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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 47 HISTORICAL USE OF THE TERM SPECIES IN IMPLEMENTATION OF THE ENDANGERED SPECIES ACT Introduction Many societies have names for kinds of organisms, usually organisms that are large and conspicuous, or of life-sustaining, life-threatening, or economic importance. The term species can be applied to many of those kinds and be an accurate scientific term as well as an accurate vernacular term, because the characteristics used to differentiate species can be the same in both cases. Largely for this reason, defining what a species is has not been a major source of controversy in implementation of the Endangered Species Act. Greater difficulties have arisen in deciding about populations or groups of organisms that are genetically, morphologically, or behaviorally distinct, but not distinct enough to have been recognized at the rank of species according to traditional criteria—i.e., subspecies, varieties, and distinct population segments. Therefore, an important part of this chapter deals with taxa identified at ranks below the rank of species. Zoological Interpretations of Species Animals have always been a particular concern of the ESA—the imperilment of large, conspicuous animals in large part drove the popular demand for passage of the act. And because they are relatively well known from scientific as well as popular standpoints, birds and mammals have captured most of the concern, research, management, and funding associated with the ESA. However, these two groups of vertebrates constitute much less than 1% of animal species. The initial focus of ESA implementation on birds and mammals was logical and reasonable, given the general state of knowledge about biodiversity 20 years ago, but today implementation of the ESA continues to focus on a relatively small portion of the imperiled biota of the United States. Remedying this situation is an enormous challenge, given the poor state of our knowledge about many groups of invertebrates. However, of the 160 taxa of animals listed or proposed for listing from 1985 through 1991, 94 (59%) were vertebrates (Wilcove et al., 1993), and of those, only 38 (40%) were birds or mammals, showing that the bias perhaps is beginning to recede. Before 1973, federal laws intended to preserve species applied only to native animal species. Passage of the ESA in that year extended coverage to all plants and invertebrate animals, bringing U.S. policy into line with the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), which also was ratified in 1973. Although plants and invertebrate animals were originally given equal status with vertebrates, use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 48 subsequent emendation in 1978 restricted the use of distinct population segments to vertebrate animals only. Our survey of vertebrate listings indicates that, with few exceptions, species and subspecies have been almost exclusively listed; as discussed by Wilcove et al. (1993), only 2% of listings have been for populations. Our examination of listing documents reveals that morphological features, such as color pattern, shape, scale patterns, and numbers of body elements, are overwhelmingly used for differentiation of taxa to be considered for protection. In part, this reflects the level of knowledge we have about the biota—practically no other information is available for most animals. In some more conspicuous or commercially valuable species, other factors are useful, such as breeding times or genetic analyses of winter-run populations of the chinook salmon, Oncorhynchus tshawytscha (Fed. Reg. 52:6041-6048). Although protection of invertebrates is not extended to population levels in the ESA, subspecies are protected. Subspecies of invertebrates have merited some attention, especially in well-studied groups like mollusks (e.g., several subspecies of the pearly mussel Epioblasma (Fed. Reg. 41:2406424067)), beetles (e.g., the valley elderberry longhorn, Desmocerus californicus dimorphus (Fed. Reg. 43:35636-35643) and the northeastern beach tiger beetle (Fed. Reg. 55:32088-32094)), and butterflies (e.g., the Oregon silverspot, Speyeria zerene hippolyta (Fed. Reg. 45:44935-44938)). The rare use of subspecies in many invertebrate groups probably reflects our general ignorance of those organisms more than any other factor. Overwhelmed by the vast numbers of taxa they must deal with, specialists have not had the time or resources to pursue the finer levels of variation in most groups. In each of the cases just cited, only morphological features were considered in differentiating subspecific taxa. Botanical Interpretations of Species When Congress passed the Endangered Species Act in 1973, it explicitly included plants, as well as fish and wildlife. After the ESA was passed, Congress requested that the Smithsonian Institution prepare a list of threatened, endangered, and extinct plants of the United States. In collaboration with botanists across the country, the Smithsonian Institution completed its list and presented it to the Congress in December 1974 (U.S. Congress, 1975). The list contained 2,832 endangered and threatened taxa and 355 presumed extinct taxa. The list contained only ferns, gymnosperms, and angiosperms. Of the endangered and threatened taxa, 1,999 were from the mainland of the United States and 833 were from Hawaii. The report recommended that the secretary of the interior review the Smithsonian's use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 49 roster and publish lists of proposed endangered and threatened plants in the Federal Register. After the initial involvement of the Smithsonian Institution, the Department of the Interior and the Department of Commerce took over responsibility for plants and animals. Responsibility for land and freshwater plants was accepted by the Fish and Wildlife Service (FWS) within the Department of the Interior, and the National Marine Fisheries Service (NMFS) in the Department of Commerce took responsibility for any marine plants proposed to be listed as threatened or endangered. To date, no marine plants have been proposed for listing. The director of FWS announced in 1975 that he intended to review the Smithsonian's list and determine eligibility of taxa for listing (Fed. Reg. 40:27823-27924). In 1976, FWS proposed that 1,726 of the taxa on the Smithsonian's register be listed (Fed. Reg. 41:2452324572), but no action was taken on the recommendation. In 1978, Section 4(f)(5) of the Endangered Species Act was amended to state that species on which action had not been taken during 2 years after the initial proposal must be withdrawn from consideration. A grace period of 1 year was provided. By late 1979, action had still not been taken on the 1,726 plant taxa, and the list was withdrawn in December 1979 (Fed. Reg. 44:238). Nevertheless, by that time 47 plant taxa had been listed, establishing a precedent for placing plants on the endangered species list. As of January 31, 1995, 516 plant taxa (484 flowering plants, 4 conifers and cycads, 26 ferns and fern allies, and 2 lichens) had been listed, all but three occurring in the United States (George Drewry, FWS, pers. commun., Feb. 28, 1995), and many are under consideration. The original Smithsonian report provided several additional recommendations and discussions. Under Recommendation 8, it was noted that the act provided differently for wildlife and fish compared with plants, in that the term species as applied to plants included subspecies but not varieties. The report also noted that the secretary of the interior did not have the authority to acquire land for conserving rare and endangered plant species unless they were listed in the appendices to CITES. Finally, in contrast to its provisions concerning