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Surname, Initial(s). (2012) Title of the thesis or dissertation. PhD. (Chemistry)/ M.Sc. (Physics)/ M.A. (Philosophy)/M.Com. (Finance) etc. [Unpublished]: University of Johannesburg. Retrieved from: https://ujcontent.uj.ac.za/vital/access/manager/Index?site_name=Research%20Output (Accessed: Date).

AN INTEGRATIVE APPROACH TOWARDS SETTING CONSERVATION PRIORITY FOR CYCAD SPECIES AT A GLOBAL SCALE

RESPINAH TAFIREI

Minor dissertation submitted in partial fulfilment of the requirements for the degree of

MASTER OF SCIENCE

ENVIRONMENTAL MANAGEMENT

Faculty of Science

UNIVERSITY OF JOHANNESBURG

August 2016

SUPERVISOR

Dr K. Yessoufou

CO-SUPERVISOR

Dr I.T. Rampedi

DEDICATION This work is dedicated to my parents.

iii

ACKNOWLEDGEMENTS

My entire family, mainly my beautiful children; Thabo, Ryan, Chloe, my nephew, Tinashe, as well as my husband: You were there for me throughout this journey. I am deeply appreciative and grateful for the support and rapport I received from my dear husband, Simon. Your patience did not go unnoticed. Thank you from the bottom of my heart.

I am also very grateful for the support and scientific guidance I received from Dr. K. Yessoufou, who was the Supervisor of the Research Project. I am thankful for the insights and constructive feedback I received from you.

My Co-Supervisor, Dr. I.T. Rampedi. You constantly encouraged me, guided me throughout the process and also reminded me of the deadlines. I acknowledge the input I received from the coursework modules you taught as well.

God bless you all.

ABSTRACT Prioritizing conservation efforts based on phylogenetic tools is gaining momentum globally. However, these efforts are almost exclusively focused on animals, and particularly vertebrate, with no equivalent efforts on plants. The main objective of the present study is to use phylogeny to inform conservation efforts of cycads, the most threatened group in plant kingdom. Specifically, four questions are investigated: 1) What is the geographic pattern of richness and evolutionary distinctiveness (ED) of cycads? 2) Would protecting elevated habitats (e.g. mountains) – traditionally thought to be refuges for ancient lineages – safeguard an ancient lineage like cycads? 3) Would protecting threatened cycads prevent the loss of high-ED species? 4) If not, how can ED and threat data be combined to inform prioritization efforts for cycads globally? Cycads have a tropical and subtropical distribution with the highest richness in Central America, eastern Southern Africa and eastern Australia. Tropical richness is traditionally attributed to a more rapid speciation and lower extinction rate in the tropics vs. temperate regions, but the restriction of cycads distribution to tropics in particular, could be the result of the tropics being a ‘‘hot spot’’ for ancient or relictual lineages. To assess this hypothesis, the first ever complete phylogeny of cycad taxa was reconstructed and used to calculate ED values for each species – an approximate measure of how ancient or unique a species is – and analyse their geographic patterns. High-ED species are likely to correspond to non-random phenotypes and uniquely divergent genomes, and habitats or regions rich in high-ED species therefore deserve particular attention. ED scores range from 10.587 million years (MY) (Cycas micronesica and Cycas zeylanica) to 98.762 MY (Microcycas calocoma) (SD = ±12.62). High average ED values are observed across all known biogeographic regions of cycads, particularly in America and Southern Africa, making America (New World) and Southern Africa priority regions for cycad conservation. There is, however, no relationship between ED and altitude, and this has also been reported recently for birds, indicating that elevated regions are not refuges for ancient cycad lineages. Nonetheless, geographic origin correlates strongly with ED, with cycad of American origin being the most evolutionarily distinct and therefore deserves much conservation efforts. There is, however, a trend towards high-ED species being highly threatened, suggesting that efforts to preserve cycads based on IUCN threat categories would also contribute to

preserving high-ED species. At the same time, there are several cases where threat-based prioritization would miss some high ED species. Threat level and ED were therefore combined to provide a more integrative option for conservation decision, using EDGE score (Evolutionary Distinctiveness and Globally Threatened) analysed within a biogeographic perspective. A complete ranking of cycad species based on EDGE score is provided. EDGE scores range from 2.497 (Cycas clivicola) to 7.375 (Microcycas calocoma) (SD = ± 1.06), making M. calocoma the one-of-the-kind cycad species to prioritize in conservation programme. The dominant genera in the top 50 EDGE species are Zamia (21 species) and Encephalartos (10 species), followed by Ceratozamia (8 species) and Cycas (6 species). From a biogeographic perspective, the cycads of the New World are dominant in the top EDGE ranking with 32 species in the top 50 EDGE species followed by the African cycads (Encephalartos; 10 species). These geographic regions (New World and Africa) therefore could be regarded as global “hot spots” of EDGE species. Several high-EDGE species are not found in protected areas, and this calls for global campaign to raise public awareness of this issue, train conservation officers on EDGE concept and design specific projects for high EDGE species. Further recommendations informed by EDGE species ranking are also provided.

Keywords: Conservation prioritization, Evolutionarily Distinct and Globally Endangered species, Biogeography of cycad diversity, New World, Africa.

TABLE OF CONTENTS

DEDICATION ...... ii ABSTRACT ...... v CHAPTER 1 ...... 1 INTRODUCTION AND RESEARCH CONTEXTUALISATION ...... 1 1.1 INTRODUCTION ...... 1 1.2 NEEDS FOR PRIORITIZING CONSERVATION EFFORTS ...... 2 1.3. EDGE APPLICATIONS ...... 5 1.4. RESEARCH PROBLEM ...... 7 1.5. CYCAD TAXONOMIC GROUP ...... 8 1.5.1. Biogeography of Cycads ...... 10 1.5.2 Species diversity and taxonomic changes in Cycads ...... 11 1.5.2.1. Family Cycadaceae ...... 12 1.5.2.2. Family Stangeriaceae ...... 12 1.5.2.3. Family Zamiaceae ...... 13 1.6 RESEARCH OBJECTIVES ...... 17 CHAPTER 2 ...... 18 METHODOLOGY ...... 18 2.1 MATERIALS AND METHODS...... 18 2.1.1 Materials ...... 18 2.1.2 Research methodology ...... 19 2.1.2.1 Assembling a complete phylogeny of Cycads ...... 19 2.1.2.2 Species distribution data and threat status ...... 21 2.2 DATA ANALYSIS ...... 43 2.2.1 Species richness, ED, and EDGE maps ...... 43 2.2.2 Statistical analysis ...... 43 CHAPTER 3 ...... 45 RESULTS AND DISCUSSION ...... 45 3.1. GEOGRAPHICAL PATTERN OF CYCAD RICHNESS ...... 45 3.2. GEOGRAPHY OF EVOLUTIONARY DISTINCTIVENESS (ED) OF CYCADS ...... 46 3.3. ARE THREATENED SPECIES EVOLUTIONARILY MORE DISTINCT THAN NON- THREATENED SPECIES? THE NEED FOR COMBINING ED SCORE AND THREAT LEVEL ...... 81 3.4 COMBINING ED AND THREAT LEVEL: CYCAD SPECIES RANKING BASED ON EDGE SCORES ...... 83 3.5 LIMITATION OF CONSERVATION ACTIONS AT REGIONAL OR CONTINENTAL LEVEL FOR THE TOP EDGE SPECIES ...... 84 CHAPTER 4 ...... 87 CONCLUSION AND RECOMMENDATIONS ...... 87 4.1 CONCLUSION ...... 87 4.2. RECOMMENDATIONS ...... 87 REFERENCES ...... 90

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List of Figures (Figures are numbered following chapters’ number)

Chapter 1

Figure 1.1. Top 3 EDGE species for mammals, birds, amphibians, and coral reefs...... 4

Figure 1.2. A hypothetical phylogeny showing for ED calculation...... 6

Figure 1.3. Global distribution map of the cycad genera ...... 10

Figure 1.4. Seed and pollen cones for the cycad genera ...... 16

Chapter 3

Figure 3.1. Geography of cycad species richness ...... 46

Figure 3.2. First complete phylogeny of cycads comprising 339 taxa ...... 48

Figure 3.3. Global spatial patterns of (a) ED and (b) EDGE values of cycad species……….79 Figure 3.4. The Geographical patterns of ED ...... 80

Figure 3.5. Relationship between ED and threat status ...... 82

List of Tables (Tables are numbered following chapters’ number)

Chapter 2

Table 2.1. An updated world list of cycad taxa and their global distribution ...... 22

Chapter 3

Table 3.1. EDGE and ED scores of all cycad species with their geographic distribution parameters (Range and altitude) ...... 50

Table 3.2. Relationships between ED and geographic parameters (Range and altitude) ...... 80

Table 3.3. ANOVA table reporting the relationships between ED and geographic origin ..... 80

Table 3.4. ANOVA table reporting the relationships between ED and threats ...... 82

viii

CHAPTER 1

INTRODUCTION AND RESEARCH CONTEXTUALISATION

1.1 INTRODUCTION

Several sources indicate that we are losing biodiversity at an unprecedented rate (Millennium Ecosystem Assessment, 2005; Ricketts et al., 2005; Vamosi and Vamosi, 2008). An early assessment revealed that current rate of species loss is 1,000–10,000 times greater than past extinction rates (Millennium Ecosystem Assessment, 2005) and that the greatest loss occurs in tropical biomes (Vamosi and Vamosi, 2008) which harbour over 50% of the global species richness. One consequence of species extinction is the loss of their contributions to overall ecosystem functioning and provision of goods and services. The loss of ecosystem goods and services is of particular concern because the future of humanity depends inextricably on these goods and services such as food production, plant pollination, medicinal plants, clean water, clean air, nutrient cycling, carbon sequestration, climate stability, recreation, and tourism (Millennium Ecosystem Assessment, 2005). The risk of species extinction is driven by various pressures, including pressure from invasive species (Winter et al., 2009), habitat destruction (Vitousek et al., 1997; Haberl et al., 2007), resource overexploitation and climate change (Willis et al., 2008, 2010), all of which are linked to human population growth and activities.

Over the last century, we have witnessed an exponential growth of human population, likely to reach 9 billion by 2050 (United Nations, 2004). This is an indication that pressure on natural ecosystems will continue to increase because of a greater demand for ecosystem goods and services that will result from human population growth. Consequently, an early prediction anticipates that future rate of species extinction will rise by at least a further order of magnitude over the next few hundred years (Mace, 2005). However, the susceptibility of species to extinction is not uniform: some taxonomic groups are more at risk in comparison to others, a pattern referred to as non-random extinction (Davies et al., 2011; Yessoufou et al., 2012). Among terrestrial vertebrates for example, a third of all known amphibians is threatened, making amphibians the most at-risk vertebrates (Wake and Vredenburg, 2008). 1

Wilson (1992) reported that nearly 12% of continental birds and 20% of continental mammals have already been lost. The loss of these animals can cause not only a severe range contraction for plants – particularly for plants that rely on them for dispersal – but also reduce ecosystem productivity (see Doughty et al., 2015). In addition 21% of fish assessed for threat level as well as 30% of the 10 000 invertebrate species assessed to date are threatened (IUCN, 2010).

As far as plants are concerned, the risk of extinction is more worrisome. For instance, over 70% of assessed flowering plants is at risk of extinction (IUCN, 2010). This proportion is much higher than that reported for vertebrate groups (22%), but only 13 000 out of > 300 000 plant species have been assessed (IUCN, 2010). However, even for plant taxonomic groups for which a comprehensive assessment is available – e.g. cycads – the proportion of threatened species remains very high (~ 70%; IUCN 2010), resulting in most cycads listed in the Convention on International Trade in Endangered Species (CITES) Appendix I. CITES Appendix I lists species that are threatened with extinction and prohibited from entering international trade except for non-commercial purpose, e.g. for scientific research. As a result of this unprecedented rate of species loss, there is a general agreement that we have entered the period of the sixth mass extinction (Barnosky et al., 2011).

1.2 NEEDS FOR PRIORITIZING CONSERVATION EFFORTS

In the face of the ongoing extinction crisis, conserving global biodiversity is the ideal remedy that would preserve the entire diversity of life forms and ensure a continued provision of ecosystem services to humanity. However, this remains an impossible and unrealistic mission for conservation planners. Financial and human resources devoted to conservation actions and conservation science are generally far below what is needed to conserve much of the world’s threatened biodiversity (Isaac et al., 2007; Waldron et al., 2013; Lung et al., 2014). Also, even if we do have enough resources, global change and primarily climate change is exerting additional pressure on biodiversity and protected areas (Araújo et al., 2004; Araújo et al., 2011). As a result, conservation planners are facing an urgent need to save what they possibly can (Weitzman, 1998) but they have to prioritise effort, i.e. they have to decide

which species or habitats need the most urgent attention (Vane-Wright et al., 1991; Isaac et al., 2007, 2012). There is therefore a need to develop a scientifically based tool or approach to inform such decision.

At local or regional scales, priority is traditionally given to threatened species, restricted- range endemics, ‘flagship’, ‘umbrella’, ‘keystone’, ‘landscape’ or ‘indicator’ species, or species with significant economic, ecological, scientific or cultural values (Entwistle and Dunstone, 2000; Myers et al., 2000; Mace et al., 2002). Also taxonomic information is sometimes used to prioritize funding allocations to conservation decisions; this is the case of the US ‘Endangered Species Act’ that gives priority to monotypic species within their genus over non-monotypic species and subspecies (Fay and Thomas, 1983). However, unique focus on species-based approach, ignoring the genetic distinctiveness of species, might be misleading given the everlasting debate around species delimitation (Isaac et al., 2004). At global scale, priority is given to restricted-range endemic species (Stattersfield et al., 1998; Myers et al., 2000; Olson et al., 2001), a major approach in IUCN threat categorization. Because endemism correlates poorly with species richness and species threat level (Orme et al., 2005), setting global conservation priority based upon endemism could lead us to miss the right target, i.e. priority species or habitats for conservation (Isaac et al., 2007).

One recent alternative and more inclusive tool has been developed and initially applied for mammals (Isaac et al., 2007). This tool gives priority to Evolutionary Distinct and Globally Endangered (EDGE) species. A global campaign is currently underway to inform stakeholders and conservation practitioners of which mammals to concentrate efforts and resources on, and this campaign is led by the Zoological Society of London through the online platform http://www.edgeofexistence.org (Owen, 2014). Later on, EDGE score has also been developed, again for animals, such as amphibians, birds, and also for coral reefs (Figure 1.1).

Figure 1.1 Examples of top three EDGE species for A) Birds, B) Mammals, C) Amphibians and D) Coral reefs. Source: http://www.edgeofexistence.org, accessed October 12th 2015

1.3. EDGE APPLICATIONS

EDGE, as indicated above, stands for Evolutionary Distinct (ED) and Globally Endangered (threat level) species. ED translates the phylogenetic relatedness of a species with others on a phylogeny. Figure 1.2 explains how to calculate ED. On this Figure, the ED score of species A is given by the sum of the ED scores for each of the branches between A and the root of the phylogeny. Species A is linked to the root by only one branch that is 2 million years (MY) long, so ED score for A is 2/1 = 2 MY. However, species B is connected to the root by two branches of 1 MY each; the first branch is a terminal branch that subtends only one species (which is B) whereas the second branch subtends two species (B and C). So ED score for B is: 1/1+1/2 = 1.5 MY. Species C has the same ED score as B because they are sister species (Figure 1.2). Species that have very few relatives will have a high ED value (e.g. species A) compared to those with several relatives (e.g. species B or C; Figure 1.2). The threat level is defined as the IUCN categorization (IUCN, 2010) of species risk assessment (DD = Data Deficient, LC = Least Concern, NT = Near Threatened, VU = Vulnerable, EN = Endangered, and CR = Critically endangered).

