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Most extinction literature focuses on prevention and prediction, not assessment. Determination of extinction can be surprisingly complicated, with diverse approaches and terminology, leading to a gray area within extinction assessment. A series of five gray-extinction categories (mitigated, regional, native range, wild, and apparent) are provided to address these ambiguities and highlight how extant lineages may be effectively extinct. For reference, we use freshwater fishes, a group in serious decline throughout the world. Categories are interwoven into a decision tree to ensure a practical assessment of extinction and maximize conservation effectiveness. To prevent premature declarations, a waiting period based on generation time (versus a fixed number of years) is proposed. We also explain how extinction is tied to multilineage and lineage-specific anthropogenic effects and how dependence on artificial selection equates to a form of extinction. Finally, we touch on the resurrection of lineages and the impact of artificial hybridization and propagation on the extinction process.
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Overview Articles April 2017 / Vol. 67 No. 4 BioScience 357
Assessing Extinction
Most extinction literature focuses on prevention and prediction, not assessment. Determination of extinction can be surprisingly complicated,
with diverse approaches and terminology, leading to a gray area within extinction assessment. A series of five gray-extinction categories
(mitigated, regional, native range, wild, and apparent) are provided to address these ambiguities and highlight how extant lineages may be
effectively extinct. For reference, we use freshwater fishes, a group in serious decline throughout the world. Categories are interwoven into a
decision tree to ensure a practical assessment of extinction and maximize conservation effectiveness. To prevent premature declarations, a
waiting period based on generation time (versus a fixed number of years) is proposed. We also explain how extinction is tied to multilineage
and lineage-specific anthropogenic effects and how dependence on artificial selection equates to a form of extinction. Finally, we touch on the
resurrection of lineages and the impact of artificial hybridization and propagation on the extinction process.
Keywords: freshwater fishes, artificial selection, endangered species, triage, conservation
Throughout evolutionary history, millions of lineages
have gone extinct, by chance or because of an inability
to adapt to new environmental conditions (Darwin 1859).
In particular, sudden global changes have led to five major
extinction events (Raup and Sepkoski 1982). Today, we
are experiencing a sixth major extinction event as a result
of global change caused by humans (Dirzo et al. 2014).
Interestingly, most people see extinction as a simple dichot-
omy: Either a species is gone from the Earth, or it is not. In
an era of rapid change, however, extinction can be surpris-
ingly hard to determine. In this article, we address the basic
question: How do you know when a lineage is extinct?
Before any assessment of extinction can be attempted, a
lineage must be formally recognized as distinct. This distinc-
tiveness can include reproductive barriers, genetic signature,
morphometrics or meristics, location, and range, to name
but a few. For most organisms, lineages are distinguished at
the level of species (IUCN 2012). Often, however, lineages
are also are recognized as subspecies, distinct population
segments (DPS; Endangered Species Act of 1973, section 4),
evolutionarily significant units (ESU; Waples 1991), desig-
natable units (SARA; Canada’s Species at Risk Act of 2002),
or management units (MU; Vogler and Desalle 1994). All
can receive the same legal protection as species, depending
on the country. Therefore, to ensure clarity and comprehen-
siveness, we simply refer to any recognized distinct taxo-
nomic group as a lineage.
From a biologist’s perspective, every evolutionary lin-
eage is unique, with a distinct role in the ecosystem(s) of
which it is part (Ehrlich and Mooney 1983). The science
of conservation biology focuses on preventing extinction
of contemporary lineages. In some countries, prevention is
mandated by law, whereas in others, it is a matter of choice.
Regardless, most countries follow the International Union
for Conservation of Nature (IUCN) system, in which lin-
eages are assessed as to their susceptibility to extinction
in the near future: vulnerable, endangered, and critically
endangered (IUCN 2012). But despite the success of this
system at decreasing extinctions (Rondinini et al. 2014),
many lineages continue to decline. The IUCN (2012) also
uses three extinction categories: regionally extinct, extinct
in the wild (known only to survive in culture, captivity, or
as a naturalized population outside their native range), and
globally extinct (i.e., “there is no reasonable doubt that the
last individual has died”). But it is often difficult to say with
certainty when the last individual is gone because most lin-
eages are cryptic at small population sizes, making it difficult
to determine “no reasonable doubt.
Determination of extinction is not simple. Is a lineage
extinct if a single individual still exists, as has happened
with some trees and tortoises (Cronk 2016)? What if a lin-
eage is wholly reliant on humans, is absent from its native
range, or has no habitat left? What if it has been genetically
modified or hybridized with another lineage? In all such
situations, the evolutionary trajectory of the lineage has
been changed. But is this change enough to consider it to
be extinct? Defining extinction can be a lot like defining a
species because it requires recognizing one lineage as being
distinct from other lineages (de Quieroz 2007). A species is
generally thought of as being one or more populations that
have separated over time from other related populations by
chance and/or natural selection acting under a particular set
of environmental conditions. As the environment changes,
a species must change as well or go extinct. Unfortunately,
BioScience 67: 357–366. © The Author(s) 2017. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
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358 BioScience April 2017 / Vol. 67 No. 4
recent anthropogenic environmental change is occurring at
such a rapid pace that evolutionary change cannot keep up,
at least for longer-lived species, such as most vertebrates.
