ISSN 2473-442X CONTENTS

Message from Dr. Patrick Griffith, Co-chair, IUCN/SSC CSG 3 Official newsletter of IUCN/SSC Specialist Group Botanic Garden: In Focus Vol. IV I Issue 2 I December 2019 Montgomery Botanical Center’s Cycad Collection – Focus on research and conservation 5 Michael Calonje & Patrick Griffith

Feature Articles Towards an approach for the conservation and illegal trade prevention of ’s endangered spp. 10 James A. R. Clugston, Michelle Van Der Bankand Ronny M. Kobongo Fire is the most important threat for conservation of merolae (espadaña) in the hill Nambiyigua, municipality of Villaflores, Chiapas, Mexico 13 Miguel Angel Pérez-Farrera & Mauricio Martínez Martínez Ex-situ Cycad Conservation [1]: Public and Private Collections 16 Chip Jones & JS Khuraijam The Cycad Specialist Group (CSG) is a component of the IUCN Research and Conservation News Survival Commission (IUCN/SSC). It consists of a group of volunteer The Cycad Extinction Crisis in South Africa 19 experts addressing conservation Wynand van Eeden & Tim Gregory issues related to , a highly What is Ceratozamia becerrae ? 21 threatened group of land . The Andrew P. Vovides, Miguel Angel Pérez-Farrera & José Said Gutiérrez-Ortega CSG exists to bring together the world’s cycad conservation expertise, Preliminary Finding: Seed longevity of Encephalartos in controlled storage 23 and to disseminate this expertise to Ngawethu Ngaka and Phakamani Xaba organizations and agencies which can use this guidance to advance cycad Meeting Reports conservation. 2nd Nong Nooch Cycad Horticulture Workshop 25 Official website of CSG: Anders Lindstrom http://www.cycadgroup.org/ Conservation Genetics Workshop 26 Co-Chairs Caroline Iacuaniello, Stephanie Steele & Christy Powell John Donaldson Patrick Griffith CSG Members 28 Vice Chairs Michael Calonje Cristina Lopez-Gallego

Red List Authority Coordinator De Wet Bosenberg

CSG Newsletter Committee JS Khuraijam, Editor Irene Terry Andrew P. Vovides Jose Said Gutierrez-Ortega Cristina Lopez-Gallego

Li Nan Maria Ydelia Sánchez-Tinoco All contributions published in Cycads are reviewed and edited by IUCN/SSC CSG Newsletter Committee and members. IUCN/SSC CSG members can send contributions to [email protected] Nguyen Tien Hiep Rita Singh Cycads, the Official newsletter of IUCN/SSC Cycad Specialist Group Cover photos ISSN 2473-442X © IUCN/SSC Cycad Specialist Group Front: Encephalartos latifrons at San Frequency: Twice a year. Available online at http://cycadgroup.org/ Diego Zoo, California. Photo by Christy Powell CSG Programme Office: Back: Encephalartos middelburgensis, Montgomery Botanical Center, 11901 Old Cutler Road, Coral Gables, FL 33156, USA South Africa. Photo by Simon Lavaud

Design & layout: JS Khuraijam Copy Editors: M Calonje & JS Khuraijam MESSAGE

Dear Friends,

A very informative issue awaits you -- I am excited to see the important content assembled here. These pages show both the severity of threats our beloved cycads face, as well as the wide diversity of approaches and techniques needed to stop the loss of these living treasures.

I am especially encouraged by the engagement and expertise brought forward to address these threats. These pages show how many kinds of methods are needed help preserve these plants -- genetics, horticulture, seedbanking, and even armed deterrence. I believe all of these methods are essential to preventing cycads extinctions, so I am glad to see our group exploring all possibilities. Integrating these ideas and practices into the broader framework of our Specialist Group strategy will lead to many positive outcomes.

I am also glad to see the detailed attention being given to cycad collections. Our strategy recognizes the vital role that assurance colonies play to prevent catastrophic loss. My own studies in this area have convinced me that the best path forward is to share these vital resources, and steward them collaboratively – the genetic evidence clearly points that way. Adapting the mindset of zoos can help us help cycads in this regard.

I am honored to have the opportunity to discuss in these pages, with my colleague Michael Calonje, our own collection at Montgomery. As I have said before to this esteemed Group – our collection is your collection. Montgomery’s work depends on your input, collaboration and expertise, so we grow these plants for you.

This is our decade to prevent cycad extinctions – keep up the great work and let no cycad vanish!

Thank you,

Patrick Griffith Co-Chair, IUCN/SSC Cycad Specialist Group Executive Director, Montgomery Botanical Center, Florida ✉[email protected]

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Dioon merolae in natural habitat Photo by Takuro Ito

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CYCADS I Volume IV I Issue 2 I December 2019 5

Botanic Garden: In Focus

Montgomery Botanical Center (MBC) is a 120- collections to the oversight of its Board of Since that time, MBC has quickly developed acre botanical garden in Coral Gables, Florida Directors. one of the most comprehensive and well- (USA) which focuses on advancing science, documented cycad collections in the world. It education, conservation, and horticultural includes 7,213 individual plants, 1,920 knowledge of tropical plants, with an accessions, and 259 taxa representing emphasis on palms and cycads. The cycad approximately two thirds of all known collection on MBC’s grounds began in 1932 species. Plants from the ten cycad genera are when the property was first developed as hosted at MBC, with the most comprehensive Colonel Robert Montgomery’s winter home. collections being those of the Neotropical Among the early introductions by genera Ceratozamia, Dioon, Microcycas, and Montgomery is a plant of the Cuban endemic . MBC develops its collections during species Microcycas calocoma (Photo at right). research expeditions in close collaboration The plant is still alive today and is likely the with partner institutions worldwide, and the largest individual of the species in cultivation collections are world-renowned for their outside of Cuba (photo, page 6). Col. scientific and conservation value, as they Montgomery continued to develop his cycad focus on first-generation, wild-collected collection until his death in 1953, and in 1959, material from well-documented sources his wife Nell Montgomery created The sampled in a way that maximizes genetic Montgomery Foundation (now Montgomery diversity. In fact, MBC has conducted Botanical Center) to support research on research on genetic capture of cycad diversity tropical plants and to honor her husband’s in ex-situ collections to better understand the names. Nell Montgomery passed away in role botanic garden ex-situ collections can 1990, leaving the property and plant play in cycad conservation, and how to plan

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Magnificent plant of Cycas conferta at MBC. Photo: Michael Calonje

