Pacific Salmon, Oncorhynchus spp., and the Definition of "Species" Under the Endangered Species Act ROBIN S. WAPLES Introduction (NMFS) and the U.S. Fish and Wildlife provide guidance at three critical stages Service (FWS), three policy position in ESA evaluations: Determination of In conjunction with a review of the papers were drafted for the consideration what constitutes a "species" under the biological status ofPacific salmon, 1 On­ ofColumbia River salmon under the En­ Act (and what, therefore, may merit pro­ corhynchus spp., initiated in 1978 by the dangered Species Act (ESA or "the tection), determination ofthresholds for National Marine Fisheries Service Act' '). The draft papers were intended to listing as threatened or endangered, and I The term" Pacific salmon" has traditionally re­ the genus Sa/mo to Oncorhynchus calls this usage Robin S. Waples is with the Coastal Zone and ferred to species of the genus Oncorhynchus, five into question. In this document, "Pacific salmon" Estuarine Studies Division, Northwest Fisheries of which (0. gorbuscha, O. keta, O. kisutch, O. is used to include anadromous forms of O. clarki Science Center, National Marine Fisheries Service, nerka, and 0. tshawytscha) occurin North America. and O. mykiss, as well as the five above mentioned NOAA, 2725 Montlake Boulevard East, Seattle, The recent decision to move the western trouts from species. WA981l2. ABSTRACT-Forpurposes ofthe Endan­ differences betweenpopulations, andevalua­ 2) Does the population occupy unusual or gered Species Act (ESA), a "species" is de­ tions ofthe efficacyofnaturalbarriers. Each distinctive habitat? fined to include "any distinct population ofthese methodshas its limitations. Identifica­ 3) Does the population show evidence of segment ofany species ofvertebrate fish or tion ofphysical barriers to genetic exchange unusual or distinctive adaptation to its envi­ wildlife which interbreeds when mature. " can help define the geographic extent of ronment? Federal agencies charged with carrying out distinctpopulations, butreliance onphysical Several types ofinformation are useful in the provisions ofthe ESA have struggledfor features alone can be misleading in the ab­ addressing these questions. Again, the over a decade to develop a consistent ap­ sence ofsupporting biological information. strengths and limitations ofeach should be proach for interpreting the term "distinct Physical tags provide information about the kept in mindin makingthe evaluation. Pheno­ population segment. " This paper outlines movements of individual fish but not the typic/life-history traits such as size,fecundity, such an approach andexplains in some detail genetic consequences ofmigration. Further­ andageandtime ofspawning mayreflect local how it can be applied to ESA evaluations of more, measurements ofcurrent straying or adaptations ofevolutionary importance, but anadromous Pacific salmonids. recolonization rates provide no direct infor­ interpretation ofthese traits is complicatedby The following definition is proposed: A mationaboutthe magnitude orconsistencyof their sensitivity to environmental conditions. population (or group ofpopulations) will be such rates in thepast. In this respect, datafrom Data from protein electrophoresis or DNA considered "distinct" (and hence a "spe­ protein electrophoresis orDNA analyses can analyses provide valuable insight into thepro­ cies ")forpurposesofthe ESA ifit represents be very useful because they reflect levels of cess ofgenetic differentiation amongpopula­ anevolutionarilysignificantunit (ESU) ofthe geneflow that have occurredoverevolution­ tions but little direct information regarding the biologicalspecies. A population mustsatisfy ary time scales. The beststrategy is to use all extentofadaptivegeneticdifferences. Habitat two criteria to be considered an ESU: available lines of evidence for or against differences suggest the possibility for local 1) It must be substantially reproductively reproductive isolation, recognizing the limita­ adaptations butdo notprove that such adap­ isolated from other conspecific population tions ofeach andtaking advantage ofthe often tations exist. units, and complementary nature ofthe different types Theframework suggested here provides a 2) It mustrepresentan importantcomponent ofinformation. focalpointfor accomplishing the majorgoal in the evolutionary legacy ofthe species. Ifavailable evidence indicates significant ofthe Act-to conserve the genetic diversity Isolation does not have to be absolute, but reproductive isolation, the nextstep is todeter­ ofspeciesandthe ecosystems theyinhabit. At it must be strong enough to permit evolu­ mine whetherthe population in question is of the same time, itallows discretion in the listing tionarily important