ISSN 2473-442X CONTENTS

Message from Dr. Patrick Griffith, Co-chair, IUCN/SSC CSG 3 Official newsletter of IUCN/SSC Specialist Group Feature Articles Vol. IV I Issue 1 I October 2019 New report of Eumaeus (: ) associated with boliviana, a cycad from Brazil and Bolivia 5 Rosane Segalla & Patrícia Morellato The Mexican National Cycad Collection 45 years on 7 Andrew P. Vovides, Carlos Iglesias & Miguel A. Pérez-Farrera

Research and Conservation News Speciation processes in Mexican : our research progress on the 10 José Said Gutiérrez-Ortega, María Magdalena Salinas-Rodrígue, Miguel Angel Pérez-Farrera & Andrew P. Vovides Cycad’s and conservation in Thailand 12 Anders Lindstrom Ancestral characteristics in modern cycads 13

The Cycad Specialist Group (CSG) is a M. Ydelia Sánchez-Tinoco, Andrew P. Vovides & H. Araceli Zavaleta-Mancera component of the IUCN Payments for services (PES). A new alternative for conservation of mexican Survival Commission (IUCN/SSC). It cycads. norstogii a case study 16 consists of a group of volunteer experts addressing conservation Miguel A. Pérez-Farrera, Héctor Gómez-Dominguez, Ana V. Mandri-Rohen & issues related to cycads, a highly Andrómeda Rivera-Castañeda threatened group of land . The CSG exists to bring together the CSG Members 21 world’s cycad conservation expertise, and to disseminate this expertise to organizations and agencies which can use this guidance to advance cycad conservation.

Official website of CSG: http://www.cycadgroup.org/

Co-Chairs John Donaldson Patrick Griffith

Vice Chairs Michael Calonje All contributions published in Cycads are reviewed and edited by IUCN/SSC CSG Newsletter Committee and Cristina Lopez-Gallego members. IUCN/SSC CSG members can send contributions to [email protected]

Red List Authority Coordinator Cycads, the Official newsletter of IUCN/SSC Cycad Specialist Group De Wet Bosenberg ISSN 2473-442X © IUCN/SSC Cycad Specialist Group Frequency: Twice a year. Available online at http://cycadgroup.org/ CSG Newsletter Committee JS Khuraijam, Editor CSG Programme Office: Montgomery Botanical Center, 11901 Old Cutler Road, Coral Gables, FL 33156, USA

Irene Terry Andrew P. Vovides Jose Said Gutierrez-Ortega Cristina Lopez-Gallego Li Nan Maria Ydelia Sánchez-Tinoco Nguyen Tien Hiep Rita Singh

Cover photos Front: siamensis at Kanchanaburi, Thailand Back: Cycas laotica at Khammouan, Laos Photos by JS Khuraijam

Design & layout: JS Khuraijam Copy Editors: M Calonje & JS Khuraijam at Chiapas, Photo by Chip Jones

CYCADS I Volume IV I Issue 1 I October 2019

MESSAGE

Cycas cairnsiana in Queensland, ; I was honored to have the privilege to work with Manuel Lujan Anzola and Nathalie Nagalingum this year. Their innovative survey and genetic methods build a greater understanding of Cycas conservation – I anticipate you will read the results in a future issue!

Dear Friends,

I write this letter from the IUCN/SSC Leaders’ Meeting in Abu Dhabi. Some of our Cycad Specialist Group are attending, and it is great to catch up and to absorb the great energy and enthusiasm here for Species Conservation. Our cycad group is moving forward solidly, and this gathering provides inspiration on how to further advance our efforts on behalf of the cycads.

I am excited to share CYCADS volume 4 with you! These pages contain a diverse selection of current science on the geography, evolution, and conservation of these living treasures. Two feature articles present an important advance in cycad ecology from Brazil, as well as a historical retrospective on the Mexican National Cycad Collection. The history provided by Dr. Vovides and his colleagues highlights the great value in collaboration among organizations and people to advance cycad science and conservation – those international links forged over the decades will create further successes

Please let me also make an important announcement: the PROCEEDINGS OF CYCAD 2015 are on the way! We will publish this work as a special upcoming volume of CYCADS. Thank you to all who have submitted their papers – I look forward to sharing these with you very soon. It will be great to add this anthology to the unbroken chain of volumes going back to the very first cycad conference – another example of how our Cycad Specialist Group keeps doing great things.

Here, among the gathered worldwide leaders of dozens of Specialist Groups, our TEAM CYCAD is held up as an example of a high- functioning, well-organized and productive network. Bravo – you earned those compliments! The diligent work of each member (see page 21) acting in concert moves cycad conservation forward. It is wonderful to be a part of such a great team – let’s keep that great momentum as we enter the next decade!

Thank you,

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

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Zamia at Bajo Calima, Valle del Cauca, Colombia. Photo by Michael Calonje

