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OCR for page 37
Chapter 3
Species Definitions and
the Endangered Species Act
Many different cultures have an extensive literature on the history of the use of the term
species, or kinds of organisms. The Endangered Species Act defines species in Section 3 (15) to
include "any subspecies of fish of wildlife or plants, and any distinct population segment of any species
or vertebrate fish or wildlife which interbreeds when maturer." The act uses species in a legal sense to
refer to any of those entities. However, species has vernacular, legal, and biological meanings.
The committee has been charged with examination of the use of the term species as it has been
interpreted for implementation of the ESA from 1973 to the present. Since the ESA became law in
1973, there have been changes in what many biologists consider the term species to represent, and
technological and philosophical innovations to find species. Nonetheless, the committee concludes that
the ESA's inclusion of species, subspecies, and distinct population segments is correct and appropriate.
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
~ However, the term endangered species excludes "members of the Class Insecta determined by the Secretary
to constitute a pest whose protection under the provisions of this Act would present an overwhelming and
overriding risk to man" (Section 3~6~.
37
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38
Science and the Endangered Species Act
captured most of the concern, research, management, anti funding associated with the ESA. However,
these two groups of vertebrates constitute much less than ~ % of animal species. The initial focus of
~ ~ .
_ . · . . . - ~ · ~ 1 ~ ~ · ~ · · ~ · ·' 1 . .
LEA implementation on onus ano mammals was logical ano reasonable, given me general stale 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 listecl 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 rececle.
Before 1973, federal laws intenclecJ 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 Tracle 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, 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 ant] 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, ant} 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. 41:24064-
24067~), beetles (e.g., the valley elderberry longhorn, Desmocerus californicus rlimorphus (Fed[. Reg.
43:35636-35643) and the northeastern beach tiger beetle (Fed[. Reg. 55:32088-32094~), and butterflies
(e.g., the Oregon silverspot, Speyeria serene 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
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Species Definitions and Endangered Species Act
of the interior review the Smithsonian's roster and publish lists of proposed endangered and threatener}
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 threatened or endangered. To date, no
marine plants have been proposed for listing. The director of FWS announcer! 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: 24523-72), but no action was taken on the recommendation. In 197S, Section 4(iF)~5) of the
Endangered Species Act was amended to state that species on which action had not been taken cluring 2
years after the initial proposal must be withdrawn from consideration. A grace period of ~ year was
providecI. 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
liste(l, establishing a precedent for placing plants on the endangered species list. As of January 31
1995, 516 plant taxa (484 flowering plants, 4 conifers ant! cycacis, 26 ferns and fern allies, and 2
lichens) had been listed, all but three occurring in the Unitecl States (George Drewry, USFWS,
personal communication, February 2S, 1995), ant! many are under consideration.
The original Smithsonian report proviclect 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 diet 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 clid 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. ~ 1 &
17.12, 19931, 342 are full species, 24 are subspecies, ant! 38 are varieties. Which intraspecific rank
has been used tends to reflect the school of the taxonomists working on the listed group of plants (see
Stuessy, 1990 for a historical review of the use of terms). It shouts! 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 ant! yeasts),
although botany departments classically taught mycology, microbiology, and phycology as well as
seecI-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,
1988~. 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
39
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Science and the Endangered Species Act
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 (lifficult 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 inctivicluals).
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 Ihelypteris pilosa
var. alabamensis (Fed. Reg. 57~131) 30165), eligibility depended in part on whether it was distinct
from T. pilosa in Mexico. Distinctiveness was cleterminect by asking experts to provide evidence of
uniqueness. The consensus of experts was that several characteristics of the leaves were ctistinct, 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.
54~461: 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 recognition of the alabamensis subspecies was based on the unique possession of several
leaf (pitcher) features in the Alabama individuals.
