Mike Maunder

Ex Situ Plant Conservation and Beyond

Abstract In recent years, the mission of many botanic gardens and arboreta has expanded from a traditional focus on developing a horticultural collection to one that includes taking a proactive role in plant conservation. To use their limited resources more effectively, many gardens are seeking ways to quantify their contributions to conservation efforts, both as a self-assessment tool to improve their effectiveness and as a way to give an explicit accounting of activities to donors and funding agencies. We suggest many ways gardens can measure the success of their conservation programs, and present results from a survey conducted to assess current conservation activities at botanic gardens.

Plant Conservation in the Caribbean Island Biodiversity Hotspot

While the Caribbean is a recognized “biodiversity hotspot”, plant conservation has not received adequate attention; particularly, given the high levels of endemism in many plant groups. Besides establishing protected areas, there needs to be a sustained effort to study the taxonomy, systematics and ecology of the flora. Recent phylogenetic studies have shown high levels of endemism and conservation studies indicate a large propotion of the flora is threatened with extinction. Eight recommendations are given for plant conservation in the region.

Seed plant endemism on Hainan Island: a framework for conservation actions.

Hainan, the second largest island of China, has the most extensive and best preserved tropical forests of this country. A network of 68 protected areas (54 of them are terrestrial) provides in situ conservation for the unique ecosystems of the island. We: (1) discuss an updated check-list of seed-plant species that are endemic to Hainan, (2) evaluate the extent to which the endemic flora has been the subject of molecular studies, and (3) investigate the conservation status of these species. We recognize 397 endemic species on the island, 271 of which are reported in the protected areas, and 144 of which have been Red-Listed (85 assigned to the Critically Endangered (40) or Endangered (45) IUCN categories). The families with the highest number of endemics are Rubiaceae (33 species), Lauraceae (27 species), and Poaceae (26 species). The island has only seven endemic genera, all of which are unispecific. Compared with other tropical islands, Hainan has a low number of endemics but our preliminary observations suggest that the island has a highly disharmonic flora when compared with that from the mainland. Nevertheless, most of the major clades of the seed-plant tree of life with representatives in China also have endemic species on the island. We argue that the low levels of endemism reflect the continental nature of Hainan and the fact that several areas of the island have not been fully inventoried. We were unable to find a single molecular systematic study focusing exclusively on the Hainan endemics; however, 24 of the endemic species have been included in phylogenetic studies targeting particular genera or families. Future research/conservation actions for the endemic flora of Hainan should focus in developing: (1) a red-list that assesses all 397 endemic species, (2) comprehensive floristic studies for the protected areas, (3) molecular phylogenetic and conservation genetic studies with a primary focus on the endemics, (4) studies to understand what ecological interactions are important in the biology of the endemic species, and (5) eco-geographical studies to identify Important Biodiversity Zones of endemism within Hainan and therefore potential new protected areas.

Sweet Drinks Are Made of This: Conservation Genetics of an Endemic Palm Species from the Dominican Republic

Pseudophoenix ekmanii is a threatened palm species endemic to the Dominican Republic. Sap from trees is extracted to make a local drink; once they are tapped the individual usually dies. Plants are also illegally harvested for the nursery trade and destroyed by poachers hunting the endemic and threatened Hispaniolan parrot. We used 7 DNA microsatellite markers to assist land managers in developing conservation strategies for this palm. We sampled 4 populations along the known distribution range of this species (3 populations from the mainland and 1 from the small island of Isla Beata), for a total sample of n = 104. We found strong evidence for genetic drift, inbreeding, and moderate gene flow (i.e., all populations had at least 4 loci that were not in Hardy-Weinberg equilibrium, at least 9 loci pairs were in linkage disequilibrium, the pairwise F(ST) values ranged from 0.069 to 0.266, and had positive F(IS) values). Data supported an isolation-by-distance model, and cluster analyses based on genetic distances resolved 2 groups that match a north-south split. The population from Isla Beata had the lowest levels of genetic diversity and was the only one in which we found pairs of individuals with identical shared multilocus genotypes.

Phylogenetic analyses of nucleotide sequences confirm a unique plant intercontinental disjunction between tropical Africa, the Caribbean, and the Hawaiian Islands.