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Cycas cairnsiana Photo: Michael Calonje

for and build genetically appropriate cycad MBC cooperates with cycad researchers one of the primary reasons for MBC’s collections (Griffith et al., 2015; Griffith et al., around the world by making its plant commitment to sharing its living collections. 2017). collections, knowledge, and expertise Seeds produced from Montgomery’s living available for study. Scientists, educators, and collections are routinely distributed to botanic students regularly visit our collections to gardens, research institutions, universities, conduct their studies or are able to receive schools, and plant societies worldwide. After materials and data useful for their research conservation, research, and educational seed projects. In the last two years, over 20 distributions are made, the remaining seeds published scientific articles made use of are auctioned off in perhaps the first-ever MBC’s cycad collection. online seed auction, in partnership with the Miami-Dade Chapter of the Florida Nursery, MBC maintains one of the most active Growers and Landscape Association (FNGLA). seedbank programs for cycads. Cycad pollen Proceeds from this auction support the is routinely collected from plants in our Montgomery Seedbank. collection and either used immediately for hand-pollination, or stored in an ultra-low Since June of 2015, MBC hosts the freezer for later use or to distribute to other Programme Office for the IUCN Species botanical institutions wanting to pollinate Survival Commission Cycad Specialist Group their cycads. Cycad seeds are recalcitrant and (CSG). In this capacity, MBC supports some of therefore cannot be reliably stored long-term. its staff members as officers of the CSG, Therefore, seeds produced at MBC are helps provide administrative and technical immediately distributed. The widespread capacity, manages funding, collaborates with distribution of artificially propagated cycads other partner organizations, and helps

Microcycas planting at MBC helps reduces pressure on wild cycad develop the next generation of cycad populations by making them abundantly conservation expertise. available in the horticultural trade, and this is

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As part of its CSG duties, MBC’s Cycad Biologist Michael Calonje serves as coordinator of The World List of Cycads, a taxonomic and nomenclatural reference for cycad research that serves as the taxonomic backbone for the IUCN Red List, CITES, and the Catalogue of Life.

To meet its mission and goals, Montgomery cherishes the participation and input of cycad experts worldwide. We are always happy to host cycad researchers, provide material for study and conservation, and to collaborate in support of cycad conservation. Supporting and working with the CSG is an essential part of this collaborative endeavor, and we look forward to working with you in the years to come.

References Griffith, M. P., M. Calonje, A. W. Meerow, F. Tut, A. T. Kramer, A. Hird, T. M. Magellan, and C. E. Husby. 2015. Can a Botanic Garden Cycad Collection Capture the Genetic Diversity in a Wild Population? International Journal of Plant Sciences 176: 1-10. Griffith, M. P., M. Calonje, A. W. Meerow, J. Francisco-Ortega, L. Knowles, R. Aguilar, F. Tut, et al. 2017. Will the same ex situ protocols give similar results for closely related species? Biodiversity and Conservation 26: 2951-2966.

Michael Calonje Patrick Griffith Montgomery Botanical Center,

Dioon spinulosum cone at MBC - largest cycad cone ever recorded. 11901 Old Cutler Road, Miami, FL 33156 ✉ [email protected] ✉ [email protected]

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Cristina Lopez-Gallego (CSG Vice Chair) and her students with Microcycas calocoma at Montgomery Botanic Center

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FEATURE ARTICLE

Figure 1. View of impressive Encephalartos collection at the Kirstenbosch National Botanic Garden, South Africa.

Cycads worldwide are under threat from these plants require identification to species associated with sequencing large and habitat destruction caused by human activity level, but the morphological characteristics complex genomes (e.g. Encephalartos c. 58 such as over-collection of plants from wild that are often used to identify them are not Gbp) are prohibitive (Roodt et al. 2017, populations, causing a reduction in the size always present (Cousins et al. 2013). The Zonneveld 2012). However, new next of these populations and increasing the advent of DNA barcoding technologies was generation sequencing approaches such as threat of extinction (Donaldson 2003). considered to help identify plants that are targeted capture sequencing (Brewer et al. Species in the genus Encephalartos Lehm. confiscated due to illegal trade (Sass et al. 2019), and restriction site associated DNA (Fig. 1) are some of the most sought after of 2007). However, due to recent radiation (in sequencing (RADseq), has been shown to be all cycads, which includes species such as E. the last 10-15 million years) of the extant very successful for both population genetics hirsutus and E. eugene-maraisii (Fig. 2). cycads and their close genetic relationship and phylogenetics (Andrews et al. 2016). These species can cost hundreds of US among many species, traditional DNA Additionally, RADseq has already been dollars per seedling due to their rarity and barcoding markers are often ineffective at shown to be successful in its application to value in private collections. This rarity has resolving close genetic relationships cycads and other orgasms with large and spurred demand for many rare species in between species (Condamine et al. 2015, complex genomes (Clugston et al. 2019). both horticultural and private collections Nagalingum et al. 2011). (Dehgan 1997), and ultimately has led to With these recent advances in mind, this their over collection from the wild and an Due to the ineffectiveness of the traditional opens new doors for testing RADseq and its increase in illegal trade (Williamson et al. methods, new approaches are needed to application to tackle conservation and track 2016). Although many of these species are help conserve Encephalartos in Africa. This illegal trade in Encephalartos. To do this, a regularly cultivated, this has been is because we need to be able to identify team of experts was formed to help insufficient to satisfy the demand for these plants in illegal trade to species level and formulate, establish and implement new species and prevent illegal collection from find out which populations they were protocols for the conservation of wild populations (Whiting et al. 1966). collected from so they can be returned to Encephalartos, led by African Centre for that same population without affecting DNA barcoding at the University of In recent years illegal trade of cycads for genetic diversity of the species (Neale Johannesburg (Prof. Michelle Van Der Bank both horticultural and medicinal purposes 2012). Recent advances in genomic and Ronny “Beads” Kobongo), Royal Botanic has caused a significant increase in sequencing and DNA fingerprinting has so Garden Edinburgh (Prof. Peter unidentified plants being confiscated by far proved valuable in understanding close Hollingsworth), The University of Sydney (Dr. authorities (Cousins et al. 2012). Many of species relationships, yet significant costs James Clugston), California Academy of

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Figure 2. James Clugston next to a large mature specimen of Encephalaertos eugene-maraisii in the wild at South Africa.

Sciences (Dr. Nathalie Nagalingum) and in spanning the diversity of angiosperms. South Africa, the Endangered Wildlife Trust Frontiers in Plant Science, 10, 1102. and the Department of Environmental Clugston, J. A. R., R. R. Milne, G. J. Kenicer, Affairs. We are actively working to develop I. Overcast, & NagalingumN. S.(2019). new methods to genotype species and RADseq as a valuable tool for plants populations of Encephalartos. Using RADseq with large genomes—a case study in methodology proposed by Clugston et al. cycads. Molecular Ecology Resources. (2019), we will not only be able to provide 19, 1610-1622. an accurate species level identification, but Condamine, F. L., Nagalingum, N. S., also determine the origin of wild Marshall, C. R., &Morlon, H. (2015). Encephalartos specimens that have been Origin and diversification of living confiscated by customs or recovered from cycads: a cautionary tale on the impact illegal trade, and facilitate their return to of the branching process prior in their original populations. Bayesian molecular dating. BMC Evolutionary Biology, 15(1), 65. We have already obtained data from a Cousins, S. R., Williams, V. L., & Witkowski, Figure 3. Ronny “Beads” Kobongo undertaking successful pilot study which was completed library preparation in the molecular laboratories E. T. F. (2013). Sifting through cycads: A in the molecular laboratories of the Royal of the Royal Botanic Garden Edinburgh. guide to identifying the stem fragments Botanic Garden Edinburgh (Fig 3). The of six South African medicinal samples from this project represented References Encephalartos species. South African multiple accessions for 23 species of Andrews, K. R., Good, J. M., Miller, M. R., Journal of Botany, 84, 115-123. Encephalartos, which will be used to Luikart, G., & Hohenlohe, P. A. (2016). Cousins, S. R., Williams, V. L., & Witkowski, develop a set of custom markers to further Harnessing the power of RADseq for E. T. F. (2012). Uncovering the cycad taxa genotype populations and species. ecological and evolutionary genomics. (Encephalartos species) traded for Ultimately, our findings will be used to build Nature Reviews Genetics, 17(2), 81. traditional medicine in Johannesburg better conservation management plans for Brewer, G. E., Clarkson, J. J., Maurin, O., and Durban, South Africa. South African wild populations and aid in the conservation Zuntini, A. R., Barber, V., Bellot, S., ... & Journal of Botany, 78, 129-138. of Encephalartos for future generations. Edwards, S. L. (2019). Factors affecting Dehgan, B. (1997). Propagation and culture targeted sequencing of 353 nuclear of cycads: A practical approach. In II genes from herbarium specimens International Symposium on Ornamental