4 FEATURE ARTICLE

The species of the genus Eumaeus Hübner, neurophyllidia D.W.Stev., (Segalla et al., 2019; Skelley & Segalla 2019, 1819 (Lepidoptera: Lycaenidae) are obligate- Miq. (DeVries 1976, 1983; Clark & Clark,1991; Segalla et al. 2019). herbivores, in the larval stage, of many Clark et al. 1992;Castillo-Guevara & Rico- Neotropical (Clark et al. 1992; Gray, 2002), Zamia encephalartoides The occurrence of E. minyas in populations of González, 2004; Castillo-Guevara, 2007; D.W.Stev. (González, 2004) and also of Dioon Z. boliviana has been recorded in situ in the Cascante-Marín & Araya, 2012; Prado et al., edule Lindl.(Castillo-Guevara, 2007). state of Mato Grosso, Brazil, over the last 2014; Ruiz-García et al., 2015). They exhibit four years and results suggest a stable co- gregarious behavior and their bright colors Zamia boliviana (Brongn.) A.DC. (Cycadales, occurrence in cycad populations of different are thought to be aposematic, serving as a Zamiaceae) occupies a distribution range cerrado areas. Voucher material has been warning signal to predators (DeVries 1977; between Bolivia (Beni, Cochabamba, La Paz deposited in the entomological collections of Bowers & Larin, 1989; Nash et al., 1992). and Santa Cruz) and Brazil, in the state of Museu de Zoologia of Universidade of São Lepidoptera, generally, are commonly studied Mato Grosso (Jørgensen et al. 2014; Skelley Paulo (MZUSP) and at the Laboratório de for their interactions with their hosts & Segalla 2019; Segalla & Calonje 2019; Scarabaeoidologia (Setor de Entomologia da (Castillo-Guevara 2007), however, many Segalla et al. 2019). The species is a small Coleção Zoológica, UFMT), Instituto de interactions between plants and , plant, up to 80cm tall, with a subterranean Biociências, Universidade Federal de Mato especially those involving cycads, are poorly stem, and 1 to 3 per crown. It inhabits Grosso, Cuiabá, Mato Grosso, Brazil. Eggs, documented in . different Cerrado (the Brazilian savanna) adults and different instars of larvae were phytosiognomies, from scrubland to observed in Z. boliviana plants (Fig. 1). Eumaeus minyas Hübn. is distributed from woodlands, across different types of , Oviposition occurred on vegetative and Mexico to Colombia, in South America and is and also on rocky outcrops (Skelley & Segalla reproductive parts of the cycad, with eggs exclusively involved in herbivory of Zamia 2019). Many populations have been being present on , petioles, leaflets feeding on of and female reproductive decimated or severely fragmented due to the and rachis, pollen and ovulate strobilus of L.f., Zamia expansion of extensive agriculture and strobilus (Fig. 1). skinneri Warsz. ex A.Dietr., Zamia ranching activities in Brazil but also Bolivia

Figure 1. Eumaeus minyas in vegetative and reproductive parts of Zamia boliviana: A-B. eggs on cataphylls and a recent emerged , C-D. larvae on petioles and , E-F. larvae on pollen strobilus and ovulate strobilus G. pupae in the abaxial side of a leaf and H. adult onZ. boliviana leaf. All photos from Cáceres, Mato Grosso State, Brazil. (Photos: Rosane Segalla).

5 Lycaenidae) a predator deterrrent? lepidoptera. Phytochemistry 31: 1955- Despite the few studies on the ecology of this Interciencia 27: 465-470. 1957. lycaenid butterfly in South America, we can Castillo-Guevara, C. 2007. Herbivores and Prado, A., Sierra, A., Windsor, D. & J.C. Bede. infer that its geographical distribution occurs chemical defenses in cycads – an 2014. Leaf traits and Herbivory levels in a concomitantly with the distribution of the ecological and evolutionary approach. In: tropical , Zamia stevensonii populations of species of Zamia, their host Vovides, A.P., D.Wm. Stevenson, & R. (Zamiaceae). American Journal of plants species. The populations of E. minyas Osborne (eds), Proceedings of Cycad 2005 101: 437–447. appeared healthy, with all stages the 7th international conference on cycad Segalla, R. & M. Calonje. 2019. Zamia observed and an uninterrupted life cycle as . Memoirs of the New York brasiliensis, a new species of Zamia expected for natural populations (Fig. 1). Botanical Garden, 97: 87-103. New York. (Zamiaceae, Cycadales) from Mato However, the destruction of cycad habitats New York Botanical Garden Press. Grosso and Rondônia, Brazil. Phytotaxa threatens the survival of this endemic Clark, D.B. & Clark, D.A. 1991. Herbivores, 404 (1): 001–011. butterfly species, as it is an obligate herbivory, and plant phenology: patterns Segalla,R., Telles, F.J., Pinheiro, F. & L.P.C., herbivore which depends on these plants for and consequences in a tropical rain-forest Morellato. 2019. A review of current the completion of its life cycle. Our cycad. In Price, P.W, Lewinsohn, T.M, knowledge of Zamiaceae, with emphasis observations suggest that the butterfly Fernandes, G.W., Benson, W.W. (Eds.) on Zamia from South America. Tropical prefers to oviposit on immature expanding Plant- interactions: evolutionary Conservation Science, (accepted). leaves or young reproductive parts. We have ecology in Tropical and Temperate Skelley, P.E. & Segalla, R. 2019. A new evidence that the vegetative and reproductive Regions. John Wiley. New York. pp. 209- species of Reitter phenology of Z. boliviana is adapted to the 225. (Coleoptera: ) from central Cerrado seasonality and that E. minyas life Clark, D.B., Clark, D.A. & M.H. Grayum. 1992. South America. Zootaxa 4590 (1): 184– cycle is in synchronicity with the emergence Leaf demography of a Neotropical rain 190. and development of Z. boliviana leaves and forest cycad, (Zamiaceae). Ruiz-García, N.,Méndez-Pérez, B.Y., Velasco- strobilus. American Journal of Botany 79(1): 28–33. García, M.V., Sánchez-de laVega, G. & DeVries, P.J. 1976. Notes on the behavior of J.L. Rivera-Nava. 2015. Distribución, ciclo Acknowledgements Eumaeus minyas (Hübn.) (Lepidoptera: biológico y tabla de vida de Eumaeus We thank Marcelo Duarte da Silva, curator of Lycaenidae) in Costa Rica. Brenesia 8: toxea (Lepidoptera: Lycaenidae) Lepidoptera of Museu de Zoologia of 103. enlaprovinciafisiográfica Costa de Universidade de São Paulo (MZUSP) and DeVries, P.J. 1977. Eumaeus minyas Hübner: Oaxaca, México. Revista Mexicana de Alexandre dos Santos of Laboratório de anaposematic lycaenid butterfly. Brenesia Biodiversidad 86: 998–1003. Fitossanidade of Instituto Federal de 12(13): 269-270.