Therefore, many species persist mainly at the sufferance of
humans: in zoos, in culture, or in the wild in carefully regu-
lated environments. This means, in turn, that frequent deci-
sions must be made that require understanding the nature
of extinction.
Regrettably, extinction of a lineage is not well defined
legally in most places in the world (with some exceptions,
such as SARA in Canada). In the United States, for example,
there is no formal policy for defining a lineage as extinct.
The Endangered Species Act of 1973 (ESA) was written to
prevent extinction and therefore does not specify how to
determine extinction. Legislation in the European Union
and Australia is similar in this regard. However, under
the implementing regulations for the ESA, the managing
agencies (the US Fish and Wildlife Service, USFWS, and
the National Marine Fisheries Service, NMFS) can delist
an endangered lineage on extinction, suggesting a discre-
tionary act rather than a mandatory procedure (50 C.F.R.
§424.11(d)(1)). This decision, however, also requires a lin-
eage be formally listed as threatened or endangered, so it can
be delisted after the normal 5-year review. This procedure
is only an indirect measure of extinction, with no formal
criteria. The IUCN, which includes over 1200 government
and nongovernment organizations (NGOs), generates most
of the endangered species recommendations but has no
listed formal extinction procedure or enforcement power for
declaring extinction, relying on individual countries to draw
their own conclusions.
To help explore the uncertainties or difficulties surround-
ing extinction, it is useful to focus on a particular taxonomic
group. One group with members especially prone to com-
plete extinction is freshwater fishes (Leidy and Moyle 1997,
Moyle etal. 2011, Burkhead 2012). In the twentieth century,
freshwater fishes had the highest extinction rate worldwide
among vertebrates, and conservative estimates project 43–86
extant species will be extinct in North America by 2050
(Burkhead 2012). Furthermore, it is difficult to “prove
extinction in most freshwater fishes because at low numbers,
they evade capture or detection in places such as deep lakes
or turbid rivers (Jelks etal. 2008). Finally, freshwater fishes
include some of the best examples of conservation-reliant
and captive species, which confound extinction declarations.
To further explore the uncertainties or difficulties sur-
rounding the assessment of extinction, we introduce what
we call gray extinction, a category between traditional IUCN
vulnerable or endangered categorizations and global extinc-
tion. This important classifcation brings to light the many
ways that a lineage may already be “extinct” to some degree
and has strong conservation implications. Multiple catego-
ries are proposed as working criteria to assess the extinction
trajectories of any freshwater fish lineage. In addition, we
have provided a decision tree to document the transition
of a lineage through these categories before reaching global
extinction. And although we focus on freshwater fishes, our
process should be adaptable to any lineage, making it an
acceptable method to assess any extinction.
Saving lineages
Human activity affects most lineages in the modern world,
both positively and negatively (Kareiva etal. 2007). These
anthropogenic effects can set a lineage’s trajectory toward
global extinction and range from multilineage to lineage-
specific, with a spectrum of effects in between the extremes.
Multilineage effects are those anthropogenic factors that
affect multiple lineages simultaneously on a habitat, land-
scape, ecosystem or even global scale. They occur as result
of lineages sharing the planet with humans and cannot be
entirely avoided (e.g., climate change). Such effects can also
mimic “natural” effects (e.g., landslides can dam rivers) and
therefore are presumably subject to evolutionary pressures
(i.e., natural selection) consistent with their evolution-
ary history. However, many multilineage anthropogenic
effects are occurring too rapidly, outside the range of nor-
mal environmental variability. Measures taken to alleviate
such effects should, in principle, have a multilineage focus
on conservation up to the planetary scale. This approach
benefits all lineages affected, not just a single lineage. It is
also usually the most cost-effective method over the long
term (Palmer etal. 1997). Approaches for freshwater fishes
might include large-scale habitat restoration, halting the use
of harmful pesticides, improving stream flows, or revers-
ing global warming. The important idea is that a lineage
subject to such conservation measures will still be in its
natural environment, susceptible to natural selection, even
if accelerated, and therefore potentially recoverable if on an
extinction trajectory.
In contrast, lineage-specific effects are those that pri-
marily affect—or at least are perceived to affect—a single
lineage. In most cases, this involves natural selection being
largely replaced by artificial selection (table 1). Artificial
selection can include trait selection, fecundity maximiza-
tion, prezygotic barrier removal, or protection from preda-
tion, among many others. As we discuss later, production
fish hatcheries are classic purveyors of multiple effects on
single lineages.
If exhaustive large-scale, multilineage approaches are
insufficient to alter extinction trajectories, lineage-specific
actions will be required. Individual lineages requiring such
actions become conservation reliant, no longer capable of
surviving on their own and requiring humans to support
their existence (Scott etal. 2005). With this support comes
some unavoidable domestication, because it is unrealistic to
expect managers to fully grasp and replicate every selective
pressure that shapes a lineage—a problem seen time and
time again in fish hatcheries (see below). These actions then
alter a lineage’s evolutionary trajectory from one driven by
natural selection to one driven by artificial selection (deBeer
1958, Akey etal. 2010). Actions to alleviate lineage-specific
problems are purposeful and come with the understanding
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Overview Articles April 2017 / Vol. 67 No. 4 BioScience 359
that maintaining an altered lineage is better than complete
disappearance. Because lineage-specific effects are generally
additive, ever-increasing artificial selection drives a lineage
further and further from its “natural” roots (Carlson et al.
