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RESEARCH ARTICLE

Evidence for a single panmictic and genetically diverse population of the coconut crab Birgus latro (Decapoda: Anomura: Coenobitidae) on Christmas Island in the Indian Ocean

C. Anagnostou A C and C. D. Schubart B
+ Author Affiliations
- Author Affiliations

A Zoological Institute, Department of Evolutionary Ecology and Genetics, Christian-Albrechts-University of Kiel, D-24118 Kiel, Germany.

B Zoologie und Evolutionsbiologie, Universität Regensburg, D-93040 Regensburg, Germany.

C Corresponding author. Email: canagnostou@zoologie.uni-kiel.de

Marine and Freshwater Research 68(6) 1165-1177 https://doi.org/10.1071/MF16031
Submitted: 5 May 2015  Accepted: 27 August 2016   Published: 29 September 2016

Abstract

For the coconut crab Birgus latro, Christmas Island in the Indian Ocean may be one of the last retreats where populations of this declining species are not threatened by overharvesting, as on many other mostly tropical Indo-Pacific islands within the species’ wide range. Nevertheless, the population on Christmas Island has experienced severe losses during the past decade owing to habitat destruction and road mortality. To assess the population’s evolutionary potential and identify the number of conservation units, we conducted a combined morphometric and population genetic analysis using microsatellite markers. The findings suggest that the population is genetically diverse and panmictic. Neither genetic nor morphometric analyses revealed any population substructuring. There was no genetic evidence for sex-biased dispersal. Single-sample estimators for the effective population size (Ne) ranged from 492 to infinity, with very wide confidence intervals; they should therefore be viewed with caution. It would be advisable to reanalyse Ne, preferably by temporal methods. Despite mixed results, there is stronger evidence against rather than for the occurrence of a recent genetic bottleneck. So far, the population of B. latro on Christmas Island may be considered as a single conservation management unit, this way simplifying future conservation efforts taken for this magnificent species.

Additional keywords: bottleneck, conservation genetics, effective population size, microsatellites, morphometry, population structure.


References

Abbott, K. L. (2005). Supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on an oceanic island: forager activity patterns, density and biomass. Insectes Sociaux 52, 266–273.
Supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on an oceanic island: forager activity patterns, density and biomass.Crossref | GoogleScholarGoogle Scholar |

Abdul Muneer, P. M., Gopalakrishnan, A., Musammilu, K. K., Basheer, V. S., Mohindra, V., Lal, K. K., Padmakumar, K. G., and Ponniah, A. G. (2012). Comparative assessment of genetic variability in the populations of endemic and endangered yellow catfish, Horabagrus brachysoma (Teleostei: Horabagridae), based on allozyme, RAPD, and microsatellite markers. Biochemical Genetics 50, 192–212.
Comparative assessment of genetic variability in the populations of endemic and endangered yellow catfish, Horabagrus brachysoma (Teleostei: Horabagridae), based on allozyme, RAPD, and microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFelsrg%3D&md5=3360489db8d686e04247724ed54e82f6CAS | 21938562PubMed |

Allendorf, F. W., Luikart, G., and Aitken, S. N. (2012). ‘Conservation and the Genetics of Populations.’ 2nd edn. (Wiley-Blackwell: Hoboken, NJ, USA.)

Anagnostou, C., and Schubart, C. D. (2014). Morphometric characterisation of adult Birgus latro on Christmas Island. The Raffles Bulletin of Zoology 30, 136–149.

Appleyard, S. A., and Ward, R. D. (2006). Genetic diversity and effective population size in mass selection lines of Pacific oyster (Crassostrea gigas). Aquaculture 254, 148–159.
Genetic diversity and effective population size in mass selection lines of Pacific oyster (Crassostrea gigas).Crossref | GoogleScholarGoogle Scholar |

Balloux, F., and Lugon-Moulin, N. (2002). The estimation of population differentiation with microsatellite markers. Molecular Ecology 11, 155–165.
The estimation of population differentiation with microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 11856418PubMed |

Beeton, B., Burbridge, A., Grigg, G., Harrison, P., How, R., Humphreys, B., McKenzie, N., and Woinarski, J. (2010). Final report of the Christmas Island Expert Working Group to the Minister for Environment Protection, Heritage and the Arts. Department of Environment Protection, Heritage and the Arts, Canberra, ACT, Australia.