Educação, Ciência e Tecnologia de Mato DeVries, P.J. 1983. Zamia skinneri and Zamia Grosso (IFMT), Campus Cáceres, Mato Grosso fairchildiana (zamia, palmera siempre Rosane Segalla for the support with the entomological verde, cycad). In Janzen, D.H. (Ed.) Costa Instituto Federal de Educação, Ciênciae specimens and their identification. We thank Rican Natural History. University Chicago Tecnologia de Mato Grosso, the IFMT for supporting the development of Press. Chicago. pp. 349-350. Campus Cáceres, Mato Grosso, Brazil. Email.: the doctoral thesis of the first author. LPCM González, F. 2004. Herbivoríaen una [email protected] receives a research productivity fellowship gimnosperma endémica de Colombia, from National Council for Scientific and Zamia encephalartoides (Zamiaceae) por Patrícia Morellato Technological Development (CNPq). We thank parte de Eumaeus (Lepidoptera: Universidade Estadual Paulista UNESP, Michael Calonje and Irene Terry for the Lycaenidae). Revista de la Academia Instituto de Biociências, Departamento de comments in the text. Colombiana de Ciencias Exactas, Fisicas y Botânica, Laboratório de Fenologia, CEP: Naturales 28(7): 233–244. 13506-900, Rio Claro, SP, Brazil References Jørgensen, P.M., Nee, M.H. & S.G. Beck. Bowers, M.D. & Z. Larin. 1989. Acquired 2014.Catálogo de las plantas vasculares chemical defense in the lycaenid de Bolivia. Monographs in Systematic butterfly, . Journal of Botany from the Missouri Botanical Chemical Ecology 15(4): 1133-1146. Garden 127 (1–2), i-viii, 1–1744. Castillo-Guevara, C. & V. Rico-Gray. 2002. Is Nash, R.J., Bell, E.A. & P.R. Ackery. 1992. The Cycasin in Eumaeus minyas (Lepidoptera: protective role of cycasin in cycad-feeding

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FEATURE ARTICLE

The Mexican National Cycad Collection at the Jardín Botánicos Francisco Javier Clavijero, Xalapa

Cycads are one of the world´s most the City of Xalapa (JBC), Veracruz began in University of Florida, Gainesville, thus we endangered plant species largely owing to 1975 with with the JBC collected living and dried material for the human activities leading to habitat accessions number 1975-002 collected near herbarium, the living material accessed into destruction and collecting by commercial the classical locality of Chavarillo where C.J. JBC to form the National Collection. Several horticulturists as well as enthusiasts. They Chamberlain once collected at the turn of new species were discovered and described. are listed in the IUCN Red List (IUCN 2019). the XXth century (Chamberlain 1919). I was When the JBC passed to the administration Their distribution is within the tropical and set the task by Arturo Gómez-Pompa the of INECOL in 1989 explorations continued sub tropical regions of the world in Asia, Director of the then biotic resources throughout the 1990´s to mid 2000s. During , , the Americas and research institute (INIREB) to work on the this transition period 1989–1990, Andrew Oceania with 355 species among ten genera Flora de Veracruz project Zamiaceae fascicle Vovides was Post Doc at Fairchild Tropical (Calonje et al., 2019). Mexico is home to 61 (Vovides et al., 1983) in collaboration with Garden (now Fairchild Tropical Botanic spp making it 2nd worldwide for species John D. Rees, a geographer form California Garden FTBG) researching cycad diversity after Australia with 87 spp State University knowledgeable on cycad syndrome with Knut Norstog and Priscilla followed by S. Africa with 39 spp. distribution and localities in Mexico and Fawcett. A Sister Garden relationship was . We did field explorations initiated in 1989 with FTBG with aims for The beginning of what was to become the in the mid 1970s and early 80s then later in plant exchange, teaching and research Mexican National Cycad Collection at the collaboration with Bart Schutzman of the projects. During the early to mid 2000s Jardín Botánico Francisco Javier Clavijero in

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collaboration with the Montgomery years we learned much about growth rate plant sales and reintroduction of plants back Botanical Center, botanical explorations and life cycle of Dioon edule as well as into habitat (Vovides et al., 2010). further incremented our living collections becoming aware of poaching through with duplicate plant material. With plant decapitation of leaf crowns for sale by street exchange we managed to have in our peddlers (Vovides, 1990; Octavio-Aguilar et national collection cycad species from Africa al., 2008) an illegal activity since cycads are ( and ), Australia protected by national legislation regarding ( and ) West Indian threatened and . and Central American as well as Asian Cycas spp. Needless to say both We learned basic cultivation and institutions are CITES registered. The well- propagation skills a rural nursery was set up documented National Cycad Collection has with the collaboration of local inhabitants at given support to researchers requiring plant Monte Oscuro in the Chavarillo district. In material for molecular studies and this area poaching of D. edule crowns systematics, anatomy, cytotaxonomy, occured for almost 30 years and the farmers palynology, and physiology discouraged this. Similar nurseries were set (Vergara et al., 2002; Vovides and Olivares, up in Chiapas state for the propagation of 1996; Gutiérrez-Ortega et al., 2014, 2017). Dioon merolae, Ceratozamia mirandae, C. matudae and Zamia soconuscensis. The Through cultivating cycads much experience idea of these nurseries is to encourage had been gained regarding propagation form conservation through propagation from and offsets, compost mixtures, where farmers have incentive to conserve The Rhopalotria mollis on fertilization and pest control. Ecological and the cycad habitat through benefits from Zamia furfuracea male cone. demographic studies over a period of several

Cycad propagation nursery at El Triunfo Biosphere Reserve, Chiapas

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References of the Mexican cycad Dioon edule Lindl. Vovides, A.P., Pérez-Farrera, M.A. & C. Calonje, M, Stevenson, D.W. & R. Osborne. (Zamiaceae): life history stages and Iglesias. 2010. Cycad propagation by 2013-2019. The World List of Cycads, management impact. Botanical Journal rural nurseries in Mexico as an online edition [Internet]. [cited 2019 Jul of the Linnean Society 157: 381-391. alternative conservation strategy: 20 11]. Available from: www.cycadlist.org. Vergara Silva, F., Iglesias, C. & A.P. Vovides. years on. Kew Bulletin 65: 603-611. IUCN 2019. The IUCN Red List of Threatened 2002. La Colección Nacional de Cícadas Vovides, A.P., J.D. Rees, & M. Vázquez- Species. Version 2019-1 del Jardín Clavijero y la investigación de Torres. 1983. Zamiaceae. In: Gómez-

Dioon merolae in Chiapas, Mexico. Photo by Michael Calonje

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RESEARCH & CONSERVATION NEWS

