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“Subpopulations are defined as geographically or otherwise distinct groups in the population between which there is little demographic or genetic exchange (typically one successful migrant individual or gamete per year or less).” (IUCN 2001)

Background

Female sea turtles tend to return to their natal regions to nest (reviewed in Miller 1996), while less is known about breeding males. Early demographic studies uncovered the striking nest site fidelity of many females (reviewed in Miller 1996). Subsequently, maternally inherited mitochondrial DNA (mtDNA) research demonstrated the isolation of many rookeries or rookery groups, supporting Carr’s (1967) natal homing hypothesis (reviewed by Bowen & Karl 1996). Analysis of male and female mtDNA from Australian green turtle breeding areas reveal similar and significant levels of population structure, indicating philopatric behavior in both sexes (FitzSimmons et al. 1997a). Tagging and telemetry data also suggest fidelity of green sea turtle males to courtship sites, at least in some locations (Balazs 1980; Dizon & Balazs 1982; Limpus 1993). Biparentally inherited non-protein coding nuclear (nDNA) markers such as microsatellites, however, indicate there may be gene flow among breeding populations. In green sea turtles, gene flow is thought to occur during spatially overlapping reproductive migrations (FitzSimmons et al. 1997a; 1997b), and may be mediated by males (Karl et al. 1992; Roberts et al. 2004). Even so, most green sea turtle rookery pairs in Australia are significantly differentiated in microsatellite as well as in mtDNA analyses (FitzSimmons et al. 1997a; 1997b). Recent preliminary research examining microsatellite loci in various sea turtle species suggests there may be significant differentiation among several rookery pairs in these analyses as well (Formia & Bruford in press; Carreras et al. 2006; Dutton 2006; Naro-Maciel 2006; Carreras et al. in press). Whether the levels of genetic differentiation elucidated in ongoing studies will meet current IUCN subpopulation criteria in some cases, however, is presently an open question.

1. Which lines of evidence are to be considered in Red Listing sea turtle subpopulations?

Genetic, mark-recapture, and satellite telemetry data are important sources of information about linkages among sea turtle populations. Although previous studies have illuminated relationships among many groups, all of these methods are impacted to some extent by biological, logistical, or analytical constraints. Tagging studies do not indicate the route taken by the turtle, and may be affected by tag loss, monitoring intensity, sample size, and other factors. Tracking research is often limited by small sample sizes or data quality issues. Certain commonly employed genetic estimates of population subdivision and numbers of migrants may suffer from lack of resolution or rest on unmet assumptions (Bossart & Prowell 1998; Pearse & Crandall 2004). Although new approaches are being developed to address such issues (for example Beerli 1998; Pritchard et al. 2000), these often come with their own sets of assumptions and constraints. An integrated approach considering results of demographic and tracking research is therefore recommended when interpreting genetic data (Dutton et al.2002).

The necessity and relative importance of insights from different fields in Red List categorization can vary. The subpopulation definition above refers to “geographically or otherwise distinct groups …between which there is little demographic or genetic exchange,” allowing for distinctiveness that need not be genetic. In some cases, subpopulations have been listed despite the need for additional genetic studies (Bearzi 2003). There is also no consensus on the relative importance of nDNA or mtDNA research in Red List categorization of sea turtles. As mentioned above, differentiation among rookeries is less pronounced in nDNA than in mtDNA analyses, possibly due to the homogenizing influence of gene flow detectable at nuclear loci. Thus, estimates of rookery isolation using microsatellites are less likely to meet the IUCN definition. Even so, and while not specifically referring to the Red List, Bowen et al. (2005) consider that “Male-mediated gene flow does not detract from the classification of breeding areas as independent populations” (p. 2398). Mrosovsky (2006), on the other hand, finds the relatively low levels of differentiation suggested by non-protein coding nDNA to be more important in IUCN subpopulation listing than the isolation indicated by mtDNA. However, if results among markers do conflict an essential first step should be to determine whether additional work is needed specifically to address issues of IUCN subpopulation Red Listing. With improving methods and technology, increased sample sizes, additional markers examined, and more sites included, apparent conflicts may be lessened or clarified in subsequent research.