Benzie, J. A. H. (2000). Population genetic structure in penaeid prawns. Aquaculture Research 31, 95–119.
Population genetic structure in penaeid prawns.Crossref | GoogleScholarGoogle Scholar |

Brown, I. W., and Fielder, D. R. (1991). Project overview and literature survey. In ‘The Coconut Crab: Aspects of the biology and Ecology of Birgus latro in the Republic of Vanuatu’. (Eds I. W. Brown and D. R. Fielder.) Monograph 8, pp. 1–11. (Australian Centre for International Agricultural Research: Canberra, ACT, Australia.)

Burstyn, H. L. (1975). Science pays off: Sir John Murray and the Christmas Island phosphate industry, 1886–1914. Social Studies of Science 5, 5–34.
Science pays off: Sir John Murray and the Christmas Island phosphate industry, 1886–1914.Crossref | GoogleScholarGoogle Scholar |

Casacci, L. P., Barbero, F., and Balletto, E. (2014). The ‘evolutionary significant unit’ concept and its applicability in biological conservation. The Italian Journal of Zoology 81, 182–193.
The ‘evolutionary significant unit’ concept and its applicability in biological conservation.Crossref | GoogleScholarGoogle Scholar |

Chambers, P. (2011). Society has been defended: following the shifting shape of state through Australia’s Christmas Island. International Political Sociology 5, 18–34.
Society has been defended: following the shifting shape of state through Australia’s Christmas Island.Crossref | GoogleScholarGoogle Scholar |

Chapuis, M. P., and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtleku7c%3D&md5=3cd9772f2b9f66d4717a8a6b035308f2CAS | 17150975PubMed |

Cornuet, J. M., and Luikart, G. (1997). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.

Cowen, R. K., and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.
Larval dispersal and marine population connectivity.Crossref | GoogleScholarGoogle Scholar | 21141044PubMed |

Davey, J. W., and Blaxter, M. L. (2010). RADSeq: next-generation population genetics. Briefings in Functional Genomics 9, 416–423.
RADSeq: next-generation population genetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXis1Wmtr4%3D&md5=6d5f66e9e8c4762f1d9801da80da3124CAS | 21266344PubMed |

Davies, C., and Beckley, L. E. (2010). Zooplankton from the inshore waters of Christmas Island (Indian Ocean) with reference to the larvae of the red land crab, Gecarcoidea natalis. Journal of the Royal Society of Western Australia 93, 43–50.

Delmotte, F., Leterme, N., Gauthier, J.-P., Rispe, C., and Simon, J.-C. (2002). Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology 11, 711–723.
Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFahsr0%3D&md5=01073fca1797c39246e7a96380a7e3f0CAS | 11972759PubMed |

Desvignes, J. F., Laroche, J., Durand, J. D., and Bouvet, Y. (2001). Genetic variability in reared stocks of common carp (Cyprinus carpio L.) based on allozymes and microsatellites. Aquaculture 194, 291–301.
Genetic variability in reared stocks of common carp (Cyprinus carpio L.) based on allozymes and microsatellites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpsVGjtQ%3D%3D&md5=d1eac334e4b6150d1b9c7c97b88278bcCAS |

Director of National Parks (2014a). ‘Christmas Island Biodiversity Conservation Plan 2014.’ (Department of the Environment: Canberra.)

Director of National Parks (2014b). Christmas Island National Park Management Plan 2014–2024. (Department of the Environment: Canberra.) Available at https://www.environment.gov.au/system/files/resources/aa0c6d7f-d787-405b-955e-3bd9d1281ca7/files/christmas-island-national-park-management-plan-2014-2024_1.pdf [Verified 30 August 2016].

Do, C., Waples, R. S., Peel, D., Macbeth, G. M., Tillett, B. J., and Ovenden, J. R. (2014). NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources 14, 209–214.
NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sbktV2nuw%3D%3D&md5=622d07751b41902a71e9fade109fcf29CAS | 23992227PubMed |

Drew, M. M., and Hansson, B. S. (2014). The population structure of Birgus latro (Crustacea: Decapoda: Anomura: Coenobitidae) on Christmas Island with incidental notes on behaviour. The Raffles Bulletin of Zoology 30, 150–161.