animals, the act did not prevent the "taking" of endangered and threatened plant species in the United States. Notwithstanding the Smithsonian report's comments about the use of the term species with regard to plants, the general practice in implementing the ESA has been to use the word subspecies in an unconventional sense to apply to either a subspecies or a variety. Despite their referring to different taxonomic categories (varieties are one rank below subspecies), the two words have effectively been used interchangeably for purposes of the act. Of the 404 plant taxa listed by 1993 [50 CFR 17.11 & 17.12, 1993], 342 are full species, 24 are subspecies, and 38 are varieties. Which infraspecific rank has been used tends to reflect the school of the taxonomists working use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 50 on the listed group of plants (see Stuessy, 1990, for a historical review of the use of terms). It should be noted, however, that in the act, the word species is used for any category eligible for listing. An analysis of the use of the term plants in the ESA and of the way in which categories have been chosen for protection under the act brings up several points. First, the term plants was specifically stated to include any member of the plant kingdom (ESA §3(13)) and was obviously meant to refer to any macroorganism that was not an animal—vascular plants, bryophytes, lichens, fungi, and so on. It seems most likely, however, that Congress did not intend to include most prokaryotes and many single-celled eukaryotes that might come under the rubric of plants (e.g., bacteria and yeasts), although botany departments classically taught mycology, microbiology, and phycology as well as seed-plant biology. Only two plants other than ferns, gymnosperms, and angiosperms have been listed (two lichens). However, there is growing recognition that the living world is not divisible into plant and animal kingdoms, and various schemes with several kingdoms have been proposed (e.g., Margulis and Schwartz, 1987). As currently written, the act could be construed as excluding a large portion of the living world, but lacking scientific knowledge about how species concepts apply in practice to many of these organisms, there is no basis for recommending the extension of the ESA's coverage to prokaryotes and many single-celled eukaryotes at this time. Plants present problems in use of the concepts of species, subspecies, and varieties. When the Endangered Species Act was passed, the biological species concept of Mayr (Mayr, 1942; 1963), Stebbins (1950), and Grant (1963) was accepted by many systematists in theory, even though it often was difficult to apply. It was particularly difficult to apply to plants, which often exhibit polyploidy, hybridize with some frequency in nature, and frequently reproduce asexually or apomictically (without exchange of gametes among different individuals). Discussions in several final listing documents for endangered species illustrate the ways species have been delimited by plant systematics. In the discussion proposing listing the fern Thelypteris pilosa var. alabamensis (Fed. Reg. 57:30165), eligibility depended in part on whether it was distinct from T. pilosa in Mexico. Distinctiveness was determined by asking experts to provide evidence of uniqueness. The consensus of experts was that several characteristics of the leaves were distinct, and therefore, the Alabama plants were recognized as an independent taxonomic variety. A similar case involved Sarracenia rubra subsp. alabamensis, a pitcher plant (Fed. Reg. 54:10150). This taxon is part of a complex of populations that reproduce both sexually and vegetatively, hybridize, and exhibit a range of variation that is determined by local environment. Taxonomic recogni use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 51 tion of the alabamensis subspecies was based on the unique possession of several leaf (pitcher) features in the Alabama individuals. Different criteria were used to designate the Malheur wire lettuce, Stephanomeria malheurensis, as a species and its eligibility for listing. This taxon derives from S. exigua, but unlike its parent, it reproduces primarily by inbreeding and differs genetically from its parent by one fixed allele. Furthermore, chromosomal structural differences between S. exigua and S. malheurensis prevent successful meiotic pairing in the offspring. In the first two instances mentioned above, primarily morphological criteria were used to delimit a taxon. In the last case, genetic data and evidence of reproductive isolation were cited as evidence for specific rank. The use of different kinds of evidence in different cases reflects the widely varying degrees of knowledge available for different kinds of plants. Such variation should be expected for the foreseeable future, for plants as well as for vertebrate and invertebrate animals. HISTORY OF SPECIES CONCEPTS BEFORE AND AFTER THE ENDANGERED SPECIES ACT Species Concepts Although Darwin's Origin of Species was ostensibly about speciation, the book really is about natural selection, or the changes that take place within species, not about how species arise from other species. Many biologists have extrapolated from Darwin's assumptions about selection to a theory of speciation. But biologists with different perspectives and problems in mind have different ideas about what a species is and what role it should play in particular areas of science. Some systematic biologists have declared that there is no single unit that can be called species, and, for example, that the concept of species used in classifying mosses might be quite different from that used for classifying species of birds with respect to population and genetic structure (Mishler and Donoghue, 1982; Mishler and Brandon, 1987; O'Hara, 1993). Such authors question why we should expect that some "unit of nature" equally meets the expectations and needs of ecologists, behaviorists, biochemists, and other kinds of biologists, and they suggest that noncongruence among species delineated using different methods often exists. This is equivalent to saying that various characteristics of organisms and interbreeding populations might change at different rates, so that differences in morphology, biochemistry, chromosome structure, breeding characteristics, and population structure, for instance, need not all arise together during differentiation. Why should the term species be so problematic? Why, after centuries of investigations, are systematic biologists unable simply and easily to tell use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 52 us which groups of organisms are species and which are not? The reason is that in the vast majority of cases, speciation is very gradual from a human perspective, taking from hundreds to thousands of years or more. We believe that speciation is occurring in many kinds of organisms, but in the extremely short time frames available to us, we cannot see the entire process unfold; we can see only what appear to be various lineages at different stages in the process. The most basic elements of speciation are isolation and differentiation. For a simple case, imagine populations of a widespread species becoming isolated due to a rising sea level that turns a small mountain range into an island chain. Under current views of evolution, populations on each island mountain-top would be expected to become different over time, and eventually to lose their ability to interbreed with each other. Whether species is defined based on differentiation or loss of interbreeding, the isolates would eventually become different species. The scenario could be expanded to include several ancestral species, each widely distributed over the mountain range, and thus with isolates on each island. On any particular