2007). At some point, such lineages become completely
adapted to artificial habitats (e.g., a fish hatchery or ponds)
and are incapable of maintaining populations in their envi-
ronment of origin. They become, for lack of a better term,
domesticated and extinct as natural lineages.
Recognition of this spectrum of effects on lineages allows
a prioritization system (best to worst case) to be set up for
establishing conservation priorities (Bottrill et al. 2008)
for lineages seemingly headed for global extinction: (a)
Lineages reliant on large-scale multilineage actions still exist
somewhere in their natural environments and will continue
to persist with minimal help for a long time, but ultimately,
they will need the benefits of actions such as the restoration
of natural-flow regimes to rivers. (b) Lineages reliant on lin-
eage-specific actions include two pathways: (1) lineages that
have sufficient genetic diversity so they can eventually be
weaned from reliance on human interference or (2) lineages
that will always require direct management to sustain them,
with evolution taking place, at least in part, through artifi-
cial selection. These lineages are likely to go globally extinct
without continuous action. (c) Lineages for which there is
little or no hope for preventing global extinction, except per-
haps as display populations in zoos or aquaria, constitute the
third category. The application of this prioritization (triage)
scheme requires a general understanding of the varieties of
The varieties of extinction
There have been a number of attempts to deal with impend-
ing extinction on a broad basis, including population viabil-
ity analysis (Boyce 1992, Beissinger and McCullough 2002)
and extensive predictive modeling (Purvis et al. 2000,
Hutchings et al. 2012). One widely used idea is that of
extinction debt, in which diverse lineages persist as declin-
ing populations in habitat so altered or diminished that
eventual extinction is likely, even though the process may
take generations (Tilman etal. 1994, Kuussaari etal. 2009).
These “living-dead” lineages may initially survive but will
gradually disappear, even without any further habitat modi-
fication. Extinction debt is especially likely to apply to
lineages with long generation times or to those already on
the threshold of extinction. Although there may be indi-
viduals present in the environment, the lineage is basically
extinct if extreme measures are not undertaken to restore
viability (Kuussaari etal. 2009, Cronk 2016). A similar idea
is functional extinction, in which individuals are present in
their habitat but are so depressed in numbers that they no
longer play a significant role in the ecological community in
which they are embedded (Şekercioğlu etal. 2004). In both
cases, however, lineages persist with an uncertain timeline to
global extinction.
Typically, a lineage is declared globally extinct if an
informal consensus of experts agrees and an extinction dec-
laration is published, usually in a regional faunal work. But
lineages determined to be extinct by this method are some-
times rediscovered (e.g., Miller Lake Lamprey Lampetra
minima, Loiron et al. 2000; Owens Pupfish Cyprinodon
radiosus, Moyle 2002). To combat this problem, the IUCN
recommends waiting 50 years before declaring extinc-
tion. Additional guidelines related to freshwater fishes are
limited. Harrison and Stiassny (1999) proposed a set of
categories contingent on taxonomic status, effective extinc-
tion date, population decline or environmental threat, and
extinction time frame (1500–1948 or 1948–1998), requiring
information often not available. Jelks and colleagues (2008)
recognized three extinction categories for their review of
extinction in North American fishes: extinct (no documen-
tation for 50 years), possibly extinct (no documentation for
20–50 years), and extirpated in nature (lineage only found
in captive populations). But these categories are only guide-
lines for determining global extinction and do not cover all
Gray extinction
As we mentioned previously, a lineage is defined by a very
specific set of criteria (e.g., location, range, appearance, and
life history) that define it as a distinct taxonomic group.
Extinction represents the loss of that distinct group. But
Table 1. Differentiation between multilineage and lineage-specific effects with regard to natural and artificial selective
pressures on certain evolutionary tenets.
Multilineage Effects Lineage-specific Effects
Tenet Natural Selection Artificial Selection
Variation in traits Different combinations of traits throughout
Reduced variation, selection for “desirable” traits
Mating success and fecundity is variable Mating success and fecundity is maximized
Heredity Surviving adults pass on their particular
Artificial mating; genetic modification
Selective pressure
on traits
Prezygotic barriers; predation; biological
interactions (mutualism, commensalism,
parasitism); limited resources; variable
habitat; coevolution; competition
No prezygotic barriers; no predation or other biological interactions;
supplemental feeding; artificial often uniform habitats; maximized
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360 BioScience April 2017 / Vol. 67 No. 4
what if that loss was only partial, in which some of the char-
acteristics were lost but not all? Would the lineage still be the
same? We argue that partial losses represent an intermediate
category between traditional IUCN categories (threatened
or endangered) and global extinction, one we call gray
extinction. This term is both a play on the black–white
dichotomy most perceive for extinction as well as a reminder
of the difficulty in assessing extinction for every situation.
Here, we describe five categories within this gray-extinction
classification, representing an amalgamation of categories
generally found in the scientific literature. The initial cat-
egory, mitigated extinction, is defined by the required use
of lineage-specific effects for maintaining the species (Ex1),
whereas categories 2–4 (Ex2–4) can be arrived at with or
without the impact of lineage-specific effects. Combinations
of both lineage-specific and multilineage effects are possible
and would be represented by two subscripts (e.g., Ex13: miti-
gated and native-range extinction).