Drew, M. M., Harzsch, S., Stensmyr, M., Erland, S., and Hansson, B. S. (2010). A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus 1767) (Anomura: Coenobitidae). Zoologischer Anzeiger 249, 45–67.
A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus 1767) (Anomura: Coenobitidae).Crossref | GoogleScholarGoogle Scholar |

Drew, M. M., Smith, M. J., and Hansson, B. S. (2013). Factors influencing growth of giant terrestrial robber crab Birgus latro (Anomura: Coenobitidae) on Christmas Island. Aquatic Biology 19, 129–141.
Factors influencing growth of giant terrestrial robber crab Birgus latro (Anomura: Coenobitidae) on Christmas Island.Crossref | GoogleScholarGoogle Scholar |

Earl, D. A., and von Holdt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Eldredge, L. G. (1996). Birgus latro (coconut crab, palm thief, robber crab). In ‘IUCN Red List of Threatened Species’, ver. 2013.2. (International Union for Conservation of Nature and Natural Resources.) Available at http://www.iucnredlist.org/details/2811/0 [Verified 18 August 2016].

Environment Protection and Biodiversity Conservation Regulations (2011). ‘Environment Protection and Biodiversity Conservation Regulations 2000 – Schedule 12 (Protected Species).’ (Office of Legislative Drafting and Publishing, Attorney-General’s Department: Canberra.) Available at http://www.austlii.edu.au/au/legis/cth/consol_reg/epabcr2000697/sch12.html [Verified 22 September 2016].

Estoup, A., Rousset, F., Michalakis, Y., Cornuet, J. M., Adriamanga, M., and Guyomard, R. (1998). Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salmo trutta). Molecular Ecology 7, 339–353.
Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salmo trutta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivVWqsb0%3D&md5=5e5737c525a79ab40f5694587cd06f34CAS | 9561790PubMed |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=f1e687e3c48a9420af129f3b3675b00aCAS | 15969739PubMed |

Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetic data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=3cb5eea1ce5fab9d714560774e9d8a2aCAS |

Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure: extension to linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| 1:CAS:528:DC%2BD3sXnvF2ntrk%3D&md5=e60286048c27ea93f5338c469e99323dCAS | 12930761PubMed |

Falush, D., Stephens, M., and Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574–578.
Inference of population structure using multilocus genotype data: dominant markers and null alleles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslOhtbc%3D&md5=736e4882a1576e8b4d227314715e7bd8CAS | 18784791PubMed |

Favre, L., Balloux, F., Goudet, J., and Perrin, N. (1997). Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London – B. Biological Sciences 264, 127–132.
Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3hsFKiuw%3D%3D&md5=1b5af587aa1a4c82dc01babe2cb3afc9CAS |

Feng, M., and Wijffels, S. (2002). Intraseasonal variability in the South Equatorial Current of the East Indian Ocean. Journal of Physical Oceanography 32, 265–277.
Intraseasonal variability in the South Equatorial Current of the East Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Fletcher, W. J. (1993). Coconut crabs. In ‘Nearshore Marine Resources of the South Pacific: Information for Fisheries Development and Management’. (Eds A. Wright and L. Hill.) pp. 643–681. (International Centre for Ocean Development: Halifax, NS, Canada.)

Frankham, R. (1995). Effective population size/adult population size ratios in wildlife: a review. Genetical Research 66, 95–107.
Effective population size/adult population size ratios in wildlife: a review.Crossref | GoogleScholarGoogle Scholar |

Frankham, R. (1997). Do island populations have less genetic variation than mainland populations? Heredity 78, 311–327.
Do island populations have less genetic variation than mainland populations?Crossref | GoogleScholarGoogle Scholar | 9119706PubMed |

Frankham, R. (1998). Inbreeding and extinction: island populations. Conservation Biology 12, 665–675.
Inbreeding and extinction: island populations.Crossref | GoogleScholarGoogle Scholar |

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2010). ‘Introduction to Conservation Genetics’, 2nd edn. (Cambridge University Press: Cambridge, UK.)