The EDGE score system combines both ED and threat level; it was first developed by Isaac et al., (2007) for mammals and allows ranking species to provide a priority list that deserves urgent conservation efforts. EDGE species are distinct not only in the history of their evolutionary past, but also in the functional roles they play in ecosystems. The extinction of EDGE species might therefore result in the loss of important ecosystem functions and services for which we have no species substitute (Yessoufou and Davies, 2016).

Figure 1.2 A hypothetical phylogeny of three species A, B and C explaining how to calculate Evolutionary Distinctiveness (ED) scores. Numbers above each branch indicate the length of the branch in million years before present; numbers below show the number of descendent species.

There are ongoing efforts spearheaded by the Zoological Society of London’s EDGE programme, and this programme, which started in 2007, specifically focuses on drawing conservation attentions on evolutionary distinct species that are at risk of extinction. Some EDGE species (e.g. elephants and pandas) are well known, but many others (e.g. Chinese giant salamanders and the peculiar long-beaked echidnas) have been overlooked by traditional conservation strategies (see Isaac et al., 2007, 2012). The Zoological Society of London’s EDGE programme has been successful so far in i) raising public awareness of the highest ranking EDGE species, ii) initiating conservation projects for those that are not already receiving conservation attention, and iii) building capacity in countries where EDGE species occur (visit http://www.edgeofexistence.org for more details on projects and ongoing actions, campaign and trainings based on EDGE). The end result of this programme is to protect one-of-a-kind species in order to avoid that these species slide to extinction unnoticed. These efforts focus so far exclusively on animals (Figure 1.1), with no equivalent efforts on plants, particularly gymnosperms. The present study aims to fill this gap, using cycads, the most threatened plant group as a case study.

1.4. RESEARCH PROBLEM

Global biodiversity is increasingly under tremendous pressure (habitat destruction, invasive species, global change, etc.), calling for renewed conservation efforts. It is impossible to conserve all species, as resources allocated for conservation actions are inadequate. Existing measures to conserving biodiversity are facing several limitations globally (Isaac et al., 2007; Lung et al., 2014). For example, limited funds are allocated for conservation (Lung et al., 2014) especially in developing countries, which are home for the vast majority of biodiversity (Rolland et al., 2014). Even existing strategies do not maximise the chance of preserving the most threatened species and protected areas in the face of climate change (Araújo et al., 2011, 2004). In addition, legislation on biodiversity particularly in Africa is not strictly enforced. Even in a country like South Africa where, for instance, legislation on cycad is one of the strictest in the world (Strydom and King, 2009), illegal poaching of cycads is still common (IUCN, 2010). All these limitations call for prioritising efforts to save threatened species that require the most urgent attention whilst traditional efforts towards conservation are still on. Priority setting will determine species that require urgent attention, and calls for actions such as raising awareness, initiating conservation projects, and building capacity towards well- informed conservation decisions (Owen, 2014). EDGE concept was proposed by Redding and Mooers (2006) and Isaac et al., (2007), and official EDGE lists have been presented for all mammals (Isaac et al., 2007; updated by Martyn et al., 2012), all amphibians (Isaac et al.,

2012), reef corals (Huang, 2012), and the world’s birds (Jetz et al., 2014). EDGE is a more inclusive approach for priority setting that combines species threat and genetic data (Sections 1.2 and 1.3). Current efforts are, however, particularly focused on mammals, birds, amphibians, and coral reefs (Figure 1.1).

There is no equivalent EDGE-based global campaign yet for plants. With cycads being the world most threatened taxonomic group (IUCN 2010; Da Silva et al., 2011), it makes more sense to use cycads as the case study in establishing the first EDGE score for a complete list of a plant taxonomic group. The overall goal of this study is to provide, for cycads, a solid global conservation framework similar to that of mammal, birds, and amphibian EDGE campaign (visit http://www.edgeofexistence.org for details) and integrate this framework within a biogeographic perspective. Such priority list will be useful for conservation planners,

conservation institutions and government on what (priority species) and where (hotspots of priority species) to spend more money and efforts. Most of species diversity of cycads (~70%) are threatened with high risk of extinction due to overexploitation, habitat destruction, and species biology and ecology (e.g. very low dispersal ability, very limited range of pollinators, very restricted distribution range, etc.; IUCN 2010). The consequence of this extinction risk is the risk of losing important evolutionary history from the tree of life (Davies and Yessoufou, 2014; Davies 2015; Yessoufou and Davies, 2016), and this will ultimately contribute to the disruption of ecosystem functions and services and other biodiversity associated with cycads. If, so far, we are not able to preserve simultaneously all species in an efficient manner, we, however, can prioritize conservation efforts on those species that represent unique evolutionary history. To do so, there are increasing evidence that focusing on Evolutionary Distinctiveness (ED); Isaac et al., 2007) as a single diversity metric (Redding et al., 2008; Jetz et al., 2014; Redding et al., 2014, 2015) or in combination with threat risk (using EDGE scores; Isaac et al., 2007, 2012) would likely lead to safeguarding most evolutionary history in a particular lineage.

1.5. CYCAD TAXONOMIC GROUP

Cycads comprise a relatively small group of gymnosperms (non-flowering seed plants) which closely resemble palms or large ferns in overall appearance (Hill et al., 2004). They, however, differ greatly in detailed structure and reproduction (Salas-Leiva et al., 2013). Cycads are distributed in the neo-tropics with more inclination to tropical and subtropical regions with high temperature and humidity (Donaldson et al., 2003; Da Silver et al., 2011; Taylor et al., 2012). Amongst the spermatophytes still living today, cycads are the most ancient group due to their ability to retain ancestral characteristics such as flagellated sperm (Vessey et al., 2004; Salas-Leiva et al., 2013).

Fossil evidence indicates that cycads originated in the Palaeozoic era, more than 300 million years ago (Donaldson et al., 2003; Pot et al., 2010; Nangalingum et al., 2011, Taylor et al., 2012). Salas-Leiva et al. (2013) estimate cycad species diversification to have taken place in the Eocene and Oligocene. They reached their peak in abundance and diversity during the Jurassic-Cretaceous, then their number started dwindling to their present 331 recognized species (Osborne et al., 2012; also, further reference can be gleaned from a taxonomic 8

treatment of cycads provided in Chapter 2: Material and Methods) as angiosperms started taking over ecosystems (Martinez, 2012).

The survival of cycads for such a long period of time with relatively similar and reproductive structures has not been entirely explained to date. Donaldson et al. (2003) and Taylor et al. (2012) link the survival to individual longevity in cycads as well as their ability to produce toxic substances which deter herbivores. The Southern African clades are thought to have survived through the development of key innovations (e.g. underground stems) (Yessoufou et al., 2013). Their subterranean stem (Hill et al., 2004) could have enabled them to adapt to high temperatures and aridity of the Pliocene- Pleistocene transition in the region (Yessoufou et al., 2013).

Morphological and molecular studies show that cycads are monophyletic (Stevenson, 1990, 1992; Hill et al., 2003; Rai et al., 2003; Bogler and Francisco-Ortega, 2004; Vessey et al, 2004, Chaw et al., 2005; Zgurski et al., 2008; Crisp and Cook, 2011; Nagalingum et al., 2011; Condamine et al., 2015). This means that they exhibit a single evolutionary origin (Donaldson et al., 2003). They are long-lived perennial evergreen plants with a thick columnar stem that gives them a palm like appearance (Taylor et al., 2012). Cycads have rosettes of compound leaves with pinules and have a height of approximately 0.2- 20 metres (Donaldson et al., 2003; Vessey et al., 2004). They exhibit a true gymnosperm nature of being dioecious, a characteristic shown by male and female cones being located on separate plants (Hill et al., 2004; Taylor et al., 2012; Salas-Leiva et al., 2013).

The order Cycadales to which cycads belong is of extraordinary scientific importance. Their unique evolutionary position provides clues that can be used in the inference of early molecular evolution of seeds, cones, and plant vegetative structures (Frohlich and Parker, 2000; Brenner et al., 2003a, b; Sass et al., 2007; Salas-Leiva et al., 2013). Furthermore, the developmental pathways of cycads play an important role in the construction of connections between early origins of seed plants and their present day counterparts (Donaldson et al., 2003). A deeper understanding of this group of plants could therefore provide evolutionary 9

insights and trends of seed plants (Zhang et al., 2004; Wang et al., 2007). This could help in the determination of connections between the origins of cycads and their present day counterparts before losing them as they are under a tremendous threat of extinction (Da Silva et al., 2011).

1.5.1. Biogeography of Cycads

The living cycad comprises three families namely Cycadaceae, Stangeriaceae, and Zamaceae (Osborne et al., 2012). These three families have 11 genera (Donaldson et al., 2003; Osborne et al., 2012; Condamine et al., 2015) distributed in Africa, Asia, Australia, North and South America with few found in oceanic islands (Figures 1.3) (Nagalingum et al., 2011; Osborne et al., 2012; Taylor et al., 2012).

Figure 1.3 Global distribution range map of the cycad genera. Source: Nagalingum et al., (2011)

Most cycad species have a highly structured distribution and a pattern of isolation by distance even at small geographical distances (Cibrian-Jaramillo et al., 2010). Generally, they occur in small populations in remote pristine vegetation (Osborne et al., 2012; Taylor et al., 2012).

Studies indicate that these small relict populations may have once been more widespread (Donaldson et al., 2003). Although Hamric (2004) argues that small and restricted populations may not necessarily result in extinction, it could have a huge impact on the general cycad diversity (Da Silva et al., 2011). It appears to have predisposed the group to a high risk of extinction in the wake of habitat destruction, over-collection, and stochastic environmental events (Salas-Leiva et al., 2013). Due to massive extinctions within the cycad group, several genera existed in the past and do not have any of their living representatives today, contributing perhaps to the patchy distribution of extant cycads that we observe today (Donaldson et al., 2003; Taylor et al., 2012; Salas-Leiva et al., 2013).

1.5.2 Species diversity and taxonomic changes in Cycads

Numerous changes have been made in the ‘world list’ of cycads as new discoveries and synonymies cause multiple readjustments in their taxonomy. Osborne and Hendricks (1985) published the initial list of cycads. Various other lists were presented by Stevenson et al. (1990), Stevenson and Osborne (1993A), Stevenson and Osborne (1993B), Stevenson et al. (1995), Osborne et al. (1999). This improved understanding of the cycad led to an increase in the number of cycad species recognised worldwide (Donaldson et al., 2003). However, as further exploration of habitats continued, and new genera and species are described or refined (Vessey et al., 2004), Hill et al. (2004a, b, c; 2007) then made significant changes to the cycad lists. Cha et al. (2005) and Lindstrom (2009) also contributed to the cycad taxonomy by reassigning two species that were in the genus Chigua to Zamia restrepoi and this reduced the number of genera from the previously accepted 11 genera down to 10. The most recent list of valid names of all extant cycads comprises 331 species presented by Osborne et al. (2012). However combining Osborne et al.’s work which is based on morphology, geography and ecology of cycads, with that of Nangalingum et al. (2011) which is based on phylogenetic data, a new treatment that include 339 taxa was obtained (see details in Materials and Methods), on which the present study focuses.

1.5.2.1. Family Cycadaceae

Cycadaceae is regarded as an early offshoot from the rest of the cycads. Cycas is the only genus belonging to the family Cycadaceae and members of this genus mostly occur in Indo- china and Australia (Donaldson et al., 2003; Da Silva et al., 2011). As opposed to most cycad clades that have a restricted geographical range, Cycas with its 110 species (Table 2.1) has the widest distribution range, from eastern Africa eastwards to the Pacific islands and from China and southern Japan southwards to Australia (Hill, 2004; Figure 1.3). The widespread distribution of this genus, thought to have originated in South China (Xiao and Möller, 2015) is a result of long-distance transoceanic dispersal events (facilitated by the development of a key innovation such as spongy endocarp, de Laubenfels & Adema, 1998), and its rapid radiation is likely a result of vicariant speciation events promoted by the physical barrier of the Red River Fault between South China and Indochina blocks mostly in the late Miocene (Xiao and Möller 2015). The genus Cycas forms a basal group (Versey et al., 2004) and is characterised by dioecious palm-like shrubs with aerial subterranean cylindrical stems and loosely arranged megasporophylls (Hill et al., 2004; Osborne et al., 2012). They are commonly understorey shrubs but can be sometimes quite large if soils are well drained or if they occur in the savannah.

1.5.2.2. Family Stangeriaceae

Stangeriaceae is the cycad family with the smallest number of species (Hill et al., 2004). It comprises two genera namely; Bowenia and Stangeria (Osborne et al., 2012; Taylor et al., 2012; Condamine et al., 2015). Bowenia is endemic to Australia and consists only of two species (Bowenia serrulata and Bowenia spectabilis) which are dioecious fern-like shrubs with a naked subterranean stem capable of producing one to many shoots(Hill et al., 2004). Leaves of the genus Bowenia are bi-pinnate and the leaflets do not bear a mid-rib. The genus Stangeria has only one species i.e. Stangeria eriopus that is endemic to South Africa (Hill et al., 2004; Osborne et al., 2012; Salas-Leiva et al., 2013). Members occur mostly in coastal grasslands and inland forests along the east coast of South Africa (Vessey et al., 2004). Stangeria, which has remained taxonomically stable (Donaldson et al., 2003; Hill et al., 2004a, 2004b, 2004c, and 2007) is characterised by pinnate leaves and leaflets that have a midrib and lateral veins. It is also dioecious and fern like. The body of the plant consists of

large tuberous root that is carrot-shaped while the stem is branched and subterranean (Osborne et al., 2012).

1.5.2.3. Family Zamiaceae

Zamiaceae is the most diverse and widespread family (Donaldson et al., 2003) and comprises three genera Encephalartos in Africa, Macrozamia and Lepidozamia in Australia as well as Zamia, Ceratozamia, Dioon, and Microcycas in North and South America (Donaldson, 2003; Nagalingum et al., 2011; Salas-Leiva et al., 2013). Encephalartos and Macrozamia inhabit humid tropical and subtropical regions. Macrozamia and Zamia commonly occupy dryer soils of low fertility.

The genus Zamia, which comes second to Cycas in term of distribution range and diversity, consists of 75 described species (Osborne et al., 2012). The Isthmus of Panama which occurs in the tropics of the western hemisphere has 17 Zamia species (Taylor et al., 2012). Of these, 12 are endemic to Panama (Donaldson, 2003; Taylor et al., 2012). This endemism, in addition to the highest cycad representatives per unit land mass than in any other region in the neo-tropics, makes the Isthmus of Panama a cycad biodiversity hotspot (Taylor et al., 2012).

The genus Encephalartos comprises 65 species (Osborne et al., 2012) that inhabit humid tropical and subtropical regions of Africa (Vessey et al., 2004). With so many changes occurring to the cycad taxonomy, no substantial changes have been noted in the genus Encephalartos. Donaldson et al. (2003) consider this genus as the better known of the cycad genera. Southern Africa has become a geographical region that is a centre of diversity for the genus Encephalartos (Donaldson et al., 2003; Golding and Hurter, 2003; Yessoufou et al., 2013). Members of this genus have pinnate leaves and contain leaflets that lack a mid-rib as well as articulation (Hill et al., 2004). Encephalartos and Lepidozamia are more closely related (Bogler and Fransisco-Ortega, 2004; Chaw et al., 2005; see also phylogeny in Chapter 3).

There are 41 species that have been documented in the genus Macrozamia (Osborne et al., 2012). Over 80 % of these species are found in eastern Australia and the rest in the central and south west of the continent (Hill et al., 2004). Like all cycads, they are dioecious. Members of this genus are unique in that they produce their new leaves one at a time unlike in other genera where leaves erupt all at once (Hill et al., 2004). Most produce subterranean palm-like trunks up to 20 feet tall or more and have thin, flat leaflets that tapper at the end (Chaw et al., 2005).

The genus Ceratozamia consists of 27 species (Osborne et al., 2012) and is well known for its sporophylls with prominent paired horns as well as pinnate compound leaves that are straight and spirally arranged (Haynes, 2011). Leaflets lack a mid-rib but have parallel side veins and are articulate at the base (Hill et al., 2004). Most species belonging to the genus Ceratozamia are endemic to the mountainous areas of Mexico, Guatemala, and Honduras (Haynes, 2011).