Ex1: Mitigated extinction. This applies to lineages that are largely
maintained by artificial selection (lineage-specific effects),
as well as to lineages subject to intentional hybridization or
genetic modification. Also included are conservation-reliant
lineages that depend on continuous or intermittent human
action to maintain viable populations, in which “threats can-
not be eliminated, only managed” (Goble etal. 2012, p. 870).
Ex2: Regional extinction. The lineage is extinct in a geographically
or genetically distinct part of its native range, although it may
be abundant elsewhere. This category is often labeled as “extir-
pation” and can vary by spatial and/or evolutionary scale. For
example, the loss of a DPS, ESU, DU, or MU would be global
extinction but would be regional extinction at the species level.
Ex3: Native-range extinction. The lineage is no longer present in
its native range but has been introduced as a “wild” lineage
successfully outside the native range.
Ex4: Wild extinction. The lineage relies on artificial propaga-
tion for its existence. It is maintained as captive popula-
tions in artificial habitats such as fish hatcheries; it may be
reintroduced into the wild, but such populations are not
Ex5. Apparent extinction. No verified observation exists any-
where despite significant efforts. A waiting period based on
generation time is observed.
Ex6: Global extinction. No verified observation exists any-
where, even after waiting period.
The first four categories are a synthesis of widely used
extinction categories, but with a more stepwise approach.
Our goal is to document the progression of extinction, from
the onset of direct human intervention (mitigated extinction)
to recognition that a lineage only exists in a zoo or captive
breeding facility (wild extinction). At each step, it becomes
more and more difficult to reintroduce a lineage back to
its native habitats, even if conditions are ameliorated. The
ever-increasing conservation reliance necessary to maintain
a long-suffering lineage changes the characters that made the
lineage unique, putting it on an evolutionary trajectory that
presumably reduces its adaptability to conditions in the wild.
This categorization of a lineage can help to determine its
conservation priority when resources are limited. Examples
of each category in fishes are given in table 2.
Time-to-extinction declaration
Categories 5 and 6 occur when no documented individu-
als are found anywhere and de facto extinction is assumed.
Current recommendations suggest waiting 50 years, but no
reason is given as to why this number is appropriate. We
argue that because different lineages have very different gen-
eration times (pupfish, approximately 1 year; sturgeon, 25
or more years; Moyle 2002), the application of a fixed time
period can be excessive in some lineages and insufficient in
others. For example, if a lineage only exists in a single spring
and the spring dries up, a 50-year wait to declare extinction
may be unnecessary. We propose a metric for the waiting
period based on generation time. This is similar to D’Elia
and McCarthy (2010), who recommended using generation
time as a metric for determining extinction risk for species
proposed for listing under the federal ESA. We specifically
recommend that for lineages with generation times of 0–5
years, the declaration should wait ten generations, whereas
those with generation times of 5 or more years should wait
five generations. These metrics are in the spirit of those
already proposed, are conservative enough to ensure no
species are “rediscovered,” and are practical enough to work
with any lineage of fishes.
Decision tree for determining extinction
Our decision tree is designed to differentiate between pre-
and postextinction declarations and different categories
of gray extinction (figure 1). To address these questions,
we propose the establishment of an extinction assessment
committee (EAC), perhaps by a professional society such as
the American Fisheries Society or the American Institute of
Biological Sciences. The EAC would be a mixture of agency,
NGO, and academic biologists who would monitor the sta-
tus of potentially extinct fish lineages. The sole purpose of
this committee would be to review information concerning
the loss of fish lineages and make objective decisions at a
series of checkpoints designated as key transitions in assess-
ing vulnerable or endangered (consistent with IUCN cat-
egories), gray-extinction, and global-extinction status. The
committee would also make decisions related to introgressed
lineages or to applying hybridization to “rescue” genetic
diversity in another lineage. This systematic approach by a
dedicated group could greatly alleviate the ambiguity cur-
rently applied to assessing extinction; it could also facilitate
strategic conservation goals that maximize the recovery
potential of any proposed lineage.
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Checkpoint 1. The evaluation of previous or novel studies
forms the basis for recommendations concerning the under-
lying causes of decline or extinction, listing as vulnerable or
endangered, and the potential to alleviate any multilineage
effects. Much of this information is readily available from
groups such as the IUCN or the Committee on the Status of
Endangered Wildlife in Canada (COSEWIC). Conservation
priority can be assigned if needed.
Checkpoint 2. This assessment of extinction includes the follow-
ing questions: Have all realistic methods to reduce multilineage
effects been exhausted? Are lineage-specific direct effects the
only way to continue the lineage? Are funds and managers in
place for a program of conservation reliance? The gray-extinc-
tion category is assigned following the decision tree.
Checkpoint 3. An annual reevaluation of gray extinc-
tion for each lineage is applied. If wild extinction has
been reached, monitoring programs should indicate that
no individuals are found anywhere. Intensive targeted
sampling efforts should be employed to look for small
populations. A waiting period is set, based on genera-
tions, if no individuals are found (apparent extinction).
If recovery efforts are sufficient to escape gray extinction
(see below), a lineage may be returned to the top of the
decision tree to be evaluated, starting as a healthy lineage
once again.
Checkpoint 4. Final information is collected and global extinc-
tion is confirmed. If rediscovered before waiting period
ends, the lineage returns to checkpoint 2 for reevaluation.