Fraser, D. J., and Bernatchez, L. (2001). Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10, 2741–2752.
Adaptive evolutionary conservation: towards a unified concept for defining conservation units.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387mvFOjtw%3D%3D&md5=58e9218de7caf841a12db6773b1bb7e8CAS | 11903888PubMed |

Gan, C.-H., Tee, S.-M., Tang, P.-C., Yang, J. M.-C., Freire, F., McGowan, A., Narriman, J., Mohammed, M. S., Hsieh, H.-L., Chen, C.-P., Sheppard, C., and Chen, C. A. (2008). Isolation and characteristics of 10 microsatellite markers from the endangered coconut crab Birgus latro. Molecular Ecology Resources 8, 1448–1450.
Isolation and characteristics of 10 microsatellite markers from the endangered coconut crab Birgus latro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsV2ksL3I&md5=5625aa929ad38520351eb1d1484ab427CAS | 21586072PubMed |

García-Verdugo, C., Sajeva, M., La Mantia, T., Harrouni, C., Msanda, F., and Caujapé-Castells, J. (2015). Do island populations really have lower genetic variation than mainland populations? Effects of selection and distribution range on genetic diversity estimates. Molecular Ecology 24, 726–741.
Do island populations really have lower genetic variation than mainland populations? Effects of selection and distribution range on genetic diversity estimates.Crossref | GoogleScholarGoogle Scholar | 25580539PubMed |

Goudet, J. (1995). FSTAT (version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.

Goudet, J., Perrin, N., and Waser, P. (2002). Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Molecular Ecology 11, 1103–1114.
Tests for sex-biased dispersal using bi-parentally inherited genetic markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1arsrc%3D&md5=2cbf09d5c40f67ee062de1ff5ba8e326CAS | 12030985PubMed |

Gray, H. S. (1995). ‘Christmas Island Naturally: The Natural History of an Isolated Oceanic Island the Australian Territory of Christmas Island Indian Ocean’, 2nd edn. (Christmas Island Natural History Association: Christmas Island.)

Hamasaki, K., Sugizaki, M., Dan, S., and Kitada, S. (2009). Effect of temperature on survival and developmental period of coconut crab (Birgus latro) larvae reared in the laboratory. Aquaculture 292, 259–263.
Effect of temperature on survival and developmental period of coconut crab (Birgus latro) larvae reared in the laboratory.Crossref | GoogleScholarGoogle Scholar |

Hauser, L., Seamons, T. R., Dauer, M., Naish, K. A., and Qhinn, T. P. (2006). Am empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA. Molecular Ecology 15, 3157–3173.
Am empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Shu7%2FN&md5=bb387718b5aaf9ed96cdbeaeb91dfbecCAS | 16968262PubMed |

Hill, W. G. (1981). Estimation of effective population size from data on linkage disequilibrium. Genetical Research 38, 209–216.
Estimation of effective population size from data on linkage disequilibrium.Crossref | GoogleScholarGoogle Scholar |

Höglund, J. (2009). ‘Evolutionary Conservation Genetics.’ (Oxford University Press: New York.)

Hubisz, M., Falush, D., Stephens, M., and Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
Inferring weak population structure with the assistance of sample group information.Crossref | GoogleScholarGoogle Scholar | 21564903PubMed |

International Air Transport Association (2011) ‘Dangerous Goods Regulations (DGR) (2011)’, 52nd edn.

Jombart, T. (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
adegenet: a R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtVais7s%3D&md5=fbb2607ff752c8e066d0bc8d976ce047CAS | 18397895PubMed |

Krieger, J., Grandy, R., Drew, M. M., Erland, S., Stensmyr, M. C., Harzsch, S., and Hansson, B. S. (2012). Giant robber crabs monitored from space: GPS-based telemetric studies on Christmas Island (Indian Ocean). PLoS One 7, e49809.
Giant robber crabs monitored from space: GPS-based telemetric studies on Christmas Island (Indian Ocean).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslyisLjJ&md5=62228aa29a880e10d92e32cff854090bCAS | 23166774PubMed |