The genus Dioon with 14 documented species (Osborne et al., 2012) is native to Mexico and Central America. Tropical forests, pine oak forests, dry hillsides, canyons, and coastal dunes are some of their habitats. Members consist of grey or blue-green pinnate leaves with non- articulated leaflets lacking a mid-rib. Megasporophylls are broadly flattened, upturned and overlapping. The presence of female cones with two seeds attached to each sporophyll is a unique feature of the cycads in the genus Dioon (Norstog and Nichols, 1997).

The genus Lepidozamia consists of 2 species (L. hopei and L. peroffskyana) (Osborne et al., 2012), both of which are endemic to eastern Australia. The two are closely related to the large southern cycad genera Macrozamia from Australia and Encephalartos from Africa in the family Zamiaceae (Donaldson et al., 2003; Hill et al., 2004). Lepidozamia has unique cuticular characteristics. The orientation of epidermal cells in the leaves of this genus relative to the axis of the pinna is unlike other genera (Hill et al., 2004; Condamine et al., 2015).

Only one species of the genus Microcycas (Microcycas calocoma) is described and this is endemic to Cuba (Donaldson et al., 2003; Hill et al., 2004; Osborne et al., 2012). Members are dioecious palm-like shrubs with tall aerial stems that bear numerous leaves (Osborne et al., 2012). Their microsporophylls and megasporophylls are spiral (Hill, et al., 2004). Microcycas and Zamia are closely related (Bogler and Fransisco-Ortega, 2004). Below, Figure 1.4 presents a photographic description of the diversity of cycad cones as published in Calonje et al. (2011).

Figure 1.4 Seed and pollen cones for all cycad genera. A) Bowenia serrulata seed cone B) Bowenia spectabilis pollen cone C) Ceratozamia decumbens seed cone D) Ceratozamia decumbens pollen cone E) Cycas couttsiana seed cone F) Cycas revoluta pollen cones G) Dioon angustifolium seed cone H) Dioon angustifolium pollen cone I) Encephalartos ferox seed cone J) Encephalartos ferox pollen cone K) Lepidozamia hopei seed cone L)

Lepidozamia peroffskyana pollen cone M) Macrozamia lucida seed cone N) Macrozamia lucida pollen cone O) Microcycas calocoma seed cone P) Microcycas calocoma pollen cones

Q) Stangeria eriopus seed cone R) Stangeria eriopus pollen cone S) Zamia imperialis seed cone T) Zamia imperialis pollen cones. Photos: all Michael Calonje except K: Larry Krauss and N: Irene Terry. Source: Calonje et al., (2011).

1.6 RESEARCH OBJECTIVES

The main objective is to inform prioritization efforts of cycads at a global scale based on phylogenetic method that combines threat level, phylogenetic distinctiveness of species and geographic data. Specifically, the following questions were investigated.

 What is the geographic pattern of cycad richness and evolutionary distinctiveness (ED)?

 Does protecting elevated habitats (e.g. mountains) – traditionally thought to be refuges for ancient lineages – safeguard an ancient lineage like cycads?

 Does protecting threatened cycads prevent the loss of high-ED species?

 If not, how can ED and threat data be combined to inform prioritization efforts for cycads globally?

CHAPTER 2

METHODOLOGY

2.1 MATERIALS AND METHODS

Numerous changes have been made to the ‘world list’ of cycads as new discoveries and changes in the taxonomy keep rendering the previous lists obsolete. Frequent updates have been made to the world list of cycads due to rapid changes in the cycad taxonomy which include approximately 50 % of the accepted species being named in the last two decades (Hill et al., 2004). Construction of a working list of cycads is therefore inevitable so that all species are captured.

2.1.1 MATERIALS

The materials used in this study are all 339 cycad taxa identified in this study as follows. The world list of cycads has changed several times owing to the high morphological similarities between species (morphological stasis), resulting in a long list of synonyms (Osborne et al., 2012). In their recent work, Osborne et al., (2012) summarised existing knowledge of morphology and ecology of cycads based on which they distinguish 331 cycad species globally, constituting the most recent world list of cycad species. Earlier, Nagalingum et al. (2011) used DNA data to assemble a comprehensive phylogeny of global cycads that include 199 species. In the present study, Osborne et al.’s (2012) list is used as the reference list, whilst also taking some nuances into account based on Nagalingum et al.’s DNA-based phylogeny. Specifically, based on their positions on the phylogeny, Nagalingum et al. (2011) distinguished Cycas media ensata and C. media, C. pectinata A and C. pectinata B as well as Zamia furfuracea A and Z. furfuracea B. Also, Z. picta, Z. lawsoniana, Z. kickxii and Z. amblyphyllidia were all maintained in Nagalingum et al., (2011) as distinct species whereas Osborne et al. (2012) considered them as synonyms of Z. variegata, Z. loddigesii, Z. pygmaea and Z. erosa, respectively based on their morphological features. Finally, following Lindström (2009), Osborne et al. (2012) did not recognize the genus Chigua whilst this genus was maintained in Nagalingum et al. (2011). In the present study, Nagalingum et al.’s (2011) DNA-based nuances are taken into account and combined with Osborne et al.’s 18

species delimitation to distinguish 339 taxa of cycads. These taxa are presented in Table 2.1 as well as their global distribution.

2.1.2 Research methodology

The first complete phylogeny of cycads was assembled following Thomas et al.’s (2013) approach detailed below in Section 2.1.2.1. An integration of a Global Biodiversity Information Facility database (GBIF), IUCN database, as well as information from Osborne et al. (2012) provided information on species distribution data and threat status.

2.1.2.1 Assembling a complete phylogeny of Cycads

To assemble a complete phylogeny of cycads, the recently proposed approach of Thomas et al. (2013) that assemble a complete phylogeny with soft taxonomic inferences was used. This approach requires i) a DNA-based phylogeny to be used as a constraint tree, and ii) taxonomic information of species missing in the constraint tree. Following Thomas et al. (2013), three types of species were defined: type 1 (comprising species for which DNA sequences are available); type 2 (species with no DNA sequence but are congeners of type 1 species); and type 3 (species that have no DNA data and have no congeners among type 1 species). In the present study, type 1 species comprise 199 species (see details below) and there is no type 3 species. Thomas et al.’s approach to integrate type 1 and type 2 species relies on two assumptions: taxonomic groups (e.g. genera) are monophyletic and there is a reasonable edge-length and topology priors. These two assumptions are met for cycads as all cycad genera are monophyletic and a DNA-based dated phylogeny, used as constraint tree, does exist (see details below).

The constraint tree was constructed using the nuclear DNA sequences of the region PHYP for 199 species (type 1 species defined above) of all 339 cycad taxa. The DNA sequences for PHYP region was retrieved from TreeBASE (visit www.treebase.org; # 11891; Nagalingum et al., 2011), includes proportional sampling within the large genera (see Nagalingum et al., 2011 for details) and comprises all the 11 currently defined genera. An XML file was

generated in the program BEAUTi, which was used to reconstruct a dated phylogeny based on a Bayesian MCMC approach implemented in the BEAST program. In the process of dated tree reconstruction, GTR + I + Γ was selected as the best model of sequence evolution based on the Akaike information criterion evaluated using MODELTEST (Nylander, 2004). Also, a Yule process was selected as the tree prior, with an uncorrelated relaxed lognormal model for rate variation among branches. Further, a normal prior distribution and several secondary calibration points extracted from Nagalingum et al., (2011) was applied: Encephalartos crown node (11.3648 Myr), Macrozamia crown node (7.4836 Myr), Lepidozamia crown node (7.914 Myr), Cycas crown node (12.7977 Myr), Zamia crown node (11.2534 Myr), Dioon crown node (12.1254 Myr), Encephalartos – Lepidozamia (39.7442 Myr) and (Encephalartos – Lepidozamia) – Macrozamia (49.037 Myr). Monte Carlo Markov Chains were run for 100 million generations with trees sampled every 10000 generations. Log files, including prior and likelihood values, as well as the effective sample size (ESS) were examined using TRACER (Rambaut & Drummond, 2007). ESS values varied between ~1058 and 7826 for the age estimates, confirming stationarity. Of the resulting 10001 trees, the first 2500 trees were removed as burn-in and the remaining trees were combined using TREEANNOTATOR (Rambaut & Drummond, 2007) to generate a Maximum Clade Credibility (MCC) tree. The following species were used as outgroups: Ginkgo biloba, Cryptomeria japonica, Araucaria heterophylla, Pinus strobes, Pseudotsuga menziesii, and Abies firma (Nagalingum et al., 2011).

To integrate the 140 type 2 species into the constraint tree, a simple taxon definition file that lists all species (types 1 and 2) along with a clade name (genus name) was constructed. Then the R library PASTIS (Thomas et al., 2013) was used to integrate type 2 species into the constraint tree as explained in Thomas et al. (2013); this results in a MrBayes input file that is executed in MrBayes 3.2 to generate a complete phylogeny of cycads that combines genetic data (type 1) and taxonomic data (type 2). This approach has recently been used to assemble a complete phylogeny for birds (Jetz et al., 2012).

2.1.2.2 Species distribution data and threat status

In absence of range maps for all 339 cycad taxa used in this study, distributional GPS coordinates of cycads worldwide were extracted from the well-known Global Biodiversity Information Facility database (GBIF, www.gbif.org, accessed June 2015). In addition, species ranges and altitudinal information (min, max and mean altitude) were all retrieved from IUCN database (IUCN, 2010). Threat status was also retrieved from IUCN database, and sometimes (when information is unavailable on IUCN), threat status was compiled from Osborne et al. (2012).

Table 2.1: An updated world list of cycad taxa and their global distribution. Species in red are the ones missing in the Nagalingum et al., (2011) list but maintained by Osborne et al., (2012) while those in green are the DNA-based nuances from Nagalingum et al., (2011). Osborne et al.’s list is based on morphology, ecology and geography of cycads, whereas Nagalingum et al.’s nuances are based on DNA data. Integration of Nagalingum et al.’s nuances into Osborne et al.’s list resulted in 339 taxa presented in this table.

Species Location

1. Cycas_aculeata Vietnam (Da Nang)

2. Cycas_apoa Indonesia (Papua), Papua New Guinea (West Sepik, Morobe)

3. Cycas_armstrongii Australia (Northern Territory,)

4. Cycas_basaltica Australia (Western Australia)

5. Cycas_beddomei India (Andhra Pradesh)

6. Cycas_bougainvilleana Papua New Guinea (Bougainville, New Britain), Solomon Islands

7. Cycas_brachycantha Vietnam (Bac Kan)

8. Cycas_cairnsiana Australia (Queensland)

9. Cycas_calcicola Australia (Northern Territory)

10. Cycas_chamaoensis Thailand (Chantaburi)

11. Cycas _chamberlainii Philippines (Luzon)

12. Cycas_chevalieri Vietnam (Ha Tinh, Nghe An, Quang Binh, Quang Tri)

13. Cycas_circinalis India (Andra Pradesh, Karnataka, Kerala, Maharashtra, Tamil Nadu)

14. Cycas_clivicola Malaysia (Kedah, Perak, Selangor), Thailand (Chumphon, Narathiwat, Phang

Nga, Phuket, Ranong, Trang)

15. Cycas_collina Vietnam (Son La)

16. Cycas_condaoensis Vietnam (Ba Ria- Vung Tau)

17. Cycas_couttsiana Australia (Queensland)

18. Cycas_debaoensis China (Guangxi)

19. Cycas_diannanensis China (Yunnan), N Vietnam

20. Cycas_dolichophylla China (Yunnan), Vietnam (Bac Kan, Cao Bang, Ha Giang, Lai Chau, Lao Cai, Ninh

Binh, Son La, Thai Nguyen, Thanh Hoa, Tuyen Quang)

21. Cycas_edentata Indonesia (Bali, Bengkulu, Jawa Barat, Jawa Tengah, Jawa Timur, Lampung,

Riau, Sumatra Utara), Malaysia (Johore, Langkawi, Malacca, Pahang, Perak, Sabah, Sarawak, Terengganu), Myanmar, Philippines (Balabac, Basilan, Cebu, Masbate, Mindanao, Mindoro, Negros, Palawan, Panay, Polillo), Singapore (Changi), Thailand (Chumphon, Narathiwat, Phang Nga, Phu Ket, Satun, Trang, Trat), Vietnam (Kien Giang)

22. Cycas_elongata Vietnam (Binh Dinh, Khanh Hoa, Ninh Thuan, Phu Yen, Quang Ngai)

23. Cycas_ferruginea China (Guangxi), Vietnam (Lang Son, Thai Nguyen)

24. Cycas_fugax Vietnam (Phu Tho)

25. Cycas_guizhouensis China (Guangxi, Guizhou, Yunnan)

26. Cycas_hainanensis China (Hainan)

27. Cycas_hongheensis China (Yunnan)

28. Cycas_lindstromii Vietnam (Ba Ria- Vung Tau, Binh Thuan, Khanh Hoa, Ninh Thuan)

29. Cycas_litoralis Indonesia (Bali, Bengkulu, Jawa Barat, Jawa Tengah, Jawa Timur, Lampung,

30. Cycas_maconochiei Australia (NT)

31. Cycas_macrocarpa Malaysia (Kelantan, Pahang, Terengganu), Thailand (Chantaburi, Chumphon, Narathiwat, Ranong)

32. Cycas_media_ensata Australia (Queensland)

33. Cycas_media_media Australia (Queensland)

34. Cycas_micholitzii (Laos), Vietnam (Dac Lak, Gia Lai, Kon Tum)

35. Cycas_micronesica Micronesia (Mariana Islands)

36. Cycas_miquellii China, Japan (Ryukyu Islands)

37. Cycas_multipinnata China (Yunnan), Vietnam (Yen Bai)

38. Cycas_nongnoochiae Philippines (Luzon)

39. Cycas_ophiolitica Australia (Queensland)

40. Cycas_panzhihuaensis China (Sichuan, Yunnan)

41. Cycas_pectinata_A Bangladesh, Bhutan, China (Yunnan), NE India, Laos, Myanmar, Nepal, Thailand

(Chiang Mai, Kanchanaburi, Mae Hong Son, Phetchabun, Phrae, Sukhothai), Vietnam (Gia Lai, Kon Tum, Lam Dong, Quang Ngai)

42. Cycas_pectinata_B Bangladesh, Bhutan, China (Yunnan), NE India, Laos, Myanmar, Nepal, Thailand

(Chiang Mai, Kanchanaburi, Mae Hong Son, Phetchabun, Phrae, Sukhothai), Vietnam (Gia Lai, Kon Tum, Lam Dong, Quang Ngai)

43. Cycas_petraea Thailand (Loei)

44. Cycas_platyphylla Australia (Queensland)

45. Cycas_revoluta China, Japan (Ryukyu Islands)

46. Cycas_riuminiana Philippines (Luzon)

47. Cycas_rumphii Philippines (Luzon)

48. Cycas_schumanniana Papua New Guinea (Eastern Highlands, Madang, Morobe)

49. Cycas_seemanii Australia (Torres Strait Islands), Fiji, New

Caledonia, Tonga, Vanuatu

50. Cycas_segmentifida China (Guangxi, Guizhou, Yunnan), ?N Vietnam

51. Cycas_semota Australia (Queensland)

52. Cycas_sexseminifera China (Guangxi), Vietnam (Cao Bang, Ninh Binh, Thanh Hoa)

53. Cycas_siamensis Cambodia, Laos, Myanmar, Thailand (Chachoengsao, Chaiyaphum, Chonburi,

Kanchanaburi, Lampang, Nakhon Ratchasima, Phetchabun, Ratchaburi, Sakon Nakhon, Tak, Uthai Thani, Uttaridit), Vietnam (Dac Lak, Gia Lai, Kon Tum, Nghe An, Thanh Hoa)