island, the degree of differentiation of the several kinds of organisms could vary, so not all the descendent populations would become species at the same time. Any given island might have entities that systematists would recognize as full species, subspecies, distinct population segments, or even the ancestral species, unaltered. To complicate matters further, a drop in sea level might allow all these isolates to meet-those that had differentiated sufficiently would not interbreed and would thus remain isolated as species, but others might interbreed, spreading their special characteristics into the other populations so that the unique identities of each isolate would be lost. Calling a group of organisms or populations a species or some other rank is a hypothesis about the past- about differentiation, population biology, and history. Speciation is a dynamic process with many factors involved, and science cannot delineate what nature itself does not. That complexity is a factor when competent scientists disagree about the status of a particular group of organisms. We cannot know what is going to happen in the future, but theories do give us models in which we can examine many assumptions about speciation, and these are the best available tools for evaluating various parts of the genealogical nexus with respect to their conservation value. Another vexing issue is whether species should or must be defined in terms of the evolutionary processes thought to result in speciation; or whether they should be defined based on their features alone. Species concepts incorporating details of the evolutionary process are the "biological," "recognition," and some versions of the "evolutionary." The species concepts that rely primarily on traits are the ''cladistic" and "phylogenetic" (see Box 3-1). In part the debate is about the extent to which species should be use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 53 construed as units of evolution or whether evolution should be envisioned as acting at other levels (Kluge, 1990). There is a vast literature on all these topics, including papers by Cracraft (1987), Davis and Nixon (1992), and Ereshefsky (1989) and by Otte and Endler (1989), Paterson (1993), and de Queiroz and Donoghue (1988). BOX 3-1 SPECIES CONCEPTS IN THE SCIENTIFIC LITERATURE Biological (BSC): Groups of interbreeding natural populations that are reproductively isolated from other such groups (Mayr, 1969; Mayr and Ashlock, 1991). Cladistic: The set of organisms between two speciation events (Ridley, 1989). Cohesion: The most inclusive group of organisms having the potential for genetic and/or demographic exchangeability. This is much like the BSC, but includes nonsexually reproducing individuals by emphasizing processes that keep populations from changing (e.g., ontogenetic constraint) (Templeton, 1989). Evolutionary (ESC): A single lineage of ancestor-descendant populations that maintains its identity from other such lineages and has its own evolutionary tendencies and historical fate (Wiley, 1981). Phylogenetic: The smallest aggregation of populations (sexual) or lineages (asexual) diagnosable by a unique combination of character states in comparable individuals (Nixon and Wheeler, 1990). Recognition: The most inclusive population of individual biparental organisms that share a common fertilization system (Paterson, 1985). Developments in population genetics since the 1920s have led systematists to focus on populations of organisms. Most species concepts began to incorporate the view that the genetic interactions within species are the major factor in maintaining species identity, and loss of those interactions is the major factor in speciation. The biological species concept was adopted generally among zoologists studying vertebrates, and to a lesser extent, among botanists and zoologists studying invertebrates. Many of the debates about the biological species concept have concerned its application to organisms without sexual reproduction. Indeed, the reproductive differences between plants and animals have fueled the different uses of species concepts among disciplines. Incorporation of genetics into plant systematics in the 1940s and 1950s led to the use of degrees of crossability as indicators of relationships (Camp and Gilly, 1943; Grant, 1957). This approach paralleled the rise and domination of the biological species concept in zoology, and in time contributed to a merging of the two. The adoption of the biological species concept ushered in an era of "biosystematics" in botany that relied heavily on the degree of interfertility as a guide to degrees of relatedness (Gilmour and Heslop- Harrison, use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 54 1954; Grant, 1959; Solbrig, 1970; Stebbins, 1970; Raven, 1974). Inability to interbreed was considered evidence of distinctiveness at the species level. However, despite this research in biosystematics, most plant systematists proceeded without a methodological or philosophical conviction that the biological species concept was applicable to most plant species. It was obvious that some entities ranked as genera on morphological and ecological grounds could cross in nature, whereas taxa judged to be nearly identical on morphological grounds might be completely reproductively isolated from one another. In addition, plants are often completely functionally or truly asexual in their reproduction and therefore are excluded even by Mayr (1942) from a definition that relies on interbreeding. The ability of an organism to interbreed is not always a safe criterion for species distinctiveness. Some organisms that are distantly related might interbreed because their reproductive systems have not differentiated. In 1974, Ghiselin's "radical solution to the species problem" restructured the debate to a consideration of the ontological status of those units of nature being called species. Ghiselin's timing was coincident with the establishment of phylogenetics in systematics after 1966, and the general rethinking of many basic assumptions that took place in those years included reexamination of species concepts as well. In phylogenetic systematics, many biologists found an approach that advocated the recognition of species as distinct lineages of differentiated organisms. Species are defined as units that are diagnosable (are distinctive) and that have a unique evolutionary role or trajectory (Wiley, 1981; Donoghue 1985; Mishler, 1985). In addition, spatiotemporal restriction for species is expected, i.e., individuals of a species will share the same broad geographic range and temporal range. This prevents similar-looking individuals that have evolved from different ancestors in different parts of the world (or in different geological times), from being considered conspecific. In adopting the phylogenetic species concept, many scientists have moved to a species concept very much like the inclusive one used in the ESA. Indeed, despite differences in theory and philosophy underlying various species concepts, systematists using different concepts usually come to substantial agreement with respect to the recognition of species, especially in vertebrates and in many higher plants. Taxonomic Units Below the Rank of Species Within the phylogenetics community, the usefulness or validity of recognition of units below the species level under a phylogenetic species concept (de Queiroz and Donoghue, 1988; Avise and Ball, 1990; Nixon and Wheeler, 1990; Davis and Nixon, 1992; Waples, in press) has been the subject of debate. One argument is that any distinctive population or group use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 55 of populations should be considered a species. Because subspecies and varieties are recognized by one or a suite of characters, they are certainly distinctive. However, the