Lavery, S., Moritz, C., and Fielder, D. R. (1995). Changing patterns of population structure and gene flow at different spatial scales in Birgus latro (the coconut crab). Heredity 74, 531–541.
Changing patterns of population structure and gene flow at different spatial scales in Birgus latro (the coconut crab).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFGqurk%3D&md5=e7e2cecd6dc0604cb8dcf9b17525861cCAS |

Lavery, S., Moritz, C., and Fielder, D. R. (1996a). Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Molecular Ecology 5, 557–570.
Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro.Crossref | GoogleScholarGoogle Scholar |

Lavery, S., Moritz, C., and Fielder, D. R. (1996b). Genetic patterns suggest exponential population growth in a declining species. Molecular Biology and Evolution 13, 1106–1113.
Genetic patterns suggest exponential population growth in a declining species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1ektr0%3D&md5=5950d71605df948f3ea96a9b28142f9eCAS |

Linnaeus, C. (1767). ‘Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species cum characteribus, differentiis, synonymis, locis. Tomus I. Pars II. Editio duodecima reformata. Holmiæ.’ (Salvius: Stockholm.)

Luikart, G., Allendorf, F. W., Cornuet, J. M., and Sherwin, W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. The Journal of Heredity 89, 238–247.
Distortion of allele frequency distributions provides a test for recent population bottlenecks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czitVKhsA%3D%3D&md5=48333d7a129f7e5360a4f5a492984683CAS | 9656466PubMed |

Misso, M., and West, J. (2014). Conservation management of the terrestrial biodiversity of Christmas Island: challenges and perspectives. The Raffles Bulletin of Zoology 30, 17–23.

Moritz, C. (1994). Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology & Evolution 9, 373–375.
Defining ‘evolutionarily significant units’ for conservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFWhsA%3D%3D&md5=a3d3c878e182572d863558b234933496CAS |

Nomura, T. (2008). Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evolutionary Applications 1, 462–474.
Estimation of effective number of breeders from molecular coancestry of single cohort sample.Crossref | GoogleScholarGoogle Scholar | 25567728PubMed |

O’Dowd, D. J., Grenn, P. T., and Lake, P. S. (2003). Invasional ‘meltdown’ on an oceanic island. Ecology Letters 6, 812–817.
Invasional ‘meltdown’ on an oceanic island.Crossref | GoogleScholarGoogle Scholar |

Orchard, M. (2012). ‘Crabs of Christmas Island.’ (Christmas Island Natural History Association: Christmas Island.)

Paetkau, D., Calvert, W., Sterling, I., and Strobeck, C. (1995). Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4, 347–354.
Microsatellite analysis of population structure in Canadian polar bears.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntValu78%3D&md5=99da114fb135ce594c0abb87f82f37acCAS | 7663752PubMed |

Palstra, F. P., and Fraser, J. (2012). Effective/census population size ratio estimation: a compendium and appraisal. Ecology and Evolution 2, 2357–2365.
Effective/census population size ratio estimation: a compendium and appraisal.Crossref | GoogleScholarGoogle Scholar | 23139893PubMed |

Palstra, F. P., and Ruzzante, D. E. (2008). Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology 17, 3428–3447.
Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence?Crossref | GoogleScholarGoogle Scholar | 19160474PubMed |

Pavesi, L., Tiedemann, R., De Matthaeis, E., and Ketmaier, V. (2013). Genetic connectivity between land and sea: the case of the beachflea Orchestia montagui (Crustacea, Amphipoda, Talitridae) in the Mediterranean Sea. Frontiers in Zoology 10, 21.
Genetic connectivity between land and sea: the case of the beachflea Orchestia montagui (Crustacea, Amphipoda, Talitridae) in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 23618554PubMed |

Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=95686093fc03106d79e4140f3e21d2fbCAS | 22820204PubMed |

Piry, S., Luikart, G., and Cornuet, J. M. (1999). BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. The Journal of Heredity 90, 502–503.
BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data.Crossref | GoogleScholarGoogle Scholar |

Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Badouin, L., and Estoup, A. (2004). GENECLASS2: a software for genetic assignment and first-generation migrant detection. The Journal of Heredity 95, 536–539.
GENECLASS2: a software for genetic assignment and first-generation migrant detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlWlsrk%3D&md5=eb65d5c784a5ea047cbf93b092e80a5eCAS | 15475402PubMed |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=66ce2554c41294b6e14ab9910238e6bcCAS | 10835412PubMed |

