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Cycad Biodiversity in the Bahamas Archipelago and Conservation Genetics of the Threatened Zamia Lucayana (Zamiaceae)

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Cycad Biodiversity in the Bahamas Archipelago and Conservation Genetics of the Threatened Zamia Lucayana (Zamiaceae) Cycad biodiversity in the Bahamas Archipelago and conservation genetics of the threatened Zamia lucayana (Zamiaceae) M ICHAEL C ALONJE,ALAN W. MEEROW,LINDY K NOWLES,DAVID K NOWLES M. PATRICK G RIFFITH,KYOKO N AKAMURA and J AVIER F RANCISCO-ORTEGA Abstract A conservation assessment for the three cycad Introduction species native to the Bahamas Islands is presented. Results 331 10 are based on field surveys on all islands where these species here are c. species of cycads in genera (Osborne 2012 occur. Zamia angustifolia is native to Eleuthera, Zamia Tet al., ) and they are often referred to as living fossils fi integrifolia is native to Abaco, Andros, Eleuthera, Grand because they rst appeared in the Triassic (Norstog & 1997 Bahama and New Providence, and Zamia lucayana is Nicholls, ). These gymnosperms are rapidly disappear- endemic to Long Island. Z. angustifolia is of the highest ing because of habitat loss and their popularity in the conservation concern because of the small number of adult ornamental plant trade, which has led to drastic declines 1995 plants, its restricted distribution and the extensive de- in population size (Osborne, ). Most cycad species are 2011 velopment occurring within its habitat. Z. integrifolia also currently on the IUCN Red List (IUCN, ) and their trade 2011 has a restricted distribution on Eleuthera and Grand is regulated by CITES (CITES, ). All cycads are dioecious Bahama and, although threatened by urban development and their pollination and dispersal biology constrain both fl in New Providence, it is relatively common on Abaco and gene ow and population recruitment to relatively small 1997 Andros. Z. lucayana comprises three populations within a geographical areas (Norstog & Nicholls, ). 2 narrow strip of land of c. 1 km ; we propose a reassignment There are two cycad genera in the Caribbean island of its current conservation status from Endangered to biodiversity hotspot: Microcycas and Zamia. The former is Critically Endangered. We assessed the genetic structure a monotypic Critically Endangered genus restricted to 2009 71 of Z. lucayana based on 15 polymorphic microsatellite Cuba (Pinares et al., ). Zamia (c. species) has a wider DNA loci; this indicated that the three known populations distribution from Bolivia to Central America, Mexico, should be considered a single management unit. However, Florida and the West Indies. The Caribbean island species the high number of private alleles suggests that genetic form a monophyletic group with c. nine recognized species, 1987 drift, indicative of recent fragmentation, is progressing. known as the Z. pumila complex (Stevenson, ). Three of We propose in situ conservation strategies, and we also these taxa occur in the Bahamas archipelago: Z. angustifolia collected germplasm from a total of 24 populations of these (also present in Cuba), Z. integrifolia (also occurring in 1 three cycad species, for ex situ conservation. Cuba and Florida), and Z. lucayana (Fig. ). The latter (Plate 1) is endemic to Long Island. Z. tenuis is another Keywords Biodiversity hotspot, Bahamas, Caribbean, species reported for the Bahamas but it is only known conservation management, cycad, genetic structure, Red from a single specimen collected in the early 19th century List, Zamia lucayana from a plant cultivated at Berlin Botanical Garden. Z. tenuis was formerly considered a synonym of Z. angustifolia by Britton & Millspaugh (1920) and is currently treated as a synonym of Z. integrifolia (Osborne et al., 2012). 22 MICHAEL CALONJE* and M. PATRICK GRIFFITH Montgomery Botanical Center, The Commonwealth of the Bahamas consists of Coral Gables, Miami, USA inhabited islands, c. 700 cays and nearly 2,400 small islets 1975 ALAN MEEROW and KYOKO NAKAMURA USDA-ARS-SHRS, National Germplasm (Albury, ). This archipelago has a fast growing Repository, Miami, USA population and a strong tourism industry, which represent LINDY KNOWLES Bahamas National Trust, Nassau, The Bahamas challenges to the protection of its unique environment 2002 DAVID KNOWLES Bahamas National Trust, Abaco National Park, Abaco, (Anonymous, ). It is estimated that this archipelago The Bahamas has 110 endemic seed plant species (c. 9% of the native flora; JAVIER FRANCISCO-ORTEGA† (Corresponding author) Department of Biological Acevedo-Rodríguez & Strong, 2012). As far as we are aware fi Sciences, Florida International University, Miami, USA. E-mail ortegaj@ u.edu no Bahamian endemic species has been the subject of a *Also at: Department of Biological Sciences, Florida