Phylogenetic analyses of nucleotide sequences of the internal transcribed spacers and 5.8 regions of the nuclear ribosomal DNA and of the trnH-psbA spacer of the chloroplast genome confirm that the three taxa of the Jacquemontia ovalifolia (Choicy) Hallier f. complex (Convolvulaceae) form a monophyletic group. Levels of nucleotide divergence and morphological differentiation among these taxa support the view that each should be recognized as distinct species. These three species display unique intercontinental disjunction, with one species endemic to Hawaii (Jacquemontia sandwicensis A. Gray.), another restricted to eastern Mexico and the Antilles [Jacquemontia obcordata (Millspaugh) House], and the third confined to East and West Africa (J. ovalifolia). The Caribbean and Hawaiian species are sister taxa and are another example of a biogeographical link between the Caribbean Basin and Polynesia. We provide a brief conservation review of the three taxa based on our collective field work and investigations; it is apparent that J. obcordata is highly threatened and declining in the Caribbean.

Endemic Seed Plant Species from Hainan Island: A Checklist

Global conservation of plant biodiversity on tropical islands is a major priority, as approximately one third of all endangered plant species are insular endemics. Checklists can be an important first step in determining conservation priorities on islands. Hainan, the largest island in the Indo-Burma Biodiversity Hotspot, and therefore an international focus for conservation, has the most extensive and best preserved tropical forests in China. In this study we enumerate the endemic seed plants of Hainan Island. The checklist was prepared by consulting: (1) several bibliographic/taxonomic data base resources, (2) relevant taxonomic treatments and floras, and (3) plant taxonomists who are actively working with Chinese plants. The checklist also contains information concerning conservation status, the occurrence of Hainan endemics in four protected areas on the island, and available molecular phylogenies. An additional checklist of the species that were until recently thought to be endemic to Hainan, but are no longer considered to be, is also presented. In a separate paper in this issue of Botanical Review the patterns of endemism on Hainan Island are discussed.

Splitting or Lumping? A Conservation Dilemma Exemplified by the Critically Endangered Dama Gazelle ( Nanger dama )

Managers of threatened species often face the dilemma of whether to keep populations separate to conserve local adaptations and minimize the risk of outbreeding, or whether to manage populations jointly to reduce loss of genetic diversity and minimise inbreeding. In this study we examine genetic relatedness and diversity in three of the five last remaining wild populations of dama gazelle and a number of captive populations, using mtDNA control region and cytochrome b data. Despite the sampled populations belonging to the three putative subspecies, which are delineated according to phenotypes and geographical location, we find limited evidence for phylogeographical structure within the data and no genetic support for the putative subspecies. In the light of these data we discuss the relevance of inbreeding depression, outbreeding depression, adaptive variation, genetic drift, and phenotypic variation to the conservation of the dama gazelle and make some recommendations for its future conservation management. The genetic data suggest that the best conservation approach is to view the dama gazelle as a single species without subspecific divisions.

What to do when we can’t bank on seeds: What botanic gardens can learn from the zoo community about conserving plants in living collections