54. Cycas_simplicipinna Laos, ?Myanmar, Thailand (Chiang Mai, Loei, Mae Hong Song, Phrae), Vietnam

(Quang Tri)

55. Cycas_sphaerica India (Orissa)

56. Cycas_szechuanensis China (Fujian, Guangdong)

57. Cycas_taitungensis China (Taiwan)

58. Cycas_tanqingii China (Yunnan), Vietnam (Lai Chau)

59. Cycas_tansachana Thailand (Saraburi)

60. Cycas_thouarsii Comoros, Kenya, Madagascar, Mozambique, Seychelles, Tanzania

61. Cycas_tropophylla Vietnam (Hai Phong, Quang Ninh)

62. Cycas_xipholepis Australia (Queensland)

63. Cycas_yorkiana Australia (Queensland)

64. Cycas_zeylanica India (Andamans and Nicobar Islands), Sri Lanka

65. Cycas_aenigma Philippines (Palawan - cult.)

66. Cycas_angulata Australia (NT, Queensland)

67. Cycas_annaikalensis India (Western Ghats)

68. Cycas_arenicola Australia (NT)

69. Cycas_arnhemica Australia (NT)

70. Cycas_badensis Australia (Queensland)

71. Cycas_balansae China (Guangxi), Vietnam (Lang Son, Quang Ninh, Thai Nguyen, Vinh Phuc)

72. Cycas_bifida China (Guangxi, Yunnan), Vietnam (Cao Bang, Lang Son, Tuyen Quang)

73. Cycas_brunnea Australia (NT, Queensland)

74. Cycas_campestris Papua New Guinea (Central, Gulf)

75. Cycas_canalis Australia (NT)

76. Cycas_candida Australia (NT)

77. Cycas_cantafolia Malaysia (Johor)

78. Cycas_changjiangensis China (Hainan)

79. Cycas_conferta Australia (NT)

80. Cycas_cupida Australia (Queensland)

81. Cycas_curranii Philippines (Palawan)

82. Cycas_desolata Australia (Queensland)

83. Cycas_elephantipes Thailand (Chaiyaphum)

84. Cycas_falcata Indonesia (Sulawesi Selatan, Sulawesi Tenggara)

85. Cycas_hoabinhensis Vietnam (Ha Nam, Ha Tay, Hoa Binh, Ninh Binh)

86. Cycas_indica A. India (Karnataka)

87. Cycas_inermis Vietnam (Da Nang, Dong Nai, Khanh Hoa, Quang Nam)

88. Cycas_javana Indonesia (Jawa Barat, Jawa Tengah, Jawa Timur)

89. Cycas_lacrimans Philippines (Mindanao)

90. Cycas_lane-poolei Australia (WA)

91. Cycas_megacarpa Australia (Queensland)

92. Cycas_montana Indonesia (Nusa Tenggara Timur)

93. Cycas_nathorstii India (Tamil Nadu), N Sri Lanka

94. Cycas_nitida Philippines (Luzon)

95. Cycas_orientis Australia (NT)

96. Cycas_pachypoda Vietnam (Binh Thuan, Ninh Thuan)

97. Cycas_papuana Indonesia (Papua), Papua New Guinea (Western)

98. Cycas_pranburiensis Thailand (Prachuap Khiri Khan)

99. Cycas_pruinosa Australia (NT, WA)

100. Cycas_saxatilis Philippines (Palawan)

101. Cycas_scratchleyana Indonesia (Papua, Maluku, West Papua), Papua New Guinea (Central, Gulf, Milne

Bay, Western)

102. Cycas_shanyaensis China (Hainan Island)

103. Cycas_silvestris Australia (Queensland)

104. Cycas_sundaica Indonesia (Nusa Ternggara Timur)

105. Cycas_taiwaniana China (Guangdong)

106. Cycas_terryana Australia (Queensland)

107. Cycas_tuckeri Australia (Queensland)

108. Cycas_vespertilio Philippines (Cebu, Leyte, Luzon, Negros, Panay, Samar)

109. Cycas_wadei Philippines (Culion)

110. Cycas_zambalensis Philippines (Luzon)

111. Bowenia_serrulata Australia (Queensland)

112. Bowenia_spectabilis Australia (Queensland)

113. Ceratozamia_decumbens Mexico (Veracruz)

114. Ceratozamia_fusco-viridis Mexico (Hidalgo)

115. Ceratozamia_huastecorum Mexico (Veracruz)

116. Ceratozamia_latifolia Mexico (Hidalgo, Querétaro, San Luis Potosí, Veracruz)

117. Ceratozamia_mexicana Mexico (?Puebla, Veracruz)

118. Ceratozamia_microstrobila Mexico (San Luis Potosí)

119. Ceratozamia_miqueliana Mexico (Chiapas, Tabasco, Veracruz)

120. Ceratozamia_mirandae Mexico (Chiapas)

121. Ceratozamia_mixeorum Mexico (Oaxaca)

122. Ceratozamia_morettii Mexico (Veracruz)

123. Ceratozamia_sabatoi Mexico (Hidalgo, Querétaro)

124. Ceratozamia_whitelockiana Mexico (Oaxaca)

125. Ceratozamia_zaragozae Mexico (San Luis Potosí)

126. Ceratozamia_alvarezii Mexico (Chiapas)

127. Ceratozamia_becerrae Mexico (Chiapas, Tabasco)

128. Ceratozamia_brevifrons Mexico (Veracruz)

129. Ceratozamia_chimalapensis Mexico (Oaxaca)

130. Ceratozamia_euryphyllidia Mexico (Oaxaca, Veracruz)

131. Ceratozamia_hildae Mexico (Querétaro, San Luis Potosí)

132. Ceratozamia_hondurensis Honduras (Atlántida)

133. Ceratozamia_kuesteriana Mexico (Tamaulipas)

134. Ceratozamia_matudae Guatemala (Huehuetenango, San Marcos), Mexico (Chiapas)

135. Ceratozamia_norstogii Mexico (Chiapas, Oaxaca)

136. Ceratozamia_robusta Belize (Cayo, Stann Creek, Toledo), Guatemala (Alta Verapaz, Petén, Quiché, Huehuetenango, Izabal), Mexico (Chiapas, Oaxaca, Veracruz)

137. Ceratozamia_santillanii Mexico (Chiapas)

138. Ceratozamia_vovidesii Mexico (Chiapas)

139. Ceratozamia_zoquorum Mexico (Chiapas)

140. Chigua_bernalii Colombia (Cordoba)

141. Dioon_edule Mexico (Hidalgo, Querétaro, San Luis Potosí, Tamaulipas, Veracruz)

142. Dioon_merolae Mexico (Chiapas, Oaxaca)

143. Dioon_purpusii Mexico (Oaxaca)

144. Dioon_spinulosum Mexico (Oaxaca, Veracruz)

145. Dioon_tomasellii Mexico (Durango, Jalisco, Nayarit)

146. Dioon_angustifolium Mexico (Nuevo León, Tamaulipas)

147. Dioon_argenteum Mexico (Oaxaca)

148. Dioon_califanoi Mexico (Oaxaca, Puebla)

149. Dioon_caputoi Mexico (Oaxaca, Puebla)

150. Dioon_holmgrenii Mexico (Oaxaca)

151. Dioon_mejiae Honduras (Colón, Olancho, Yoro)

152. Dioon_rzedowskii Mexico (Oaxaca)

153. Dioon_sonorense Mexico (Sinaloa, Sonora)

154. Dioon_stevensonii Mexico (Guerrero, Michoacán)

155. Encephalartos_aemulans South Africa (KwaZulu- Natal)

156. Encephalartos_altensteinii South Africa (E Cape)

157. Encephalartos_aplanatus Swaziland

158. Encephalartos_arenarius South Africa (E Cape)

159. Encephalartos_barteri Benin (Bergu), Ghana, Nigeria

160. Encephalartos_bubalinus Kenya, Tanzania (Masai)

161. Encephalartos_caffer South Africa (E Cape)

162. Encephalartos_cerinus South Africa (KwaZulu- Natal)

163. Encephalartos_concinnus Zimbabwe (Mberengwa, Runde)

164. Encephalartos_cupidus South Africa (Mpumalanga)

165. Encephalartos_cycadifolius South Africa (Eastern Cape)

166. Encephalartos_dolomiticus South Africa (Limpopo)

167. Encephalartos_dyerianus South Africa (Limpopo)

168. Encephalartos_ eugene-maraisii South Africa (Limpopo)

169. Encephalartos_ferox Mozambique, South Africa (KwaZulu- Natal)

170. Encephalartos_friderici- South Africa (Eastern Cape, KwaZulu- guilielmi Natal)

171. Encephalartos_ghellinckii South Africa (Eastern Cape, KwaZulu- Natal)

172. Encephalartos_gratus Malawi, Mozambique

173. Encephalartos_hildebrandtii Kenya (Kilifi, Lamu), Tanzania (Lushoto, Tanga, Zanzibar Island)

174. Encephalartos_horridus South Africa (Eastern Cape)

175. Encephalartos_humilis South Africa (Mpumalanga)

176. Encephalartos_inopinus South Africa (Limpopo)

177. Encephalartos_ituriensis Democratic Republic of Congo, Uganda

178. Encephalartos_kisambo Kenya (Taita- Taveta)

179. Encephalartos_laevifolius South Africa (Eastern Cape, KwaZulu- Natal, Limpopo, Mpumalanga), Swaziland

180. Encephalartos_lanatus South Africa (Mpumalanga)

181. Encephalartos_laurentianus Angola, Democratic Republic of Congo

182. Encephalartos_lebomboensis Mozambique, South Africa (KwaZulu- Natal), Swaziland

183. Encephalartos_lehmannii South Africa (Eastern Cape)

184. Encephalartos_longifolius South Africa (Eastern Cape)

185. Encephalartos_ macrostrobilus Northern Uganda

186. Encephalartos_manikensis Mozambique (Manica), Zimbabwe

187. Encephalartos_middleburgensis South Africa (Mpumalanga)

188. Encephalartos_msinganus South Africa (KwaZulu- Natal)

189. Encephalartos_munchii Mozambique (Manica)

190. Encephalartos_natalensis South Africa (KwaZulu- Natal)

191. Encephalartos_ngoyanus South Africa (KwaZulu- Natal), Swaziland

192. Encephalartos_nubimontanus South Africa (Limpopo)

193. Encephalartos_paucidentatus South Africa (Mpumalanga), Swaziland

194. Encephalartos_princeps South Africa (Eastern Cape)

195. Encephalartos_pterogononus Mozambique (Manica)

196. Encephalartos_schaijesii Democratic Republic of Congo (Lualaba)

197. Encephalartos_schmitzii Democratic Republic of Congo (Haut- Katanga), Zambia

198. Encephalartos_sclavoi Tanzania (Tanga)

199. Encephalartos_senticosus South Africa (KwaZulu- Natal), Swaziland

200. Encephalartos_septentrionalis Sudan, Uganda

201. Encephalartos_tegulaneus Kenya

202. Encephalartos_transvenosus South Africa (Limpopo)

203. Encephalartos_trispinosus South Africa (Eastern Cape)

204. Encephalartos_turneri Mozambique (Nampula)

205. Encephalartos_villosus South Africa (Eastern Cape, KwaZulu- Natal), Swaziland

206. Encephalartos_whitelockii Uganda

207. Encephalartos_woodii South Africa (KwaZulu- Natal)

208. Encephalartos_brevifoliolatus South Africa (Limpopo)

209. Encephalartos_chimanimaniensis Mozambique, Zimbabwe

210. Encephalartos_delucanus Tanzania (Mpanda)

211. Encephalartos_equatorialis Uganda

212. Encephalartos_heenanii South Africa (Mpumalanga), Swaziland

213. Encephalartos_hirsutus South Africa (Limpopo)

214. Encephalartos_latifrons South Africa (Eastern Cape)

215. Encephalartos_mackenziei Sudan

216. Encephalartos_marunguensis Democratic Republic of Congo (Tanganyika)

217. Encephalartos_poggei Democratic Republic of Congo (Lulua, Lomami, Lualaba)

218. Encephalartos_relictus Swaziland

219. Encephalartos_umbeluziensis Mozambique, Swaziland

220. Lepidozamia_hopei Australia (Queensland)

221. Lepidozamia_peroffskyana Australia (North South Wales, Queensland)

222. Macrozamia_crassifolia Australia, (Queensland)

223. Macrozamia_diplomera Australia (North South Wales)

224. Macrozamia_douglasii Australia, (Queensland)

225. Macrozamia_dyeri Australia (Western Australia)

226. Macrozamia_elegans Australia (North South Wales)

227. Macrozamia_flexuosa Australia (North South Wales)

228. Macrozamia_fraseri Australia (Western Australia)

229. Macrozamia_glaucophylla Australia (North South Wales)

230. Macrozamia_johnsonii Australia (North South Wales)

231. Macrozamia_lomandroides Australia (Queensland)

232. Macrozamia_lucida Australia (North South Wales, Queensland)

233. Macrozamia_macdonnelli Australia (Northern Territory)

234. Macrozamia_miquelii Australia (Queensland)

235. Macrozamia_montana Australia (North South Wales)

236. Macrozamia_moorei Australia (Queensland)

237. Macrozamia_mountperriensis Australia (Queensland)

238. Macrozamia_pauli-guilielmi Australia (Queensland)

239. Macrozamia_platyrhachis Australia (Queensland)

240. Macrozamia_plurinervia Australia (North South Wales)

241. Macrozamia_polymorpha Australia (North South Wales)

242. Macrozamia_reducta Australia (North South Wales)

243. Macrozamia_riedlei Australia (Western Australia)

244. Macrozamia_serpentine Australia (Queensland)

245. Macrozamia_spiralis Australia (North South Wales)

246. Macrozamia_stenomera Australia (North South Wales)

247. Macrozamia_cardiacensis Australia, (Queensland)

248. Macrozamia_communis Australia (North South Wales)

249. Macrozamia_concinna Australia (North South Wales)

250. Macrozamia_conferta Australia, (Queensland)

251. Macrozamia_cranei Australia, (Queensland)

252. Macrozamia_fawcettii Australia (North South Wales)

253. Macrozamia_fearnsidei Australia, (Queensland)

254. Macrozamia_heteromera Australia (North South Wales)

255. Macrozamia_humilis Australia (North South Wales)

256. Macrozamia_longispina Australia (Queensland)

257. Macrozamia_machinii Australia (Queensland)

258. Macrozamia_macleayi Australia (Queensland)

259. Macrozamia_occidua Australia (Queensland)

260. Macrozamia_parcifolia Australia (Queensland)

261. Macrozamia_secunda Australia (North South Wales)

262. Macrozamia_viridis Australia (North South Wales)

263. Microcycas_calocoma Cuba (Pinar del Río)

264. Stangeria_eriopus South Africa (E Cape, KwaZulu- Natal)

265. Zamia_acuminata Costa Rica (San José), Nicaragua, Panama (Coclé, Panamá)

266. Zamia_amblyphyllidia Cuba, Jamaica, Puerto Rico

267. Zamia_angustifolia Bahamas (Eleuthera), Cuba (Guantánamo, Oriente, Santiago de Cuba)

268. Zamia_chigua Colombia (Chocó, Valle del Cauca)

269. Zamia_dressleri Panama (Colón, Kuna Yala)

270. Zamia_elegantissima Panama (Colón, Panamá)

271. Zamia_fairchildiana Costa Rica (Puntarenas, San José), Panama (Chiriquí)

272. Zamia_furfuracea_A Mexico (Veracruz)

273. Zamia_furfuracea_B Mexico (Veracruz)

274. Zamia_hymenophyllidia Colombia (Amazonas), Peru (Loreto)

275. Zamia_integrifolia Bahamas, Cayman Islands, Cuba, USA (Florida, Georgia)

276. Zamia_ipetiensis Panama (Panamá, Kuna Yala)

277. Zamia_katzeriana Mexico (Chiapas, Tabasco, Veracruz)

278. Zamia_kickxii Cuba (W Cuba, Isla de la Juventud)

279. Zamia_lacandona Mexico (Chiapas)

280. Zamia_lawsoniana Mexico(Chiapas, Hidalgo, Oaxaca, Tabasco, Tamaulipas, Veracruz)

281. Zamia_lecointei Brazil (Pará), Colombia (Amazonas), Peru (Loreto), Venezuela (Amazonas)

282. Zamia_loddigesii Mexico (Chiapas, Hidalgo, Oaxaca, Tabasco, Tamaulipas, Veracruz)

283. Zamia_manicata Colombia (Antioquia, Chocó), Panama (Darién)

284. Zamia_muricata Colombia (La Guajira, Meta,), Venezuela (Carabobo, Falcón, Guárico, Lara, Miranda, Yaracuy)

285. Zamia_neurophyllidia Costa Rica, S Nicaragua, Panama (Bocas

del Toro)