Different criteria were Deli 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 user! to (lelimit 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 ~iiffierent kinds of plants. Such variation should be expected for the
foreseeable future, for plants as well as for vertebrate ant! 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 decIareci that there is no single unit that can be called species, anal, 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, 19931. Such authors question why we should expect that some "unit of
nature" equally meets the expectations and needs of ecologists, behaviorists, biochemists, and other
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Species Definitions and Endangered Species Act
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 (lifferent rates, so that differences in morphology,
biochemistry, chromosome structure, breeding characteristics, and population structure. for instance.
need not all arise together during differentiation.
.
41
(, 4,
Why should the term species be so problematic? Why, after centuries of investigations, are
systematic biologists unable simply and easily to tell us which groups of organisms are species and
which are not? The reason is that in the vast majority of cases, speciation is very graclual 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 unfoict; 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 wiclespreact 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 definer! 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 ciistributec3 over the mountain range, and thus with
isolates on each island. On any particular island, the degree of differentiation of the several kinds of
orgainisms could vary, so not all the descen(lent 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 floes 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 clo 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 shouIct or must be defined in terms of the evolutionary
processes thought to result in speciation; or whether they should be clefined 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 "cIadistic" and "phylogenetic" (see Box 3-11. In part the debate is about the extent to
which species should be construer} as units of evolution or whether evolution should be envisioned as
acting at other levels (Kluge, 19901. There is a vast literature on all these topics, inclu(ling papers by
Cracraft (1987), Davis and Nixon (1992), anti Ereshefsky (1989) and by Otte and EndIer (1989),
Paterson (1993), and de Queiroz and Donoghue (1988~.
Developments in population genetics since the 1920s have lee! 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
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Science anti the Enclangererl Species Act
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 ant! 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 ablution 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 HesIop-Harrison, 1954; Grant, 1959; Solbrig, 1970;
Stebbins, 1970; Raven, 19741. 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 rankest 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 clifferentiatecI.
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; MishIer, 19851. 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-Iooking individuals that have evolved from ciifferent ancestors in different parts of the world (or
in different geological times), from being consi(lerecl nonspecific. In adopting the phylogenetic species
concept, many scientists have moved to a species concept very much like the inclusive one user! in the
ESA. Indeed, despite (lifferences 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 (cle 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 of populations should be
considered a species. Because subspecies ant! 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.
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Species Definitions and Enciangerec! Species Act
43
Biological (BSC): Groups of interbreeding natural populations that are reprocluctively isolated from
other such groups (Mayr, 1969; Mayr ant} Ashiock, 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 inclucles nonsexually
reproducing inclividuals by emphasizing processes that keep populations from changing (e.g.,
ontogenetic constraint) (Templeton, 19891.
Evolutionary (ESC): A single lineage of ancestor-clescendant populations that maintains its identity
from other such lineages ant! 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, 19854.
BOX 3-1 Species concepts in the scientific literature.
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 asker! 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 listecl 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 clisciplines. Many of the subspecific and population-level taxa in the iS % 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 cIadistics rank is cle-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
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Science and the Endangered Species Act
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.
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 clefinable 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 hiolo~ic~l meaning ~nr1 ~vol~,tion~rv
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 shouic! also help to meet Congress's
challenging expectation that (listinct population segments be listed "sparingly and only when biological
evidence indicates that such action is warranted" (S. Rep. 151, 96th Congress. ist Session, 19791.
Species and Subspecies
The ESA is clear that species and subspecies of fish, wilcilife, or plants defined in the act to
include all members of the plant and animal kingdoms are eligible for protection. Given the intent of
the ESA to protect biological diversity, the coverage in the ESA has a sound scientific basis. In
practice, it is often necessary to rely on the judgments of competent systematists to identify taxa,
especially subspecies.
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Species Definitions and Endangered Species Act
Distinct Population Segments
45
To help in identifying distinct population segments we developed the concept of an evolutionary
unit (EUN2. An EU is a group of organisms that represents a segment of biological diversity that shares
A_ , I, ~ I, ~ ~ ~ . ,,
. . . ~ ~ _ _ ~ 1 ~ 1 r ~ 1 . ~ c . ~ ~ T. _ _ _ Hi: ~ _ _ ~ ~ ~ _ _ ~ _ __ 1~ _
evolutionary lineage and contains the potential for a unique evolutionary future. its uniqueness can oe
sought in, but is not limited to, attributes of morphology, behavior, physiology, and biochemistry. A
basic characteristic of a EU is that it is distinct from other EUs. In most cases, an EU will also occupy
a particular geographical area. Clearly, most currently recognized species and subspecies are also
EUs. Thus, the following discussion provides a practical approach to identifying distinct population
segments.
