Abstract
Madagascar has a high diversity of endemic palm species and the Masoala Peninsula is a hotspot for their diversity. Several species are critically endangered and their populations known to be in decline due to a combination of land clearance, destructive harvesting for heart of palm and potentially unsustainable commercial seed collection. The critically endangered Voanioala gerardii and the endangered Lemurophoenix halleuxii are two palm species from monospecific genera endemic to Madagascar that overlap in their distribution within this region. This project undertook field surveys of all known populations of these two species to document their population sizes and locations. We modelled their area of potentially suitable habitat within the region and undertook genetic analysis to investigate genetic diversity and relatedness among populations of each species. The study found overlapping but contrasting patterns of potential habitat. It also found contrasting levels and patterns of genetic diversity between the two species that were not consistent with the modelled habitat distributions. We found that Voanioala gerardii populations are critically small but contain unexpectedly high levels of genetic diversity, which may indicate as yet undiscovered populations remaining. An active program to change methods of seed collection and to involve local villagers and land managers in the conservation of these species would be required to prevent their extinction.
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References
Adler GH, Lambert TD (2008) Spatial and temporal variation in the fruiting phenology of palms in isolated stands. Pl Sp Biol 23:9–17
Andrianarimisa A, Bachmann L, Ganzhorn J, Goodman S, Tomiuk J (2000) Effects of forest fragmentation on genetic variation in endemic understory forest birds in central Madagascar. J Ornith 141:152–159
Arroyo-Rodriguez V, Aguirre A, Benitez-Malvido J, Mandujano S (2007) Impact of rain forest fragmentation on the population size of a structurally important palm species: Astrocaryum mexicanum at Los Tuxtlas, Mexico. Biol Cons 138:198–206
Bacles C, Burczyk J, Lowe AJ, Ennos R (2005) Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59:979–990
Bakker J, van Rijswijk M, Weissing F (2010) Consequences of fragmentation for the ability to adapt to novel environments in experimental Drosophila metapopulations. Cons Gen 11:435–448
Biebach I, Keller L (2010) Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Cons Gen 11:527–538
Bijlsma R, Westerhof M, Roekx L, Pen I (2010) Dynamics of genetic rescue in inbred Drosophila melanogaster populations. Cons Gen 11:449–462
Billotte N, Risterucci A, Barcelos E, Noyer J, Amblard P, Baurens F (2001) Development, characterisation, and across-taxa utility of oil palm (Elaeis guineensis Jacq.) microsatellite markers. Genome 44:413–425
Billotte N, Couvreur T, Marseillac N, Brottier P, Perthuis P, Vallejos M, Noyer J-L, Jacquemoud-Collet J-P, Risterucci A-M, Pintaud J-C (2004) A new set of microsatellite markers for the peach palm (Bactris gasipaes kunth); characterisation and across-taxa utility within the tribe Cocoeae. Mol Ecol Notes 4:580–582
Bouzat J (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Cons Gen 11:463–478
Brito DG, CEV, Boubli J (2008) Is the Atlantic Forest protected area network efficient in maintaining viable populations of Brachyteles hypoxanthus? Biodiv Cons 17: 3255-3268
Brook B, Tonkyn D, O’Grady J, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Cons Ecol 6:16
Byg A, Balslev H (2001a) Diversity and use of palms in Zahamena, eastern Madagascar. Biodiv Cons 10:951–970
Byg A, Balslev H (2001b) Traditional knowledge of Dypsis fibrosa (Arecaceae) in Eastern Madagascar. Econ Bot 55:263–275
