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When a widely distributed species is abundant and increasing in some places but perilously depleted in other places, how should it be categorized on lists of threatened species? If weight is put on the depleted populations, and a high degree of threat is assigned to the species as a whole, that may influence in inappropriate ways the regulations that are applied to the thriving populations. But if more weight is put on the populations that are doing well, on the logical grounds that they will be likely to prevent the species as a whole from going extinct, then it may affect the enthusiasm and attention devoted to conservation in areas where the species is barely clinging on.
The obvious solution is to list different populations separately, rather than the species as a whole. At the 24th Turtle Symposium in Costa Rica in 2004, the Red List Authority (RLA) of the IUCN Marine Turtle Specialist Group (MTSG) spoke optimistically about a regional approach. But IUCN either instructed or strongly encouraged the MTSG first to make a listing for the species as a whole.
However, IUCN also allows listing below the species level. Examples of subpopulations listed differently from the species as a whole occur with gray whales and Irrawaddy dolphins. The Asian stock of gray whales is considered Critically Endangered (formerly Endangered), but the species as whole is put in a lower risk category (Baillie & Groombridge 1996; IUCN 2004). Some subpopulations of Irrawaddy dolphins are listed as Critically Endangered, but the species as a whole is in the Data Deficient category (Baillie & Groombridge 1996; IUCN 2004).
But for listing a subpopulation separately, in a different category from that of the species globally, certain considerations should be kept in mind. One must distinguish between regional listing and subpopulation listing. Anyone can make a list of threatened animals in a particular region. They can use the IUCN regional criteria (IUCN 2003a), or some other criteria (e.g., De Iongh et al. 2003). But, although IUCN encourages regional listing, it does not permit such listings to be part of its official Red Lists. To exert quality control on such a potentially huge number of listings appears to be beyond its resources.
In contrast, subpopulations may be part of the official IUCN Red Lists, provided that they meet the definition of a subpopulation:
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)
Green turtles in the Mediterranean.
For sea turtles only one such subpopulation listing has been made so far, that for Mediterranean green turtles, listed as Critically Endangered separately from other green turtles which were listed as Endangered (Baillie & Groombridge 1996; IUCN 2004). The present article argues that this subpopulation listing is currently inappropriate and not justified by IUCN’s own criteria.
The evidence from studies of DNA strongly suggests that there is genetic interchange between green turtles in the Mediterranean and those elsewhere in the Atlantic (Roberts et al. 2004). Male mediated gene flow is thought to contribute importantly to this interchange, on the basis of comparisons between mitochondrial (mt) and nuclear (n) DNA (Roberts et al. 2004).
What this amounts to is that one must distinguish between green turtles in the Mediterranean -- a regional matter -- and the Mediterranean green turtle. The latter does not exist. The current evidence indicates that there is exchange of genetic material between turtles in the Mediterranean and those in other regions. Therefore, green turtles in the Mediterranean should not be classified in the Red Lists as a separate subpopulation.
Three assumptions.
In arriving at this conclusion, three assumptions have been made. First, it is assumed that for determining whether individuals in a particular area constitute a genetically isolated subpopulation, the onus of proof is on those who propose this is so. The default option, in the absence of data, must be that animals in that region are part of a larger population. Otherwise small numbers of animals in marginal habitats at the edge of a species’ range could be designated as subpopulations and then, probably, given some threatened status.
Second, it is assumed that a combination of mt and nDNA provides a more complete and therefore better basis for understanding population structure than relying on mtDNA alone. The latter, being maternally inherited, limits its use to evaluating the population structure of females. Genetic interchange through the males may be missed. To learn about genetic isolation/exchange and about differences in life histories between males and females, data on both mt and nDNA are helpful, but for the purposes of red listing subpopulations as defined by IUCN, the information on nDNA is the more important. And after all, it is the nDNA that provides the principal coding for the proteins and the physiological and behavioural phenotype of the animal.
Third, it is assumed that in the definition of 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. Indeed one wonders whether those who drafted this section really meant gamete exchange per generation, rather than per year. Using generation times is one of the few concessions the Red Lists allow for species differences. For an animal that may take two or more decades to mature, the opportunity for genetic interchange in a year is severely limited compared to that for a species that has one or more generations per year. Fortunately, the word typically in the definition of subpopulation above allows room for flexibility and common sense. Most accounts of differentiation of populations use gamete/migrant exchange per generation.