Application of the evolutionary unit concept should result in no substantive change in the
application of conservation laws. The committee believes its use will move decisions of eligibility for
protection away from arguments about taxonomic ranks and into a realm where more substantive views
about the degree to which populations are evolutionarily significant and new techniques can be applied.
The term distinct population segment has been applied two ways in implementing the ESA.
One way is that the distinct population segment corresponds to an EU-an evolutionarily distinct
population segment that is geographically or otherwise isolated from other population segments. In
some cases, the population segment being referred to is a metapopulation, i.e., a larger population
made up of smaller, local breeding populations that have some genetic and ecological interactions
among them. A good example of a metapopulation is salmon in a large river system. In this case
(e.g., winter-run chinook salmon in the Sacramento River of California, listed as endangered), the local
breeding populations are the fish that spawn in each small tributary stream. A recent NRC report
(NRC, 1995) described the metapopulation concept as it applies to salmon in great detail, and Waples
(in press) discussed the applicability of the ESU to metapopulations. Although identifying an EU might
be more difficult if the population in question is a metapopulation, it is no different in concept from
identifying a single population as an KU.
Political boundaries also have been used to designate population segments. Although those
boundaries can be appropriate to delineate population segments for management, they often do not
delineate EUs, especially when the political boundaries do not coincide with major natural geographic
boundaries. Although there can be good policy reasons for such delineations, there are not sound
scientific reasons to delineate species only in accordance with political boundaries.
Distinctiveness
The fundamental characteristic of an EU is that it is distinct from other EUs, and distinction
implies an independent evolutionary future. Estimates of distinctiveness (circumscription of EUs) are
based on genetic, molecular, behavioral, morphological, or ecological information. But a single kind
of information often will fail to provide compelling evidence of distinctiveness. Determination of
2 The EU is similar but not identical to the "evolutionarily significant unit" (ESU) proposed by NMFS for
managing anadromous Pacific salmonids (NOAA, 1991; Waples, 1991; Waples, in press). The EU does not
stress reproductive isolation as a criterion, because reproductive isolation is often difficult to assess directly, and it
stresses evolutionary future more explicitly than the ESU does. By omitting the word "significant," it recognizes
that significance is a continuum, a point clearly expressed also by Waples (in press). However, it seems likely
that the application of either the EU or the ESU concept would lead to similar results most of the time, especially
for vertebrates.
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Science and the Endangered Species Act
distinctiveness and the associated inference of an independent evolutionary future usually requires the
careful integration of several lines of evidence. In this section, we discuss some of the experimental
and observational tools currently user! to assess ctistinctiveness.
Genetic Isolation
Because possession of a unique potential for evolution is an important characteristic of an KU,
genetic difference of a population from other populations is an important aspect of distinctiveness. It is
also evidence for physical or reproductive isolation, because populations whose members interbreed
cannot become completely differentiatecl genetically. Isolation over a prolonged perioc! is usually
associated with sufficient genetic divergence to ensure an inclependent evolutionary future. Measures
of genetic divergence or genetic distance between populations can be user! as surrogate measures of the
degree of genetic isolation between them. A large degree of genetic divergence or genetic distance
between two populations is prima facie evidence of distinctiveness. That is because even a small
amount of interbreeding between two populations will recluce the genetic divergence between them
unless there is strong differential selection between the two populations. If there is strong differential
selection between two populations, they are likely to diverge genetically after a time.