The idea that extant cycad genera had Because branching in phylogenetic important suggestions for effective synchronous bursts of diversification during represent events of lineage divergence, conservation (e. g. Meerow et al., 2018). the Cenozoic era has been well supported by phylogenetic methods are useful to multiple recent studies that have applied understand the spatial and temporal patterns A first case that called our attention is that phylogenetic methods (e. g. Nagalingum et in cycad evolution. However, speciation is a occurring within the species Dioon merolae. al., 2011; Salas-Leiva et al., 2013). This process that occurs at the population level, Dioon merolae occurs at both sides of the evidence is interesting, because it implies and it is influenced by demographic history, Isthmus of Tehuantepec, which is one of the that all modern cycad species evolved in the ecological relationships and natural most important geographic barriers same niches that better favored the selection regimes, which are factors not promoting allopatric divergence in many evolution of angiosperms: whereas easily detected by phylogenetic methods. plant and animal taxa in Mexico (Peterson et angiosperms became the dominant plant Therefore, revealing the mechanisms that al., 1999). This isthmus separates the D. group on Earth, cycads were restricted to occur during the inter-species and inter- merolae populations into two geographic- very specific niches that allowed their population divergence is useful to ecological groups: the western populations persistence through evolutionary times. Yet, understand how and why speciation occurs. occur in tropical forests co-occurring with how did extant cycad genera persist and The obtained information from studies in xeric plant communities, whereas the diversify ? We are now trying to answer this speciation will not only contribute to reveal eastern populations occur in more mesic question by emphasizing on Mexican cycads. the origin of species and the validity of forests (Fig. 1). accepted taxa, but it will also provide

Figure 1. Dioon merolae is distributed in both sides of the Isthmus of Tehuantepec. The western populations are distributed in more arid environments than the eastern populations. The numbers of populations in each photo (Pop1—4) correspond to those indicated in the inset map. The base map was produced with GeoMapApp (http://www.geomapapp.org).

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Figure 2. Hypothetical speciation pathway that might be followed by Dioon merolae. Three populations are represented: West (left), Isthmus of Tehuantepec (center) and East (right). In the Stage 1, the three populations are assumed to be connected by ancestral humid forests (green shades). In Stage 2, aridification (yellow shade) starts, and dry conditions eliminate the population in the lowlands of the isthmus; this event separates the western and the eastern populations. In Stage 3, arid conditions reach the western population, promoting constant stabilizing selection. In Stage 4, the western side would be adapted to arid conditions, allowing for the distinction of the western population as a new species (in blue).

We ask whether the presence of the isthmus would like to encourage our colleagues to northern Mesoamerica. PloS One 8: and the different environmental conditions of also deal with the clarification of the e56283. both sides have influenced the divergence in mechanisms that produce speciation in other Peterson, A.T., Soberón, J. & V. Sánchez- D. merolae. We hypothesize that the cycads in Mexico or other countries around Cordero. 1999. Conservatism of divergence of D. merolae is following a the world. ecological niches in evolutionary time. speciation pathway that is described in Fig. Science 285: 1265–1267. 2: References Salas-Leiva, D.E., Meerow, A.W., Calonje, • Stage 1: In the past, D. merolae occupied Gutiérrez-Ortega, J.S., Yamamoto, T., M., Griffith, M.P., Francisco-Ortega, J., an ancestral niche in humid tropical Vovides, A.P., Pérez-Farrera, M.A., Nakamura, K., Stevenson, D.W., Lewis, forests (suggested in Gutiérrez-Ortega et Martínez, J.F., Molina-Freaner, F., C.E. & S. Namoff. 2013. Phylogeny of the al., 2018). Watano, Y. & T. Kajita. 2018b. cycads based on multiple single-copy Aridification as a driver of biodiversity: A nuclear genes: congruence of • Stage 2: Aridification of southern Mexico case study for the cycad genus Dioon concatenated parsimony, likelihood and made the Isthmus of Tehuantepec an (Zamiaceae). Annals of Botany 121: 47– species inference methods. Annals unsuitable habitat for Dioon (Ornelas et 60. of Botany 112: 1263–1278. al., 2013), maintaining D. merolae Meerow, A.W., Salas-Leiva, D.E., Calonje, populations in the mountainous areas and M., Francisco-Ortega, J., Griffith, M.P., José Said Gutiérrez-Ortega preventing gene flow between the two Nakamura, K., Jiménez-Rodríguez, F., Department of Biology, Faculty of Science, sides of the isthmus. Lawrus, J. & A. Oberli. 2018. Contrasting Chiba University, Chiba 263-8522, • Stage 3: Arid conditions reached the Demographic History and Population populations in the western side of the Structure of Zamia (Cycadales: María Magdalena Salinas-Rodríguez isthmus, promoting constant stabilizing Zamiaceae) on six islands of the Greater Herbario Jerzy Rzedowski, Facultad de selection through many generations in the Antilles suggests a model for population Ciencias Naturales, Universidad Autónoma western D. merolae. diversification in the Caribbean of de Querétaro, Querétaro 76221, Mexico • Stage 4. After many generations, the the genus. International Journal of Plant western side would gain adaptations to Sciences 179: 730–757. Miguel Angel Pérez-Farrera counteract aridity, allowing for the Nagalingum, N.S., Marshall, C.R., Quental, Laboratorio de Ecología Evolutiva, Herbario distinction of speciation. T.B., Rai, H.S., Little, D.P. & S. Mathews. Eizi Matuda, Instituto de Ciencias Biológicas, 2011. Recent synchronous radiation of a Universidad de Ciencias y Artes de Chiapas, With this hypothesis in mind, we are living . Science 334:796–799. Tuxtla Gutiérrez 29039, Mexico collecting evidence from morphological, Ornelas, J.F., Sosa, V., Soltis, D.E., Daza, genetic and environmental variables. When J.M., González, C., Soltis, P.S., Gutiérrez- Andrew P. Vovides we finish this first step with the Mexican Rodríguez, C., Espinosa de losMonteros, Departamento de Biología Evolutiva, cycad D. merolae, we believe our study will A., Castoe, T.A., Bell, C. et al. 2013. Instituto de Ecología, A.C., Xalapa 91070, clarify the history of a possible case of Comparative phylogeographic analyses Mexico incipient speciation in a cycad species. We illustrate the complex evolutionary history of threatened cloud forests of