Table 2. Examples of fish lineages exemplifying different extinction categories.
priority Location Comments
Mitigated Extinction
Winter-run Chinook salmon
(Oncorhynchus tshawytscha)
1a California, United States Conser vation hatchery, artificial flows
Fall-run Chinook salmon
(O. tshawytscha)
2California, United States Production hatcheries maintain populations but some natural
Yangtze sturgeon
(Acipenser dabryanus)
1b Yangtze River, China Maintained by hatchery; no wild reproduction
Regional Extinction
Bull trout
(Salvelinus confluentus)
2California, United States Extinct in California but widespread in the western United
States and Canada
Yellowfin madtom
(Noturus flavipinnis)
1a Southeast United States Gone from most of native range but reintroduced from extant
Native-range extinction
Sacramento perch
(Archoplites interruptus)
2California, United States Abundant in reser voirs outside native range
Mojave tui chub
(Siphatales mohavensis)
1a California, United States In ponds near former range (Mojave River)
Wild extinction
Charco Palma pupfish
(Cyprinodon longidorsalis)
1b Mexico Home spring dry but four populations in captivity
Red-tailed shark
(Epalzeorhynchus bicolor)
1b Thailand Popular aquarium fish; no recent records from wild
Apparent Extinction
Shortnose cisco
(Coregonus reighardi)
3Lakes Huron and
Michigan, United States
Last seen 1985
Alabama sturgeon
(Scaphirhynchus suttkusi)
3Alabama, United States Last seen 2007
Longspine bream
(Acanthobrama centisquama)
3Amik Lake, Turkey Amik Lake drained; possibly present in nearby lake (polluted)
but no records
Global Extinction
Blue pike
(Sander vitreus glaucus)
3Lake Erie, United States Last collected 1983
New Zealand grayling
(Prototroctes oxyrhynchus)
3New Zealand Last collected 1930s; declared extinct 1986
Thicktail chub
(Gila crassicauda)
3California, United States Last collected 1955
Note: Information from IUCN Red List (2012) and Moyle (2002).
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362 BioScience April 2017 / Vol. 67 No. 4
Numbers/habitat limited and/or decreasing?
Checkpoint #1
List as vulnerable or endangered?
Are there multi-lineage effects that can be ameliorated?
Checkpoint #2
Lineage is healthy
Special concern?
Is the lineage found
somewhere in its native
Is the lineage found in the
Ex3– Native-
Range Extinction
Checkpoint #3
Is the lineage found
Has the appropriate waiting period been completed?
Checkpoint #4
Ex6–Global Extinction
Are lineage-specific anthropogenic effects being
Cs – Conservation Success
Traditional IUCN
Figure 1. A decision tree to assess the extinction progression of a lineage. The checkpoints represent important decision
nodes based on the best available information, and the boxes represent extinction categories. Following checkpoint 2,
two trajectories are indicated, one reflecting decreasing habitat availability (left) and the second reflecting increasing
conservation reliance and decreasing habitat availability (right).
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Relevance to conservation
The differences between applying multilineage and lineage-
specific methods to avert extinction has considerable finan-
cial and ecological ramifications. Multilineage methods
benefit all lineages, with the focus on restoring the habitat,
not the lineage. Costs may be substantial but often have
anthropogenic benefits (ecosystem services). Once a system
is restored, it presumably requires only traditional manage-
ment expenditures (Odling-Smee 2005). In contrast, apply-
ing lineage-specific methods leads to artificial selection and
conservation reliance (Lorenzen etal. 2012); every lineage
on an extinction trajectory is treated as unique and must be
supported independently. In addition, lineages undergoing
lineage-specific management can rarely fulfill their former
role in a natural system (Ehrlich and Mooney 1983). It may
initially seem cost effective, but as more and more lineages
approach extinction, costs will be overwhelming. However,
even for lineages dependent on lineage-specific methodolo-
gies, their natural habitats could still be restored if reintro-
duction into the wild in some form is likely to be successful.
Conservation success
In the event that conservation reliance can be ended and/
or natural habitat restored, can extinction (categories 1–5)
be reversed? The answer, unfortunately, is yes and no. The
restoration of natural habitat to support a self-sustaining
lineage subject to natural selection would constitute the
recovery of a lineage. The recent removal of a number of
dams (e.g., Elwha Dam) has the potential for this kind of
recovery of certain fishes (O’Conner et al. 2015, Thornton
et al. 2016). However, the lineage would likely have been
altered through artificial selection, potentially removing
lineage-specific identifiers such as courtship behavior or
unique genetic alleles. Therefore, the current lineage may
be different from its wild predecessor, although just how
different would depend on the number of individuals in the
lineage, the amount of artificial selection applied, and the
length of time the selection was applied. Therefore, there is
no direct answer to this question. Our approach is to leave
this difficult decision in the hands of the EAC to be handled
on a case by case basis, with the understanding that in order
to be a conservation success (figure 1), the lineage must be
completely free of human reliance and sufficiently stable
so as to be self-sustaining. We would also recommend the
lineage be labeled “Cs” (similar to endangered, Ex2, etc.).
This would serve the dual purpose of promoting success-
ful conservation efforts and identifying those lineages that
experienced gray extinction.
Resurrection? “Jurassic Park” lineages
As technology continues to improve, biologists are faced
with a difficult question: Do we bring back ancestral or
recently extinct lineages (Friese and Marris 2014, Seddon
etal. 2014)? This avenue has interesting possibilities along
with unprecedented complications and fears (Sandler 2014).