2. To what extent do sea turtle breeding populations worldwide qualify as IUCN Red List subpopulations?

While philopatric behavior tends to isolate rookeries, does gene flow homogenize them enough that they fail to meet the currently accepted IUCN subpopulation definition? Does the only sea turtle subpopulation ever to appear on the IUCN Red List separately from the species in fact meet these criteria? To address these questions, a complete compilation of all pertinent information, including mark-recapture, satellite telemetry, and genetics, is an essential first step. Supplementary research specifically designed to address the question of IUCN subpopulation status may also be required. A regional assessment of green sea turtles in the Mediterranean is currently underway, and may provide the necessary justification for relisting (Mast et al. 2006). For now, consideration of readily accessible data about these turtles, which may not be comprehensive, indicates all females tracked after nesting in Cyprus have remained inside the Mediterranean (Broderick et al. 2006b; Godley et al. 2002). Differentiation of Cyprus from Atlantic rookeries is indicated by the unique nature of the mtDNA haplotypes, to date found only in the Mediterranean, and significant pairwise estimates of population subdivision in mtDNA analyses (Encalada et al. 1996; Kaska 2000). A comprehensive global study of four microsatellite loci, however, reports male-mediated gene flow among many rookeries (Roberts et al. 2004). This research also focuses on the molecular evolutionary history of these markers, detecting possible deviations from commonly assumed models of evolution (Roberts et al. 2004). These findings underscore the need for further attention to methodological and historical issues in ongoing microsatellite analyses.

3. Is the IUCN subpopulation definition inappropriate for sea turtles?

Lastly, the appropriateness of the IUCN subpopulation definition was questioned for sea turtles due to their life history characteristics by Mrosovsky (2006): “… it is assumed that in the definition of a subpopulation given above, for slowly maturing species with a long generation time, to base genetic isolation on one or fewer migrants or gamete exchanges per year is inappropriate… Most accounts of differentiation of populations use gamete/migrant exchange per generation” (p. 2). While these estimates, particularly in genetic analysis, do in fact tend to be given per generation, changing the definition without correspondingly increasing the numbers of migrants allowed would make subpopulation qualification more difficult. Despite possible shortcomings of the IUCN definitions for sea turtles (Mrosovsky 2004; Seminoff 2004; Mrosovsky 2006), Red List criteria are designed “to provide an explicit, objective framework for the classification of the broadest range of species according to their extinction risk” (Introduction, Section 1, IUCN 2001). The IUCN also states “[t]here is sufficient range among the different criteria to enable the appropriate listing of taxa from the complete taxonomic spectrum, with the exception of micro-organisms” (Preamble, Section 1, IUCN 2001). In light of the comprehensive nature of the IUCN Red List and its intended applicability across taxa, any proposed changes to the subpopulation definition for sea turtles should at the very least take into account similar decisions made by other specialist groups, and be considered within the larger context of the IUCN goals.

Acknowledgements: We would like to thank Annette Broderick, Carlos Carreras, Matthew Godfrey, Stephen Karl, Jeffrey Seminoff, Manjula Tiwari, and two anonymous reviewers for helpful comments, information, materials, and/or discussions.

BALAZS, G. H. 1980. Synopsis of biological data on the green turtle in the Hawaiian Islands. NOAA Tech. Memo, NOAA-TM-NMFS-SWFC-7.

BEARZI, G. 2003. Delphinus delphis (Mediterranean subpopulation). In: IUCN 2006. 2006 IUCN Red List of Threatened Species. <http://www.iucnredlist.org>. Downloaded on 07 August 2006.