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RESEARCH & CONSERVATION NEWS

Because cycads are dioecious the collection, of cycad pollen are of significant scientific, Encephalartos and Zamia) and assessed storage and creation of pollen banks for horticultural and conservation importance. viability after long-term storage in 22 medium to long-term preservation and Our project, supported by The Stanley Smith species. She tested earlier researchers’ germplasm exchange is highly desirable. (UK) Horticultural Trust and in collaboration media as well as added her own media for Indeed, artificial pollination is necessary in with Kew Millennium (UK) and trial. Germination was tested using several cycad ex situ collections to ensure the Mahidol University (Thailand), aims to media and the initial result was that setting of viable seed. Several recent assess the pollen quality (by in vitro different species have their specific studies show that cycads are host specific germination) of a range of cycad species optimum media for germination. The and often pollinated by a specific pollinator after storage in the freezer, even as long as experiments were performed in Prof. Kanchit and thus habitat and location of ex situ 17 years Thammasiri’s laboratory at Mahidol collections may mean a lack of suitable University. In another project, supported by . Moreover, pollen preservation From February to April 2019, Anna Nebot the Mohammed bin Zayed Species could alleviate the risks from -change undertook research on the viability of cycad Conservation Fund, pollen quality is being induced asynchronous production of male pollen. In the six weeks she stayed in investigated in a critically endangered cycad and female cones of cycads. The long-term Thailand, she developed specific of Uganda. storage stability of cycad pollen is hardly germination conditions for 35 freshly known, yet recommendations on the banking harvested species (in the genera Cycas,

Figure 1. Anna Nebot, Anders Lindstrom, and Kanchit Thammasiri at Mahidol University (left); freshly harvested and stored Cycad pollen was tested for viability from species cultivated at Nong Nooch Tropical Botanical Gardens (right). Photos by Anna Nebot.

Team and collaborators Prof. Hugh W. Pritchard (Kew, UK), Dr. Daniel Ballesteros (Kew, UK), Dr. Anna Nebot (Kew, UK), Prof. Kanchit Thammasiri (Mahidol University, Bangkok, Thailand), Mr. Anders Lindstrom (Nong Nooch Tropical Botanical Garden, Thailand), Dennis Kamoga (JERA, Uganda)

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RESEARCH & CONSERVATION NEWS

Figure 1. Ceratozamia tenuis. Cross section of the nucellus in the micropylar region. Antherozoid (a) with cilliar bands (c), nucleus (n), starch grains inside the (s) and pollen tube (t). Stained with Safranin-fast green. (Scale bar=20 µm). (From Sánchez-Tinoco et al., 2000).

Cycads conserve ancestral characters and are efficient transport of the male Thomas, 1989). Another ancestral trait is the considered relicts from the past or “living toward the female gametophyte cytoplasm of stellar anatomy and pachycaulous habit with ”, however the living species today are the central cell thus later effecting very little , a throwback to the stellar of origin (Nagalium et al., 2011). fertilization of the egg cell (Norstog 1972; anatomy of the Medullosaceae (Greguss, Outstanding ancestral characters are the Sánchez-Tinoco et al., 2018) (Fig. 2). 1968, Nagalium et al., 2011). This contrasts ciliated and motile antherozoids, male and with adaptations of the living cycads female enclosed within micro- The dehiscence lines in the micropylar region considered derived, such as the contractile and respectively giving rise to an observed in the seed sclerotesta, support stem in some species of Zamia, the epiphytic independence of free for fertilization to Benson's synangial hypothesis, which habit in Zamia pseudoparasitica of the take place, in other words the seed habit. postulates the as a transformation of Panamanian rain forests, the central venation This harks back to the Pteridosperms or seed grouped sporangia and subsequent abortion in leaflets of the genera Cycas and Stangeria, of which the Medullosan ferns are of the peripheral sporangia, to form a ring of considered their ancestors (Ikeno, 1986; and transfusion tissue in leaflets of Cycas free tegumentary lobes surrounding a single Norstog and Nicholls, 1997; Sánchez-Tinoco (Brenner et al., 2003). central fertile megasporangium (Takhtajan, et al., 2000) (Fig. 1). Outstanding is the female sexual organ or archegonium, this is 1981; Sánchez-Tinoco & Engleman, 2004). The pachychalaza (fusion of tegument and nucellus) present in ¾ of the length of the embedded in tissue of the ovule or female The open female strobilus with several gametophyte. The archegonium resembles a ovule. According to Corner (1976), the course marginal of Cycas is reminiscent of flask, with a neck and body. The neck is of evolution was simplified, suggesting its the fossil Crossozamia (Gao & equipped with two neck-cells that assist the primitive character.

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Figure 2. Ceratozamia tenuis. Cross section of the archegonium in the micropylar region, growth stage of the central cell showing two neck cells with cell wall (w), cytoplasm (cy), nucleus (n), and nucleolus (arrow). Unstained. Free hand section. (Scale bar=40 µm).

among others, the synangial and large vacuole (lv), solid and amorphous neosynangial hypotheses on the origin of the tannin bodies (t) and parenchyma cells with ovule (Benson, 1904; Kenrick & Crane, 1997). starch grains (p). Stained with Safranin-fast green. (Scale bar=200 µm).

The fleshiness of the sarcotesta is a common character for the majority of seed-coats in the . In terms of phylogeny, seeds with this characteristic are considered primitive (Corner, 1976)). Large-sized cells with large nuclei and several nucleoli, observed in the transfer cells (archegonial jacket), the central cell and egg cell, considered the largest in the plant , are primitive (Figs. 3-4) (Maheswari & Singh, 1967; Sánchez-Tinoco et al, 2018).