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Palms & other Monocots from the genome duplication in the cycad lineage. (Cycadophyta: Encephalartos) at two Tropics 486 (pp. 123-132). PloS one, 12(9), e0184454. traditional medicine markets in South Nagalingum, N. S., Marshall, C. R., Quental, Sass, C., Little, D. P., Stevenson, D. W., & Africa using DNA barcoding. Genome, T. B., Rai, H. S., Little, D. P., & Mathews, Specht, C. D. (2007). DNA barcoding in 59(9), 771-781. S. (2011). Recent synchronous radiation the cycadales: testing the potential of Zonneveld, B. J. M. (2012). Genome sizes for of a living . Science, 334(6057), proposed barcoding markers for species all genera of Cycadales. Plant Biology, 796-799. identification of cycads. PloS one, 2(11), 14(1), 253-256. Neale, J. R. (2012). Genetic considerations e1154. in rare plant reintroduction: practical Union internationale pour la conservation de James A. R. Clugston, applications (or how are we doing?). In la nature et de sesressources. (2003). Ronny M. Kobongo Plant reintroduction in a changing Cycads: status survey and conservation Royal Botanic Garden Edinburgh Edinburgh, climate (pp. 71-88). Island Press, action plan. J. S. Donaldson (Ed.). IUCN-- United Kingdom Washington, DC. the World Conservation Union. ✉[email protected] Roodt, D., Lohaus, R., Sterck, L., Swanepoel, Williamson, J., Maurin, O., Shiba, S. N. S., R. L., Van de Peer, Y., &Mizrachi, E. Van der Bank, H., Pfab, M., Pilusa, M., & Michelle Van Der Bank (2017). Evidence for an ancient whole Van der Bank, M. (2016). Exposing the Department of Botany and Plant illegal trade in cycad species Biotechnology, University of Johannesburg

Cycas tansachana, Saraburi Province, Thailand Photo by Simon Lavaud

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FEATURE ARTICLE

Adult D. merolae burning on the fire, April 2019 at the hill Nambiyigua

Dioon merolae is a cycad species endemic to One of the localities registered for Dioon Chiapas and Oaxaca states (Chemnick et al., merolae in the original publication by De 1997). This species grows in the Luca and Sabato et al. (1981) "Cerro Grande, physiographic regions of the sierra madre district of Villaflores", is located in the and in the central depression of Chiapas; in Central Depression of Chiapas (Fig. 1) and is Oaxaca it grows in the Sierra Madre Sur in known locally as “cerro Nambiyigua” the deciduous tropical forest and in the pine- (Nambiyigua in the Chiapanec language oak forest between 500 and 1200 mls, means hill of the witch monkey (Mangue reaching up to 5 m in height. This species and Montesinos, 1991). This site is suffering has been studied from the ethnobotanical a great tragedy at this moment in that the (Pérez-Farrera & Vovides 2006), ecological cycad population is being impacted by fire (Lazaro-Zemeño et al., 2011), eco- (Fig. 2) caused by the drought, winds and physiological (Pérez-Farrera et al., 1999), agricultural activities. The individuals of morphogenetic (Cabrera-Hilerio et al., 2008) Dioon merolae in this locality grow on steep and genetic points of view (Cabrera-Toledo slopes of up to 45º and begin to grow from et al., 2010; 2012) and recently its 900 to 1200m in pine-oak forest. morphological variation has been studied through its geographical distribution range Due to the cultural and biological (Pérez-Farrera et al., 2018). Figure 1. Geographic localization of Nambiyigua importance of this species, the municipal hills, Villaflores, Chiapas. government of Villaflores, Chiapas

CYCADS I Volume IV I Issue 1 I October 2019 13

established an in-situ nursery in the municipality of Villaflores for propagation and reintroduction purposes. In this sense, the municipal government reintroduced more than 2000 seedlings to Nambiyigua. However, this locality has suffered constant burning throughout different years in 1998, 2000, 2018, 2019. Last year (2018) more than 50 ha were affected. In this year since the mountain began to burn, more than 100 hectares of forest have been destroyed.

Figure 3. Population structure by reproductive condition in D. merolae.