evolutionary independence of such units (whether there is a significant amount of interbreeding among them) can be disputed, as can whether their recognition as separate species obscures the degree of relationship among them. Despite of the lack of consensus about species concepts, the scientific and popular cultures attach special significance to the rank of species, leading to debates over the importance of groups of organisms ranked below the species level, such as subspecies, varieties, races, or population segments. Former Secretary of the Interior M. Lujan once asked whether we have to save every subspecies (Lancaster, 1990). The implicit assumption was that species have greater value than lower ranks. In practice, recent application of the law has been primarily to entities considered species by systematists. A review of listings for 1985-1991 found that only 18% of listed vertebrate taxa were subspecies, and only 2% were distinct population segments (Wilcove et al., 1993). Missing from most discussions about rank of taxa to be preserved is the crucially important recognition that different concepts of species, subspecies, and other ranks are often applied between and even within disciplines. Many of the subspecific and population-level taxa in the 18% just mentioned were birds. In part, this is due to the ornithological tradition of recognizing certain kinds of variation at "subspecific" rather than "specific" level. A fish biologist looking at a similar kind of variation might well have used the species rank in describing what an ornithologist would consider a subspecies. Even within a discipline, recognition of degrees of variation can vary over time, among systematists subscribing to different schools, and between practitioners from different countries. In addition, in phylogenetics or cladistics, rank is de-emphasized. Some phylogenetic classifications eschew rank altogether, except for ranks required by codes of nomenclature (e.g., every species must be placed in a genus). Thus, since ranking of a taxon may vary for any number of reasons, we find the ESA's inclusion of all three categories for preservation—species, subspecies, and distinct population segments (at least of vertebrates)—correct and appropriate. Moreover, there is no scientific reason that the ESA's inclusion of all three ranks should not apply to all groups of organisms. But Secretary Lujan's question about preservation of all subspecies has relevance for policy makers. Unless we agree to preserve all endangered or threatened organisms of all taxonomic ranks, we must find ways to identify those groups of organisms we consider to be significant. use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 56 A CONCEPT OF SPECIES FOR THE PURPOSES OF THE ENDANGERED SPECIES ACT Introduction After centuries of debate, no one doubts that natural groups of organisms exist. Scientists now are concerned with methods of classification and circumscription of taxonomic boundaries. For the purposes of the ESA, whether an entity is a species in the vernacular sense is less important than whether the entity is a group of individuals that can be held to be distinct from other such groups, with all that such distinctiveness implies regarding population structure and evolutionary potential. Fortunately, the groups of organisms called species and subspecies by taxonomists usually are also distinct in their population structure and evolutionary potential. The most difficult questions generally arise at taxonomic levels below the subspecies level. Because evolutionary units at such levels are not discrete but exist along a continuum, it is a policy judgment as well as a science judgment to determine the significance of an evolutionary unit. In other words, science alone does not lead to a conclusion that any objectively definable degree of distinctiveness is more significant than another. But science can provide the tools for identifying and measuring biological components of distinctiveness; it also can provide objective criteria for ranking the distinctiveness of evolutionary units. Evolutionary Units and Their Identification The following provides some guidelines for measuring the distinctiveness of natural entities to serve the purposes of the ESA. The committee focused on the biological meaning and evolutionary importance of distinctiveness. To be clear on this matter, the committee considered what distinctiveness means separately from considering how to assess whether a particular population is in need of protection. The committee believes that separating the two issues—as the ESA does—would help policy makers and managers as well. What follows will bring increased scientific objectivity to the current and appropriate case-by-case examination of whether a given population or taxon below the rank of subspecies is eligible for protection by the ESA. It should also help to meet Congress's challenging expectation that distinct population segments be listed "sparingly and only when biological evidence indicates that such action is warranted" (S. Rep. 151, 96th Congress. 1st Session, 1979). use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 60 BOX 3-2 Enormous advances in genetic technologies have been made since the ESA was first passed in 1973. The most widely applied technology is the isozyme method. This method permits the detection of genetic differences in enzymatic proteins based on the physical separation of protein molecules in a supporting medium (usually some form of gel, such as starch or polyacrylamide). Because all protein molecules are electrically charged (under defined pH conditions), they can be physically separated by applying an electric field to a gel for a specified period. The distance migrated is a function of the resistance of the protein in the gel (largely a function of protein size) and the net charge of the protein (the larger the net charge differential, the greater the rate of migration). Roughly one-third of all mutational differences among individuals will cause a change in a particular amino acid in protein coding genes. A subset of amino acid substitutions have the property of altering the net charge of a protein. Consequently, a small fraction of all mutations in protein coding genes can be detected as changes in the mobility of the protein in an electric field. The final step in the isozyme method is the application of a histochemical stain to the gel to make the sites of enzymatic activity visible. Histochemical stains contain the substrate for a specific enzyme (e.g. alcohol for alcohol dehydrogenase) and a coupling agent that reacts with the product of the enzymatic reaction to cause the precipitation of a dye at the site of enzyme activity. Genetic differences among individuals are read as differences in banding locations on the gel. At present, nearly 100 different enzymatic proteins can be resolved in humans. About 25 to 30 are routinely resolved in most plant and animal species. As a consequence, average levels of genetic divergence can be estimated from reasonably large samples of genes that determine protein products. In addition, the isozyme method is relatively easy to implement, and it is not difficult for an experienced laboratory to screen several hundred individuals per day. Because of ease of application and because the isozyme method was invented more than 30 years ago, it has been widely applied in population genetics and in systematics. A large data base has been accumulated that spans hundreds of plant and animal species. The statistics calculated from isozyme data are numerous, but most involve estimating the gene frequencies for a particular genetic locus and then calculating a measure of genetic diversity averaged over loci (Weir, 1990). Gene frequencies are estimated by counting the number of copies of a particular