We sustain that cycads are not living fossils,

Figure 3. Ceratozamia tenuis. Tangential although they maintain traits considered section of the archegonial jacket showing primitive, they are an integral part of transfer cells with cytoplasm (cy), nucleus (n), modern tropical and subtropical and nucleoli (arrows). Stained with Safranin- and provide benefits such as fast green. (Scale bar=20 µm). Figure 4. Ceratozamia tenuis. a. Longitudinal beneficial to their habitats (Grove et al. section of the gametophyte during the 1980). The only threat to their existence is The double vascular supply in cycad seeds is growth stage of the central cell showing an humanity, whose daily activities of habitat shared with and (Loconte archegonium with central cell (cc), destruction are driving cycads to . & Stevenson, 1990; Sánchez-Tinoco, et al., archegonial chamber (ac), transfer cells (tc) 2007). The stomata in the sarcotesta refer to forming the archegonial jacket (arrows), the origin of the tegument and supports, vacuolated cytoplasm of the central cell (cy),

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Acknowledgement Kenrick, P. & P.R. Crane. 1997. The Origin and transfer cells and the central cell during The authors give special acknowledgement Early Diversification of Land Plants: a its growth stages in Ceratozamia to the altruistic work of Dr. Timothy Gregory, Cladistic Study. Smithsonian Institution mexicana Brongn., and Zamia furfuracea who supports the professional training of Press.Washington and London.441 pp. L.f. (CYCADALES). Memoirs of the New those who contribute to the study of cycads. Loconte, H. & D.W. Stevenson. 1990. York Botanical Garden 117: 33-42. In particular, the doctorate of the first co- Cladistic of the spermatophyta. Brittonia Takhtajan, A.L. 1981. Flowering Plants.Origin author of this contribution. 42:197-211. and Dispersal. (Translated from the Maheshwari, P. & H. Singh. 1967. The female Russian). Bishen Singh Mahendra Pal References gametophyte of gymnosperms. Biological Singh & Otto Koeltz Science Publishers. Benson, M. 1904. Telangium scottii, a new Reviews 42:88-130. 310 pp. species of Telangium showing structure. Nagalingum N.S., Marshall, C.R., Quental, Zhifeng, G. & B.A. Thomas. 1989. A review of Annals of Botany 18:161-177. T.B., Rai, H.S., Little, D.P. & S. Mathews. fossil cycad megasporophylls, with new Brenner, E.D., Stevenson, D.W. & R.W. 2011. Recent Synchronous Radiation of a evidence of Crossozamia pomel and its Twigg. 2003. Cycads: evolutionary . Science, 334(11): 796-799. associated leaves from the Lower innovations and the role of plant-derived Norstog, K. 1972. Role of archegonial neck Permian of Taiyuan, .Review of . Trends in Plant Science 8(9): cells of Zamia and other cycads. Palaeobotany and Palynology 60(3- 446-452. Phytomorphology 22(2): 125-130. 4):205-223. Corner, E.J.H. 1976. The Seeds of the Norstog, K. & T.J. Nicholls. 1997. The Biology Dicotyledons. Vol. 2. Cambridge of the Cycads. Cornell University Press, University Press. London. 552 pp. Ithaca, NY. 363pp. M. Ydelia Sánchez-Tinoco Gao, Z. & B. A. Thomas. 1989.A review of Sánchez-Tinoco, M.Y., Engleman, E.M. & [email protected] fossil cycad megasporophylls, with new Vovides, P.A. 2000. Cronología Instituto de Investigaciones Biológicas, evidence of Crossozamia pomel and its reproductora de Ceratozamia mexicana Universidad Veracruzana associated leaves from the lower (Cycadales). Boletín de la Sociedad D. Sc., Colegio de Postgraduados permian of Taiyuan, China. Review of Botánica de México 66:15-23. Montecillo, Texcoco, Edo. de México, México Palaeobotany and Palynology 60 (3–4): Sánchez-Tinoco, M.Y. & Engleman, E.M. 205-223. 2004. Seed coat anatomy of Ceratozamia A.P. Vovides Greguss, P. 1968. Xylotomy of the Living mexicana (Cycadales). The Botanical Departamento de Biología Evolutiva, Instituto Cycads. Akadémiai Kiadó. 260 pp. Review 70(1): 24-38. de Ecología, A.C., México Grove, T.S., O´Connell, A.M. & N. Malajezuk. Sánchez-Tinoco, M.Y., Engleman, E.M. & S.D. 1980. Effects of fire on the growth, Koch. 2007. The vascularization of the H. Araceli Zavaleta-Mancera nutrient content and rate of nitrogen seed of Ceratozamia mexicana Botánica, Colegio de Postgraduados, fixation of the cycad . (Zamiaceae). Memoirs of the New York Montecillo, Texcoco, Edo. de México, México Australian Journal of Botany 28: 271-281. Botanical Garden 97: 223-235. Ikeno, S. 1896. Spermatozoiden von Cycas Sánchez-Tinoco, M.Y., Engleman, E.M. & A.P. revoluta. Botanical Magazine Tokyo 10: Vovides. 2018. Anatomical description of 367-368. the cytoplasmic connections between the

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RESEARCH & CONSERVATION NEWS

Mexico has the second highest diversity of cycad species (Vovides, 2000). Around 355 species have been recorded worldwide and in Mexico there are 62 of which more than 94% are endemic (Calonje et al., 2019) and more than 50% grow in southern Mexico.