2012). In 2018 a group of students from The Dioon merolae De Luca, Sabato & Eizi Matuda Herbarium, Universidad de Vázquez-Torres (, Cycadales) Ciencias y Artes de Chiapas (UNICACH) a partir de megagametofitos y evaluated two populations, one with embriones cigóticos. Interciencia 32(12): disturbance (through fires) and the other 929-934 without disturbance, and evaluated the Cabrera-Toledo D., J. González-Astorga, F. Figure 2. Dioon merolae locality on fire at abundance and structure of the population Nicolalde-Morejón, F. Vergara-Silva, A. Nambiyigua Hill. by reproductive condition and they found P. Vovides. 2010. Allozyme diversity significant differences in relation to their levels in two congeneric Dioon spp. This population is important for the abundance; the population conserved (Zamiaceae, Cycadales) with contrasting following reasons: denominated "The Mangal" had a total of rarities. Plant Syst. and Evol. 290(1–4): a) it is one of the localities where the 295, whereas the population of "San Angel" 115–125. espadañeros arrive to collect for which is considered with disturbance had Cabrera-Toledo D., J. González-Astorga, J. the ritual of the festivity of “Santa Cruz” 158 individuals (Fig. 3). Unfortunately, the C. Flores-Vázquez. 2012. Fine-scale in Suchiapa, Chiapas (Pérez-Farrera & study cannot be continued due to the current spatial genetic structure in two Mexican Vovides, 2006), great fire, where the conserved populations cycad species Dioon caputoi and Dioon b) it is one of the original localities were affected. However, this same problem merolae (Zamiaceae, Cycadales): referenced in the publication by De Luca has prompted us, to begin in August 2019 a Implications for conservation. Bioch. and Sabato et al., (1981) describing D. research study to assess the situation and Syst. and Ecol. 40: 43-48. merolae and its morphological variation, the state of conservation of newly Chemnick J., T. Gregory, S. Salas –Morales. c) the hill Nambiyigua is an area that has discovered populations of D. merolae in the 1997. A revision of Dioon tomasellii been proposed as a natural reserve with area of La Frailesca Chiapas (Villaflores, (Zamiaceae) from western México, a approximately 4127 has for the national Villacorzo and La Concordia municipalities). range extension of D. merolae and commission of protected natural areas These Dioon populations will be evaluated clarification of D. purpusii. Phytologia. (CONANP), although this has not yet through various population parameters 83(1):1-6 been done officially, and it is an area (abundance, class structure, spatial Comisión Nacional de Áreas Naturales within the La Sepultura biosphere distribution, sex ratio), dendrometry and Protegidas, 2012. Estudio Previo reserve, allometry (height, diameter of trunk, number Justificativo para el establecimiento del d) It was an important place for the of leaves, width and long) and this data Área Natural Protegida Área de Chiapanec culture. In this place, several will be correlated with the history of use of Protección de Flora y Fauna “Cerro archaeological remains of this culture the cycads, also a study about effect fire on Nambiyugua”, en el Estado de Chiapas, have been found (Navarrete, 1966), population dynamic of Dioon merolae will México. 68 páginas + 2 Anexos e) on this site individual of Dioon merolae be evaluated and the land with the purpose Lázaro-Zermeño J.L., M. González-Espinosa, up to 5 m high have been registered of providing information that generates a A. Mendoza, M. Martínez-Ramos, P. F. (Martínez com. pers.), strategy for conservation. Quintana-Ascencio. 2011. Individual f) it represents one of the populations with growth, reproduction and population the greatest abundance of individuals References dynamics of Dioon merolae (Zamiaceae) within their range of geographic De Luca P., Sabado S., M. Vazquez-Torres underdifferent leaf harvest histories in distribution (Conanp, 2012) 1981. Dioon merolae a new species from Central Chiapas, Mexico. Forest Ecology Mexico. Brittonia 33:179-185 and Management 261(3): 427-439 In 2011, 447 individuals were registered in Cabrera Hilerio S.L., V. M. Chávez-Ávila, E. Pérez-Farrera M.A. , A. P. Vovides, J. S. three sites within the Nambiyigua hill (Las Sandoval-Zapotitla, R. E. Litz, F. Cruz Gutiérrez-Ortega. 2018. Morphological Anonas, El Pashtal and San Angel) (Conanp, Sosa. 2008. Morfogénesis in vitrode variation of Dioon merolae. The 11th

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Conference on Cycad biology, White Central Depression of Chiapas, México. Miguel Angel Pérez-Farrera River, South Africa 19-23 August. Bol. Soc. Bot. Mex. 78:107-113 Mauricio Martínez Martínez Pérez-Farrera M.A., A., P. Vovides and J.G. Manguen E., J Montesinos . 1991. Los Laboratorio de Ecología Evolutiva, Herbario Eizi Álvarez Moctezuma. 1999. A study on Chiapanecas. Guerreros de la Historia. Matuda, Instituto de Ciencias seed germination of the cycad Dioon Vol. 1. Gobierno del Estado de Chiapas, Biológicas, Universidad de Ciencias y merolae (Zamiaceae). New Plantsman Tuxtla Gutiérrez. Artes de Chiapas, Tuxtla Gutiérrez 6(4): 214-218. Navarrete C. 1966. TheChiapanec. History 29039, Mexico Pérez Farrera M.A., A.P. Vovides. 2006. The and Culture. New World Archaeological ✉ [email protected] ceremonial use of the threatened Foundation Publications, Brigham Young

“espadaña” cycad (Dioon merolae, University, Provo. Zamiaceae) by a community of the

Cycas panzhihuaensis Photo: Patrick Griffith

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FEATURE ARTICLE

Figure 1. World distribution of cycads (356 species, Calonje et al., 2019).

When you hear the word “collection” many theoretically indefinite time. An individual things might come to mind in the context of might see a herbarium as a destructive cycads. Botanists, horticulturalists, sample for few to see and prefer to keep conservationists, public, and private living collections of whole plants. Too often plantsmen have connotations of collection. there is a dichotomy between individuals The definition of collection from Merriam with collections and professionals who Webster is an accumulation of objects collect specimens for botanical gardens or gathered for study, comparison, or exhibition herbaria. Occasionally the two sides of or as a hobby. A collection is typically collecting join. This article is introduction to thought to be a group of objects or people the public gardens and private collections, together but can refer to a single specimen and we plan to have a follow-up on detail or a verb as the act of collecting. Often a collection information in next issue. plant collection is thought to be a living group of plants brought together for a Cycad collections in Botanic Gardens purpose. Collections can be privately owned Name of Botanic Garden No. of Taxa by individuals. Often larger cycads 1. Nong Nooch Tropical Garden, Pattaya*: 347 2. Montgomery Botanical Center, Florida : 261 collections are kept by institutions, Figure 2. A magnificent Cycas debaoensis at 3. The Huntington, California : 178 museums and botanical gardens collectively Nong Nooch Tropical Garden, Thailand 4. Lotusland, California : 142 called public gardens. Public gardens offer [Right to left: A Vogel, A Lindstrom, W Tang & JS Khuraijam] 5. Flamingo Gardens, Florida : 120 varying degrees of access to plant 6. University of California Botanical Garden : 114 Botanical gardens are collections of living collections often keeping rare or sensitive 7. Fairchild Tropical Garden, Florida : 105 species in more secure areas. A collection 8. Royal Botanic Gardens, Kew : 81 plants often used by botanists and other can be for professional reasons such as a 9. CSIR-NBRI Botanic Garden, Lucknow : 72 researchers. The botanical garden can specimen collection for a botanist who 10. Kirstenbosch NBG, Capetown: 52 reduce the need for extensive travel to would see the value of a herbarium *Private Garden analyze multiple specimens or species. In collection to preserve details of a plant for a

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Figure 3. Cycad Collection at Kirstenbosch National Botanical Garden, South Africa. addition to the value to science gardens can mature size and usually space for multiple Pollen viability research and access to -80 educate individuals and give an introduction specimens. Also, most public gardens have freezers and stand-by generators assure to the living world to people of all ages and security, an infrastructure for maintenance pollen banks function for sexual especially to children. Public gardens often and record keeping. propagation. Botanical gardens often follow a mission statement describing produce seeds and distribute plants. Plant purposes of horticulture and education and distribution furthers conservation efforts and conservation. Cycads are among the most removes pressure for illegal collecting. If an threatened plants with extinction and well individual can obtain a plant from a local suited to fit the missions of most botanical botanical garden there is little chance that gardens. Many individuals cannot obtain individual would want to collect from specimens of rare plants due to scarcity, habitat. price, and legal protections placed on cycads. Botanical gardens are an important In collecting data from public collections way for individuals to appreciate and better some observations are made. With only 10 understand cycads. In the way zoos have genera and 356 species of extant cycads breeding programs and assurance colonies (www.cycadlist.org, see Fig. 1), many for research and conservation so too botanical gardens have complete or near botanical gardens play important roles in complete collections of cycad genera (Table cycad research and conservation. 1). Most collections focus on endemic species to the region of the garden. For Public gardens can easily obtain important example Kirstenbosch National Botanical representations of cycad taxa and often Garden is known to have an impressive serve as sites for ex-situ conservation for collection of cycads of both tax and living collections of rare cycads. CITES is specimen quality and yet has few non- virtually impossible for individuals but Figure 4. Chip Jones at a private collection in endemic taxa other than African relatively easy via CITES institutional South Africa. Encephalartos and . A public exchange (Conf. 11.15 Rev. CoP18) garden in Brazil, Inhotim, in 2011, joined the www..org. Most botanical gardens Public gardens have staff that can watch for Brazilian government's official botanical have ample space for plants to achieve coning events and document phenology.