286. Zamia_obliqua Colombia (Antioquia, Chocó, Valle del Cauca), Panama (Darién, Panamá)

287. Zamia_paucijuga Mexico (Colima, Guerrero, Jalisco, Michoacán, Nayarit, Oaxaca)

288. Zamia_picta Belize (Toledo), Guatemala (Alta Verapaz, Izabal), Mexico (Chiapas)

289. Zamia_poeppigiana Brazil (Acre), Peru (Amazonas, Huánuco, Loreto, Pasco, San Martin, Ucayali)

290. Zamia_portoricensis W Puerto Rico

291. Zamia_pseudomonticola Costa Rica (Puntarenas), Panama (Chiriquí)

292. Zamia_pumila Cuba, Domican Republic, Puerto Rico

293. Zamia_purpurea Mexico (Oaxaca, Veracruz)

294. Zamia_pygmaea Cuba (W Cuba, Isla de la Juventud)

295. Zamia_skinneri Panama (Bocas del Toro)

296. Zamia_spartea Mexico (Oaxaca)

297. Zamia_standleyi Guatemala (Izabal), Honduras (Atlántida, Colón, Cortés, Olancho, Santa Barbara,

Yoro)

298. Zamia_variegata Belize (Toledo), Guatemala (Alta Verapaz, Izabal), Mexico (Chiapas)

299. Zamia_amazonum Brazil (Amazonas), Colombia, (Amazonas, Vaupés), Ecuador (Morona- Santiago, Napo, Sucumbíos), Peru

(Loreto), S Venezuela

300. Zamia_amplifolia Colombia (Valle del Cauca)

301. Zamia_boliviana North Bolivia, Brazil

302. Zamia_cremnophila Mexico (Tabasco)

303. Zamia_cunaria Panama (Colón, Panamá, Kuna de Wargandi, Kuna Yala)

304. Zamia_decumbens Belize (Cayo, Stann Creek, Toledo)

305. Zamia_disodon Colombia (Antioquia)

306. Zamia_encephalartoides Colombia (Santander)

307. Zamia_fischeri Mexico (Hidalgo, Querétaro, San Luis Potosí, Tamaulipas)

308. Zamia_gentryi Ecuador (Carchi, Esmeraldas)

309. Zamia_gomeziana Costa Rica (Limón)

310. Zamia_hamannii Panama (Bocas del Toro)

311. Zamia_herrerae El Salvador (Sonsonate), Guatemala (Quetzaltenango Retalhuleu, Santa Rosa, Suchitepéquez), Mexico (Chiapas)

312. Zamia_imperialis Panama (Coclé, Panamá, Veraguas)

313. Zamia_incognita Colombia (Antioquia, Boyacá, Santander)

314. Zamia_inermis Mexico (Veracruz)

315. Zamia_lindenii Ecuador (Azuay, Bolivar, Chimborazo, El Oro, Esmeraldas, Guayas, Los Ríos,

Manabi, Pichincha), Peru (Tumbes)

316. Zamia_lindleyi Panama (Bocas del Toro, Chiriqui)

317. Zamia_lucayana Bahamas (Abaco, Long Island)

318. Zamia_macrochiera Peru (Loreto)

319. Zamia_meermanii Belize (Belize, Cayo)

320. Zamia_melanorrhachis Colombia (Antioquia, Córdoba, Santander)

321. Zamia_montana Colombia (Antioquia, Risaralda)

322. Zamia_monticola Guatemala (Alta Verapaz)

323. Zamia_nesophila Panama (Bocas del Toro)

324. Zamia_onan-reyesii Honduras (Cortés)

325. Zamia_oreillyi Honduras (Atlántida)

326. Zamia_prasina Belize (Belize, Cayo, Orange Walk, Stann Creek, Toledo), Guatemala (Petén),

Mexico (Campeche, Chiapas, Tabasco, Quintana Roo, Yucatán)

327. Zamia_pseudoparasitica Panama (Bocas del Toro, Coclé, Colón, Veraguas)

328. Zamia_pyrophylla Colombia (Chocó)

329. Zamia_restrepoi Colombia (Cordoba)

330. Zamia_roezlii Colombia (Amazonas, Chocó, Nariño, Valle del Cauca), Ecuador (Esmeraldas,

Imbabura)

331. Zamia_sandovalii Honduras (Atlántida)

332. Zamia_soconuscensis Mexico (Chiapas)

333. Zamia_stricta Cuba (Oriente)

334. Zamia_tolimensis Colombia (Tolima)

335. Zamia_tuerckheimii Guatemala (Alta Verapaz)

336. Zamia_ulei W Brazil, Colombia (Amazonas, Guainía), Ecuador (Napo, Pastaza), Peru (Loreto, Madre de Dios)

337. Zamia_urep Peru (Huánuco)

338. Zamia_vazquezii Mexico (Veracruz)

339. Zamia_wallisii Colombia (Antioquia)

2.2 DATA ANALYSIS

Species richness, mean ED, and mean EDGE were determined per grid cells and simple regression and one-way ANOVA were used in the assessment of the relationship between variables.

2.2.1 Species richness, ED, and EDGE maps

The cycad distribution is well known and most species are endemic to very restricted regions. Based on this knowledge, species distribution data retrieved from GBIF was cleaned to avoid duplicate and remove all obviously false species occurrence. The clean distribution was then projected onto a Behrmann equal-area cylindrical projection in ArcMap v.10, and gridded at a resolution of 50 X 50 km. A series of maps were generated to capture spatial variation in species richness (SR), mean ED and mean EDGE per grid cells. Species richness is simply the number of species in a grid cell. ED is defined above (Chapter 1) and calculated using the R library Picante (Kembel et al., 2010).

2.2.2 Statistical analysis

The relationships between ED and both geographic range and altitude were assessed using simple linear regression. However, the relationships between ED and both geographic origins of species and threats (threat status: threatened vs. non-threatened; threat level: LC, NT, VU etc.) were assessed using one-way ANOVA.

Prior to EDGE evaluation, Data Deficient species were excluded from the dataset and GE (Global Endangerment) was coded as follows: Least Concern = 0, Near Threatened and Conservation Dependent = 1, Vulnerable = 2, Endangered = 3, Critically Endangered = 4 (Butchart et al., 2005). EDGE scores were then calculated for all species using the standard algorithm (Isaac et al., 2007):

EDGE = ln(1+ED) + GE * ln(2).

Then IUCN database was explored to identify species with high EDGE scores that are not included in any of protected areas.

CHAPTER 3

RESULTS AND DISCUSSION Cycads occur in the tropics and sub tropics and in all these biogeographical regions, ED values are on average quite high with cycads of American origin being the most evolutionary distinct. ED values do not strongly correlate with geographical parameters i.e. range, size, and altitude. The assessment of threat categories versus ED revealed that most of the species with high ED values are highly threatened but there are cases of mismatch.

3.1. GEOGRAPHICAL PATTERN OF CYCAD RICHNESS

Figure 3.1 shows the overall distribution pattern of cycad worldwide using information retrieved from GBIF. Cycad species have a tropical and subtropical distribution. The highest richness is found in Central America, eastern Southern Africa and eastern Australia. The diversity of cycads is concentrated in tropical and sub-tropical regions in warm and dry climate. This is a general geographic pattern for species richness, irrespective of lineages (e.g. angiosperms, Jansson et al., 2008; mammals, Rolland et al., 2014), which is potentially the result of a rapid speciation and low extinction rate in the tropics in comparison to temperate regions (Rolland et al., 2014). Climate and environmental heterogeneity as well as energy availability are also potential explanations for high species richness in the tropics (Hawkins et al., 2003; Field et al., 2008; Jansson and Davies, 2008). Although these factors may have been important in constraining biodiversity spatial distribution in general, the restriction of cycads distribution to tropics in particular, could be the results of the tropics being a ‘‘museum’’ for ancient or relictual lineages (Chown and Gaston, 2000); these ancient lineages (here cycads) underwent recent radiations triggered by historical global climate change that shapes current diversity of cycads (Nagalingum et al., 2011; Yessoufou et al., 2014; Condamine et al., 2015).

(e) SR

af_freq.img Value 26High : 11

1Low : 1

Figure(f) PD 3.1 Geography of cycad species richness

3.2. GEOGRAPHY OF EVOLUTIONARY DISTINCTIVENESS (ED) OF CYCADS

af_freq.img Value All the phylogenetic analyses are based on the first ever complete phylogeny of cycads that 1034.97High : 11 was reconstructed and shown in Figure 3.2 below. This phylogeny comprises all 339 extant cycad taxa149.72Low : 1 recognised in this study and distributed among 11 genera. No misplacement of taxa is noted with regard to known cycad topological structure.

Cycad species play important ecological roles which include inter alia mutualistic symbiotic relationships with legumes, actinorhizal plants, and cyanobacteria (Vessey et al., 2004). Their loss would therefore disrupt several ecological functions, and renewed attention should be given to prioritizing efforts to safeguard as much cycad diversity as possible. Such prioritization could be guided using ED or EDGE scores. On the global ranking, ED scores range from 10.587 MY (Cycas micronesica and Cycas zeylanica) to 98.762 MY (Microcycas calocoma) (SD = ±12.62) (Table 3.1). The geographical pattern of ED is shown in Figure 3.3a which depicts the average ED values per grid cell. High average ED values are observed across all known biogeographic regions of cycads, and are particularly more pronounced in America and Southern Africa. When ED, a diversity metric that captures evolutionary

differences between species (Isaac et al., 2007), is high, this may correspond to non-random phenotypes (Redding et al., 2010) and uniquely divergent genomes (Warren et al., 2008) and thus captures a large proportion of total evolutionary history of a particular clade (here cycads) (Redding et al., 2008). High ED can therefore guide prioritization efforts (Faith et al., 1992) or inform us on spatially efficient conservation planning (e.g. see Jetz et al., 2014 for spatial prioritization of birds). From that perspective, Southern Africa and America are priority regions to maximize phylogenetic diversity of cycads.

Cryptomer ia japonica Araucar ia heteroph ylla Ginkgo biloba Abies fir ma Outgroup Pseudotsuga menziesii Pinus strob us Microcycas calocoma Zamia herrer ae Microcycas Zamia encephalar toides Zamia pur purea Zamia montana Zamia lacandona Zamia macrochier a Zamia v azquezii Zamia incognita Zamia amb lyphyllidia Zamia kickxii Zamia amaz onum Zamia pumila Zamia disodon Zamia restrepoi Zamia str icta Zamia por toricensis Zamia integr ifolia Zamia decumbens Zamia angustif olia Zamia imper ialis Zamia p ygmaea Zamia ulei Zamia h ymenoph yllidia Zamia pseudopar asitica Zamia cunar ia Zamia iner mis Zamia pseudomonticola Zamia oreillyi Zamia roezlii Zamia f airchildiana Zamia tolimensis Zamia acuminata Zamia lecointei Zamia Zamia m uricata Zamia amplif olia Zamia neuroph yllidia Zamia lindle yi Zamia poeppigiana Zamia lindenii Zamia ipetiensis Zamia hamannii Zamia manicata Zamia luca yana Zamia tuerckheimii Zamia onan−re yesii Zamia chigua Zamia meer manii Zamia dressler i Zamia w allisii Zamia melanorrhachis Zamia cremnophila Zamia ob liqua Zamia elegantissima Zamia boliviana Zamia gentr yi Zamia paucijuga Zamia spar tea Zamia urep Zamia loddigesii Zamia la wsoniana Zamia furfur acea A Zamia pr asina Zamia furfur acea B Zamia socon uscensis Zamia katz eriana Zamia picta Zamia fischer i Zamia sando valii Zamia v ariegata Zamia standle yi Zamia nesophila Zamia monticola Zamia p yrophylla Zamia gomeziana Zamia skinner i Chigua ber nalii Chigua Bowenia spectabilis Bowenia serr ulata Bowenia Lepidozamia peroffsky ana Lepidozamia hopei Lepidozamia Encephalar tos mack enziei Encephalar tos ghellincki Encephalar tos fr ider iciguilielmi Encephalar tos humilis Encephalar tos lae vifolius Encephalar tos lanatus Encephalar tos cycadif olius Encephalar tos dyerianus Encephalar tos inopin us Encephalar tos latifrons Encephalar tos villosus Encephalar tos aplanatus Encephalar tos altensteinii Encephalar tos natalensis Encephalar tos ngo yanus Encephalar tos caff er Encephalar tos longif olius Encephalar tos woodii Encephalar tos transvenosus Encephalar tos hirsutus Encephalar tos paucidentatis Encephalar tos bre vifoliolatus Encephalar tos middleb urgensis Encephalar tos cupidus Encephalar tos aem ulans Encephalar tos lehmannii Encephalar tos equator ialis Encephalar tos arenar ius Encephalar tos tr ispinosus Encephalar tos horr idus Encephalar tos cer inus Encephalar tos pr inceps Encephalar tos lebomboensis Encephalar tos senticosus Encephalar tos pterogonon us Encephalar tos manik ensis Encephalartos Encephalar tos chimanimaniensis Encephalar tos delucan us Encephalar tos munchii Encephalar tos concinn us Encephalar tos septentr ionalis Encephalar tos macrostrobilus Encephalar tos bar teri Encephalar tos heenanii Encephalar tos msingan us Encephalar tos schmitzii Encephalar tos schaijesii Encephalar tos relictus Encephalar tos bubalin us Encephalar tos hildebr andtii Encephalar tos scla voi Encephalar tos kisambo Encephalar tos tegulaneus Encephalar tos laurentian us Encephalar tos whitelockii Encephalar tos itur iensis Encephalar tos mar unguensis Encephalar tos ferox Encephalar tos gr atus Encephalar tos tur neri Encephalar tos poggei Encephalar tos dolomiticus Encephalar tos nubimontan us Encephalar tos umbeluziensis Encephalar tos eugenemar aisii Macrozamia fr aseri Macrozamia fle xuosa Macrozamia stenomer a Macrozamia plur iner via Macrozamia lomandroides Macrozamia maclea yi Macrozamia macdonnelli Macrozamia spir alis Macrozamia machinii Macrozamia elegans Macrozamia humilis Macrozamia conf erta Macrozamia cr assifolia Macrozamia platyrhachis Macrozamia comm unis Macrozamia occidua Macrozamia concinna Macrozamia diplomer a Macrozamia longispina Macrozamia polymor pha Macrozamia pauliguilielmi Macrozamia glaucoph ylla Macrozamia secunda Macrozamia dy eri Macrozamia Macrozamia f awcettii Macrozamia reducta Macrozamia montana Macrozamia heteromer a Macrozamia moorei Macrozamia lucida Macrozamia douglasii Macrozamia mountperr iensis Macrozamia cardiacensis Macrozamia ser pentine Macrozamia r iedlei Macrozamia f earnsidei Macrozamia miquelii Macrozamia parcif olia Macrozamia vir idis Macrozamia johnsonii Macrozamia cr anei Dioon spin ulosum Dioon angustif olium Dioon tomasellii Dioon holmgrenii Dioon pur pusii Dioon calif anoi Dioon sonorense Dioon merolae Dioon mejiae Dioon Dioon rz edowskii Dioon argenteum Dioon edule Dioon ste vensonii Dioon caputoi Ceratozamia mir andae Ceratozamia bre vifrons Ceratozamia miqueliana Ceratozamia hondurensis Ceratozamia whitelockiana Ceratozamia mix eorum Ceratozamia v ovidesii Ceratozamia sabatoi Ceratozamia kuester iana Ceratozamia eur yphyllidia Ceratozamia me xicana Ceratozamia norstogii Ceratozamia latif olia Ceratozamia rob usta Ceratozamia matudae Ceratozamia huastecor um Ceratozamia Ceratozamia fusco viridis Ceratozamia z oquor um Ceratozamia morettii Ceratozamia decumbens Ceratozamia santillanii Ceratozamia chimalapensis Ceratozamia alv arezii Ceratozamia microstrobila Ceratozamia hildae Ceratozamia becerr ae Ceratozamia zar agozae Stanger ia er iopus Cycas conf erta Stangeria Cycas taiw aniana Cycas balansae Cycas pr anburiensis Cycas ferruginea Cycas sz echuanensis Cycas nitida Cycas taitungensis Cycas re voluta Cycas terr yana Cycas ar nhemica Cycas hoabinhensis Cycas petr aea Cycas candida Cycas or ientis Cycas hongheensis Cycas chamaoensis Cycas pectinata A Cycas siamensis Cycas clivicola Cycas elongata Cycas nongnoochiae Cycas tuck eri Cycas condaoensis Cycas angulata Cycas tansachana Cycas badensis Cycas pectinata B Cycas papuana Cycas lindstromii Cycas annaikalensis Cycas sphaer ica Cycas cantaf olia Cycas elephantipes Cycas pr uinosa Cycas circinalis Cycas beddomei Cycas indicaA. Cycas silv estris Cycas desolata Cycas arenicola Cycas calcicola Cycas media media Cycas aenigma Cycas schumanniana Cycas apoa Cycas bifida Cycas montana Cycas maconochiei Cycas xipholepis Cycas ar mstrongii Cycas wadei Cycas Cycas platyph ylla Cycas megacar pa Cycas pach ypoda Cycas cair nsiana Cycas semota Cycas couttsiana Cycas ophiolitica Cycas basaltica Cycas zambalensis Cycas campestr is Cycas saxatilis Cycas yorkiana Cycas media ensata Cycas bougain villeana Cycas seemanii Cycas lane−poolei Cycas r umphii Cycas thouarsii Cycas micronesica Cycas zeylanica Cycas litor alis Cycas edentata Cycas shan yaensis Cycas chamber lainii Cycas r iuminiana Cycas macrocar pa Cycas vesper tilio Cycas ja vana Cycas br unnea Cycas panzhihuaensis Cycas aculeata Cycas canalis Cycas dolichoph ylla Cycas changjiangensis Cycas tanqingii Cycas cupida Cycas che valier i Cycas simplicipinna Cycas collina Cycas br achycantha Cycas tropoph ylla Cycas guizhouensis Cycas debaoensis Cycas diannanensis Cycas falcata Cycas m ultipinnata Cycas sundaica Cycas sexseminif era Cycas scr atchle yana Cycas miquellii Cycas lacr imans Cycas nathorstii Cycas segmentifida Cycas micholitzii Cycas fugax Cycas iner mis Cycas curr anii Cycas hainanensis