allele in the sample and then, for diploid organisms, dividing by twice the number of individuals in the sample (recall that every diploid individual received one copy of a particular gene from each parent, and hence there are twice as many genes as individuals in the sample). The most commonly employed diversity measures are based on calculating the average probability of drawing two different copies of a gene at a locus. This measure is then averaged over loci. A large body of population genetic theory relates diversity measures to processes of drift, mutation, and migration (see, e.g., Nei, 1987; Weir, 1990). "Molecular methods" usually refer to the set of methods that involve direct assay of either DNA or RNA. A large number of techniques fall under this use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 61 rubric. Moreover, there continues to be a rapid rate of innovation in molecular technology. Accordingly, we restrict our comments to technologies involving comparisons of DNA sequences or patterns of restriction fragments. Both these technologies now rely heavily on the use of PCR (polymerase chain reaction) methods that permit the rapid and accurate generation of large amounts of DNA for the gene or molecular region of interest. The PCR method was invented in the mid-1980s, and it is now beginning to be widely applied in population genetics and systematics. The PCR method depends on some prior knowledge of the DNA sequence of the gene of interest for the design of primers for the DNA polymerase enzyme (except for the RAPD application, which is discussed below). The primers together with a heat stable DNA polymerase and a thermal cycling apparatus allow the geometric amplification of the DNA region of interest (a region of up to roughly 4,000 to 5,000 base pairs in size might be amplified). Once a DNA fragment has been amplified by PCR, the fragment size can be compared among samples using gel electrophoresis, or the fragment can be further analyzed by more sophisticated methods. Changes in fragment size imply mutational changes resulting from the insertion or deletion of DNA segments. Among more sophisticated methods are (1) the direct sequencing of PCR products to identify particular mutations at the ultimate level of detail, the amino acid bases, or (2) further dividing the PCR- amplified fragment using a class of enzymes known as restriction endonucleases (restriction enzymes) to detect mutational changes in "restriction sites." DNA sequencing has been employed in several specific cases at the population level, but current technology still limits this application to relatively small samples. Restriction-site analysis is based on the fact that restriction enzymes cut double-stranded DNA molecules at precisely defined DNA sequences (e.g., GAATTC is the restriction site for the enzyme EcoR1), and a change in fragment pattern must therefore be due to a mutational change in a recognition site. A recent innovation in the PCR method, know as the RAPD method, is based on short random primers (usually 10 nucleotides in length). PCR based on short random primers causes random regions in the genome bounded by sequences complementary to the primer to be amplified. This method is easy to implement and it is beginning to be widely applied in population biology; however, more limited genetic information is contained in RAPD analyses because banding patterns are usually not codominant (codominant means that in the case of heterozygosity, both gene products will appear on the gel as two distinguishable bands; in the case of dominance, only one band will appear, and thus less information can be obtained). Current applications of PCR-based methods in endangered species management and research involve (1) the use of PCR in determining genealogical relationships to better manage breeding programs; (2) the use of PCR in law enforcement, where the taking of particular specimens can be established through forensic use of DNA; and (3) limited population surveys to establish genetic relationships among the elements of a metapopulation. Like the isozyme method, these other molecular methods help establish whether a population or system of populations is distinctive in the sense of constituting an EU. use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 62 differences in behavior or reproductive mechanisms. Populations of many fish species have very specific times and places where they spawn, so their spawning behavior prevents the populations from interbreeding. Differences in courtship behaviors—including songs and other vocalizations often lead to reproductive isolation (e.g., Lack, 1971). The degree to which population segments in the wild are independent units or part of a larger genetic entity is often unclear because of difficulties in ascertaining historical and current levels of gene flow. A key question is the extent to which the population segments have adapted to local environments in ways that would substantially reduce the probability of successful establishment in other portions of the species range. Tests for distinctiveness are most difficult to apply in cases where systems of populations are in the process of diverging to independent status. Because the process of evolutionary change is dynamic, it is inevitable that ambiguous cases will arise, especially as we further understand the complex population structures of some widespread species. As for any difficult and technical activity, the judgment of professional experts is essential. Despite such difficulties, the number of ambiguous cases is a small fraction of the total number of cases so far dealt with in the practical implementation of the ESA, and probably will remain so. Examples of Circumscription of Evolutionary Units Of the terrestrial vertebrate taxa that already have been listed under the ESA, the majority qualify as EUs. Few would doubt the taxonomic distinctiveness of such well-known animals as the American alligator, bog turtle, California condor, whooping crane, or black-footed ferret. Traditionally, rather subtle differences between closely related terrestrial vertebrate taxa, such as the various forms of grizzly (brown) bear and gray wolf, have been recognized at the subspecies or distinct population segment level. When such distinctions can be demonstrated as valid using any of the recognition criteria we have outlined, the taxon would qualify as an EU. An example of an EU is the Allegheny woodrat, Neotoma magister, which occurs (or did until very recently) from southeastern New York and westernmost Connecticut through the foothills and higher elevations of the Appalachians to Kentucky, Tennessee, northernmost Alabama, and eastern North Carolina. In spite of morphological information on its distinctiveness (Goldman, 1910), the Allegheny woodrat had been considered conspecific with the more widespread Eastern woodrat (N. floridana) since the 1940s. However, recent studies have provided substantial additional evidence that N. magister is distinct from N. floridana in its morphology (Hayes and Richmond, 1993) and have demonstrated distinctiveness of mitochondrial DNA (Hayes and Harrison, 1992), as well as behavior and ecology (Wiley, use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 63 1980; Hayes and Harrison, 1992). These new data are pertinent to the ESA because, during the past several decades, the populations of N. magister have declined precipitously along the entire northern margin of its range. The species no longer occurs in Connecticut, New York, and New Jersey, and is rare in Pennsylvania, Ohio, Indiana, and Illinois. Bones from archeological and paleontological sites in New York and Indiana show that N. magister occurred in pre-European times even farther north than indicated by its range in the 19th and 20th centuries (Richards, 1971; Steadman, 