Prugnolle, F., and de Meeus, T. (2002). Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88, 161–165.
Inferring sex-biased dispersal from population genetic tools: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387oslGluw%3D%3D&md5=fd23159c4cbf01347edd1e30d419263bCAS | 11920116PubMed |

Pudovkin, A. I., Zaykin, D. V., and Hedgecock, D. (1996). On the potential for estimating the effective number of breeders from heterozygote excess in progeny. Genetics 144, 383–387.
| 1:STN:280:DyaK2s%2Fjt12msQ%3D%3D&md5=84da55426125ad550dfee7e643633b3fCAS | 8878701PubMed |

Reese, E. S. (1968). Shell use: an adaptation for emigration from the sea by the coconut crab. Science 161, 385–386.
Shell use: an adaptation for emigration from the sea by the coconut crab.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvgs1Crtw%3D%3D&md5=83022bb6067efdd6a60d50d8d4fc3b25CAS | 17776741PubMed |

Reese, E. S., and Kinzie, R. A. (1968). The larval development of the coconut or robber crab Birgus latro (L.) in the laboratory (Anomura, Paguridae). Crustaceana 2, 117–144.

Rumpff, H. (1986). Ethology, ecology and population biology field studies of the coconut crab Birgus latro L. (Paguridea, Crustacea, Decapoda), on Christmas Island (Indian Ocean). Ph.D. Thesis, Westfälische Wilhelms-Universität Münster.

Sato, T., and Yoseda, K. (2008). Reproductive season and female maturity size of coconut crab Birgus latro on Hatoma Island, southern Japan. Fisheries Science 74, 1277–1282.
Reproductive season and female maturity size of coconut crab Birgus latro on Hatoma Island, southern Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1WmtA%3D%3D&md5=a46a91ac22117541c1dab4cdd1033257CAS |

Sato, T., Yoseda, K., Abe, O., and Shibuno, T. (2008). Male maturity, number of sperm, and spermatophore size relationships in the coconut crab Birgus latro on Hatoma Island, southern Japan. Journal of Crustacean Biology 28, 663–668.
Male maturity, number of sperm, and spermatophore size relationships in the coconut crab Birgus latro on Hatoma Island, southern Japan.Crossref | GoogleScholarGoogle Scholar |

Schiller, C.B. (1988). Spawning and larval recruitment in the coconut crab (Birgus latro) on Christmas Island, Indian Ocean. Consultancy Report prepared for the Australian National Parks and Wildlife Service. University of Queensland, Zoology Department, St Lucia, Qld, Australia.

Schubart, C. D., Cuesta, J. A., Diesel, R., and Felder, D. L. (2000). Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 15, 179–190.
Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs12qtbk%3D&md5=110bba981a5cd086b2fe86df7061ebcfCAS | 10837150PubMed |

Scribner, K. T., Arntzen, J. W., and Burke, T. (1994). Comparative analysis of intra- and interpopulation genetic diversity in Bufo bufo, using allozyme, single-locus microsatellite, minisatellite, and multilocus minisatellite data. Molecular Biology and Evolution 11, 737–748.
| 1:CAS:528:DyaK2cXmt1ensrs%3D&md5=cdd6f0ad7eb05b81034b56b3d7fc18edCAS | 7968487PubMed |

Silva, I. C., and Paula, J. (2008). Is there a better chela to use for geometric morphometric differentiation in brachyuran crabs? A case study using Pachygrapsus marmoratus and Carcinus maenas. Journal of the Marine Biological Association of the United Kingdom 88, 941–953.
Is there a better chela to use for geometric morphometric differentiation in brachyuran crabs? A case study using Pachygrapsus marmoratus and Carcinus maenas.Crossref | GoogleScholarGoogle Scholar |

The Secretariat of the Convention on Wetlands (2016) The list of wetlands of international importance. (The Secretariat of the Convention on Wetlands: Gland, Switzerland.) Available at http://www.ramsar.org/sites/default/files/documents/library/sitelist.pdf [Verified 22 September 2016].