Figure 3.2. First complete phylogeny of cycads comprising 339 taxa in 11 genera. See text for technique of reconstruction. All 11 genera are highlighted in the figure (Cycas, Stangeria, Ceratozamia, Dioon, Macrozamia, Encephalartos, Lepidozamia, Bowenia, Chigua, Zamia and Macrocycas).

Table 3.1: EDGE and ED scores of all cycad species with their geographic distribution parameters. Species are listed in decreasing order of EDGE values. Geographic parameters are spatial distribution range and altitude. Global endangerment was measured following IUCN threat categories: LC, least Concern; NT, Near Threatened; VU, Vulnerable; EN, Endangered and CR, Critically Endangered.

Range Minimu Maximu m m altitude Ranking altitude Global (m above (km2) Endangerme ED scores EDGE (m above sea level) Species nt (MY) scores sea level)

1 Microcycas calocama CR 98.76152685 7.375371 NA NA NA

2 Chigua bernalii CR 92.77870776 7.313527 NA NA NA

3 Zamia vazquezii CR 66.91129942 6.990938 NA NA NA

4 Encephalartos dyerianus CR 47.18980637 6.647736 0.3 NA 700

5 Encephalartos inopinus CR 46.26646889 6.62839 NA 600 800

6 Zamia macrochiera CR 45.24071863 6.606449 NA NA NA

7 Ceratozamia zoquorum CR 44.33579558 6.586686 40 NA NA

8 Cycas szechuanensis CR 42.39771664 6.542996 NA NA NA

9 Zamia spartea CR 41.82244706 6.529651 1235 NA NA

10 Ceratozamia chimalapensis CR 39.54590223 6.475023 NA NA NA

11 Ceratozamia fuscoviridis CR 39.03436558 6.462327 NA NA NA

12 Ceratozamia huastercorum CR 39.03436558 6.462327 NA NA NA

13 Zamia urep CR 38.73881806 6.454917 30 NA NA

14 Cycas fugax CR 37.99666306 6.436065 NA NA 200

15 Encephalartos cupidus CR 34.96229599 6.35506 58 700 1 500

16 Encephalartos NA 1 100 1 400 middleburgensis CR 34.96229599 6.35506

17 Zamia hymenophyllidia CR 34.88072687 6.352789 NA NA NA

18 Zamia imperialis CR 34.74486641 6.348995 NA NA NA

19 Encephalartos whitelockii CR 34.4420844 6.340489 NA 1 000 1 300

20 Cycas curranii CR 34.03290306 6.328876 NA NA NA

21 Ceratozamia decumbens CR 33.73551899 6.320351 NA NA NA

22 Ceratozamia santillanii CR 33.73551899 6.320351 NA NA NA

23 Zamia prasina CR 33.45520758 6.312249 NA NA NA

24 Zamia monticola CR 31.85847478 6.264798 NA NA NA

25 Zamia onan-reyesii CR 31.72164993 6.260626 NA NA NA

26 Zamia tolimensis CR 31.59700529 6.256809 NA NA NA

27 Zamia nesophila CR 31.01836428 6.238898 NA NA NA

28 Encephalartos dolomiticus CR 30.92972888 6.236126 NA 1 100 1 500

29 Ceratozamia zaragozae CR 30.23118189 6.214006 45 NA NA

30 Cycas taiwaniana EN 60.36197811 6.196232 NA 400 1 100

31 Dioon caputoi EN 60.02894657 6.19079 NA NA NA

32 Zamia hamannii CR 29.18056715 6.179787 NA NA NA

33 Dioon spinulosum EN 58.1311588 6.170667 NA NA NA

34 Zamia decumbens CR 28.15189141 6.145109 NA NA NA

35 Cycas hongheensis CR 28.09396076 6.143119 NA 400 600

36 Zamia wallisii CR 28.07088709 6.142326 NA NA NA

37 Macrozamia cranei EN 54.6574816 6.098658 NA 400 600

38 Encephalartos aemulans CR 26.60506999 6.090588 NA 600 1 100

39 Zamia inermis CR 26.59267689 6.090139 NA NA NA

40 Zamia gentry CR 26.08392961 6.071529 5 NA NA

41 Cycas kuesteriana CR 25.53290348 6.050974 NA NA NA

42 Zamia pyrophylla CR 25.36689544 6.044698 NA NA NA

43 Encephalartos pterogononus CR 24.90164089 6.026895 35 700 1 000

44 Encephalartos laevifolius CR 24.40140887 6.007393 NA 950 1 800

45 Zamia pygmaea CR 24.13964507 5.997035 NA NA NA

46 Zamia montana CR 23.94413954 5.989228 NA NA NA

47 Zamia purpuria CR 23.94413954 5.989228 NA NA NA

48 Zamia skinneri EN 47.67761744 5.964661 6250 NA NA

49 Encephalartos hirsutus CR 23.22916216 5.960146 NA 800 1 000

50 Ceratozamia morettii EN 47.26377399 5.956123 10 NA NA

51 Ceratozamia miqueliana CR 22.91371599 5.947041 NA NA NA

52 Encephalartos cerinus CR 22.75749149 5.940487 NA 500 900

53 Encephalartos latifrons CR 22.23855256 5.918401 NA 200 600

54 Zamia amplifola CR 21.18935565 5.872201 NA NA NA

55 Ceratozamia mexeorum EN 42.82402982 5.859624 25 NA NA

56 Stangeria eriopus VU 86.06691786 5.852971 NA 10 750

57 Dioon stevensonii CR 20.61607388 5.846026 NA NA NA

58 Cycas annaikalensis CR 20.23621295 5.828297 NA NA 940

59 Cycas zambalensis CR 20.19838475 5.826514 NA NA NA

60 Ceratozamia euryphyllidia CR 20.08057361 5.820941 NA NA NA

61 Ceratozamia hondurensis CR 19.85266019 5.81007 NA NA NA

62 Ceratozamia alvarezii EN 39.54590223 5.781876 16 NA NA

63 Cycas pachypoda CR 19.21076297 5.778804 NA NA NA

64 Cycas wadei CR 19.06554934 5.771593 NA 20 50

65 Zamia lacandona EN 38.76276788 5.762373 3 400 NA NA

66 Zamia variegate EN 36.92315299 5.715003 NA NA NA

67 Encephalartos heenanii CR 17.77268043 5.704991 300 750 1 750

68 Encephalartos msinganus CR 17.77268043 5.704991 10 900 1 200

69 Ceratozamia hildae EN 36.39391589 5.70095 NA NA NA

70 Cycas cantafolia CR 17.23081084 5.675702 NA NA NA

71 Zamia katzeriana EN 34.87334824 5.659436 NA NA NA

72 Ceratozamia mirandae EN 34.77023182 5.656558 NA NA NA

73 Cycas hainanensis EN 34.03290306 5.635729 NA 0 1200

74 Zamia furfuracea_A EN 33.70254139 5.626254 630 NA NA

75 Zamia disodon CR 16.34563319 5.62593 NA NA NA

76 Zamia restrepoi CR 16.34563319 5.62593 NA 75 150

77 Macrozamia elegans EN 33.38726199 5.617128 112 120 150

78 Cycas tansachana CR 15.77084129 5.59223 10 NA 400

79 Cycas chamoensis CR 14.78945112 5.531931 NA NA NA

80 Zamia kickxii CR 14.68817057 5.525496 NA NA NA

81 Ceratozamia becerrae EN 30.23118189 5.520859 1 000 NA NA

82 Cycas elephantipes EN 29.13189834 5.485026 NA NA NA

83 Cycas changjiangensis EN 29.0368105 5.481865 NA 600 800

84 Cycas javana EN 28.43630201 5.46167 NA NA NA

85 Encephalartos eugenemaraisii EN 28.26662054 5.455889 NA 1 400 1 500

86 Encephalartos umbeluziensis EN 28.26662054 5.455889 336 50 120

87 Zamia dressleri EN 28.07088709 5.449179 2 530 NA NA

88 Encephalartos munchii CR 13.48623715 5.445788 3 1 000 1 100

89 Zamia lucayana EN 27.68496665 5.435815 13 NA NA

90 Zamia meermanii EN 27.52500143 5.430222 NA NA NA

91 Encephalartos equatorialis CR 12.85206894 5.401023 5 NA 1 000

92 Zamia ipentiensis EN 26.52220215 5.394435 50 NA NA

93 Encephalartos ngoyanus VU 53.41135673 5.382867 NA 200 600

94 Zamia picta EN 25.88300299 5.370936 NA NA NA

95 Zamia fischeri EN 25.79943714 5.367822 2770 NA NA

96 Zamia herrerae VU 52.42318283 5.364539 NA NA NA

97 Encephalartos gratus VU 52.39442418 5.364001 NA 650 900

98 Cycas taitungensis EN 25.68127028 5.363403 65 400 900

99 Macrozamia spiralis EN 25.61487566 5.360912 NA NA NA

100 Cycas beddomei EN 25.56325424 5.35897 388 300 900

101 Cycas circinalis EN 25.56325424 5.35897 NA 300 1000

102 Ceratozamia sabatoi EN 25.53290346 5.357827 NA NA NA

103 Ceratozamia matudae EN 24.96245108 5.336093 5 000 NA NA

104 Cycas candida EN 24.93180331 5.334912 55 NA NA

105 Dioon califanoi EN 2465399859 5.324141 126 NA NA

106 Cycas hoabinhensis EN 24.43045531 5.315389 NA 50 150

107 Encephalartos sclavoi CR 11.67276377 5.315389 NA 1 800 2 100

108 Zamia neurophyllidia VU 48.38625065 5.285966 NA NA NA

109 Macrozamia flexuosa EN 22.74607533 5.246859 NA NA NA

110 Cycas debaoensis CR 10.80661968 5.241249 NA 300 1300

111 Macrozamia humilis VU 45.99115911 5.236254 NA NA 600

112 Dioon sonorense EN 22.43077809 5.233492 NA NA NA

113 Cycas macrocarpa VU 45.82548691 5.232722 NA NA NA

114 Ceratozamia norstogii EN 22.39374741 5.23191 1 100 NA NA

115 Zamia furfuracea_B EN 21.53129458 5.194347 631 NA NA

116 Cycas elongate EN 21.47247138 5.191733 NA 50 200

117 Dioon holmgrenii EN 21.43384545 5.190012 NA NA NA

118 Cycas pranburiensis VU 43.33354594 NA 5 30

5.178036

119 Dioon rzedowskii EN 20.82433129 5.162467 25 NA NA

120 Ceratozamia latifolia EN 20.70880668 5.15716 NA NA NA

121 Ceratozamia robusta EN 20.70880668 5.15716 NA NA NA

122 Ceratozamia microstrobila VU 41.76928923 5.142115 1 000 NA NA

123 Cycas lindstromii EN 20.23621295 5.135149 4280 0 30

124 Encephalartos lebomboensis EN 20.10179349 5.1288 NA 500 1 000

125 Ceratozamia whitelockiana EN 19.85266019 5.116923 NA NA NA

126 Zamia elegantissima EN 19.60962709 5.1052 100 NA NA

127 Zamia cunaria VU 39.96309189 5.098966 3140 NA NA

128 Macrozamia pauliguilielmi EN 18.55765384 5.052825 NA 5 25

129 Cycas platyphylla EN 18.53765384 5.051785 NA 400 750

130 Cycas inermis VU 37.99666306 5.04977 NA NA NA

131 Cycas multipinnata EN 18.43632098 5.046585 27 040 200 1300

132 Cycas micholitzii VU 36.43867597 5.008999 NA 130 600

133 Cycas segmentifida VU 36.43867597 5.008999 NA 600 900

134 Encephalartos concinnus EN 17.17823109 4.979666 NA 800 900

135 Zamia portoricensis EN 16.55332369 4.944685 220 NA NA

136 Zamia creminophila EN 16.38093259 4.934815 53 NA NA

137 Zamia melanorrhachis EN 16.38093259 4.934815 NA NA NA

138 Macrozamia machinii VU 33.38726199 4.923981 460 320 460

139 Macrozamia plurinervia EN 15.77149983 4.899123 NA NA NA

140 Zamia acuminate VU 32.43503846 4.895899 NA NA NA

141 Macrozamia crassifolia VU 32.28496411 4.8914 160 340 420

142 Macrozamia conferta VU 32.28496411 4.8914 423 600 750

143 Macrozamia viridis EN 15.17074349 4.862645 1 000 NA NA

144 Zamia standleyi VU 31.01836428 4.852604 NA NA NA

145 Cycas panzhihuaensis VU 30.05926101 4.822191 14 500 1 100 2000

146 Cycas balansae NT 60.96541261 4.819724 NA 100 800

147 Cycas collina VU 29.8268445 4.81468 20 000 400 900

148 Cycas lacrimans EN 14.35800448 4.811078 NA NA NA

149 Cycas conferta NT 60.36197811 4.809938 NA NA NA

150 Cycas riuminiana EN 14.32453779 4.808897 NA 615 800

151 Encephalartos NA NA 1 000 chimanimaniensis EN 14.30221365 4.807439

152 Cycas armstrongii VU 29.42156612 4.801446 NA NA NA

153 Encephalartos horridus EN 13.80458849 4.781111 NA 100 400

154 Encephalartos macrostrobilus EN 13.78089777 4.772777 50 900 1 400

155 Encephalartos angustifolia VU 28.15189141 4.758814 9 000 NA NA

156 Encephalartos delucanus EN 13.48623715 4.752641 NA 1 200 1 950

157 Encephalartos marunguensis VU 27.0007844 4.718527 7 500 1 400 1 700

158 Encephalartos arenarius EN 12.5367299 4.707876 450 100 200

159 Encephalartos caffer NT 53.41135673 4.68972 NA 300 700

160 Macrozamia lomandroides EN 12.5367299 4.684848 NA NA NA

161 Cycas condaoensis VU 26.07318304 4.684838 20 NA NA

162 Cycas chamberlainii EN 12.51480679 4.683227 NA 615 800

163 Ceratozamia vovidesii VU 25.25.92662591 4.67941 NA 1 000 1 700

164 Zamia encephalartoides VU 25.66209454 4.669537 266 NA NA

165 Zamia gomeziana VU 25.36689544 4.658404 NA NA NA

166 Cycas brachycantha NT 51.24649223 4.64912 NA NA NA

167 Cycas tropophylla NT 51.24649223 4.64912 400 NA NA

168 Macrozamia secunda VU 24.76861886 4.635452 NA NA NA

169 Encephalartos humilis VU 24.40140887 4.621099 NA NA NA

170 Encephalartos kisambo EN 11.67276377 4.618897 NA 800 1 800

171 Encephalartos paucidentatis VU 23.34009366 4.578419 424 1 000 1 500

172 Cycas terryana VU 23.34009366 4.576505 NA NA NA

173 Encephalartos princeps VU 22.75749149 4.554192 1 870 200 800

174 NA NA NA Dioon merolae VU 22.43077809 4.540345