The “resurrection” of an extinct lineage requires using
DNA as a blueprint in one of two ways: pure ancient DNA,
in which a lineage is produced using only DNA from the
known lineage, or mixed DNA, in which an incomplete
genome requires using closely related lineages or known
conserved regions” universal to freshwater fishes for com-
pletion. On the basis of criteria proposed in this article,
these lineages would be considered domesticated and fall
under the mitigated category of extinction. If the lineages
get beyond being treated as novelties and are proposed for
introduction into the wild, we recommend they should be
treated as a potentially invasive species. An exception might
be given to recently globally extinct lineages in which the
ecosystem may still support habitats recently vacated by
the lineage. But timing would be everything, because other
lineages will quickly use resources that once supported the
lost lineage. Ideally, “resurrection” would be the ultimate last
resort, occurring when a lineage reaches apparent or global
Hybridization and/or genetic modification
Conceptual ideas related to artificial and natural hybridiza-
tion are similar to those for extinction. Allendorf and col-
leagues (2004) argued that any introgression from artificial
hybridization equals lineage loss. In contrast, Campton and
Kaeding (2005) contended that if a lineage looks and behaves
like a true lineage, it should be considered one. So how much
introgression is allowable before the lineage is considered a
novel lineage or extinct? What if introgression levels are high
(more than 50%), but a unique lineage-specific gene or allele
is still present? Even more challenging is directed hybrid-
ization as a means of introducing genetic diversity into a
lineage to avert global extinction (Levins 2002, Harbicht
etal. 2014). This is similar to genetic modification, in which
specific genes are targeted artificially to improve traits such
as parasite resistance or growth rates (Hedrick 2001). We
would argue, except in cases of natural hybridization, that
all of the above represent artificial selection and a lineage-
specific impact of humans on fish lineages; they are there-
fore a form of extinction, in this case mitigated extinction
(Ex1). Even though lineages are not conservation reliant per
se, their genomes are permanently altered by humans. But
unlike Allendorf and colleagues (2004), who suggested that
any artificially introgressed population should be eradicated,
we think a lineage that has some resemblance to the original
lineage is superior to none at all, especially if it exists as a
population in the wild that is subject to natural selection.
Devils Hole pupfish: Should we hybridize?
An example of the controversy surrounding the use of
directed hybridization to prevent extinction is the Devils
Hole pupfish (DHP) Cyprinodon diabolis, the most endan-
gered fish in the world (Pister 1990, Martin CH etal. 2016).
Living in Nevada, this lineage has been isolated for tens of
thousands of years (Sağlam etal. 2016) and reduced to 30
individuals at times. Artificial feeding and separate captive
populations are currently ongoing while hybridization (with
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Overview Articles
364 BioScience April 2017 / Vol. 67 No. 4
nearby Ash Meadows Amargosa pupfish, C. nevadensis)
has been tested as a possible method to combat inbreeding
(Martin AP et al. 2012). A small population still exists in
Devils Hole, although it would probably be globally extinct in
the absence of human protection of its habitat (e.g., through
fencing or lawsuits). Would DHP be regarded as extinct
(Ex6), or perhaps as a mitigated extinction (Ex4), if all indi-
viduals had a modified genome that enabled them to persist
in their tiny habitat, as long as they looked and behaved like
DHP? Would they then lose the protection afforded them
by the federal Endangered Species Act of 1973? As of the
writing of this article, DHP are still a natural population in
their natural habitat and not reliant on humans for survival.
Therefore, they would not qualify as mitigated extinction.
Managers will ultimately have to decide whether hybridiza-
tion in, the introduction of captive-bred fish to, or reliance
on human-provided food in Devils Hole would change their
status to some form of extinction.
Salmon and steelhead: Do hatcheries cause
In many countries, large-scale fish culture, especially for
salmon and trout (Salmonidae), became established to miti-
gate for dams and to increase availability of desirable fish.
Much of this aquaculture was designed to support capture
fisheries by rearing fish through embryo and juvenile stages,
when mortality is highest, before releasing them into the
wild. This strategy has been enormously successful, with
high percentages of salmon and trout caught along the
Pacific Coast now being of hatchery origin. The problem
with hatchery fish is that they quickly become domesticated.
Christie and colleagues (2016) found that steelhead rainbow
trout (Oncorhynchus mykiss) showed genetic-based adapta-
tions to the hatchery environment after just one generation.
This problem has been overcome in part by releasing juve-
niles in increasingly large numbers into the wild to over-
come high postrelease mortality. Large numbers of hatchery
fish returning or straying impede and hybridize with wild
spawners, greatly reducing natural production and increas-
ing reliance on hatcheries. Bowlby and Gibson (2011) found
that hatcheries could thus reduce extinction probabilities in
Atlantic salmon (Salmo salar) populations in the short run
but make extinction more likely in the long run.
In California’s Sacramento–San Joaquin River basin, arti-
ficial propagation resulted in a genetically uniform popula-
tion of Central Valley (CV) steelhead, listed as a threatened
DPS under the ESA and treated as if it were a distinct lineage.