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Figure 5. Cycad Collection, Montgomery Botanical Center, USA Photo by Michael Calonje garden association, and the staff has begun collections. Exotic plants from faraway Any information to further this goal is an inventory of its 5,000 plant species, places make good stories for curators that appreciated and can be sent to us by email. including 1,300 types of palm alone. Inhotim write interpretation for botanical displays. has only 2 Dioon, 2 Cycas, 2 Encephalartos, The living fossil moniker is as popular as and a few Zamia accessions (pers. comm.). dinosaur food in describing the history of Chip Jones In 2018, Inhotim received its 3 millionth cycads in evolutionary terms. 5301 SW 82nd Avenue Davie, FL 33328 USA visitor while the same year Kirstenbosch ✉ [email protected] National Botanical Garden saw over 2 Public garden collections have a unique million visitors (SANBI annual report opportunity to introduce millions of people JS Khuraijam 2017/18). Conversely where cycads are not to cycads. Because of habitat degradation, Botanic Garden, CSIR-National Botanical native we see high diversity in collections public garden collections might be the only Research Institute, Lucknow, India such as Europe (zero extant native cycads) opportunity for some people to see a cycad. ✉ [email protected] and the United States (one endemic The introduction to cycads could lead to species). This is explained by climate and public awareness and further support for the interests of the public in exotic or conservation. charismatic flora. Horticulturalists know what plants will survive and perform well in The authors would like to compile a the soils and climates where they maintain database of living collections worldwide.

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RESEARCH & CONSERVATION NEWS

Figure 1. Armed guards at Lillie Flora Nature Reserve, protecting E. dyerianus around the clock.

The IUCN Red List lists only four species of reserves. The only exception to this is Lillie cycad as extinct in the wild (EW) and all four Flora Nature Reserve in which E. dyerianus is were endemic to South Africa. Only one, growing and the cycads have survived only Encephalartos woodii, was known from one because armed guards are on duty 24/7. single clone. All the others were multiple plants or even populations, although they To remedy the lack of focus, a new occurred in a confined area.All four species conservation oriented, non-profit company, Wild Cycad Conservancy NPC, or WCC, was became extinct due to human intervention registered in South Africa this year, with the and specifically for the horticultural trade. If aim to acquire land on which endangered one considers that fourteen more species of Encephalartos are now listed as critically cycad species occur, to have this land endangered (CR) or endangered (E) and that a declared as reserves and to make the few of these are functionally extinct in the reserves sustainable. The reserves will be managed by the WCC and as far as possible wild already, the South African situation is in co-operation with the original landowner. dire indeed! Nowhere else in the world are cycads so sought after and do they fetch such As a non-profit organisation, the WCC is run high prices, as in South Africa. by volunteers and entirely dependent on donations.WCC will be registered as a public What can be done about this? benefit organisation (PBO) in South Africa and a 501c3 in the US. The management Figure 2. Healthy seedlings of E. horridus in Currently only a few species occur in official structure currently is made up of a board of what will soon be the first reserve to protect reserves where some kind of protection is directors and an advisory board with the species. offered. However, most reserves focus on members from across the world. animals and not specifically the plants and it Encephalartos horridus has come under is usually a coincidence if cycads do occur in severe pressure from poachers lately. A

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property was identified with a healthy point to get other landowners to collaborate Wynand van Eeden population that will be the pilot project for and work with WCC to stop E. horridus from University of Stellenbosch WCC. A preliminary population survey was moving from being listed as EN to CR in the ✉ [email protected] done by Alicia Wain, a botanist and expert on future. habitat restoration, and it has shown healthy Tim Gregory Securing land for reserves is the main, but recruitment with seedlings, as well as sub- UC Berkeley Botanical Garden Berkeley, adults, in the population. The sex ratio not only, activity of WCC. Future projects will California, U.S.A. appears to be close to 1:1 and pollinators are expand their scope to include the ✉ [email protected] present. Once this reserve has been establishment of assurance populations of threatened species, as well as re- established, it will be an excellent starting introduction programmes when possible.

Encephalartos latifrons in natural habitat at Eastern Cape Province, South Africa Photo by Simon Lavaud