Turlure, C., Vandewoestijne, S., and Baguette, M. (2014). Conservation genetics of a threatened butterfly: comparison of allozymes, RAPDs and microsatellites. BMC Genetics 15, 114.
Conservation genetics of a threatened butterfly: comparison of allozymes, RAPDs and microsatellites.Crossref | GoogleScholarGoogle Scholar | 25367292PubMed |

Turner, L. M., Hallas, P. J., Smith, M. J., and Morris, S. (2013). Phylogeography of the Christmas Island blue crab, Discoplax celeste (Decapoda: Gecarcinidae) on Christmas Island, Indian Ocean. Journal of the Marine Biological Association of the United Kingdom 93, 703–714.
Phylogeography of the Christmas Island blue crab, Discoplax celeste (Decapoda: Gecarcinidae) on Christmas Island, Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=ef2000248f2bb58bef70f9977c655eadCAS |

Wang, F.-L., Hsieh, H.-L., and Chen, C.-P. (2007). Larval growth of the coconut crab Birgus latro with a discussion on the development mode of terrestrial hermit crabs. Journal of Crustacean Biology 27, 616–625.
Larval growth of the coconut crab Birgus latro with a discussion on the development mode of terrestrial hermit crabs.Crossref | GoogleScholarGoogle Scholar |

Wang, J., Brekke, P., Huchard, E., Knapp, L. A., and Cowlishaw, G. (2010). Estimation of parameters of inbreeding and genetic drift in populations with overlapping generations. Evolution 64, 1704–1718.
Estimation of parameters of inbreeding and genetic drift in populations with overlapping generations.Crossref | GoogleScholarGoogle Scholar | 20100220PubMed |

Waples, R. S. (2005). Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Molecular Ecology 14, 3335–3352.
Genetic estimates of contemporary effective population size: to what time periods do the estimates apply?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitbvK&md5=a5587d13d7b2c000cc9c066a9e5cb8deCAS | 16156807PubMed |

Waples, R. S. (2006). A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conservation Genetics 7, 167–184.
A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci.Crossref | GoogleScholarGoogle Scholar |

Waples, R. S., and Antao, T. (2014). Intermittent breeding and constraints on litter size: consequences for effective population size per generation (Ne) and per reproductive cycle (Nb). Evolution 68, 1722–1734.
Intermittent breeding and constraints on litter size: consequences for effective population size per generation (Ne) and per reproductive cycle (Nb).Crossref | GoogleScholarGoogle Scholar | 24611912PubMed |

Waples, R. S., and Do, C. (2010). Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped source for applied conservation and evolution. Evolutionary Applications 3, 244–262.
Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped source for applied conservation and evolution.Crossref | GoogleScholarGoogle Scholar | 25567922PubMed |

Waples, R. S., Antao, T., and Luikart, G. (2014). Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197, 769–780.
Effects of overlapping generations on linkage disequilibrium estimates of effective population size.Crossref | GoogleScholarGoogle Scholar | 24717176PubMed |

Waser, P. M., and Strobeck, C. (1998). Genetic signatures of interpopulation dispersal. Trends in Ecology & Evolution 13, 43–44.
Genetic signatures of interpopulation dispersal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFyiuw%3D%3D&md5=82a61927f1e5ddbf83603a92ca9041ccCAS |

Weeks, A. R., Smith, M. J., van Rooyen, A., Maple, D., and Miller, A. D. (2014). A single panmictic population of endemic red crabs, Gecarcoidea natalis, on Christmas Island with high levels of genetic diversity. Conservation Genetics 15, 909–919.

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Willi, Y., Van Buskirk, J., and Hoffmann, A. A. (2006). Limits to the adaptive potential of small populations. Annual Review of Ecology and Systematics 37, 433–458.
Limits to the adaptive potential of small populations.Crossref | GoogleScholarGoogle Scholar |

Wright, S. (1949). The genetical structure of populations. Annals of Eugenics 15, 323–354.
The genetical structure of populations.Crossref | GoogleScholarGoogle Scholar |

Zhdanova, O., and Pudovkin, A. I. (2008). Nb-HetEx: a program to estimate the effective number of breeders. The Journal of Heredity 99, 694–695.
Nb-HetEx: a program to estimate the effective number of breeders.Crossref | GoogleScholarGoogle Scholar | 18703539PubMed |