One of the endemic and rarest species of cycads in southern Mexico is . It has aerial trunks, leaflets that are inserted into the rachis in spiral form,and extremely narrow (0.3-0.5 mm) chanelled leaflets. It grows in the or pine-oak forests of Chiapas and Oaxaca, Mexico between 800 and 1600 msl (Pérez- Farrera et al., 2001) (Fig. 1). This species, given its rarity, has a of Endangered (EN) by the IUCN (Vovides et al., 2010a) and Protected (P) by the Mexican conservation authorities through NOM-059- 2010 (SEMARNAT, 2010). It has been extensively studied from the systematic (Pérez-Farrera et al., 2004), ecological (Martínez-Meléndez 2012), genetic (Pérez- Farrera et al., 2017), anatomical and Figure 1. Ceratozamia norstogii in habitat morphological perspectives (Pérez-Farrera et al 2014). threatened species: 1) ex situ (the mechanism is the poor representation of the Although this species has been relatively propagation and conservation of species in phenotypic and genetic variation of the well studied, problems with the botanical gardens) (BGCI, 2015) and 2) in situ natural populations. conservation of its populations continue. (establishment of nurseries in situ) (Pérez- One year after its description by Stevenson, Farrera, 1999; Vovides et al., 1999; Vovides Regarding the conservation in-situ (1982) the species was widely collected; et al., 2002; Vovides et al., 2010c). mechanism, a network of in-situ nurseries Tang (1983) mentions that a shipment of has been established in Mexico. These 25,000 individuals of C. norstogii was With respect to conservation ex situ, in nurseries have been established as UMAs = confiscated in the , with the Mexico, it is known that C. norstogii is Management Units for the conservation of result that one of the two previously known protected in a few botanical gardens wildlife. This mechanism has been promoted populations was decimated. Currently about (Vovides et al 2010a; Vovides et al., 2013) by the Secretary of Environment and Natural seven populations of this species are known (National collection of cycad in the Botanical Resources (SEMARNAT) for several species, with few individuals. It grows in the Garden Francisco Javier Clavijero of the among which we can highlight Dioon Cintalapa and Ocozocoautla municipalities Instituto de Ecology AC, Xalapa, Veracruz; merolae, Ceratozamia mirandae, Zamia of Chiapas, and along the border of the Botanical Garden Faustino Miranda, Tuxtla soconuscensis in Chiapas, Dioon edule, Chimalapas, region of Oaxaca (Fig. 2) Gutiérrez, Chiapas and the Ethnobotanical Zamia furfuracea, Ceratozamia tenuis in Garden, in the city of Oaxaca). However, Veracruz, in Oaxaca, In Mexico, for the case of cycads, two main apparently this species is cultivated in some in Puebla, Dioon sonorense in alternatives have been put forward for their private gardens in the eastern United States. Sonora (Tang et al, 2018). Although this conservation and especially for the most One of the problems with this conservation scheme has the potential to greatly impact

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Figure 2. Geographic distribution of Ceratozamia norstogii in southern Mexico the pressure problems of the conservation of generation of some benefit derived from the is a civil association created in 2002 with natural populations, it has not had the operation of the ecosystem (such as carbon the objective of contributing to the economic impact and viability expected capture, conservation of biodiversity or conservation and sustainable development because of the bureaucratic problems that watersheds) through a payment or economic of the ecosystems represented in the El Semarnat itself has implemented for the compensation to the owners of the forests. Triunfo Biosphere Reserve and the Protected UMA mechanisms. This type of approach has yielded good Natural Areas of its area of influence. results on several continents, including FONCET supports financing strategic, long- In recent years a new conservation scheme several Latin American countries such as term project that seek to ensure the has been promoted for the conservation of Costa Rica and Brazil (Börner et al., 2011; conservation of the site and the forests in Mexico. Since 2002, this program Ezzine et al., 2017). The basis of the PES development of its inhabitants, contributions has been promoted by the Mexican mechanism is the model of the "polluter it’s goal is to achieve a harmonious and government through the National Forestry pays" principle: or "the one who conserves comprehensive development of the country Commission (CONAFOR). The concept receives compensation". and to preserve biodiversity for future consists of stimulating the conservation of generations as a heritage. lands or important forest areas by the The El Triunfo Conservation Fund (FONCET)

Figure 3. Geographical location of the properties under the PES project, approximately 14 hectares oak forest.

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development opportunities that would go We consider that this is a good opportunity beyond the years of payments. The results of to carry out a solid program of management this program surpassed the expectations, and conservation for this species and that and the learning led to create a similar the continued monitoring of its populations scheme for the conservation of areas where is of vital importance for the success and cycad populations were found viability of it’s long-term conservation.

In 2017 FONCET and the Herbarium Eizi Acknowledgement Matuda of the University of Sciences and The authors give special thanks to the Arts of Chiapas (UNICACH) joined efforts for anonymous donor who has awarded the the conservation of Ceratozamia norstogii. funds for the conservation of Ceratozamia Funds were received for a PES for 10 years norstogii through Payment for Ecosystem for the conservation of 14 hectares of oak Services (PES) to farmers in the forest where C. norstogii grows (Fig. 3). communities. The authors also wish to thank During that time the farmers will receive Maria Lourdes Gómez Tolosa and Sergio economic incentives to preserve and protect López Mendoza for their help in the the reserve and they will have to actively elaboration maps. conserve the cycad populations, technical Figure 4. Activities carried out by the assistant to address causes of deforestation, References farmers as part of the PES project (fire and finally education in to create BGCI. 2015. Cycads: a model group for ex breaks inside and outside the fences). conscious about the importance of the situ plant conservation. Botanic species, the forest and the ecosystem Gardens Conservation International, FONCET was created by the National services the area provides. Related to the Glencoe. Commission of Protected Natural Areas conservation of this species are associated Börner J., S. Wunder, A. Armas. 2011. (CONANP), the Directorate of the El Triunfo activities related to the conservation of their Pagos por carbono en América Latina: Biosphere Reserve (REBITRI), the Institute of habitat, such as: a) restoration of the oak de la experiencia de proyectos piloto a Natural History and Ecology (IHNE but forests where the cycad grows (assisted la implementación a gran escala. currently known as the Secretary of restoration), b) creation and maintenance of Revista Española de estudios Environment and History (SEMANH), the fire lines (Fig. 4), c ) creation of C. norstogii Agrosociales y Pesqueros. 228: 115- Mexican Fund for the Conservation of nurseries for propagation, and reintroduction 137. Nature (FMCN), Institute for Sustainable of seedlings to the habitat (Fig. 5). Likewise, Calonje M, Stevenson DW, Osborne R. The Development in Mesoamerica A.C. parallel to these activities are research World List of Cycads, online edition (IDESMAC), Pronatura Sur, and four private activities on the species with students and [Internet]. 2013-2019. [cited 2019 Mar individuals interested in the Fund (Alfredo herbarium researchers, among which are: a) 25]. Available from: www.cycadlist.org Cuarón, Claudia Virgen Montesinos, Fulvio assessment of the conservation status of the Ezzine. D., Le Coq J., A. Guevara Sangines. Eccardi and Alejandro Hernández Yañez). populations and the impact of the project on (coordinadores). (2017). Los pagos por its population dynamics, b) evaluation of servicios ambientales en América In 2008, FONCET and CONAFOR created a growth and survival of seedlings under Latina. Gobernanza, impactos y Matching Fund for ecosystem payments, different habitat conditions (rock, trunk, perspectivas. Universidad where the federal program was improve, as shrub, bare ), c) study on the structure, Iberoamericana AC, México DF. the payment was part of an holistic program composition, and floristic diversity of the oak Martínez-Meléndez M-. 2012. Ecología de that not only compensated the owner for forests, habitat of C. norstogii (Fig. 6) and d) poblaciones de Ceratozamia norstogii conserving their land, but also generated a evaluation and determination of other D.W. Stev. (Zamiaceae) en Cintalapa, model that would allow to identify the conservation elements (plants or animals) Chiapas. Tesis de Licenciatura. causes of deforestation and address them. that are under some category of protection UNICACH. Tuxtla Gutierrez, Chiapas The program included education, technical by national or international laws within the assistance in productive areas and conserved habitat.