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Cycad descriptions are traditionally based on suggest a clear species distinction of C. that we are preparing, we propose the vegetative morphology, especially, leaf, becerrae. recognition of C. becerrae as a valid taxon. leaflet and strobilar traits. Anatomical characters, as aid to species delimitation in References cycads, have been particularly useful when González, D., & A.P. Vovides (2002). Low compared with molecular data, at times intralineage divergence in the genus ratifying or contradicting previously reported Ceratozamia Brongn. (Zamiaceae) phylogenetic relationships. Anatomical traits detected with nuclear ribosomal DNA have enabled us to bring Ceratozamia ITS and chloroplast DNA trnL-F non- brevifrons out of synonymy with C. mexicana coding region.Systematic Botany 27(4): (Vovides et al., 2012). Likewise, a 654-661. morphology and leaflet anatomy study has Kadereit, G., Piirainen, M., Lambinon, J., & helped the definition of the species within Vanderpoorten, A. (2012). Cryptic taxa the complex (Pérez- should have names: Reflections in the Farrera et al., 2014). glasswort genus Salicornia (Amaranthaceae). Taxon 61(6): 1227- Ceratozamia becerrae in the C. miqueliana 1239. species complex has recently come under Martínez-Domínguez, L., F. Nicolalde- scrutiny questioning its validity by Martínez- Morejón, F. Vergara-Silva, D.Wm. Domínguez et al. (2017) based on the Stevenson, & E. del Callejo. (2017). absence of overall variation among some Cryptic diversity, sympatry, and other morphological traits, and the lack of integrative scenarios in the variation in the internal transcribed spacer Mexican Ceratozamia miqueliana Figure 1. Camera Lucida illustrations. A; (ITS) of the ribosomal DNA. The close complex (Zamiaceae). Organisms, transverse section Ceratozamia zoquorum leaflet, geographic distribution of C. becerrae to that Diverstity and Evolution 17: 727-752. shaded areas h = lignified hypodermis; gs = girder of C. zoquorum has also added to the sclerenchyma. B; transverse section of C. Medina-Villarreal, A., J. González-Astorga, confusion between the two species. becerrae leaflet, note lack of lignified hypodermis & A. Espinosa de los Monteros (2019). However, this study ignored previous and very scarce girder sclerenchyma. Bars = Evolution of Ceratozamia cycads: A morphological and molecular evidence 20µm. proximate-ultimate approach. Molecular reported in the studies by González and Phylogenetics and Evolution 139: 1-14. Vovides (2002) and Vovides et al. Pérez-Farrera, M.A., A.P. Vovides, & S. (2004).Also, the recent molecular study by For meaningful taxonomic changes in Avendaño (2014). Morphology and Medina-Villarreal et al., (2019) places the cycads, such as the invalidation or raising of leaflet anatomy of the Ceratozamia two species on different clades; C. zoquorum lumped of taxa, it is necessary to identify norstogii (Zamiaceae, Cycadales) species on the C. mexicana clade and C. becerrae on the potential mistakes that previous studies complex in Mexico with comments on the C. miqueliana clade. Morphologically, have committed, re-evaluate the total relationships and speciation. the two species are distinguishable mainly biological evidence that is known, and International Journal of Plant Sciences by number of leaflets and spacing between propose the new taxon status based in 175(1): 110-121. them, leaflet shape and articulation width. explicit predictions leading to testable Pérez-Farrera, M.A., A.P. Vovides & C. Megastrobili are erect in C. becerrae but hypotheses. Furthermore, it is well known Iglesias (2001). A new species of decumbent in C. zoquorum, see Pérez- that cycad species show low genetic Ceratozamia (Zamiaceae) from Chiapas, Farrera et al. (2001) and Vovides et al. differentiation (e. g. González and Vovides, Mexico. Botanical Journal of the Linnean (2004). In our recent analyses, we have 2002; Salas-Leiva et al., 2013), and we Society 137: 77-80. found that the leaflet anatomy of the two discourage the delimitation of cycad species Vovides, A.P., S. Avendaño, M.A. Pérez- species also differs. Transverse sections of based in the variation in only one molecular Farrera, & D. Wm. Stevenson (2012). leaflets taken midway along the leaf show marker. Poor criteria might be problematic What is Ceratozamia brevifrons that C. zoquorum presents a continuous for the taxonomy of cycads, as in textual (Zamiaceae)? Brittonia 64(1): 35-42. lignified hypodermis and very pronounced words of Kadereit et al. (2012) “Lumping Vovides, A.P., M.A. Pérez-Farrera, B. girder sclerenchyma associated with the similar species into single taxa would Schutzman, C. Iglesias, L. Hernánez- vascular tissue whereas these two traits are therefore produce polyphyletic taxa, which is Sandoval, & M. Martínez (2004). A new absent in C. becerrae (Fig. 1). Furthermore, unacceptable to any taxonomist who species of Ceratozamia (Zamiaceae) the leaflets of C. zoquorum are much thicker believes that species should reflect from Tabasco and Chiapas, Mexico. than those of C. becerrae. These results Botanical Journal of the Linnean Society evolutionary history ”. With the rationale mentioned above, and additional evidence 146: 123-128.

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Andrew P. Vovides Universidad de Ciencias y Artes de Chiapas, Departamento de Biología Evolutiva, Tuxtla Gutiérrez 29039, Mexico Instituto de Ecología, A.C., México ✉ [email protected] ✉ [email protected] José Said Gutiérrez-Ortega Miguel Angel Pérez-Farrera Department of Biology, Chiba University, Laboratorio de Ecología Evolutiva, Herbario Eizi Chiba 263-8522, Japan Matuda, Instituto de Ciencias Biológicas, ✉ [email protected]

Cycas pectinata at MBC, Florida Photo by Patrick Griffith

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RESEARCH & CONSERVATION NEWS

Introduction altensteinii, E. aemulans, E. natalensis, E. Encephalartos species drops with an Cycads have the oldest currently known trispinosus, E. lebomboensis, and E. increase in years of storage. Results indicate seed lineage and seed is reported to be horridus. Rescued seed embryos of all the that cycads loose moisture during storage recalcitrant (Forsyth & Van Staden, 1983; above seed were treated with tetrazolium from > 30% at the first year to < 20% by the Woodenberg et al., 2007). Recalcitrant chloride to determine the viability of the seventh year (Fig 1). Moisture content seeds are defined as seeds that are seeds (de Carvalho et al., 2014). Viable consistently drops with years of storage in sensitive to desiccation and cannot be dried seeds were confirmed after treated embryos all species, although seed viability is not below a certain critical moisture level turned pink; non-viable seed did not change consistent in all the species (Fig 2). (Farrant et al., 1989). Since cycads seeds are colour (Fig 1). To determine seed moisture recalcitrant, this means traditional seed content, fresh and dry weight were The tetrazolium test conducted showed banking methods cannot be employed to measured. After fresh weight was highly significant difference in seed viability conserve seeds. Moreover, cycads are one determined, seed was then dried in an oven that was stored for different years(휒2, p < of the most threatened living plant species for 17 hours at 103°C (Tang and Sokhansanj, 0.05.) (Fig 2). Viability in seeds stored for to date (IUCN, 2010). Knowledge and 1991) then both weights were subtracted to one year ranged between 70−90%.The understanding in cycad seed longevity and determine seed moisture content. The results confirm that Encephalartos cycad storage is scant, therefore limiting number of experimental samples in each seed are desiccation sensitive, as stated by conservation efforts. This preliminary study species is (n =10). Berjak and Pammenter (2008) & Chin et al. is aimed at broadening the understanding of (1989), and seed viability drops with an cycad seeds longevity in storage. Results and Discussion increase in years of storage. Seed moisture is considered to be one of the Materials and Methods important factors determining seed longevity Seed viability drops in the second year and The research was conducted in 2018 at (Baskin & Baskin, 2007). Results show that, none are viable after seven years, a result Kirstenbosch National Botanical Garden Encephalartos seed species stored for one consistent with desiccation sensitive seed (KNBG) to determine seed longevity of year had variation of <5%amongst the two behaviour. However, E. aemulans seed different Encephalartos cycad species, by species E. altensteinii and E. horridus (Fig. stored for three years was inconsistent with analysing seed moisture content and 2). However, seeds stored between two and seed desiccation storage period compared to viability in seed stored at different periods. seven years showed consistent drop one and two years storage. Perhaps the Encephalartos were hand pollinated and amongst the four species tested with an inconsistency is a result of original harvested upon naturally disintegrating. average mean of 21%. The results also environmental conditions (Osborne, 1995) Seed was cleaned and stored at 15RH and show that there is significant difference in and genetic variation of different species. 15°C at KNBG Seed Department. seed moisture content of different Seeds stored for seven (7) years tend to be Encephalartos seed of the six species, that Encephalartos seed stored over different non-viable. were available at the time at KNBG, were periods (in years) (ANOVA, P < 0.05), used for the experiment, included E. however, seed moisture content in

Figure 1. Results of seed viability test in Encephalartos aemulans, (left) example of viable seed with pink stain embryos, (right) example of non-viable seed with no colour stain.

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Figure 2. Seed moisture content and seed viability in Encephalartos seed stored at different years. Al = Encephalartos altensteinii, Ho = Encephalartos horridus, TR = Encephalartos trispinosus, AE = Encephalartos aemulans, LE = Encephalartos lebomboensis, NA= . Trend lines indicating drop in seed moisture content and seed viability. Seed stored at 15%RH and 15°C, each species (n =10).