The most direct test of isolation is testing for the ability of individuals from different
populations to interbreed. Genetic analysis also includes tests to see if differences in morphological or
behavioral characteristics between populations have a genetic basis, and molecular methods for
assessing genetic variation directly. Box 3-2 describes several of the methods currently in use for
assessing variation in the genetic material and in the proteins that genes produce. The wide application
of these methods (particularly the isozyme method) to plant, animal, and microbial species has provided
a general picture of the average genetic divergence associates! with various levels of taxonomic
ctistinction. However, average values cannot be applied to particular situations. Rather, distinction
must be assesses! on a case-by-case basis.
Many species are composed of a network of populations (a metapopulation system) distributed
across a heterogeneous physical environment. Understanding this aspect of population structure is
important for protecting some endangered populations, because a particular population of concern
might depend for its long-term survival on occasional interbreeding with other populations in the
metapopulation of which it is a part. Particular populations within a metapopulation can exchange
genes through migration. But barriers to genetic exchange ultimately lead to genetic isolation, and
when genetic exchange is at a sufficiently low level, populations can be effectively isolated. As a
result, they and perhaps the whole metapopulation might be more vulnerable to extinction.
Geographic and Temporal Isolation
Many methods help to detect geographic isolation between populations. One technique uses
tags or markers to follow individuals to see if they move into areas occupied by other populations.
Some tags that have been used are natural morphological variations, a variety of artificial marks, and
natural molecular or isozyme markers. An interesting example of isolation is provided by pink salmon
(Oncorhynchus nerka) of the Pacific coasts of North America, Russia, and Japan. Pink salmon have
rigid 2-year life cycles, so fish spawned 1 year apart (referred to as "odd-year" and "even-year" fish)
almost never interbreed, even though they spawn in the same streams (Hearst, 1991~.
- r-r
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47
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 indivicluals 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 methoc! 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 (lehyclrogenase) 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 react 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 resolver} 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 ciata 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, 19901. Gene frequencies are estimated by counting the number of copies
of a particular allele in the sample and then, for ctiploict organisms, dividing by twice the number of
individuals in the sample (recall that every cliploid 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., Weir, 1990; Nei, 1987~. (Box 3-2 continued" on following paged
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BOX 3-2 (Continued "Molecular methods" usually refer to the set of methods that involve direct
assay of either DNA or RNA. A large number of techniques fall uncler this rubric. Moreover,
there continues to be a rapist 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-l9SOs, 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 discusser! 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 (~) 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 employecl 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 EcoRl), and a change in fragment
pattern must therefore be clue 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 bounciest 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 limiter! 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 ctistinguishable bands; in the case of dominance, only one
band will appear, and thus less information can be obtained.
Current applications of PCR-based methocis in enciangereci 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
establisher! through forensic use of DNA; ant! (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 is the
sense of constituting an KU.
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Species Definitions and Endangered Species Act
Behavioral ant! Reproductive Isolation
49
Populations of many organisms are isolated from each other because of 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 ant! 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. ~ ~ v~.~ ~v. -^ ~ . .:_ ~:v-: -: ~ : ::: .. :
American alligator, bog turtle, California condor, whooping crane, or black-footed ferret.
Few wn~lr1 cln~ht the taxonomic distinctiveness of such well-known animals as the
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 KU.
An example of an EU is the Allegheny wooclrat, 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 (GoIciman, 1910), the
Allegheny woodrat had been considered nonspecific with the more widespread Eastern woodrat (N.
?oridana) since the 1940s. However, recent studies have provided substantial adclitional evidence that
N. magister is distinct from N. J?oridana in its morphology (Hayes ant! Richmond, 1993) and have
demonstrates! distinctiveness of mitochondrial DNA (Hayes and Harrison, 1992), as well as behavior
and ecology (Wiley, 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, personal communication, September 1993~; because of events related to
human activities (e.g., expansion of suburbs, loss of large predators, decline of hunting and trapping of
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Science and the Endangered Species Act
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 cleclining because of habitat loss, differs from other populations genetically
(Peterson, 1992) and in its behavior and ecology (Woolfenclen 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, personal
communication, 1995~. Waples (in press) desribed in detail the identification of EUs (ESUs in NMFS
terminology) of anacIromous 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
Adonis 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) clescribed by Kettlewell
(1961), the dark forms continue to interbreed with the light forms, so the dark forms do not constitute
an KU. Similarly, a growing body of evidence suggests that (lifferent 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 regulates! locally, with hunting allowed or protection bestowed baser! on political
boundaries. The American alligator is an KU, but the regulated and unregulated populations are not
EUs. The American brown bear (Ursus horrib~Zis) 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 cleclinect 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. There is very little
genetic variation in the Big Cypress panthers, and those 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~. In ad(lition, 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~. Thus, 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 Floricia."