Species loss due to human activities is occurring at an unprecedented pace ( Barnosky et al., 2011 ), and over the last few decades, botanic gardens have responded by expanding their conservation activities ( CBD, 2010 ). Botanic gardens play a particularly critical role in the development of ex situ (off -site) collections of threatened plant species, and the botanic garden community has helped develop current best practices for ex situ conservation and reintroduction (e.g., via the Center for Plant Conservation; Guerrant et al., 2004 ). Th e majority of plant species are amenable to seed banking or at least vegetative propagation (horticultural or tissue culture), which allows them to be preserved for decades or even centuries before regeneration is necessary and before genetic and demographic viability become an issue ( Havens et al., 2004 ). Consequently, much of the research geared to support ex situ plant conservation has focused on understanding how to effi ciently capture wild genetic diversity to enable successful future reintroduction eff orts ( Guerrant et al., 2004 ). However for “exceptional” plant species that either do not produce seeds or produce seeds that are recalcitrant (i.e., desiccation intolerant so they cannot be dried and frozen), maintaining demographic viability and genetic diversity ex situ can be particularly challenging ( Pence, 2014 ). To date, less effort has been dedicated to ensuring that these living collections, once brought into ex situ cultivation, remain genetically diverse and demographically viable over the long term to support reintroduction eff orts (but see Havens et al., 2004 ). For many exceptional species, living plant collections are the only currently available ex situ conservation option, and the maintenance of these living collections introduces numerous genetic and demographic challenges associated with small, isolated populations. If not curated correctly, these small populations are subject to founder eff ects, genetic drift , and inbreeding, and can experience selective pressure from biotic and abiotic conditions in the ex situ environment. Th ese factors could compromise future reintroduction eff orts and ultimately lead to loss of the species from ex situ collections altogether. In the future, cryopreservation and/or tissue culture may be viable ex situ approaches for exceptional species, thus minimizing immediate concerns about genetic and demographic losses. However, the techniques required for these alternative germplasm conservation approaches are oft en species-specifi c and currently unavailable for many threatened species ( Pence, 2014 ). In addition, capacity and resources to develop and maintain cryopreservation protocols is limited or lacking in many regions. Until research and resources reach a point where all exceptional species can be cryopreserved, living collection management will continue to be critical. Despite the value of ex situ collections, some threatened plant species and valuable genetic resources have already been lost from botanical collections ( Govaerts, 2010 ). Of 844 plant taxa identifi ed as extinct in the wild in 2010, 9% were curated in collections, while another 5% had been in collections but subsequently lost ( Govaerts, 2010 ). While the cause of these losses was not reported, it is likely that at least some were the result of genetic or demographic collapse. It is clear that an integrated and more collaborative approach is needed to eff ectively conserve threatened species ex situ. For example, Brighamia insignis (Campanulaceae), an endemic Hawaiian succulent species, is functionally extinct in the wild with only one remaining extant individual. It is cultivated ex situ in at least 57 botanical collections around the world, but in need of an integrated management plan. Th is species can be seed banked, but seeds lose 1 Manuscript received 30 June 2016; revision accepted 15 August 2016. 2 Department of Plant Science and Conservation, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60035 USA; 3 Department of Science and Conservation, National Tropical Botanical Garden, 3530 Papalina Road, Kalāheo, Hawai‘i 96741 USA; 4 Department of Conservation Science, Chicago Zoological Society, Brookfi eld, Illinois 60513 USA; 5 International Center for Tropical Botany, Florida International University and the National Tropical Botanic Garden, Th e Kampong, 4013 South Douglas Road, Coconut Grove, Florida 33133 USA; and 6 Botanic Gardens Conservation International, 199 Kew Road, Richmond, Surrey TW9 3BW UK 7 Author for correspondence (e-mail: khavens@chicagobotanic.org) doi:10.3732/ajb.1600247 O N T H E N AT U R E O F T H I N G S : E S S AY S New Ideas and Directions in Botany

A conservation framework for the Critically Endangered endemic species of the Caribbean palm Coccothrinax

With 30 threatened species (14 categorized as Critically Endangered and 16 as Endangered, sensu IUCN), Coccothrinax (c. 54 species) is the flagship palm genus for conservation in the Caribbean Island Biodiversity Hotspot. Coccothrinax has its centre of taxonomic diversity in these islands, with c. 51 endemic species. We present a conservation framework for the 14 Critically Endangered species, found in Cuba, Haiti or the Dominican Republic. Only two species ( C. jimenezii , C. montana ) occur in more than one country (Haiti and the Dominican Republic). Immediate threats include oil drilling and nickel mining, intrusion of saline water into soil, urban and agricultural development, low population recruitment, uncontrolled fires, interspecific hybridization, and unsustainable ethnobotanical practices. Coccothrinax bermudezii , C. borhidiana , C. crinita ssp. crinita , C. leonis and C. spissa are not conserved in protected areas. Coccothrinax bermudezii , C. jimenezii , C. leonis and C. nipensis are not part of ex situ collections. Based on results from a conservation project targeting C. jimenezii , we recommend international cooperation between the three range states to implement integrative conservation management plans, plant exploration initiatives, taxonomic revisions, outreach, and fundraising. The ultimate aim of this review is to provide baseline information that will develop conservation synergy among relevant parties working on Coccothrinax conservation in Cuba, Haiti and the Dominican Republic. Such collaborations could also benefit through partnerships with botanists working in other countries.