1993a, b). The cause of the decline of N. magister is uncertain, although an ascarid roundworm transmitted via raccoon feces is likely to be involved (A. Hicks, New York Department of Environmental Conservation, pers. commun., Sept. 1993); because of events related to human activities (e.g., expansion of suburbs, loss of large predators, decline of hunting and trapping of raccoons), raccoon populations have expanded greatly in the past several decades. At the present rate of decline, N. magister may be eliminated from its entire range within the next 100 years. Other examples of EUs are the distinct populations of otherwise western or tropical species found in peninsular Florida. The Florida populations (such as the burrowing owl, Athena cunicularia floridana) generally are distinct morphologically and traditionally have been recognized as subspecies endemic to Florida. The endemic Florida population of the scrub jay (Aphelocoma coerulescens coerulescens), which is declining because of habitat loss, differs from other populations genetically (Peterson, 1992) and in its behavior and ecology (Woolfenden and Fitzpatrick, 1984) and has recently been recognized by the American Ornithologists' Union's Committee on Classification and Nomenclature as a full species, Aphelocoma coerulescens (Richard Banks, president, AOU, pers. commun., 1995). Waples (in press) described in detail the identification of EUs (ESUs in NMFS terminology) of anadromous Pacific salmon, including some difficulties encountered. Some kinds of genetic mutations occur commonly and sporadically in populations of organisms but do not usually result in speciation. Melanism is one of these. In many areas of the country, populations of squirrels (including the grey squirrel, Sciurus carolinensis and the fox squirrel, Sciurus niger) are either partially or primarily composed of black individuals. These populations do not qualify as EUs, because they are not isolated from adjacent populations that lack the gene for melanism or have it only at low frequencies. Similarly, melanism is a common mutation in the mosquitofish (Gambusia affinis or G. holbrooki). In this case, patterns of distribution indicate that dark individuals are the result of mutations occurring spontaneously throughout the range of the species. Even in cases where the melanism is known to be adaptive, as in the pepper moth (Biston betularia) described by Kettlewell (1961), the dark forms continue to interbreed with the light forms, so the dark forms do not constitute an EU. Similarly, a use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 64 growing body of evidence suggests that different genetic variants at the major histocompatibility complex (MHC) loci in humans confer differential adaptation to disease, but we would not argue that the set of individuals who possess a particular MHC variant constitutes an independent evolutionary lineage, because such individuals continue to interbreed with other humans. Other examples of organisms that would not be considered EUs are the American alligator (Alligator mississippiensis) populations that are regulated in the southern United States. Alligator populations may be regulated locally, with hunting allowed or protection bestowed based on political boundaries. The American alligator is an EU, but the regulated and unregulated populations are not EUs. The American brown bear (Ursus horribilis) is an EU (or perhaps several), but in many cases its protection status involves political boundaries and is based more on management and aesthetic criteria than on whether the populations are EUs or something like them. More problematic is the status of populations of the American bald eagle of the contiguous United States. Those populations declined seriously before passage of the ESA, although Alaskan and Canadian populations remained large. In this case, especially because there is no discontinuity between the Canadian and U.S. distributions of the eagle, the EU is based on political boundaries. We cannot argue that a biological difference arises when a Canadian eagle flies across the border into the United States. The Florida panther (Felis concolor coryi) is another problematic case. Little genetic variation is evident in the Big Cypress panthers. Panthers in the Everglades, which were introduced from stock descended from Latin American populations, have hybridized with those in the Big Cypress area (Roelke et al., 1993; Barone et al., 1994). The Big Cypress population is so small and so lacking in genetic variation that it is unlikely to survive without further introduction of panther genes from elsewhere (Roelke et al., 1993; Barone et al., 1994). Florida panthers are no longer genetically distinct from other populations of panthers in the southeastern U.S., so the question becomes, as an FWS official put it to the committee, ''whether we are protecting the Florida panther or protecting the panther in Florida." In the case of the American bald eagle, and in other similar cases, there might well be persuasive reasons to conserve taxa distinguished by political jurisdiction (including ethical and aesthetic reasons). Large carnivores often play a major role in ecosystems, so there can be additional ecological arguments for protecting them. Others have argued that refusal to list only geographic segments of a species could deny protection to genuinely endangered populations and local ecosystems and might allow a widely distributed EU to decline until the entire species becomes endangered. This kind of argument has been applied in criticism of the application of the ESU concept (see Waples (in press) for a discussion of these and other criti use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 65 cisms), and it is a difficult aspect of the problem. A biologically sound method of identifying distinct population segments does not recognize political boundaries, although it does recognize the validity of asking whether a particular population within a political boundary is distinct and imperiled.3 This kind of criticism of an EU concept confounds identification of distinctiveness with a decision as to whether a particular population is in need of protection. Both are needed, but considering them separately helps the analyses. It is surely true that many listed species are endangered because widely distributed EUs were permitted to decline until they became imperiled, but this is not a flaw of the EU concept. Such a management strategy is bad for conservation, but the ESA and its regulations are intended to protect threatened and endangered species, not to prevent them from becoming threatened and endangered. Preventing species from becoming threatened and endangered is essential for preserving biological diversity, and additional conservation and management plans beyond the provisions of the ESA are needed to achieve that goal. Some of those are discussed in Chapter 10. The Fate of Hybrids under the Evolutionary Unit Concept Many organisms, especially plants, are descended from hybrids. In cases where the populations have become independent evolutionary units whose persistence no longer depends on hybridization among other such units, an EU can be recognized (Funk, 1985) if the population meets the criteria discussed above. In most zoological cases, hybrids will not be considered as EUs because they are temporary products of a breakdown in species boundaries and require continued contact and interbreeding among these species for their existence (Parsons et al., 1993). For example, the North American flickers (Colaptes auratus broadly defined) are widespread in North America and consist of three major types, each of which has been recognized by various authorities as distinct at either the species or subspecies level: the eastern yellow-shafted flicker (C. auratus auratus); the western and montane red-shafted flicker (C. auratus cafer broadly defined); and the southwestern gilded flicker (C. auratus chrysoides). Hybrids of C. a. auratus use the print version of this publication as the authoritative version for attribution. 