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Species Definitions ant] Endangered Species Act
In the case of the American bald eagle, and in other similar cases, there might well be
persuasive reasons to conserve taxa distinguishes! 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 (leny 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 criticisms), and it is a difficult aspect of the problem. A
biologically sound methoc! 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 (e.g., a country) is distinct and imperiled3.
This kind of criticism of an EU concept confounds identification of distinctiveness with a
decision as to whether a particular population is in neec! 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 clecline 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 intencled to protect threatened and endangered species, not to prevent them from
becoming threatened and endangered. Preventing species from becoming threatened ant! endangered! is
essential for preserving biological diversity, anct additional conservation and management plans beyond
the provisions of the ESA are neecled to achieve that goal. Some of those are discussed in Chapter 10.
51
The Fate of Hybrids under the Evolutionary Unit Concept
Many organisms, especially plants, are clescendeci 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 consiclered 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 (listinct at either the
species or subspecies level: the eastern yellow-shafted flicker (C. auratus auratus); the western and
montane red-shafted flicker (C. auratus caper broadly clefined); and the southwestern gil~ied flicker (C.
auratus ch7ysoicles). Hybrids of C. a. auratus and C. a. caper can be found along a north-south zone
east of the Rocky Mountains, while hybrids of C. a. caper 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 bircts. Furthermore, the hybrids are common within much of their limited
range ant} almost always occur alongside pure forms. Even the least common and most localizes!
3 A 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 Copulation of organisms in the United States is distinct and endangered.
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Science and the Endangered Species Act
hybrid flicker (C. a. caper x C. a. chrysoid~es) would not be considered an KU, 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 KU. The two species hybridize readily, producing viable offspring (Gill, 1980) that are
sometimes called Brewster's or Lawrence's warblers. The GW is cleclining over much of its range
(Confer and Knapp, 19921. 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 clue to succession), with other factors being
brooct parasitism by cowbirds, ant} hybridization with the BW. Where the GW and BW come together
(in many localities in the Northeast and upper Midwest), the long-term (decacial) 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 KU, 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.
Application of 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 enclangered parental species. Modern genetic
techniques routinely find examples of interbreeding that has left the parent species' lineages essentially
unchanged phenotypically.
Many clevelopments in theoretical population genetics ant} 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 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 rapidly take advantage of this expertise in a
nonpolitical way and with the allocation of resources towards research and implementation. Decisions
relevant to the ESA can be made more objectively than they have been, and this objectivity should
ltim~t~.lv rerlllce costs of implementing and enforcing the act bY facilitating the clecision-making
~ r D ~ ~ -~ at,
process and reducing court costs.
Conclusions and Recommendations
~ The ESA's emphasis on species and subspecies is soun(lly justified by current scientific
knowledge ant! shouicl be retained. Often, competent systematists will be required to delineate
subspecies, and sometimes species as well.
~ The ESAts emphasis on (listinct population segments i.e., taxa below the rank of
subspecies is also soundly baser! on scientific evidence. To help provide scientific objectivity in
identifying these population segments, the concept of the evolutionary unit (KU) should be aclopted.
We define the EU as a segment of biological diversity that contains a potential for a unique
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Species Definitions and Endangered Species Act
evolutionary future. Criteria to establish identity of an EU primarily concern assessment of its
diagnosibility, or distinctiveness, relative to ether 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 recommencI that coverage be extended to prokaryotes and most
single-celled eukaryotes, such as yeasts.
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Representative terms from entire chapter:
species act