Cadotte M, Rakotonasolo F, Reza L, Lovett-Doust J (2002) Tree and shrub diversity and abundance in fragmented littoral forest of southeastern Madagascar. Biodiv Cons 11:1417–1436
Cardoso S, Eloy N, Provan J, Cardoso M, Ferreira P (2000) Genetic differentiation of Euterpe edulis Mart. populations estimated by AFLP analysis. Mol Ecol 9:1753–1760
Cibrian-Jaramillo A, Hahn W, Desalle R (2008) Development of microsatellite markers of the Mexican understorey palm Chamaedorea elegans, cross-species genotyping, and amplification in congeners. Mol Ecol Notes 8:322–324
Colpaert N, Cavers S, Bandou E, Caron H, Gheysen G, Lowe AJ (2005) Sampling tissue for DNA analysis of trees: trunk Cambium as an alternative to canopy leaves. Sil Genet 54:265–269
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allelic frequency data. Genetics 144:2001–2014
Craul M, Chikhi L, Sousa V, Olivieri G, Rabesandratana A, Zimmermann E, Radespiel U (2009) Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biodiv Cons 142:2862–2871
Davis A, Lewis C, Francisco-Ortega J, Zona S (2007) Differentiation among insular and continental populations of Coccothrinax argentata (Arecaceae): evidence from DNA markers and a common garden experiment. Taxon 56:103–111
Dew J, Wright P (1998) Frugivory and seed dispersal by four species of primates in Madagascar’s eastern rain forest. Biotrop 30:425–437
Dowe J, Benzie J, Ballment E (1997) Ecology and genetics of Carpoxylon macrospermum H Wendl. and Drude (Arecaceae), an endangered palm from Vanuatu. Biol Cons 79:205–216
Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phyto Bull 19:11–15
Dransfield J (1989) Voanioala (Arecoideae: Cocoeae: Butiinae), a new palm genus from Madagascar. Kew Bull 44:191–198
Dransfield J, Beentje H (1995) The palms of Madagascar. Royal Botanic Gardens Kew and the International Palm Society, Kew
Dransfield J, Uhl N, Asmussen C, Baker W, Harley M, Lewis C (2008a) Genera palmarum: the evolution and classification of palms. Kew Publishing, Royal Botanic Gardens, Kew
Dransfield J, Uhl N, Asmussen C, Baker W, Harley M, Lewis C (2008b) Genera palmarum: the evolution and classification of palms. Kew Publishing, Royal Botanic Gardens
Dransfield J, Rakotoarinivo M, Baker WJ, Bayton RB, Fisher JB, Horn JW, Bruno LB, Metz X (2008c) New coryphoid palm genus from Madagascar. Bot J Linn Soc 156:79–91
Du Puy D, Moat J (1996) A refined classification of the primary vegetation of Madagascar based on the underlying geology: using GIS to map its distribution and to assess its conservation status. In: Lourenco WR (ed) Biogeography of Madagascar. ORSTOM, Paris, pp 205–218
Dumetz N (1999) High plant diversity of lowland rainforest vestiges in eastern Madagascar. Biodiv Cons 8:273–315
El-Kassaby Y, Ritland K (1996) Impact of selection and breeding of the genetic diversity in Douglas-fir. Biodiv Cons 5:795–813
Ellstrand N, Elam D (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242
Freville H, Colas B, Riba M, Caswell H, Mignot A, Imbert E, Olivieri I (2004) Spatial and temporal demographic variability in the endemic plant species Centauria corymbosa (Asteraceae). Ecol 85:694–703
Gaiotto F, Brodani R, Grattapaglia D (2001) Microsatellite markers for heart of palm: Euterpe edulis and E.oleracea Mart. (Arecaceae). Mol Ecol Notes 1:86–88
Gaiotto F, Grattapaglia D, Vencovsky R (2003) Genetic structure, mating system, and long-distance gene flow in heart of palm (Euterpe edulis Mart.). J Hered 94:399–406
Galetti M, Donatti C, Pires A, Guimaraes P Jr, Jordano P (2006) Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Bot J Linn Soc 151:141–149
Gitzendanner M, Soltis P (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792
Gonzalez-Perez M, Caujape-Castells J, Sosa P (2004) Allozyme variation and structure of the Canarian endemic palm tree Phoenix canariensis (Arecaceae): implications for conservation. Hered 93:307–315