3A draft joint FWS and NMFS policy on recognition of distinct vertebrate population segments under the ESA (Fed. Reg. 59:65884, 12/21/1994) incorporates this criterion. The policy has three elements: discreteness, significance, and status. One of the criteria for discreteness is the delimitation of a population "by international boundaries within which differences in control of exploitation, management of habitat, conservation status, or regulatory mechanisms exist that are significant. . ." In other words, the criterion leads to a question such as whether a population of organisms in the United States is distinct and endangered.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 66 and C. a. cafer can be found along a north-south zone east of the Rocky Mountains, while hybrids of C. a. cafer and C. a. chrysoides are found locally in the southwestern United States and northwestern Mexico. Virtually everywhere they occur, all pure forms of C. auratus are common birds. Furthermore, the hybrids are common within much of their limited range and almost always occur alongside pure forms. Even the least common and most localized hybrid flicker (C. a. cafer x C. a. chrysoides) would not be considered an EU, because it is genetically dependent on the parent species. The hybridization between the blue-winged warbler, Vermivora pinus (BW), and golden-winged warbler, V. chrysoptera (GW), is a more complex situation from the standpoint of recognition as an EU. The two species hybridize readily, producing viable offspring (Gill, 1980) that are sometimes called Brewster's or Lawrence's warblers. The GW is declining over much of its range (Confer and Knapp, 1992). Smith and coworkers (1993) assessed the status of 82 species of migratory birds in the Northeast and rated the GW on a par with the cerulean warbler (Dendroica cerulea) as the most jeopardized species. The decline is due mostly to a loss of habitat (the GW prefers thickets with small, scattered trees, a habitat that often is ephemeral due to succession), with other factors being brood parasitism by cowbirds, and hybridization with the BW. Where the GW and BW come together (in many localities in the Northeast and upper Midwest), the long-term (decadal) results of hybridization often favor the BW, with the GW becoming scarce or absent (Gill, 1980, 1985; Confer and Knapp, 1981). The BW prefers forest edges (especially with aspens), a type of habitat that is common today because of the patchiness of the second-growth forests. The GW on its own qualifies as an EU, but today's reality is that some percentage of phenotypic GWs share genetic material with the BW. Given that it is not feasible to assess the genetic make-up of all birds across a broad range, the phenotypic GWs should be recognized as an evolutionary unit in spite of the fact that some percentage of these birds contain BW genetic material. Hybrids that are phenotypically intermediate could not be diagnosed as part of the GW evolutionary unit. The EU can easily be applied to hybrids. The principle would be to protect individuals that might have some introgressed genetic material (especially, for example, mitochondrial DNA) but that remain phenotypically much like the endangered parental species. Modern genetic techniques routinely find examples of interbreeding that has left the parent species' lineages essentially unchanged phenotypically. Many developments in theoretical population genetics and in molecular technology since 1973 will frequently aid in resolving hybridization questions. They should play a central role in deliberations concerning decisions to list. This country has substantial expertise (in academia, museums, federal and state institutions, environmental organizations, and industry) on the use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 67 systematics, population genetics, and ecology of representatives of most groups of plants and many animals, as well as a strong academic base in the broader fields of molecular evolution and genetic data analysis. A mechanism needs to be implemented allowing the federal government to take advantage of this expertise rapidly in a nonpolitical way and with the allocation of resources toward research and implementation. Decisions relevant to the ESA can be made more objectively than they have been, and this objectivity should ultimately reduce costs of implementing and enforcing the act by facilitating the decision-making process and reducing court costs. CONCLUSIONS AND RECOMMENDATIONS • The ESA's inclusion of species and subspecies is soundly justified by current scientific knowledge and should be retained. Often, competent systematists will be required to delineate subspecies and sometimes, species as well. • The ESA's inclusion of distinct population segments—i.e., taxa below the rank of subspecies—is also soundly based on scientific evidence. To help provide scientific objectivity in identifying these population segments, the concept of the evolutionary unit (EU) should be adopted. We define the EU as a segment of biological diversity that contains a potential for a unique evolutionary future. Criteria to establish identity of an EU primarily concern assessment of its diagnosibility, or distinctiveness, relative to other units. Determinants of distinctiveness include morphology, behavior, genetics, molecular make- up, physiology, and so on. An analysis might include such factors as reproductive isolation, genetic variation, ecological distinctiveness and importance, details of reproductive ecology and dispersal, geographic isolation, and historic and prehistoric range changes and their causes. To clarify the analyses, identifying an EU should be separate from deciding whether it is in need of protection. • The ESA explicitly covers species and subspecies of all plants and animals. As currently written, however, it covers taxonomic ranks below the subspecies level (distinct population segments) only for vertebrate animals. There is no scientific reason to exclude any EUs of invertebrate animals and plants from coverage under the ESA. • Although the way organisms are divided into kingdoms has changed since the ESA was enacted in 1973, current scientific knowledge about how species concepts apply in practice to many of these organisms does not lead us to recommend that coverage be extended to prokaryotes and most single- celled eukaryotes, such as yeasts. use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 68 REFERENCES Avise, J.C., and R.M. Ball. 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv. Evol. Biol. 7:45-67. Barone, M.A., M.E. Roelke, J. Howard, J.L. Brown, A.E. Anderson, and D.E. Wildt. 1994. Reproductive characteristics of male Florida panthers: Comparative studies from Florida, Texas, Colorado, Latin America, and North American zoos. J. Mammal. 75:150-162. Camp, W.H., and C.L. Gilly. 1943. The structure and origin of species with a discussion of intraspecific variability and related nomenclatural problems. Brittonia 4: 323-385. Confer, J.L., and K. Knapp. 1981. Golden-winged warblers and blue-winged warblers: The relative success of a habitat specialist and a generalist. Auk 98:108-114. Confer, J.L., and K. Knapp. 1992. Golden-winged warbler Vermivora chrysoptera. Pp. 369-383 in Migratory Nongame Birds of Management Concern in the Northeast, K.J. Schneider and D.M. Pence, eds. U.S. Department of the Interior, Fish and Wildlife Service, Newton Corner, Mass. Cracraft, J. 1987. Species concepts and the ontology of evolution. Biol. Philos. 2:329-346. Davis, J.I., and K.C. Nixon. 