However, during the 1950s, CV steelhead were hybridized in
hatcheries with north-coast steelhead, another genetically
distinct lineage. These fish were brought in to “improve” the
fishery with larger fish, irrevocably altering allele frequen-
cies in all CV steelhead. To complicate things further, steel-
head and resident (nonmigratory) rainbow trout typically
have two distinct life history patterns within a single lineage.
Today, the Sacramento River and its tributaries support
populations of resident rainbow trout that are large enough
to support fisheries; these trout are genetically identical to
CV steelhead but rarely produce individuals that go to sea.
Most “true” steelhead (i.e., anadromous rainbow trout) in
the river are of hatchery origin because hatcheries select for
steelhead life history (Zimmerman and Reeves 2000). This
raises the questions: Are CV steelhead effectively extinct
(mitigated extinction, Ex4)? Is a return to an anadromous
population subject to natural selection possible? The answer
to the first question depends on continued defining of CV
steelhead as a separate lineage when the actual lineage con-
sists of both steelhead and resident trout, with different life
histories. The issue is made even more complicated because
a hybrid lineage has replaced the original lineage and is
quite successful as resident trout. Therefore, the answer to
the first question is that steelhead cannot be declared extinct
as a lineage because they are a life-history alternative, not
a lineage. The lineage to which they belong is in no danger
of extinction. The answer to the second question is yes,
because resident hybrid rainbow trout have the capacity to
genetically switch to the steelhead life history if conditions
are right in the river, estuary, and ocean (Zimmerman and
Reeves 2000, Hayes etal. 2012).
A better example of a hatchery-dependent (Ex4) lineage is
the Sacramento winter-run Chinook salmon (Oncorhynchus
tshawytscha). Listed as an ESU under the ESA, large num-
bers of these salmon are reared in a conservation hatchery.
Unlike production hatcheries used to support fisheries, con-
servation hatcheries are designed to produce wild-type fish,
using careful genetic monitoring to reduce domestication
(Winship etal. 2014). Shasta Dam on the Sacramento River
denies access to historical spawning grounds upstream,
so most of the population is maintained by the hatchery
and by spawning below the dam. Flows below the dam are
regulated by cold-water releases, and there is active gravel
augmentation to create spawning habitat. A recent drought
caused “natural” spawning to fail 2 years in a row, making
the population entirely reliant on the conservation hatchery.
Therefore, Sacramento winter-run Chinook salmon is a
good example of mitigated extinction (Ex4) that will require
continuous human intervention to maintain the lineage, if
on a somewhat different trajectory.
Overall, these examples suggest that hatcheries, which pro-
duce millions of salmon and steelhead each year in the Pacific
Northwest, have a major impact on the nature of regional
linages (ESUs, DPSs); this impact can lead to mitigated
extinctions (Ex4) in which lineages will have to be maintained
by artificial means in perpetuity. The release of millions of
hatchery salmonids into the rivers used by wild fish can
replace distinct wild lineages adapted for natural conditions
with lineages maintained through artificial selection. There is
considerable potential for such practices to ultimately lead to
global extinction (Ex6) of distinct salmonid lineages.
Delta smelt: Headed for extinction
The initial impetus for this article is the possible extinc-
tion of delta smelt, Hypomesus transpacificus. This small
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Overview Articles April 2017 / Vol. 67 No. 4 BioScience 365
planktivorous fish has a 1-year life cycle and is endemic
to the Sacramento–San Joaquin Delta, the central node for
much of California’s water-supply system (Moyle 2002).
Delta smelt is listed as an endangered species and in recent
years has nearly disappeared from both general and focused
fish surveys (Moyle etal. 2016). Extinction in the wild (Ex4)
or global extinction (Ex6) is likely in the near future and has
major implications for water management. However, mak-
ing the final determination with complete certainty will be
difficult because it is a small fish that can move up and down
the estuary and can have local resident populations. There
are two captive populations in which individuals are reared
through their entire life cycle, but they need a continual
influx of wild fish to maintain genetic diversity (Moyle etal.
2016). However, they are currently (as of 2016) not planted
in the wild. If delta smelt disappeared from all fish surveys,
by our criteria, a finding of wild extinction (Ex4) should
occur after 10 years. But consideration would then have to
be given to the two captive populations and their potential
for both domestication and reintroduction into the wild. As
the salmonid example illustrates, domestication can occur
very rapidly in fish (e.g., Lorenzen etal. 2012). Delta smelt
have a 1-year generation time, so the potential for successful
reintroduction into the wild will diminish with each pass-
ing year. If a reintroduction program allows some smelt to
complete their life cycle in the wild but reproductive success
is low and requires continuous input of hatchery-reared
fish, then the lineage will fit into the mitigated extinction
category (Ex1); however, it would be on a different evolu-
tionary trajectory from wild “natural” delta smelt, especially
if the wild population was too small to allow for capture of
individuals to supplement hatchery populations. If such a
program fails, delta smelt would then be considered globally
extinct (Ex6) after 10 years (although Ex4 designation might
be politically more acceptable if a domesticated population
continued to exist, displayed in public aquaria). Delta smelt
therefore illustrate how extinction criteria can help manag-
ers decide on management goals. What level of extinction is
The ongoing extinction crisis requires that extinction be
dealt with systematically, with priorities established for the
use of limited funds available to prevent global extinction
of distinct lineages. Lineages no longer subject to natural
selection in their native habitats can be regarded as suffer-
ing gray extinction, as can lineages dominated by artificial
selection. However, as lineages of hatchery salmonids illus-
trate, lineages totally dependent on aquaculture can persist
and replace natural lineages, at least visually and sometimes
in fisheries. Global (complete) extinction is often hard to
determine, especially in groups such as fishes, so guidelines
for the determination of such extinctions are needed, as
we propose here. Therefore, our decision tree allows for a
straightforward assessment of the extinction of any lineage
and represents a step in the right direction. Although we can
hope extinctions in freshwater fishes and other organisms
will be less than anticipated, this seems unlikely. It is there-
fore time to identify extinction in a more realistic manner.
