants by any standard. Cyprzpedium firmosanum has been propagated in some quantity; fortunately this lovely orchid divides easily and is one of the easiest species to grow from seed. Cypripedium htuckiense, C. fasciculatum, C. yatabeanum, C. bardolphianum var. bardo&hianum, C. maqaritaceum and C. lichiangenese have all been grown in cultivation in recent years; in all cases as far as we know from wild-collected material. Cypripedium kentuckiense, and possibly some of the other species, have been germinated but too recently for nursery-raised material to be available. Currently, the only source of 21 of the 23 taxa listed is from the wild, but developments in raising hardy slipper orchids from seed suggests that this may not long be the case. Results ofthe application of the UCN Red List categories and the CTES Criteria The results of this exercise are subject to peer review, and we hope to publish them shortly.

CONSERVATON STATUS OF CYPRZPEDUM SPECES 189 Majority rule Selenipedium 100 100 L C. dickinsonianum C. californicum C. fasciculatum C. franchetii C. tibeticum C. yunnanense 100 C. arietinum C. plectrochilum C. himalaicum C. passerinum C. flauum C. reginae C. shanxiense C. farreri C. fasciolatum C. henryi 67-7 C. segawai 5 C. calceolus C. parviflorum C. montanum C. kentuckiense 5 C. candidum C. cordigerurn C.~uttatum 92 100 85 C. elegans,100 C. palangshanense Figure 2. Majority rule cladogram of @pn$edzurn species based on 42 morphological characters (Cribb & Simpson, in prep.)

1'10 P. CRBB..LUD 31. S SL4XDSOS On the available evidence, it appears that nearly half of the species of Qprzpedium may be considered threatened and in need of some legal protection if the plants are to survive in the wild. We conclude that this work has identified a need to esaniine the conservation status of the taxa in this genus more closely, using thc available information to test them against both the UCN categories and the CTES criteria. This work is currently under way, in consultation with other authorities, and we hope to publish our findings shortly. t is, however, evident that more information, particularly of slipper orchid populations and demography, is needed to properly assess the current status of (~ypl-$edium species in the wild. The lack of information on Chinese species, where little work of this nature has been attempted to date, is a major, but not the only gap in our knowledge. Howe\rer, even where we have more information, as in Europe and North America, it is usually of a local or regional nature and this severely limits the formulation and implementation of conservation measures to protect the species as a whole. REFERESCES Anon. 1994. Resolution ofthe G@-rence ofthe Parties lo CTES 9.24. Citeria for the Amendment of ilibpendix and 11. CTES Secretariat, Geneva, Switzerland. Cribb PJ. 1997. 'The genus Cjpripedium. Portland, Oregon: Timber Press. Dodoens R. 1568. Florum, et comnarium adoratumque nonnullannn herbaium historia. Antwerp: C. Platini. Farrer R. 1919. The English rockgarden. London: T. Nelson. UCN. 1994. 'The C%\* Red List Catqorits. UCK Species Survival Commission, UCN, Gland, Switzerland. Parkinson J. 1640. 'Theatrum botanicuni: he theatre ofplants. London: T. Cotes. Rafinesque CS. 1828. Medual Flora; OF manual of the mtdical botay of th Unitpd States ofno~o7th America. Philadelphia: Atkinson & Alexander. Zhu YC. 1989. Orchidaceae. PLantae Mc.cii.inah Chinw Box -Orient.: 182-185.