1992. Genetic variation, populations, and the delimitation of phylogenetic species. Syst. Biol. 41:421-435. de Queiroz, K., and M.J. Donoghue. 1988. Phylogenetic systematics and the species problem. Cladistics 4:317-338. Donoghue, M.J. 1985. A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 88:172-181. Ereshefsky, M. 1989. Where's the species? Comments on the phylogenetic species concepts. Biol. Philos. 4:89-96. Funk, V. 1985. Phylogenetic patterns and hybridization. Ann. Mo. Bot. Gard. 72:681-715. Ghiselin, M. 1974. A radical solution to the species problem. Syst. Biol. 23:536-544. Gill, F.B. 1980. Historical aspects of hybridization between golden-winged and blue-winged warblers. Auk 97:1-18. Gill, F.B. 1985. Whither two warblers? Living Bird Q. 4:4-7. Gilmour, J.S.L., and J. Heslop-Harrison. 1954. The deme terminology and the units of microevolutionary change. Genetica 27:147-161. Goldman, E.A. 1910. Revision of the wood rats of the genus Neotoma. North Am. Fauna 31:1-124. Grant, V. 1957. The plant species in theory and practice. Pp. 39-80 in The Species Problem, E. Mayr, ed. American Association for the Advancement of Science, Washington, D.C. Grant, V. 1959. Natural History of the Phlox Family. Systematic Botany, Vol. 1. The Hague, Netherlands: Nijhoff. Grant, V. 1963. The Origin of Adaptations. New York: Columbia University Press. Hayes, J.P. and R.G. Harrison. 1992. Variation in mitochondrial DNA and the biogeographic history of woodrats (Neotoma) of the eastern United States. Syst. Zool. 41:331-344. Hayes, J.P. and M.E. Richmond. 1993. Clinal variations and the morphology of woodrats (Neotoma) of the eastern United States. J. Mammal. 74(1): 204-216. Heard, W.R. 1991. Life history of pink salmon. Pp. 119-230 in Pacific Salmon Life Histories, C. Groot and L. Margolis, eds. Vancouver, B.C.: UBC Press. Kettlewell, H.B.D. 1961. The phenomenon of industrial melanism in Lepidoptera. Annu. Rev. Entomol. 6:245-262. Kluge, A.G. 1990. Species as historical individuals. Biol. Philos. 5:417-431. Lack, D. 1971. Ecological Isolation in Birds. Cambridge, Mass.: Harvard University Press. Lancaster, J. 1990. Lujan: Endangered Species Act too tough, needs changes . Washington Post, May 12. use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 69 Margulis, L., and K.V. Schwartz. 1987. Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth. 2nd Ed. New York: W.H. Freeman. Mayr, E. 1942. Systematics and the Origin of Species from the Viewpoint of a Zoologist. New York: Columbia University Press. Mayr, E. 1963. Animal Species and Evolution. Cambridge, Mass.: Belknap. Mayr, E. 1969. Principles of Systematic Zoology. New York: McGraw-Hill. Mayr, E., and P.D. Ashlock. 1991. Principles of Systematic Zoology. 2nd Ed. New York: McGraw-Hill. Mishler, B.D. 1985. The morphological, developmental, and phylogenetic bases of species concepts in bryophytes. Bryologist 88:207-214. Mishler, B., and R. Brandon. 1987. Individuality, pluralism, and the phylogenetic species concept. Biol. Philos. 2:397-414. Mishler, B.D., and M.J. Donoghue. 1982. Species concepts: A case for pluralism. Syst. Zool. 31:491-503. Nei, M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press. Nixon, K.C., and Q.D. Wheeler. 1990. An amplification of the phylogenetic species concept. Cladistics 6:211-223. NOAA (National Oceanic and Atmospheric Administration). 1991. Policy on applying the definition of species under the Endangered Species Act to Pacific salmon. Fed. Reg. 56:58612-58618. NRC (National Research Council). 1995. Upstream: Salmon and Society in the Pacific Northwest. Washington, D.C.: National Academy Press. O'Hara, R.J. 1993. Systematic generalization, historical fate, and the species problem. Syst. Biol. 42:231-246. Otte, D., and J. Endler. 1989. Speciation and Its Consequences. Sunderland, Mass.: Sinauer Associates. Parsons, T.J., S.L. Olson, and M.J. Braun. 1993. Unidirectional spread of secondary sexual plumage traits across an avian hybrid zone. Science 260:1643-1646. Paterson, H.E.H. 1985. The recognition concept of species. Pp. 21-29 in Species and Speciation, E.S. Vrba, ed. Transvaal Museum Monogr. 4. Pretoria: Transvaal Museum. Paterson, H.E.H. 1993. Evolution and the recognition concept of species: Collected writings, S.F. McEvey, ed. Baltimore, Md.: The Johns Hopkins University Press. Peterson, A.T. 1992. Phylogeny and rates of molecular evolution of the Aphelocoma jays (Corvidae). Auk 109:133-147. Raven, P.H. 1974. Plant systematics 1947-1972. Ann. Mo. Bot. Gard. 61:166-178. Richards, R.L. 1971. The woodrat in Indiana: Recent fossils. Proc. Indiana Acad. Sci. 81:370-375. Ridley, M. 1989. The cladistic solution to the species problem. Biol. Philos. 4:1-16. Roelke, M.E., J.S. Martenson, and S.J. O'Brien. 1993. The consequences of demographic reduction and genetic depletion in the endangered Florida panther . Curr. Biol. 3:340-350. Smith, C.R., D.M. Pence, and R.J. O'Connor. 1993. Status of neotropical migratory birds in the Northeast: A preliminary assessment. Pp. 172-188 in Status and Management of Neotropical Migratory Birds, D.M. Finch and P.W. Stangel. eds. Gen. Tech. Rep. RM229. U.S. Department of Agriculture Forest Service, Rocky Mountain Forest and Range Experimental Station, Fort Collins, Colo. Solbrig, O. 1970. Principles and Methods of Plant Biosystematics. Toronto: Macmillan. Steadman, D.W., L.J. Craig, and J. Bopp. 1993a. Diddly Cave: A new late Quaternary vertebrate fauna from New York State. Curr. Res. Pleist. 9:110-112. Steadman, D.W., L.J. Craig, and T. Engel. 1993b. Late Pleistocene and Holocene vertebrates from Joralemon's (Fish Club) Cave, Albany County, New York. Bull. N.Y. State Archaeol. Assoc. 105:9-15. use the print version of this publication as the authoritative version for attribution.

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About this PDF file: This new digital representation of the original work has been recomposed from XML files created from the original paper book, not from the original typesetting files. Page breaks are true to the original; line lengths, word breaks, heading styles, and other typesetting-specific formatting, however, cannot be retained, and some typographic errors may have been accidentally inserted. Please SPECIES DEFINITIONS AND THE ENDANGERED SPECIES ACT 70 Stebbins, G.L. 1950. Variation and Evolution in Plants. New York: Columbia University Press. Stebbins, G.L. 1970. Biosystematics: An avenue toward understanding evolution . Taxon 19:205-214. Stuessy, T. 1990. Plant Taxonomy. New York: Columbia University Press. Templeton, A. 1989. The Meaning of Species and Speciation: A Genetic Perspective. Pp. 327 in Speciation and Its Consequences, D. Otte and J. Endler, eds. Sunderland, Mass.: Sinauer Associates. U.S. Congress. 1975. Committee on Merchant Marine and Fisheries 94-A, House Document 94-51. Washington, D.C.: U.S. Government Printing Office. Waples, R.S. 1991. Pacific salmon, Oncorhynchus spp., and the definition of "species" under the Endangered Species Act. Marine Fish. Rev. 53:11-22. Waples, R.S. In press. Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. In Evolution and the Aquatic Ecosystem, J.L. Nielsen and D.A. Powers, eds. American Fisheries Society, Bethesda, Md. Weir, B. S. 1990. Genetic Data Analysis. Sunderland, Mass.: Sinauer Associates. Wilcove, D.S., M. McMillan, and K.C. Winston. 1993. What exactly is an endangered species? An analysis of the U.S. Endangered Species list: 1985-1991. Conserv. Biol. 7(1):87-93. Wiley, E. 1981. Phylogenetics: The Theory and Practice of Phylogenetic Systematics. New York: John Wiley & Sons. Wiley, R.W. 1980. Neotomafloridana. Mamm. Species 139:1-7. Woolfenden, G.E. and J.W. Fitzpatrick. 1984. The Florida Scrub Jay: Demography of a Cooperative Breeding Bird. Princeton, N.J.: Princeton University Press. use the print version of this publication as the authoritative version for attribution.