Conclusion deCarvalho. T.C., de Souza Grzybowski, C.R., Schutte, B.J., Regnier, E.E & Harrison, S.K. From the results presented above, it can be de Castro Ohlson, O. & Panobianco, M. 2008.The association between seed size concluded that seeds of Encephalartos 2014.Adaptation of the tetrazolium test and seed longevity among maternal species loose viability as years of storage method for estimating the viability of families in Ambrosia trifida L. increases, therefore consistent with reports sorghum seeds. Journal of Seed Science popoulations. Cambridge University of desiccation sensitive seeds. Moisture 36 (1): 246–252. Press 18 (4): 201–211. content of the seeds consistently drops with Donaldson, J. 2008. South African Tang, J & Sokhananj, S. 1991. years of storage, as seeds stored at greater Encephalartos Species. Available on: Determination of moisture content of years (seven years) had the least moisture https://cites.unia.es/file.php/1/files/WG whole kernel lentil by oven method. content among the species. Encephalartos 3-CS4.pdf. Accessed [14 Nov 2019]. Transaction of the ASAE 34 (1): 255– cycad seeds remain viable for a short period Farrant, J.M., Pammenter, N.W. & Berjak, P. 256. of time, optimum one year and no viability at 1989. Germination-associated events Tweddle, J.C., Dickie, J.B., Baskin, C.C. & seven years. However, Encephalartos cycad and the desiccation sensitivity of Baskin, J.M. 2003.Ecological aspects of seed viability in controlled storage varies recalcitrant seeds – a study on three seed desiccation sensitivity. Journal of with species over time of storage. This trend unrelated species. Planta 178: 189–198. Ecology 91: 294–304. needs to be further investigated; particularly Forsyth, C. & Van Staden, J. 1983. Woodenberg, W., Erdery, D., Pammenter, N. is highly threatened species, so as to Germination of cycad seeds. South W. & Berjak, P. 2007. Post-shedding optimise conservation. African Journal of Science 79: p. 8-9. seed behaviour of selected International Union for Conservation of Encephalartos species. South African References Nature Red List. 2010. The IUCN Red List Journal of Botany 73: p. 496. Ambika, S., Monomani, V & Somasundaram, of Threatened Species October 2010 G. 2014. Review on effect of seed size update, Cycad facts. Available on: on seedling vigour and seed yield. https://www.iucn.org/downloads/cycad Ngawethu Ngaka Research Journal of Seed Science 7 (2): _factsheet_final.pdf. Accessed [14 Nov Phakamani Xaba 31-38. 2019]. Kirstenbosch National Botanical Garden, Baskin, C.C. & Baskin, J.M. 2001. SEEDS McDonald, M.B. 2007. Seed moisture and South Africa ecology, biogeography, and evolution of the equilibrium seed moisture content ✉ [email protected] dormancy and germination.1st ed. curve. Seed Technology 29 (1): 7–18.

Academic Press, San Deigo and London. Rajjou, L. & Debeaujon, I. 2008. Seed Berjak, P. & Pammenter, N.W. 2008.Seed longevity: Survival and maintenance of Recalcitrance in perspective. Annals of high germination ability of dry seeds. Botany 101: 213–228. Biologies 331: 796–805.

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MEETING REPORT

This year, the workshop was held from the 13-19 October at Kanchanaburi, Western Thailand and also at Nong Nooch main garden in Pattaya, Thailand. The workshop was attended by 39 participants from 11 countries. The participants enjoyed a guided tour of the extensive and world class cycad propagation and collections of cycads. Hands-on sessions with hand pollination, pollen collecting and storage as well as seed storage and even grafting of cycads were demonstrated.

A fantastic selection of speakers presented and shared their knowledge about cycad horticulture, Paul Mills from Ganna Walska Lotusland, U.S.A. was talking about their cultivation and propagation of Encephalartos heenanii, Gary Roberson from Huntington Botanical Garden, U.S.A. showed the latest Anders with participants of the workshop landscape developments including the Cycad walk dedicated to the late Loren Whitelock. Growth rate of cycads and its application to At the 1st Cycad Horticulture workshop in climate change was presented by 2016, all participants contributed with their UPhakamani Xaba from Kirstenbosch knowledge to cycad horticulture and all this Botanical Garden, South Africa and ground data was summarized by Willie Tang into an breaking pollen germination studies were updated version of his cycad horticulture presented by Anna Nebot, Spain. booklet and was released during the workshop. Presentations from private gardens and collectors by Chip Jones, U.S.A. and we Anders Lindstrom learned how to transplant giant cycads from Nong Nooch Tropical Garden, Thailand Hendrik Wentzel, South Africa. ✉ [email protected]

25 MEETING REPORT

Photo by Jennifer Schwenk

The application of genomic tools to plant funding support from the SDZG Priority under what conditions genetic rescue of a conservation is advancing our ability to Species Project. Forty-eight attendees from species should be attempted, how long an make informed decisions about management across the U.S. including representatives intervention should continue, and what and reintroduction of rare and endangered from botanical gardens, research institutes, levels of survivability should be expected. species. To advance San Diego Zoo Global’s universities, plant nurseries, and Participants further deliberated over how to (SDZG) mission of saving species worldwide, government agencies convened to discuss best represent genetic diversity across plant conservationists at SDZG are their latest research programs, how genomic species within live collections and seed harnessing genomic information to guide research can be applied to conservation of banks, how to bridge lab-work with management of threatened species both endangered plant species, and how to conservation action, and plant-specific within the zoo’s extensive horticultural overcome common research, analytical, and climate related concerns. collection and within natural plant bioinformatic challenges. Much of the presented research was populations of conservation concern. While genomic data can greatly benefit Small groups formed to brainstorm about focused on cycads, IUCN red-listed priority management decisions, plant species solutions to common problems and share species at the zoo. Cycad-specific talks provide unique challenges, from difficulties resources. Discussions involved what covered conservation genetics, population sequencing and bioinformatic pipeline distribution, and other conservation obtaining genetic material to the analysis of methods worked for plants, as well as those concerns. A core group of cycad focused large and complex genomes. In recognition that did not. For example, many of the individuals, including Jeff Chemnick, Manuel of the difficulties inherent to plant genomic research and the importance of conserving bioinformatic pipelines that are currently Luján, Paul Mills, Stephanie Shigematsu, plant species, Christy Powell (SDZG being used were developed for diploid Christy Powell, Mike Diaz, Michael Letzring, organisms thus polyploidy presents unique Ruby Iacuaniello and Vanessa Handley Horticulture) and Caroline (Ruby) Iacuaniello complications. Another topic that was gathered to discuss cycad-specific issues. (SDZG Plant Conservation) led a Plant addressed was genetic rescue, with One large challenge to cycad management is Conservation Genetics Workshop with consideration being given to when and that natural seed production is not possible

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for some species due to distance between individuals. In order to assist reproduction, compatible pollen must be accessible when threatened cycads set cones. A database of individual plants, pollen, and seed availability would offer a possible solution to this problem. How to best create such a database and the specific difficulties surrounding individual plants in private collections was deliberated over. Other stated concerns included the anthropogenic loss of cycad habitat, changing climate conditions, and the likelihood of increasing fire frequency. Separately, a conversation was started about how to best transfer a collection of cycads including Encephalartos kisambo, Encephalartos turneri, and Encephalartos arenarius from the U.C. Botanical Garden to the San Diego Zoo and the Huntington Botanical Gardens.