11250 NA NA 000

175 Cycas micronesica EN 10.58724336 4.529346

176 Cycas seemani VU 21.69838755 4.508588 NA 0 600

177 Zamia soconuscensis VU 21.53129458 4.5012 NA NA NA

178 Dioon purpusii VU 21.43384545 4.496865 NA 1 000 1 500

179 Encephalartos altensteinii VU 21.40559109 4.495605 NA 0 600

180 Cycas cairnsiana VU 21.22964922 4.487721 NA 450 500

181 Cycas ferruginea NT 43.33354594 4.484889 7215 NA NA

182 Encephalartos barteri VU 21.02188177 4.478331 NA 400 1 400

183 Dioon argenteum VU 20.82433129 4.46932 350 1 100 1 600

184 Cycas silvestris VU 20.74771168 4.465803 NA NA NA

185 Cycas cupida VU 20.616169 4.459736 60 NA NA

186 Encephalartos senticosus VU 20.10179349 4.435652 NA 300 800

187 Ceratozamia Mexicana VU 20.08057261 4.434646 NA NA NA

188 Encephalartos schmitzii VU 19.82233343 4.42232 NA 1 000 1 400

189 Encephalartos ghellincki VU 19.81469597 4.421954 NA 700 2 400

190 Cycas nongnoochiae VU 19.79711088 4.421108 NA 50 100

191 Cycas tuckeri VU 19.79711088 4.421108 15 NA NA

192 Cycas saxatilis VU 19.20190975 4.392072 NA NA NA

193 Encephalartos aplanatus VU 19.12329106 4.388172 295 100 600

194 Dioon angustifolium VU 18.87281058 4.375647 NA NA NA

195 Dioon tomasellii VU 18.87281058 4.375647 NA 600 1 850

196 Zamia loddigesii NT 38.73881806 4.375476 NA NA NA

197 Cycas bifida VU 18.72093951 4.367975 NA 100 300

198 Cycas megacarpa VU 18.53765384 4.358638 NA 150 300

199 Cycas aculeate VU 18.22700347 4.34261 10 NA NA

200 Cycas pectinata_B VU 17.56072929 4.307342 NA 600 1 300

201 Zamia oreillyi VU 17.15521714 4.285252 NA NA NA

202 Encephalartos ferox NT 35.18108407 4.281684 NA 20 100

203 Zamia pseudoparasitica NT 34.88072687 4.273347 NA NA NA

204 Encephalartos manikensis VU 16.90228432 4.271223 NA 600 1 400

205 Encephalartos lanatus NT 34.20526447 4.254343 NA 1 200 1 500

206 Zamia stricta VU 16.55332369 4.251538 25 NA NA

207 Cycas desolata VU 16.41264168 4.243491 NA 450 550

208 Zamia lawsoniana NT 33.70254139 4.23996 NA NA NA

209 Macrozamia platyrhachis VU 15.78571553 4.206823 NA NA NA

210 Zamia integrifolia NT 32.54882493 4.206149 NA NA NA

211 Macrozamia fawcettii NT 32.37059711 4.200822 5 500 5 550

212 Cycas couttsiana NT 31.82361505 4.184295 NA NA 700

213 Macrozamia occidua VU 15.18300583 4.170256 10 800 1 000

214 Macrozamia cardiacensis VU 15.18194666 4.170191 14 500 640

215 Macrozamia parcifolia VU 15.17074349 4.169498 NA 60 220

216 Encephalartos longifolius NT 30.93709813 4.156915 NA 200 700

217 Cycas ophiolitica VU 14.90585325 4.152982 NA 150 250

218 Cycas semota NT 30.74310522 4.150823 NA NA NA

219 Zamia incognita VU 14.74109482 4.142569 NA NA NA

220 Zamia amblyphyllidia VU 14.68817052 4.139201 NA NA NA

221 Cycas brunnea NT 30.05926101 4.129044 NA NA NA

222 Cycas simplicipinna NT 29.8268445 4.121533 NA 600 1 300

223 Cycas nathorstii VU 14.35800448 4.117931 NA 30 300

224 Cycas sexseminifera VU 14.11838029 4.102206 NA NA NA

225 Zamia manicata NT 29.18056715 4.100345 NA NA NA

226 Encephalartos trispinosus VU 13.90458849 4.087963 NA 100 600

227 Cycas vespertilio NT 28.43630201 4.075376 NA NA NA

228 Cycas pectinata_A VU 13.66021178 4.071432 NA 600 1 300

229 Zamia tuerckeimii NT 27.68496665 4.04952 NA NA NA

230 Zamia chigua NT 27.52500143 4.043928 NA NA NA

231 Encephalartos ituriensis NT 27.0007844 4.02538 NA 1 100 1 200

232 Macrozamia johnsonii LC 54.6574816 4.019217 222 NA NA

233 Zamia boliviana NT 26.80183661 4.018249 NA NA NA

234 Encephalartos schaijesii VU 12.5674151 3.993965 NA 1 450 1 500

235 Zamia paucijuga NT 26.08392961 3.992088 NA NA NA

236 Cycas shanyaensis VU 12.51480679 3.99008 10 700 800

237 Zamia sandovalii NT 25.79943714 3.981528 NA NA NA

238 Zamia pumila NT 25.78334669 3.980927 NA NA NA

239 Cycas nitida NT 25.68127028 3.977109 NA NA NA

240 Encephalartos mackenziei NT 24. 78281687 3.942855 NA 1 800 2 000

241 Cycas bougainvilleana NT 24.69741468 3.939538 NA NA NA

242 Bowenia serrulata LC 50.14995324 3.934762 NA 30 150

243 Bowenia spectabilis LC 50.14995324 3.934762 NA 0 750

244 Zamia fairchildiana NT 24.51522014 3.932422 NA NA NA

245 Cycas petraea NT 24.43045531 3.929095 60 NA NA

246 Zamia ulei NT 24.13964507 3.917593 NA NA NA

247 Cycas siamensis VU 11.14556768 3.883259 NA NA 300

248 Macrozamia longispina NT 23.2755697 3.882618 50 200 700

249 Encephalartos cycadifolius LC 47.18980637 3.875148 290 1 200 1 800

250 Cycas diannanensis VU 11.02611836 3.873375 NA 600 1 800

251 Cycas falcate VU 11.02611836 3.873375 1350 NA NA

252 Zamia lecointei NT 22.97656965 3.870224 NA NA NA

253 Macrozamia stenomera NT 22.74607533 3.860564 NA NA NA

254 Cycas guizhouensis VU 10.80661968 3.854955 NA 400 1300

255 Cycas montana NT 22.60174471 3.854468 NA NA NA

256 Cycas zeylanica VU 10.58724336 3.836199 NA 5 50

257 Encephalartos turneri LC 45.29298688 3.83499 NA 600 1 200

258 Zamia pseudomonticola NT 21.74730214 3.817594 NA NA NA

259 Cycas chevalieri NT 21.6838055 3.814798 NA NA NA

260 Zamia lindenii NT 21.50498881 3.806884 NA NA NA

261 Cycas papua NT 21.47898495 3.805728 NA NA NA

262 Encephalartos natalensis NT 21.40559109 3.802458 NA 200 1 200

263 Zamia muricata NT 21.18935565 3.79276 NA NA NA

264 Lepidozamia hopei LC 43.35002121 3.792113 NA 0 1 000

265 Lepidozamia peroffskyana LC 43.35002121 3.792113 NA 0 1 000

266 Encephalartos lehmannii NT 21.01598319 3.784916 NA 400 1 000

267 Cycas tanqingii NT 20.616169 3.766589 80 NA 800

268 Dioon edule NT 20.61607388 3.766584 NA NA NA

269 Encephalartos NA 700 1 400 fridericiguilielmi NT 19.81469597 3.728806

270 Zamia obliqua NT 19.60967709 3.718905 NA NA NA

271 Cycas campestris NT 19.20190975 3.698924 20 000 NA NA

272 Zamia poeppigiana NT 19.07345031 3.692545 NA NA NA

273 Cycas dolichphylla NT 18.87450817 3.682585 NA NA NA

274 Zamia amazonum NT 18.78899749 3.678273 NA NA NA

275 Cycas badensis NT 17.56072929 3.614195 NA NA NA

276 Encephalartos laurentianus NT 17.44729335 3.608065 NA 450 550

277 Zamia roezlii NT 17.15521714 3.592105 NA NA NA

278 Encephalartos hildebrandtii NT 16.6308956 3.5628 NA 0 600

279 Cycas arenicola NT 16.41264168 3.550344 NA NA NA

280 Macrozamia moorei NT 16.16683711 3.536127 NA 300 500

281 Cycas anhemica LC 32.74662295 3.51888 NA NA NA

282 Cycas yorkiana NT 15.78572935 3.513676 11 530 NA NA

283 Cycas apoa NT 15.77197351 3.512856 NA NA NA

284 Encephalartos bubalinus NT 15.6287761 3.504282 NA 1 300 2 150

285 Macrozamia serpentine NT 15.18194666 3.477043 850 NA NA

286 Encephalartos poggei LC 30.92972888 3.463538 NA 500 1 000

287 Macrozamia fraseri LC 29.77537824 3.426715 NA NA NA

288 Cycas rumphii NT 14.37566603 3.425933 NA 10 200

289 Cycas scratchleyana NT 14.13015235 3.409837 NA 5 900

290 Cycas pruinosa LC 29.13189834 3.405584 NA NA NA

291 Encephalartos septentrionalis NT 13.78089777 3.386483 NA 500 2 500

292 Cycas orientis LC 28.09396076 3.370531 NA NA NA

293 Macrozamia dyeri LC 28.07961636 3.370037 NA NA NA

294 Cycas edentate NT 13.48672619 3.36638 1 000 NA NA

295 Macrozamia mountperriensis LC 27.25840935 3.341391 NA 50 400

296 Cycas schumanniana NT 12.87560451 3.323219 NA NA 1 600

297 Macrozamia douglasii LC 26.54739011 3.315908 NA 0 150

298 Macrozamia lucida LC 26.54739011 3.315908 NA 30 600

299 Cycas litoralis NT 12.58177486 3.301876 1000 NA NA

300 Macrozamia glaucophylla LC 24.76861886 3.249157 NA NA NA

301 Macrozamia diplomera LC 24.60611978 3.242831 NA NA 500

302 Cycas revolute LC 23.29359995 3.190213 NA 0 300

303 Encephalartos transvenosus LC 23.22916216 3.187557 NA 600 1 500

304 Dioon mejiae LC 22.89612329 3.173716 NA NA NA

305 Cycas miquellii LC 21.02825668 3.092326 NA 0 300

306 Encephalartos villosus LC 19.12329106 3.001878 NA 100 600

307 Cycas thouarsii LC 18.70990103 2.981121 NA 0 200

308 Macrozamia polymorpha LC 18.5579877 2.973384 NA NA NA

309 Cycas canalis LC 18.22700347 2.956316 NA NA NA

310 Cycas media LC 17.49625418 2.917568 NA 0 860

311 Macrozamia reidlei LC 17.26146916 2.904793 NA NA NA

312 Cycas calcicola LC 17.06050018 2.893727 NA 123 155

313 Cycas maconochiei LC 15.93740571 2.829525 NA 0 40

314 Cycas xipholepis LC 15.93740571 2.829525 NA NA NA

315 Cycas media ensata LC 15.78572935 2.820529 NA 0 860

316 Macrozamia communis LC 15.78571553 2.820528 NA 0 300

317 Cycas angulate LC 15.77084129 2.819642 NA 0 30

318 Macrozamia heteromera LC 15.27230078 2.789464 NA NA 200

319 Macrozamia concinna LC 15.18300583 2.783962 NA 800 1 100

320 Macrozamia macdonnelli LC 14.90585325 2.773662 NA NA NA

321 Cycas basaltca LC 14.90585325 2.766687 NA 230 260

322 Cycas lane-poolei LC 14.37566603 2.732786 NA 300 370

323 Cycas sundaica LC 14.11838029 2.715911 NA NA NA

324 Macrozamia montana LC 13.91429658 2.70232 NA NA NA

325 Macrozamia reducta LC 13.91429658 2.70232 NA NA NA

326 Encephalartos tegulaneus LC 13.12263127 2.647779 NA 1 400 2 300

327 Macrozamia fearnsidei LC 13.06858849 2.643945 NA 300 600

328 Macrozamia miquelii LC 13.06858849 2.643945 NA 0 500

329 Macrozamia macleayi LC 12.5367299 2.605407 NA 100 500

330 300 NA 60 Cycas clivicola LC 11.14556768 2.496964 000

331 Cycas_sphaerica NA 300 1 000

DD 17.23081084 NA

332 Cycas_aenigma 12.87560451 NA NA NA

DD NA

333 Cycas_indicaA. 33.75954797 NA NA NA

DD NA

334 Ceratozamia_brevifrons 26.68981432 NA NA NA

DD NA

335 Encephalartos_nubimontanus 34.26228554 NA NA 1 000

NA NA

336 Encephalartos_woodii 30.93709813 NA NA NA

NA NA

337 Encephalartos_brevifoliolatus 23.34009366 NA 1 300 1 500

NA NA

338 Encephalartos_relictus 12.5674151 NA 400 600

NA NA

339 19.07345031 NA NA NA Zamia_lindleyi

DD NA

Encephalartos dyerianus has the lowest geographic range (0.3 km2) whilst Cycas micronesica has the largest range value (11 250 000 km2) (Table 3.1). Several species occur at sea level (e.g. Cycas hainanensis) with Encephalartos septentrionalis occurring at the highest altitude of 2 500 m above sea level (Table 3.1). There is, however, no strong correlation between ED and cycad range size (P = 0.525; Table 3.2; Figure 3.4a) – range size is a positively correlated variable with IUCN threat categories – suggesting that prioritizing actions based on threat may not lead to preserving high-ED species. There is also no relationships between ED and altitude irrespective of how altitude was measured (average altitude, P=0.834; minimum altitude, P = 0.759; maximum altitude, P = 0.984; Table 3.2 and Figure 3.4b). This has also been reported for birds (Jetz et al., 2014), indicating that, at our scale of analysis, prioritizing elevated regions (e.g. mountains) because they are traditionally regarded as refuges for ancient lineages (Fjeldsa and Lovett, 1997; Jetz et al., 2004; Fjeldsa° et al., 2012) – here ancient lineages are approximated by high-ED species (Jetz et al., 2014) – is also not a good approach to maximise ED preservation. Nonetheless, geographic origin correlates strongly with ED, with cycads of American origin being the most evolutionarily distinct (Table 3.3; Figure 3.4c).