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Let 8:993–1009
Guisan A, Broennimann O, Engler R, Vust M, Yoccoz N, Lehmann A, Zimmermann N (2006) Using niche based models to improve the sampling of rare species. Cons Biol 20:501–511
Hardesty BD, Dick CW, Hamrick JL, Degen B, Hubbell SP, Bermingham E (2010) Geographic influence on genetic structure in the widespread Neotropical tree, Simarouba amara (Simaroubaceae). Trop Pl Biol. 3:28–39
Hedrick P, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Cons Gen 11:615–626
Hegarty MJ, Hiscock SJ (2009) Allopolyploid genomes; the complex nature of allopolyploid plant genomes. Heredity 103:100–101
Henderson A (2002) Evolution and ecology of palms. The New York Botanical Gardens Press, Bronx
Henderson S, Billotte N, Pintaud J-C (2006) Genetic isolation of Cape Verde Island Phoenix atlantica (Arecaceae) revealed by microsatellite markers. Cons Gen 7:213–223
Honnay O, Jacquemyn H, Bossuyt B, Hermy M (2005) Forest fragmentation effects on patch occupancy and population viability of herbaceous plant species. New Phytol 166:723–736
Horandl E, Greilhuber J (2002) Diploid and autotetraploid sexuals and their relationships to apomicts in the Ranunculus cassubicus group: insights from DNA content and isozyme variation. Pl Syst Evol 234:85–100
Irwin M, Johnson S, Wright P (2005) The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx 39:204–218
IUCN (2009) IUCN red list of threatened species: version 2009.2. www.iucnredlist.org. Accessed 8 March 2010
Jarvis A, Williams K, Williams D, Guarino L, Caballero PJ, Mottram G (2005) Use of GIS for optimizing a collecting mission for a rare wild pepper (Capsicum flexuosum Sendtn.) in Paraguay. Gen Res Crop Evol 52:671–682
Johnson MAT (1989) An unusually high chromosome number in Voanioala gerardii (Palmae: Arecoideae: Cocoeae: Butiinae) from Madagascar. Kew Bull 44:207–210
Johnson MAT, Kenton AY, Bennett MD, Brandham PE (1989) Voanioala gerardii has the highest known chromosome number in the monocotyledons. Genome 32:328
Keller L, Waller D (2002) Inbreeding effects in wild populations. Tree 17:230–241
Kumar A, Pushpangadan P, Mehrotra S (2003) Extraction of high-molecular-weight DNA from dry root tissue of Berberis lyceum suitable for RAPD. Pl Mol Biol Rep 21:309
Leducq J-B, Gosset C, Poiret M, Hendoux F, Vekemans X, Billiard S (2010) An experimental study of the S-Allee effect in the self-incompatible plant Biscutella neustriaca. Cons Gen 11:497–508
Lehtinen R, Ramanamanjato J-B, Raveloarison J (2003) Edge effects and extinction proneness in a herpetofauna from Madagascar. Biodiv Cons 12:1357–1370
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952
Luna R, Epperson BK, Oyama K (2007) High levels of genetic variability and inbreeding in two Neotropical dioecious palms with contrasting life histories. Hered 99:466–476
Maizura I, Rajanaidu N, Zakri A, Cheah S (2006) Assessment of genetic diversity in oil palm (Elaeis guineensis Jacq.) using restriction fragment length polymorphism (RFLP). Gen Res Crop Evol 53:187–195
Manel S, Williams H, Ormerod S (2001) Evaluating presence-absence models in ecology: the need to account for prevalence. J Appl Ecol 38:921–931
Marie C, Sibelet N, Dulcire M, Rafalimaro M, Danthu P, Carriere S (2009) Taking into account local practices and indigenous knowledge in an emergency conservation context in Madagascar. Biodiv Cons 18:2759–2777
Maschinski J (2006) Implications of population dynamic and metapopulation theory for restoration. In: Falk D, Palmer M, Zedler J (eds) Foundations of restoration ecology. Island Press, Washington DC, USA
Maschinski J, Duquesnel J (2006) Successful reintroductions of the endangered long-lived Sargent’s cherry palm, Pseudophoenix sargentii, in the Florida Keys. Biol Cons 134:122–129