BEERLI, P. 1998. Estimation of migration rates and population sizes in geographically structured populations. In: G.R. Carvalho (Ed.). Advances in Molecular Ecology. IOS Press, Amsterdam. pp. 39-54.

BOSSART, J.L. & D.P. PROWELL. 1998. Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends in Ecology and Evolution 13: 202-205.

BOWEN, B.W. & S.A. KARL. 1996. Population genetics, phylogeography, and molecular evolution. In: Lutz, P.L. & J.A. Musick (Eds) The Biology of Sea Turtles. CRC Press, Inc., Boca Raton, Florida. pp. 29-50.

BOWEN, B.W., A. L. BASS, L. SOARES & R. J. TOONEN. 2005. Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Molecular Ecology 14: 2389-2402.

BRODERICK, A.C., R. FRAUENSTEIN, F. GLEN, G. C. HAYS, A.L. JACKSON, T. PELEMBE, G.D. RUXTON & B.J. GODLEY. 2006a. Are green turtles globally endangered? Global Ecology and Biogeography 15: 21-26.

BRODERICK, A.C., M.S. COYNE, F. GLEN, W.J. FULLER & B.J. GODLEY. 2006b. Foraging site fidelity of adult green and loggerhead turtles. In: Frick, M., A. Panagopoulou, A.F. Rees & K. Williams (Compilers) Book of Abstracts. Twenty Sixth Annual Symposium on Sea Turtle Biology and Conservation. International Sea Turtle Society, Athens, Greece. p. 83.

CARR, A.F. 1967. So Excellent a Fishe: A Natural History of Sea Turtles. Scribner, NY. 292 pp.

CARRERAS, C., L. CARDONA, A. MARCO, M. PASCUAL, A. AGUILAR, D. MARGARITOULIS, A. REES, J.J. CASTILLO, J. TOMAS, J.A. RAGA, G. FERNÁNDEZ, M. SANFÉLIX, O. TURKOZAN, Y. LEVY, A. GASITH, M. AUREGGI, M. KHALIL, C. RICO & S. ROQUES. 2006. Degree of isolation of the Mediterranean nesting populations of the loggerhead sea turtle using nuclear markers. In: Frick, M., A. Panagopoulou, A.F. Rees & K. Williams (Compilers) Book of Abstracts. Twenty Sixth Annual Symposium on Sea Turtle Biology and Conservation. International Sea Turtle Society, Athens, Greece. p. 186.

CARRERAS, C., M. PASCUAL, L. CARDONA, A. AGUILAR, D. MARGARITOULIS, A. REES, O. TURKOZAN, Y. LEVY, A. GASITH, M. AUREGGI & M. KHALIL. In press. The genetic structure of the Mediterranean loggerhead sea turtle (Caretta caretta) as revealed by nuclear and mitochondrial DNA and its conservation implications. Conservation Genetics.

DIZON, A.E. & G.H. BALAZS. 1982. Radio telemetry of Hawaiian green turtles at their breeding colony. Marine Fisheries Review 44: 13-20.

DUTTON, P.H. 2006. Geographic variation in foraging strategies of leatherback populations: a hedge against catastrophy? In: Frick, M., A. Panagopoulou, A.F. Rees & K. Williams (Compilers) Book of Abstracts. Twenty Sixth Annual Symposium on Sea Turtle Biology and Conservation. International Sea Turtle Society, Athens, Greece. p. 189.

DUTTON, P.H., D. BRODERICK & N. FITZSIMMONS. 2002. Defining management units: molecular genetics. In: I. Kinan (Ed.). Proceedings of the Western Pacific Sea Turtle Cooperative Research and Management Workshop. Honolulu, Hawaii, USA, February 5-8, 2002, Western Pacific Regional Fishery Management Council, Honolulu, HI. pp. 93-101.