International University, comprehensive study focusing on (1) its conservation status, Miami, USA 2 3 †Also at: Fairchild Tropical Botanic Garden, Coral Gables, Miami, USA ( ) challenges for management, ( ) conservation genetics, 4 5 Received 19 October 2011. Revision requested 11 January 2012. ( ) ex situ conservation, and ( ) current threats. Such studies Accepted 6 February 2012. are particularly relevant to the Bahamas as this archipelago © 2013 Fauna & Flora International, Oryx, 47(2), 190–198 doi:10.1017/S0030605312000129 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 02 Oct 2021 at 13:02:15, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605312000129 Cycad biodiversity 191 FIG. 1 Distribution of the three species of Zamia in the Bahamas Islands. Each point represents a population included in our field studies. Population symbols overlap on Andros, Eleuthera, and New Providence. Plants from Tilloo Cay, Abaco, were identified as Zamia cf. integrifolia for this study. See Table 1 for number of populations and species studied on each island. The inset indicates the location of the Bahamas in the Caribbean. PLATE 1 Zamia lucayana: (A) male cones, (B) female cone, (C) hermit crab Coenobita clypeatus feeding on the fleshy seed coat, (D) adult male individual. © 2013 Fauna & Flora International, Oryx, 47(2), 190–198 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 02 Oct 2021 at 13:02:15, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605312000129 192 M. Calonje et al. is part of the Caribbean island biodiversity hotspot A modified version of the enrichment/hybridization (Maunder et al., 2008). Here, we formulate conservation method of Edwards et al. (1996) was used with genomic assessments of Bahamian Zamia species, with special DNA of Florida Z. integrifolia (Meerow & Nakamura, 2007; emphasis on the Long Island endemic Z. lucayana. Meerow et al., 2007, 2012a,b). The second methodological approach involved retrieving of microsatellite loci in the Zamia expressed sequence tag (EST) databases Methods available in GenBank using the Simple-Sequence Repeat Identification Tool in GRAMENE (Ware et al., 2002). Collecting sites Six of the 15 loci (Zam28, Zam33, Zam34, Zam39, Zam40, 45 Prior to our field studies we compiled a list of historical sites Zam ) have been previously published (Meerow & 2007 fi for the target species as recorded by collections deposited in Nakamura, ). Protocols for PCR ampli cation seven herbaria (BW, BNH, C, FTG, GH, MO, NY; acronyms and subsequent visualization of SSR fragments follow 2007 follow Thiers, 2011). In addition, we consulted floristic and Meerow & Nakamura ( ). 2 taxonomic treatments that include information concerning Descriptive statistics (Table ) were generated with 6 41 2005 the distribution of the genus in the Bahamas (Britton, GenAlEx v. (Peakall & Smouse, ). Tests for – 1907, 1909; Hill, 1974; Eckenwalder, 1980; Correll & Correll, Hardy Weinberg equilibrium and the U test (Rousset 1995 fi 1982), and gathered provenance information from living & Raymond, ) for heterozygote excess or de ciency 4 0 10 000 collections at Montgomery Botanical Center and Fairchild were run with GenePop v. using , Monte Carlo 1992 Tropical Botanic Garden. Between December 2009 and Markov chain iterations (Guo & Thompson, ). Linkage July 2011 we conducted field studies on the five islands disequilibrium (LD) was tested for each population with 3 5 ffi 2005 where the three species occur (Table 1, Fig. 1). Each island ARLEQUIN v. (Exco er et al., ) using a likelihood- ffi 1996 has only one species, except Eleuthera, where Z. angustifolia ratio test (Slatkin & Exco er, ). A Monte Carlo Markov 100 000 and Z. integrifolia co-occur, although their distribution chain method was applied with , iterations, a burn-in 10 000 fi , 0 001 ranges do not overlap (Fig. 1). We visited a total of 24 of , and the signi cance level set at P . populations (Fig. 1, Table 1) and we also explored areas Analysis of molecular variance (AMOVA) among 10 000 where the species were not previously reported. populations, and permuted calculation of FST ( , permutations) were generated with GenAlEx. An additional measure of gene diversity, D (Jost, 2008), was calculated Conservation assessments and demographic surveys est with SMOGD (Crawford, 2010). For each site and island we gathered information pertinent Genetic distance among populations and individuals to the cycads’ conservation status and threats. Field studies was calculated with POPULATIONS v. 1.2.31 (Langella, were more exhaustive for Z. lucayana, for which we 2010), using Da (Nei et al., 1983). The population distance estimated total distribution area, number of adult and matrix was used for permuted (10,000 iterations) Mantel juvenile plants, and the approximate ratio of males to (1967) tests for isolation
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