McConnell W, Sweeney S (2005) Challenges of forest governance in Madagascar. Geog J 171:223–238
McKay J, Christian C, Harrison S, Rice K (2005) “How local is local?” A review of practical and conceptual issues in the genetics of restoration. Rest Ecol 13:432–440
McKean S (2003) Toward sustainable use of palm leaves by a rural community in Kwazulu-Natal, South Africa. Econ Bot 57:65–72
Moat J, Smith P (2007) Atlas of the vegetation of Madagascar. Kew Publishing UK, p 124
Montufar R, Mariac C, Pham J-L, Pintaud J-C (2007) Isolation of 23 polymorphic microsatellite loci in the Neotropical palm (Oenocarpus bataua) Martius (Arecaceae). Mol Ecol Notes 7:75–78
Namoff S, Husby C, Francisco-Ortega J, Noblick L, Lewis C, Griffith M (2010) How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population? Biol Cons 143:1110–1117
Nazareno A, de Carvalho D (2009) What the reasons for no inbreeding and high genetic diversity of the neotropical figure tree Ficus arpazusa? Cons Gen 10:1789–1793
Norscia I (2008) Pilot survey of avahi population (woolly lemurs) in littoral forest fragments of southeast Madagascar. Primates 49:85–88
Novaes R, Rodrigues J, Lovato MB (2009) An efficient protocol for tissue sampling and DNA isolation from the stem bark of Leguminosae trees. Gen Mol Res 8:86–96
Nucci S, Azevedo-Filho J, Colombo C, Priolli R, Coelho R, Mata T, Zucchi M (2008) Development and characterization of microsatellites markers from the macaw. Mol Ecol 8:224–226
Olmsted I, Alvarez-Buylla E (1995) Sustainable harvesting of tropical trees: demography and matrix models of two palm species in Mexico. Ecol Appl 5:484–500
Oostermeijer J, Luijten S, den Nijs J (2003) Integrating demographic and genetic approaches in plant conservation. Biol Cons 113:389–398
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Ann Rev Gen 34:401–437
Palmer J (1988) Chloroplast DNA variation and plant phylogeny. Ann Miss Bot Gard 75:1180–1206
Peakall R, Smouse P (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pearson RG, Raxworthy CJ, Nakamura M, Peterson AT (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeog 34:102–117
Perera L, Russell JR, Provan J, Powell W (1999) Identification and characterisation of microsatellite loci in coconut (Cocos nucifera L.) and the analysis of coconut populations in Sri Lanka. Mol Ecol 8:335–346
Pettit NE, Dowe JL (2003) Distribution and population structure of the vulnerable riparian palm Livistona lanuginosa AN Rodd (Arecaceae) in the Burdekin River catchment, north Queensland. Pac Cons Biol 9:207–214
Pfab MF, Witkowski ETF (1997) Use of geographic information systems in the search for additional populations, or sites suitable for re-establishment, of the endangered northern province endemic Euphorbia clivicola. S Af J Bot 63:351–355
Phillips SJ, Dudik M (2008) Modelling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modelling of species geographic distributions. Ecol Model 190:231–259
Powell M, Accad A, Austin MP, Low Choy S, Williams KJ, Shapcott A (2010) Assessment of loss and fragmentation of a rare species habitat with niche models developed from compiled ecological data. Biol Cons 143:1385–1396
Rakotoarinivo M (2008) Analyse de la distribution et de la conservation des palmiers (Arecaceae) de Madagascar par l’utilisation du système d’information géographique. Thèse de Doctorat, Université d’Antananarivo.
Rakotoarinivo M, Dransfield J (2010) New species of Dypsis and Ravenea (Arecaceae) from Madagascar. Kew Bull 65:279–303
Rakotoarinivo M, Ranarivelo T, Dransfield J (2007) A new species of Beccariophoenix from the High Plateau of Madagascar. Palms 51:63–75
Rakouth B, Roger E (2011) Guide pour l’identification des graines de palmiers malgaches commercialisees. Autorité Scientifique Flore CITES, p 60.