Figure 5. Nurseryin situ of Ceratozamia norstogii for reintroduction to their habitat.

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Pérez-Farrera M.A. 1999. Estrategias de conservación para las plantas amenazadas de Chiapas. Un caso de estudio: las Palmas y las Cycadas. Amaranto 12(3): 13-17 Pérez-Farrera M.A., A.P. Vovides & C. Iglesias. 2001. TheCycadCeratozamia norstogii D.W. Stev. (Zamiaceae) fromSouthern México: New information on distribution, habitat and vegetative morphology. Botanical Journal of The Linnean Society 137:71-76. Pérez-Farrera M. A., A. P. Vovides, L. Hernández-Sandoval, D. González, M. Martínez. 2004. A morphometric analysis of the Ceratozamia norstogii Stevenson complex (Zamiaceae) In Terrence Walters and Roy Osborne. (Editores). Cycad classification: concepts and recommendations. Publisher: Cabi Publisher; Wallingford, United Kingdom. Pérez-Farrera M.A., Vovides A.P., Avendaño S. 2014. Morphology and Figure 6. Study of the structure, composition and floristic diversity of the oak forests where leaflet anatomy of the Ceratozamia Ceratozamia norstogii grows. Research activities carried out by students of the Eizi Matuda norstogii species complex (Zamiaceae, Herbarium of UNICACH. Cycadales). International of Journal Plant Science 175(1):110-121.

Pérez-Farrera M.A. Vovides A.P., S. López- escala: un caso de cycada en Veracruz. e.T42102A10645100. Mendoza, L. Hernández-Sandoval, M. Plumeria 7:445-453 http://dx.doi.org/10.2305/IUCN.UK.2010 Martínez 2017. Estimation of genetic Vovides A.P.,C. Iglesias, M.A. Pérez-Farrera, -3.RLTS.T42102A10645100.en. variation in closely related cycad M. Vázquez-Torres And U. Schippmann. Downloaded on 08 April 2019. species in Ceratozamia (Zamiaceae, 2002. Peasant Nurseries: A concept for Vovides A.P., C. Iglesias, V. Luna, T. Balcázar. Cycadales) using RAPDs markers. an integrated conservation strategy for 2013. Los Jardines botánicos y la crisis Revista de Biologíatropical 65(1): 305- cycads in México. In M. Maunder, C. de la biodiversidad. Botanical Science. 319. Clubbe, C. Hankamer And M. Groves 91 (3): 239-250. Secretaria de Medio Ambientey Recursos (Editores) Plant conservation in The Naturales. 2010. Norma Oficial . The Royal Botánical Gardens, Miguel Angel Pérez-Farrera, Mexicana NOM-059-SEMARNAT-2010, Kew. U.K. Héctor Gómez-Dominguez Protección ambiental-Especies nativas Vovides, A., Chemnick, J. & Gregory, T. 2010a. Laboratorio de Ecología Evolutiva, Herbario de México de flora y fauna Ceratozamia norstogii. The IUCN Red Eizi Matuda, Instituto de Ciencias Biológicas, silvestres-Categorías de riesgo y List of Threatened Species 2010: Universidad de Ciencias y Artes de Chiapas, especificaciones para su inclusión, e.T42102A10645100. Tuxtla Gutiérrez 29039, Mexico exclusión o cambio-Lista de especies http://dx.doi.org/10.2305/IUCN.UK.2010 en riesgo. Jueves 30 diciembre 2010 -3.RLTS.T42102A10645100.en. Ana V. Mandri-Rohen, Diario Oficial Downloaded on 08 April 2019 Andrómeda Rivera-Castañeda Stevenson D. 1982. A new species of Vovides A. P., E. Linares, R. Bye. 2010b. Fondo de Conservación el Triunfo, Calle San Ceratozamia (Zamiaceae) from Chiapas, Jardines botánicos de México: historia y Cristóbal #8 Fracc. Residencial La Hacienda, Mexico. Brittonia 34:181-184. perspectiva.Editado Secretaría de Tuxtla Gutiérrez 29030, Chiapas, México Tang W. 1983. Letterstothe editor. The Cycad Educación de Veracruz del Gobierno del Newsletter 6: 5-6. Estado de Veracruz. 232 pp. Tang W., A. P Vovides, M. A.Pérez-Farrera, T. Vovides A. P., M. A. Pérez-Farrera & C. Steyn, D. Kamoga & J.S. Khuraijam. Iglesias. 2010c. Cycad propagation by 2018. Village nursery projects for rural nurseries in Mexico as cycads: Review and assessment. analternative conservation strategy: 20 Cycads, IUCN/SSC Cycad Specialist years on. Kew Bulletin 65: 603-611 Group 3(2): 5-11 Vovides, A., Chemnick, J. & Gregory, T. 2010a. Vovides A.P., C. Iglesias y M.A. Pérez-Farrera. Ceratozamia norstogii. The IUCN Red 1999. El uso sostenible a pequeña List of Threatened Species 2010:

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Cycas siamensis at Kanchanaburi, Thailand. Photo by JS Khuraijam

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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, 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, [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 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& 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 merolae at Chiapas, Mexico. Photo by Michael Calonje CYCADS I Volume IV I Issue 1 I October 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 CYCADS I Volume IV I Issue 1 I October 2019