Delisting is not the same as devaluing conservation.
Recognizing that the evidence currently available does not warrant designating green turtles in the Mediterranean as a separate subpopulation does not devalue conservation efforts undertaken on behalf of turtles in that region. Those who treasure green turtles in the Mediterranean may decide to do everything they can to prevent them disappearing from that region. I hope they will meet with success.
Controversy and agreement.
Red listing of widespread and slowly maturing species is not always straightforward. For further reading on listing of green turtles, see Seminoff (2004a; 2004b) and Mrosovsky (2003; 2004). Although differences in outlook and disagreements on technical matters may sometimes seem salient, not too far in the background there is agreement on some essential points: “the system often fails when it comes to globally distributed species such as sea turtles”, and “the risk of extinction as indicated by Red List global assessments (e.g. Endangered, Critically Endangered) does not always reflect the actual risk of extinction in the wild” (Seminoff 2004b). The same points, put less diplomatically, are to be found in Mrosovsky (2003).
Although much hard work and thought have gone into the documentation for the green turtle listing (Seminoff 2004a), and some useful compilations and information presented, it remains unsatisfactory when despite their Endangered status “which means ‘considered to be facing a [very] high risk of extinction in the wild (IUCN 2001)’…. few ... would agree that the species is going extinct anytime soon” (Seminoff 2004b).
So what are the options? Stick with a global listing of Endangered that is probably meaningless? Reform the criteria by which such a conclusion was reached? But IUCN (2003b) has indicated it does not want to change its red list process at present. Concentrate on either regional or subpopulation listing? That would avoid or at least diminish the problems of a single category for a widespread species.
It is in the context of the latter that clarification of the listing of green turtles in the Mediterranean is sought. Even if IUCN insists on some meaningless global listing for the green turtle with its diverse populations in their various predicaments, subpopulation or regional lists would at least allow people to focus in on specific areas and problems. I hope IUCN and the MTSG will examine the views put down here, and the underlying assumptions. If they are found wanting, then the RLA should come up rapidly with documentation justifying and supporting a subpopulation listing for greens in the Mediterranean as Critically Endangered; this listing was first made in 1996. If, however, my points are considered sound, then I hope that, in the absence of any new data or insights from studies of nDNA, subpopulation status will be withdrawn from green turtles in the Mediterranean, and that the MTSG will press ahead with regional or well-supported subpopulation listing of sea turtles.
BAILLIE, J., AND GROOMBRIDGE, B. (Compilers and Editors) 1996. 1996 IUCN Red List of Threatened Animals. IUCN, Gland, Switzerland and Cambridge, UK.
DE IONGH, H.H., O.S. BÁNKI, W. BERGMANS & M.J. VAN DER WERFF TEN BOSCH. 2003. The Harmonization of Red Lists for threatened species in Europe. In: Proceedings of an International Seminar 27 and 28 November 2002, The Netherlands Commission for International Nature Protection, Mededelingen No. 38, Leiden.
IUCN. 2001. IUCN red list categories and criteria: version 3.1. IUCN Species Survival Commission, Gland, Switzerland. 30 pp.
IUCN. 2003a. Guidelines for application of IUCN Red List criteria at regional levels: Version 3.0. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, UK. ii + 26 pp.
IUCN. 2003b. Guidelines for using the IUCN Red List categories and criteria.
IUCN. 2004. 2004 IUCN Red List of threatened species.
MROSOVSKY, N. 2003. Predicting extinction: fundamental flaws in IUCN’s Red List system, exemplified by the case of sea turtles. <http://members.seaturtle.org/mrosovsky/>
MROSOVSKY, N. 2004. Conceptual problems with the IUCN Red Listing assessment for the green turtle: Move over Raine Island. Marine Turtle Newsletter 106:1-3.
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 166:1857-1970.
SEMINOFF, J.A. 2004a. MTSG global assessment of green turtles for the IUCN Red List.
SEMINOFF, J.A. 2004b. Sea turtles, red listing and the need for regional assessments. Marine Turtle Newsletter 106:4-6.