(a) ED

af_freq.img Value 98.76High : 11

10.59Low : 1

(b) EDGE

af_freq.img Value 7.38High : 11

2.50Low : 1

Figure(c) CW 3.3 EGlobal spatial patterns of (a) ED and (b) EDGE values of cycad species per grid cells.

af_freq.img Value 1.00High : 11

0.077Low : 1

(d) PE

af_freq.img Value 404.5High : 11

2.80Low : 1 Table 3.2 Relationships between ED and geographic parameters. Geographic parameters are measured as geographic range and altitude (average, minimum and maximum).

Estimate Std. Error t value P

Geographic range -0.011 0.017 -0.639 0.525

Average altitude 0.0046 0.035 0.134 0.894

Minimum altitude -0.013 0.042 -0.309 0.759

Maximum altitude 0.0014 0.071 0.020 0.984

Table 3.3 ANOVA table reporting the relationships between ED and geographic origin. Four geographic origins were distinguished: Africa, America, Asia and Australia

Df Sum Sq. Mean Sq. F value P

Geographic origin 3 3.79 1.2628 7.545 6.8e-05

Residuals 324 54.22 0.1674 - -

A B C ) D E ( g o l 2.5 3.0 3.5 4.0 4.5 2.5 3.0 3.5 4.0 4.5 2.5 3.0 3.5 4.0 4.5

0 5 10 15 3 4 5 6 7 Africa America Asia Australia Open Rubric log(range) log(average altitude) Continent 80

Figure 3.4 Global geographical patterns of cycad Evolutionary Distinctiveness (ED). This figure shows the patterns of the relationships between ED vs. geographic range (A), ED vs. average altitude (B) and ED vs. geographic origins of cycad species.

3.3. ARE THREATENED SPECIES EVOLUTIONARILY MORE DISTINCT THAN NON- THREATENED SPECIES? THE NEED FOR COMBINING ED SCORE AND THREAT LEVEL

When all cycads are categorized as threatened (≥ VU) versus non-threatened (LC and NT), these two categories are not significantly different with respect to their ED (P = 0.228, Table 3.4a; Figure 3.5a). However there is a trend towards high-ED species being highly threatened when individual threat level is considered (P=0.0276; Table 3.4b; Figure 3.5b), suggesting that efforts to preserve cycads based on IUCN categories would also contribute to preserving high-ED species. For example, in the top 50 EDGE species, 44 species are Critically Endangered (CR) and the remaining 6 species are Endangered (EN) (Table 3.1). No correlation between ED and threat level was earlier reported for birds (Jetz et al., 2014). The opposite finding reported in this study supports perhaps Davies et al.’s (2011) original ideas that the evolutionary pattern of extinction risk is different between plants and animals (Schwartz et al., 2001; Davies et al., 2011).

Although the findings in this study indicate that prioritisation of conservation based on the IUCN Red list would save the most evolutionarily distinct cycad species, there are, however, several cases where threat-based prioritization would miss high ED species. For instance, most NT species have on average higher ED values than VU species (Figure 3.5b). Few additional concrete examples include the Endangered Cycas taiwaniana and Dioon cuputoi which have higher ED values than all the Critically Endangered species ranging from the 4th to the 29th position in the EDGE score ranking (i.e. from Encephalartos dyerianus to Ceratozamia zaragozae; Table 3.1). There are many other examples of less threatened species displaying higher ED values than highly threatened species (see Table 3.1). Owing to

this mismatch between threat and ED, current conservation efforts based on threat levels need to integrate ED to provide a more inclusive option for conservation decision.

Table 3.4 ANOVA table reporting the relationships between ED and threats. In A) threat status was measured as threatened vs. non-threatened whereas in B) threat level was measured by IUCN categories (LC, NT, VU, EN and CR).

Df Sum Sq. Mean Sq. F value P

Threat status 1 0.26 0.2589 1.456 0.228

Residuals 328 58.32 0.1778 - -

Df Sum Sq. Mean Sq. F value P

Individual threat level 4 1.93 0.4820 2.765 0.0276

Residuals 325 56.65 0.1743 - -

A B ) D E ( g o l 2.5 3.0 3.5 4.0 4.5 2.5 3.0 3.5 4.0 4.5

non−threatened threatened LC NT VU EN CR Threat status Threat categories Open Rubric

Figure 3.5 Relationships between threat and ED

3.4 COMBINING ED AND THREAT LEVEL: CYCAD SPECIES RANKING BASED ON EDGE SCORES

EDGE scores range from 2.497 (Cycas clivicola) to 7.375 (Microcycas calocoma) (SD = ± 1.06) (Table 3.1), making M. calocoma the cycad species to prioritize in conservation programme. M calocoma, the top 1 species on both ED and EDGE lists, is endemic to Cuba where it faces anthropogenic pressures in addition to reproductive failure due to pollinator extinction. Assuringly, this species which belongs to a monospecific genus, is on Appendix I of the CITES Appendices and found within protected areas namely, Vinales National Park, Mil Cumbres, and the National Botanical Garden of Cuba (IUCN, 2010). The second top EDGE species, however, found in a single location with less than 50 species (Lindstrom, 2009) has no known members in protected areas.

The top 50 EDGE species include 44 CR (88 %) and 6 EN (12 %) and, in the top 100 EDGE species there are 65 CR, 31 EN and 4 VU, suggesting that top EDGE species are also threatened species (Table 3.1). In term of taxonomy, the dominant genera in the top 50 EDGE species are Zamia (21 species) and Encephalartos (10 species), followed by Ceratozamia (8 species) and Cycas (6 species). The other genera in the top 50 are Dioon (2 species), Microcycas (1 species), Macrozamia (1 species), and Chigua (1 species). When all the 339 taxa are considered, there are 67 (CR), 70 (EN), 78 (VU), 68 (NT), 47 (LC), and 9 (DD), indicating that 215 species are threatened and 115 are non-threatened with 9 species having an unknown threat status (i.e. DD category). From a biogeographic perspective, the cycads of the New World are dominant in the top EDGE ranking with 32 species in the top 50 EDGE species followed by the African cycads (Encephalartos; 10 species), and five species from China (3 species), Vietnam (1 species) and Philippines (1 species). An almost similar pattern is found in the top 100 EDGE species with the New World totalling 56 species, African cycads 21 species, and Asia 18 species. Australia has the lowest number with only 5 species. These geographic regions (New World and Africa) therefore could be regarded as global “hot spots” of EDGE species (see Figure 3.3b and Table 3.1).

Most high-EDGE species have shown over 80 % decline over 3 or 4 generations (IUCN, 2010), and some (e.g. Cycas fugax) are actually extinct in the wild (Whitelock, 2002). Most 83

of the causes for the decline are habitat destruction due to agricultural expansion, deforestation, over-collection for ornamental and medicinal purposes, droughts, and fires. An unusual but highly destructive factor is large troops of baboons which remove the Encephalartos inopinus’ young cones, explaining the rarity of seedlings for this species (IUCN, 2010). Members of E. whitelockii face a massive decline as a result of the construction of a hydroelectric power plant in its range area, destroying both young and mature plants.

3.5 LIMITATION OF CONSERVATION ACTIONS AT REGIONAL OR CONTINENTAL LEVEL FOR THE TOP EDGE SPECIES

The genus Encephalartos is endemic to Africa, and 10 of its species are in the top 50 of EDGE score and 21 are in the top 100. The first is E. dyerianus (4th position on global EDGE score) which occurs only on a single granite mountain in Limpopo province of South Africa. Although this species is included in a reserve (Lillie Flora Reserve within Selati Game Reserve), this measure seems not to be efficient as 107 plants have been lost recently due to poaching (IUCN, 2010). The findings from this study that this species is one of the top African and global EDGE priority species imposes renewed commitment for stronger protection measures from conservation authorities. The 5th, 15th, 16th, 19th, 28th, 38th, 43rd, as well as the 44th and 49th species on EDGE global ranking (Table 3.1) are all Encephalartos species. Although some of them are found in protected areas (e.g. E. laevifolius in Lekgalameetse Nature Reserve, the Blyde River Canyon National Reserve, the Starvation Creek Nature Reserve in South Africa and the Malolotja Nature Reserve in Swaziland; E. cupidus is protected in the Blyderivierspoort Nature Reserve, and E. aemulans in a private nature reserve), many others, particularly those outside South Africa’s borders – e.g. E. pterogonus and E. whitelockii – are not included in any protected areas (IUCN, 2010). One exception is E. msinganus which is native to South Africa but not recorded in any protected areas. E. whitelockii is native to Uganda, found within the Queen Elizabeth National Park but 90% of its population is found outside the park (IUCN, 2010). This raises, once more, the need for revisiting the frontiers of protected areas network to include species that need particular attention (Heller et al., 2009).

The genus Ceratozamia, the seventh most species-rich in the EDGE species is native to the New World. Currently, there are 27 extant species with most endemic to Mexico, Guatemala, Hondura and Belize (all listed under CITES Appendix I, Whitelock, 2002) where they face intense poaching pressures (Christenhusz et al., 2011). Similar to Encephalartos, not all species are in protected areas. An early report indicates that only 14%, 50% and 58% of Cuban, Mexican and Panamanian cycads, respectively, are found in protected areas whilst none of the cycads in Colombia, Peru, or Guatemala occur within reserves (Donaldson, 2003). Strong actions have, however, been taken towards preserving the genus from loss; for example, the Montgomery Botanical Centre in the USA has already representative GenBank accessions for many New World cycads (Chavez et al.,1998). Members of Ceratozamia mirande, which is amongst the top 100 EDGE species, are protected in Le Sepultura Biosphere Reserve that overlaps with their natural geographical range.

A reasonable number of cycads of the New World in the top 100 EDGE species are in protected areas. Ceratozamia euryphylidia is found in Jardin Botanico Clavijiero, Zamia lacandona protected in Palenque National Park as well as in Montes Azulez Biosphere Reserve, Zamia katzeriana in Ocote Biosphere Reserve. In Las Orquideas National Park, Indios Ecological Reserve, Los Taxlas Biosphere Reserve, Zamia wallisii, Zamia pygmaea, and Ceratozamia miqueliana respectively are protected (IUCN, 2010). Even with all these efforts, a lot still needs to be done for those species with high EDGE scores (top 100) found outside protected areas, e.g. Zamia skinneri, Zamia montana, Ceratozamia morrettii, Ceratozamia zaragozae, Ceratozamia hildae, and Zamia disodon. For example Zamia monticola is amongst species that have shown over 80 % decline over the past 60 years (IUCN, 2010) but still not in protected areas. These species might slide into extinction unnoticed; there is therefore a need for global EDGE campaign similar to the ongoing EDGE campaign for vertebrate.

Asian cycads have the least number of top EDGE species in protected areas. Apart from Cycas hainanensis found in Tongguling National Nature Reserve in China, Cycas changjiangensis in Bawangling Nature Reserve, and Cycas taitungensis in Taitung Hongyeh Village Cycas Nature reserve, the rest in the top 100 EDGE species are either not in protected areas or do not have assessment information concerning their protection status (IUCN, 2010). 85

Australia harbours only 5 of the top 100 EDGE species. Of these, Macrozamia elegans is protected in the Blue Mountains National Park and Macrozamia spiralis is found in Werakata National Park, Windsor Downs National Reserve as well as Agnes Banks National Reserve (IUCN, 2010). Overall conservation measures, including in situ and ex situ conservation programmes need to be fuelled to ensure that high-EDGE cycads are protected all over the world.

CHAPTER 4

CONCLUSION AND RECOMMENDATIONS

4.1 CONCLUSION

Globally, biodiversity is in crisis particularly under the tropics (Vamosi and Vamosi, 2008). This crisis has led to the loss of entire lineages (e.g. 14 mammalian genera and 3 families since AD 1500, MacPhee and Flemming, 1999). Preserving the tree of life and subsequent ecosystem services therefore requires pragmatic triage solutions. Such solutions could be well informed by EDGE scores, a metric that takes risk of extinction and species phylogenetic originality into account. EDGE-based priority setting has already been implemented for several phyla (Owen, 2014), and helped build conservation capacity in several parts of the world (Isaac et al., 2012). However, equivalent effort is still lacking for the most threatened plant groups, i.e. cycads. This study provides the first ever EDGE score for cycad of the world and shows that several ‘gap species’ (Rodrigues et al., 2004) i.e. priority species not found in protected areas, have high EDGE scores and thus deserve prompt actions. Similarly, species that are less threatened (based on IUCN categorization) but score high on EDGE ranking were identified. Although most cycads are on CITES Appendix I list – a measure that regulates international trade of threatened species – renewed attention at local level is urgently required especially for species that are a priori not of concern but score high in EDGE ranking.

4.2. RECOMMENDATIONS

Even in regions where funding and strong policy instruments are available (e.g. European Union, Trouwborst, 2009), only 17% of protected species have a favourable conservation status (Condé et al., 2010), and this status could be further depressed in the face of the ongoing climate change (Araújo et al., 2011). The study proposes the following actions to be implemented for cycads.

Firstly, an EDGE-based cycad conservation campaign that would build on the ongoing EDGE campaigns for mammals, birds, amphibians and corals using the online platform 87

http://www.edgeofexistence.org by the Zoological society of London is recommended. Such a campaign would have to build upon the EDGE priority ranking that this study provides. This ranking would be fine-tuned in the future as data become available for species in the Data Deficient category.

Secondly, there is a need to redesign network of protected areas to include not only species of urgent conservation need, but also ‘retention areas’ (Araújo et al, 2004), i.e. areas suitable climatically for cycads currently and those projected to be so in the future. Ex situ conservation efforts also need to be promoted for cycads (creation of national gene banks for DNA sequences and genome, inclusion in botanical and home gardens, etc.).

Thirdly, the national legislations need to be stricter than it is especially in regions identified as hotspots of priority species, i.e. the New World and Africa. This will require a national policy adjustment to enforce the identification and management of retention areas for cycads and a legal connectivity of existing protected areas with retention areas. This legislation must also be accompanied by adequate means (e.g. well-trained conservation biologists and law enforcement officers, etc.) for rigorous implementation actions and enforcement of regulations.

Fourthly, although the IUCN Red list is important, inadequate resources hinder the protection of all the 339 cycad taxa. A proposal that the top 100 EDGE species generated by this study be urgently included in protected areas is therefore put forward. Alternatively, the species in the list could be subject of awareness-raising campaign or specifically be subject of special conservation projects. The mismatch that exists between threat level and ED of some species suggests that preserving only threatened species would not guarantee the survival of evolutionarily unique species from the ongoing extinction crisis. The high proportion of threatened cycad species is indicative of a high probability that many species may have died out in the wild (Donaldson, 2003). By ranking priority species, and identifying hotspots of priority species, this study provides ways of supporting and furthering the ongoing international campaign to prevent the branches of the cycad tree of life from being disproportionately pruned. 88

Finally, further research on the Data Deficient species mentioned in this study should be made a priority. They are only 9 species but as long as there is no information about their threat status, and EDGE scores, a high proportion of genetic diversity could be lost because these DD species may not draw any conservation attention as a result of unknown threat status.

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