differences to accrue in substantial ecological/genetic importance to ofpopulations by requiring that they represent different population units. The second cri­ the species as a whole. In other words, ifthe units ofreal evolutionary significance to the terion would be met if the population con­ population became extinct, would this event species. Further, this framework provides a tributes substantiallyto the ecological/genetic represent a significant loss to the ecological/ means ofaddressing several issues ofpar­ diversity ofthe species as a whole. geneticdiversity ofthe species? In making this ticularconcemfor Pacific salmon, including Insights intothe extentofreproductive isola­ determination, the following questions are anadromouslnonanadromous population tion can beprovidedbymovements oftagged relevant: segments, differences in run-timing, groups fish, natural recolonization rates observedin 1) Is thepopulationgeneticallydistinctfrom ofpopulations, introducedpopulations, and otherpopulations, measurements ofgenetic other conspecific populations? the role ofhatcheryfish. 53(3),1991 11 consideration of the possible role of ar­ plants, and any distinct population seg­ lations under the ESA. The approach tificial propagation in recovery plans for ment of any species of vertebrate fish adopted here is an attempt to balance listed "species. " or wildlife which interbreeds when these themes in a framework consistent On receipt of petitions (April-June mature." Unfortunately, although the with both the letter and intent ofthe ESA. 1990) to list several populationsofPacif­ Act thus allows listing ofpopulations that Definition: A vertebrate population ic salmon as threatened or endangered are' 'distinct," it does not explain how will be considered distinct (and hence a "species" under the Act, NMFS sought population distinctness shall be evaluated "species") for purposes ofconservation public comments on draft Policy Position or measured. under the Act ifthe population represents Paper #1, "Definition of Species" (a Nevertheless, there is some guidance an evolutionarily significant unit3 (ESU) summary ofa longerdocument by Utter relevant to this issue. A review oflegis­ of the biological species. An ESU is a (1981». Based on that paper and public lative history indicates that an important population (orgroup ofpopulations) that: comments on it, discussions ofthe issue motivating factor behind the Act was the by the ESA Technical Committee, and desire to preserve genetic variability, 1) Is substantially reproductively iso­ ideas discussed at a Vertebrate Popula­ both within and between species. For lated from other conspecific population tion Workshopconvened inJune 1990by example, the House of Representatives units, and FWS and NMFS, Waples (1991a) pre­ described the rationale for House Resolu­ 2) Represents an important component pared a NOAA Technical Memorandum tion 37, a forerunner to the Act, in the in the evolutionary legacy ofthe species. that formed the basis for NMFS' "In­ following terms (H.R. Rep. 412, 93d terim Policy on Applying the Definition Cong., 1st Sess., 1973): Note that the dual criteria reflect two ofSpecies Underthe Endangered Species common meanings of "distinct": The Act to Pacific Salmon" (56 FR 10542; "Fromthe most narrow possible point of criterion of reproductive isolation em­ March 13, 1991). Afterconsideringpub­ view, it is in the best interests ofmankind phasizes the concept of "separate" or lic comments on the Interim Policy and to minimize the losses of genetic varia­ "apart from," whereas the criterion of the supporting NOAA Technical Memo­ tions. The reason is simple: They are evolutionary importance focuses on randum, NMFS published a Final Policy potential resources. They are keys to characteristics that are "different" or on this issue (56FR 58612; Nov. 20, puzzles which we cannot yet solve, and "unique. " 1991). Those comments were also con­ may provide answers to questions which Isolation does not have to be absolute, sidered in preparation of this paper. we have not yet learned to ask. " but it must be strong enough to allow evolutionarily important differences to Background of the On the other hand, in 1979 the General accrue in different population units. Endangered Species Act Accounting Office (GAO? recom­ Population characteristics that are impor­ The stated purposes ofthe Endangered mended that the authority to list verte­ tant in an evolutionary sense must have Species Act of 1973, as amended (16 brate populations under the ESA be a genetic basis; therefore, the second U.S.C. 1531 et seq) are to "provide a removed. Although this recommenda­ criterion would be satisfied ifthepopula­ means whereby the ecosystems upon tion was not adopted, the Senate Report tion in question