ENCALADA S.E., P.N. LAHANAS, K.A. BJORNDAL, A.B. BOLTEN, M.M MIYAMOTO & B.W. BOWEN. 1996. Phylogeography and population structure of the Atlantic and Mediterranean green turtle Chelonia mydas: a mitochondrial DNA control region sequence assessment. Molecular Ecology 5: 473-483.

FITZSIMMONS, N.N., C.J LIMPUS, J.A. NORMAN, A.R. GOLDIZEN, J.D. MILLER & C. MORITZ. 1997a. Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proceedings of the National Academy of Sciences USA 94: 8912-8917.

FITZSIMMONS, N.N., C. MORITZ, C.J. LIMPUS, L. POPE & R. PRINCE. 1997b. Geographic structure of mitochondrial and nuclear gene polymorphisms in Australian green turtle populations and male-biased gene flow. Genetics 147: 1843-1854.

FORMIA, A. & M.W. BRUFORD. In press. Preliminary microsatellite DNA analysis of African green turtle populations. Proceedings of the 24th Annual Symposium on Sea Turtle Biology and Conservation. San Jose, Costa Rica, 2004.

GODLEY, B.J., S. RICHARDSON, A.C. BRODERICK, M.S. COYNE, F. GLEN & G.C. HAYS. 2002. Long-term satellite telemetry of the movements and habitat utilization by green turtles in the Mediterranean. Ecography 25: 352-362.

IUCN. 2001. IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission, Gland, Switzerland. 30 pp (Available at: <http://www.iucnredlist.org/info/categories_criteria>).

IUCN. 2004. Red List of Threatened Species. www.iucnredlist.org.IUCN. 2006. Red List of Threatened Species. <http://www.iucnredlist.org>.

KARL, S.A., B.W. BOWEN & J.C. AVISE. 1992. Global population structure and male-mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear DNA regions. Genetics 31: 163-173.

KASKA, Y. 2000. Genetic structure of Mediterranean sea turtle populations. Turkish Journal of Zoology 24: 191-197.

LIMPUS, C.J. 1993. The green turtle, Chelonia mydas, in Queensland: breeding males in the Southern Great Barrier Reef. Wildlife Research 20: 513-523.

MAST, R.B., J.A SEMINOFF, B.J. HUTCHINSON & N.J. PILCHER. 2006. The role of the IUCN MTSG in setting priorities for sea turtle conservation. Marine Turtle Newsletter 113:16-18.

MEYLAN, A. 1995. Sea turtle migration - evidence from tag returns. In: K.A. Bjorndal (Ed.) Biology and Conservation of Sea Turtles. 2nd Edition. Smithsonian Institution Press, Washington D.C. pp. 91-100.

MILLER, J.D. 1996. Reproduction in sea turtles. In: Lutz, P.L. & J.A. Musick (Eds) The Biology of Sea Turtles. CRC Press, Inc., Boca Raton, Florida. pp. 51-81.

MROSOVSKY, N. 2004. Conceptual problems with the IUCN Red Listing assessment for the green turtle: move over Raine Isand. Marine Turtle Newsletter 106:1-3.

MROSOVSKY, N. 2006. Does the Mediterranean green turtle exist? Marine Turtle Newsletter 111:1-2.

NARO-MACIEL, E., 2006. Connectivity and structure of Atlantic green sea turtles (Chelonia mydas): a genetic perspective. PhD. Dissertation. Columbia University, NY, USA.

PEARSE, D.E. & K.A. CRANDALL 2004. Beyond FST: analysis of population genetic data for conservation. Conservation Genetics 5: 585-602.

PRITCHARD, J.K., M. STEPHENS & P. DONNELLY. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.

ROBERTS, M.A., T.S. SCHWARTZ & S.A. KARL. 2004. Global population genetic structure and male-mediated gene flow in the green sea turtle (Chelonia mydas): analysis of microsatellite loci. Genetics 166: 1857-1870.

SEMINOFF, J. 2004. Sea turtles, Red Listing, and the need for regional assessments. Marine Turtle Newsletter 106:4-6.