Ratsirarson J, Silander J, Richard A (1996) Conservation and management of a threatened Madagascar palm species, Neodypsis decaryi, Jumelle. Cons Biol 10:40–52
Raxworthy CJ, Martinez-Meyer E, Horning N, Nussbaum RA, Schneider GE, Orteg-Huerta MA, Peterson AT (2003) Predicting distributions of known and unknown reptile species in Madagascar. Nature 426:837–841
Ren H, Zhand Q, Wang Z, Guo Q, Wang J, Liu N, Liang K (2010) Conservation and possible reintroduction of an endangered plant based on an analysis of community ecology: a case study of Primula tabacum Hance in China. Pl Sp Biol 25:43–50
Rodríguez-Buriticá S, Orjuela MA, Galeano G (2005) Demography and life history of Geonoma orbignyana: an understory palm used as foliage in Colombia. For Ecol Manag 211:329–340
Röser M (1994) Pathways of karyological differentiation in palms (Arecaceae). Pl Syst Evol 189:83–122
Saghai-Maroof M, Soliman K, Jorgensen R, Allard R (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Nat Acad Sci USA 81:8014–8018
Schurr FM, Midgley GF, Rebelo AG, Reves G, Poschlod P, Higgins SI (2007) Colonization and persistence ability explain the extent to which plant species fill their potential range. Glob Ecol Biogeog 16:449–459
Shapcott A (1998a) The genetics of Ptychosperma bleeseri a rare palm from the Northern Territory, Australia. Biol Cons 85:203–209
Shapcott A (1998b) The patterns of genetic diversity in Carpentaria acuminata (Arecaceae), and rainforest history in northern Australia. Mol Ecol 7:833–847
Shapcott A (1999) Comparison of the population genetics and densities of five Pinanga palm species at Kuala Belalong, Brunei. Mol Ecol 8:1641–1654
Shapcott A (2000) Conservation and genetics in the fragmented monsoon rainforest in the Northern Territory, Australia: a case study of three frugivore-dispersed species. Aust J Bot 48:397–407
Shapcott A, Powell M (2011) Demographic structure, genetic diversity and habitat distribution of the endangered, Australian rainforest tree Macadamia jansenii help facilitate an reintroduction program. Aust J Bot 59:215–225
Shapcott A, Rakotoarinivo M, Smith R, Lysakova G, Fay M, Dransfield J (2007) Can we bring Madagascar’s critically endangered palms back from the brink? Genetics, ecology and conservation of the critically endangered palm Beccariophoenix madagascariensis. Bot J Linn Soc 154:589–608
Shapcott A, Dowe J, Ford H (2009a) Low genetic diversity and recovery implications of the vulnerable Bankouale Palm Livistona carinensis (Arecaceae), from North-eastern Africa and the Southern Arabian Peninsula. Cons Gen 10:317–327
Shapcott A, Olsen M, Lamont RW (2009b) The importance of genetic considerations for planning translocations in the rare heathland species Boronia rivularis. Ecol Rest 27:47–57
Stockwell DRB, Peterson AT (2002) Effects of sample size on accuracy of species distribution models. Ecol Model 148:1–13
Teulat B, Aldam C, Trehin R, Lebrun P, Barker J, Arnold G, Karp A, Baudouin L, Rognon F (2000) An analysis of genetic diversity in coconut (Cocos nucifera) populations from across the geographic range using sequence-tagged microsatellites (SSR’s) and AFLPs. TAG 100:764–771
Tomlinson PB (1990) The structural biology of palms. Clarendon Press; Oxford University Press, Oxford
Uchiyama K, Goto S, Ide Y (2009) Effects of population density on male and female reproductive success in the wind-pollinated, wind-dispersed tree species Betula maximowicziana. Cons Gen 10:1265–1275
Acknowledgments
Funding from the International Palm Society Endowment Fund and the University of the Sunshine Coast (USC), with in-kind support from The Royal Botanic Gardens (RBG) Kew. Dr Bill Baker, Stuart Cable, Dr Helene Ralimanana, Andrianaivoravelona Bakoly and Rajaovelona Landy, Jao Aridy ANGAP, Dr Franck Rakotonasolo Parc Botanique et Zoologique de Timbazaza, and field guides Regis, Oclino, Be Leonor, and Tsimanimba. The USC Genecology research group, especially Rob Lamont, Anna Kuballa and Daniel Powell.
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Shapcott, A., Quinn, J., Rakotoarinivo, M. et al. Contrasting patterns of genetic diversity between two endangered palms with overlapping distributions, Voanioala gerardii (Arecoideae) and Lemurophoenix halleuxii (Arecoideae), from North-east Madagascar. Conserv Genet 13, 1393–1408 (2012). https://doi.org/10.1007/s10592-012-0382-6
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DOI: https://doi.org/10.1007/s10592-012-0382-6