Overall, plant conservation researchers built many new connections, shared a multitude of resources, and generated many new ideas about how to better apply genomic tools to the conservation of endangered plants. Generous support from an Institute Museum and Library Services grant to the Center for Plant Conservation allowed many of the presentations to be filmed; these are available for viewing at https://academy.saveplants.org/tag/plant- conservation-genetics-workshop-2019.

Caroline Iacuaniello Stephanie Steele Christy Powell San Diego Zoo, California, USA Encephalartos latifrons at the San Diego Zoo. Photo by Christy Powell ✉[email protected]

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IUCN/SSC Cycad Specialist Group Members

Alan Meerow Chip Jones Fernando Nicolalde-Morejón [email protected] [email protected] [email protected] USDA-ARS-SHRS, National Germplasm Instituto de Investigaciones Biológicas Repository Miami, Florida, U.S.A. Christopher Krieg Universidad Veracruzana Xalapa, Veracruz, University of Florida Mexico Alberto Taylor [email protected] [email protected] Gabriel Brull Puebla Facultad de Ciencias Naturales, Exactas y Christy Powell [email protected] Tecnología Universidad de Panamá Panamá, San Diego Zoo Global Empresa Nacional para la Protección de la Panamá [email protected] San Diego, Flora y la Fauna (ENPFF) MINAG Cuba California, USA Alicia Wain George Sparkman Ecologia Cristina Lopez-Gallego [email protected] [email protected] [email protected] Fallbrook, California, U.S.A. Instituto de Biología Universidad de Antioquia Anders Lindstrom Medellín, Antioquia, Colombia Irene Terry [email protected] [email protected] Nong Nooch Tropical Botanical Garden De Wet Bösenberg Department of Biology University of Utah Salt Sattahip, Chonburi, Thailand [email protected] Lake City, Utah, U.S.A. South African National Biodiversity Institute Andrew Vovides Kirstenbosch National Botanical Garden Cape JS Khuraijam [email protected] Town, South Africa [email protected] Laboratorio de Biología Evolutiva Instituto de Botanic Garden, CSIR-National Botanical Ecología, A.C. Xalapa, Veracruz, Mexico Dennis Stevenson Research Institute Lucknow, India [email protected] Angélica Cibrian Jaramillo The New York Botanical Garden Bronx, New James Clugston [email protected] York, U.S.A. [email protected] Langebio Cinvestav Guanajuato, México Royal Botanic Garden Edinburgh Edinburgh, Doris Francis United Kingdom Anita Varghese [email protected] [email protected] Javier Francisco-Ortega Keystone Foundation Nilgiris District, Esperanza M. Agoo [email protected] Tamil Nadu, India [email protected] Department of Biological Sciences Florida Biology Department De La Salle University International University Miami, Florida, U.S.A. Brian Dorsey Manila, Philippines Fairchild Tropical Botanical Garden Miami, [email protected] Florida, U.S.A. The Huntington Library, Art Collections and Botanical Gardens

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Jeff Chemnick Miguel Pérez-Farrera Roy Osborne [email protected] [email protected] [email protected] Santa Barbara California, U.S.A. Herbario Eizi Matuda (HEM) Instituto de Founder of Cycad Society of South Africa Ciencias Biológicas Universidad de Ciencias y Senior Chemist, Queensland Government John Donaldson Artes de Chiapas Tuxtla Gutierrez, Chiapas, [email protected] Mexico Santiago Mario Vázquez Torres South African National Biodiversity Institute [email protected] Kirstenbosch National Botanical Garden Cape Mike Diaz Instituto de Investigaciones Biológicas Town, South Africa San Diego Zoo Global [email protected] Universidad Veracruzana Xalapa, Veracruz, San Diego, California, USA Mexico Jorge González Astorga [email protected] Nathalie S. Nagalingum Terence Suninuy Laboratorio de Genética de Poblaciones [email protected] [email protected] Instituto de Ecología, A. C. Xalapa, Veracruz, California Academy of Sciences Mexico Tien Hiep Nguyen Patrick Griffith [email protected] Jorge Mendieta [email protected] Vietnam Center for Plant Conservation Ha Noi, [email protected] Montgomery Botanical Center Coral Gables, Vietnam Florida, U.S.A. José Said Gutiérrez-Ortega Tim Gregory [email protected] Paul Forster [email protected] Department of Biology, Chiba University [email protected] Brisbane Botanic UC Berkeley Botanical Garden Berkeley, Chiba, Japan Gardens Toowong, Queensland, Australia California, U.S.A.

Julio Lazcano Lara Paul Mills Tim Uebergang [email protected] [email protected] The University of Melbourne Departamento de Biología Universidad de Ganna Walska Lotusland Santa Barbara, [email protected] Puerto Rico, Río Piedras San Juan, Puerto Rico California, U.S.A. Tommie Steyn Leonie Stanberg Phakamani Xaba [email protected] [email protected] [email protected] Mpumalanga Tourism and Parks Agency Royal Botanic Gardens& Domain Trust South African National Biodiversity Institute Sydney, Australia Kirstenbosch National Botanical Garden Cape Tracy Magellan Town, South Africa [email protected] Li Nan Montgomery Botanical Center Coral Gables, [email protected] Quentin Luke Florida, U.S.A. Shenzhen Key Lab on Biodiversity of Southern [email protected] Subtropical Plant Diversity Fairylake Botanical East African Herbarium National Museums of Vanessa Handley Garden, Shenzhen & CAS Shenzhen, China Kenya Nairobi, Kenya [email protected] University of California Botanic Garden Maria Ydelia Sánchez Tinoco Ramona Oviedo Prieto Berkeley, California, U.S.A. [email protected] [email protected] Laboratorio de Anatomía Vegetal Instituto de Instituto de Ecología y Sistemática (CITMA) Willie Tang Investigaciones Biológicas Universidad Cuba [email protected] Veracruzana 91000 Xalapa, Veracruz, México USDA APHIS PPQ South Florida Miami, Rita Singh Florida, U.S.A. Mark Bonta [email protected] [email protected] University School of Environment Management Wynand van Eeden GGS Indraprastha University New Delhi, India University of Stellenbosch Michael Calonje [email protected] [email protected] Rosane Segalla Montgomery Botanical Center Coral Gables, [email protected] Florida, U.S.A. Instituto Federal de Educação, Ciência e Tecnologia de Mato Grosso

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Dioon caputoi Photo by Takuro Ito

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Cycas siamensis, Kanchanaburi, Thailand. Photo by Simon Lavaud

CYCADS I Volume IV I Issue 2 I December 2019

Encephalartos middelburgensis Middelburg, Mpumalanga, South Africa

ISSN 2473-442X

Official newsletter of IUCN/SSC Cycad Specialist Group Vol. IV I Issue 1 I October 2019

Website: http://www.cycadgroup.org

ISSN 2473-442X

Official newsletter of IUCN/SSC Cycad Specialist Group Vol. IV I Issue 2 I December 2019

CYCADS I Volume IV I Issue 2 I December 2019 Website: http://www.cycadgroup.org