JB was funded through a postdoctoral research fellowship
from the UC Davis Center for Watershed Sciences. We thank
the members of the Moyle Laboratory and many others who
listened to our presentations as ideas developed and gave us
welcome critiques and questions.
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Jason Baumsteiger ( is a postdoctoral research fel-
low at the Center for Watershed Services and Peter Moyle (pbmoyle@ucdavis.
edu) is a distinguished emeritus professor of the Department of Fish Wildlife
and Conservation Biology at the University of California, Davis. JB studies
the evolution of freshwater fishes using genetic or genomic approaches, and
PBM studies the ecology and conservation of freshwater and estuarine fishes.
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... Successful reintroduction could potentially place the lineage into the mitigated extinction category. Contrary to the legally identical status of wild and released laboratory-raised fish under a 10(a)1(A) permit, Baumsteiger and Moyle (2017) point out that a reliance on the FCCL would put the species "on a different evolutionary trajectory from wild 'natural' Delta Smelt, especially if the wild population was too small to allow for capture of individuals to supplement hatchery populations." The failure of such a program would eventually result in global extinction or extinction in the wild "if a domesticated population continued to exist, displayed in public aquaria" (p. ...
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... Defining an appropriate threshold below which populations are considered extinct or extirpated is a long-debated topic in the ecological community. Extinction has been defined variably, such as the threshold below which population declines result in changes to community function and stability, the population size leading to loss of other species in the community, or when reproductive failure occurs (Bull et al. 2009, Säterberg et al. 2013, Baumsteiger and Moyle 2017, all of which are further complicated in plant species by lag times between extinction events and loss of the last individual (Vellend et al. 2006, Cronk 2016. Because functional loss can occur before loss of the last individual, we chose to focus on functional extirpation. ...
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Climate change is transforming forest structure and function by altering the timing, frequency, intensity, and spatial extent of episodic disturbances. Wildland fire regimes in western U.S. coniferous forests are now characterized by longer fire seasons and greater frequency, with further changes expected. Identifying the impacts of altered fire regimes on forest resources may enable land managers to plan miti-gation strategies or prepare for novel or altered communities. We created a stochastic, density-dependent, matrix projection model for a whitebark pine (Pinus albicaulis) metapopulation to estimate the impacts of increasing fire frequency on metapopulation persistence. Whitebark pine is a widely distributed foundation species of management concern found in upper subalpine and tree line forests of the Northern Rocky Mountains. We parameterized the model using empirically based demographic data from the Greater Yel-lowstone Ecosystem (GYE) and validated the model by comparing observed whitebark pine densities to those projected by the model when parameterized with historical demographic rates and fire frequencies. We reparameterized the model with current demographic rates including mortality from insect outbreaks and exotic disease. We compared odds of functional extirpation among six scenarios comprising three altered fire frequencies (fires suppressed, historical fire return interval of 268 yr, and decreasing fire return intervals from current to 97 yr) and two seed dispersal probabilities. Historical parameterization with high dispersal probability projected median whitebark pine densities (40.95 trees/ha, first and third quartiles: 21.89, 67.25), which were similar to empirically estimated densities (40.62 trees/ha, first and third quartiles: 12.04, 114.15). Odds of functional extirpation with increasing fire frequency were 8.26 and 139.91 times higher than historical fire frequency and fire suppression, respectively. In decreasing fire return interval scenarios, odds of functional extirpation were 1.76 times higher in low than high dispersal probability scenarios. These findings suggest that fire suppression may be required to maintain whitebark pine metapop-ulations in the GYE and that maintaining stand networks connected by high rates of seed dispersal could increase metapopulation resiliency.
... In reality, most of the current recovery plans do not call for increase in numbers of individuals or numbers of populations and geographic range [9,10]. Several works are also performed [11,12,13,14] to discuss this important issue. The persistence time of the population for a dynamical system is obtained in [15,16] which can be used to find the time to extinction of a population. ...
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The extinction of different species from the earth is increasing at an alarming rate. So, assessment of probability of extinction of different important species in our ecosystem could help us to take proper conservation policy for those population whose chance of extinction is high. In this paper a method is developed to find the probability of extinction of populations in a general n-trophic food chain model under demographic stochasticity. The birth-death process is used to incorporate the demographic stochasticity and the necessary mathematical expressions are obtained. The theoretical finding is validated by numerical simulation for a two dimensional predator-prey system.
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Revisitation studies use historical information from literature or museum collections to assess rates of local extinction. However, revisitation studies suffer from the bias that they can only detect decline or stasis relative to the number of historical sites, as newly colonized sites are not detected. This drawback can be avoided with complete resurveys of study areas. We used 100‐year‐old historical information on 99 mountain plants from a 174 km2 area in Switzerland and performed a revisitation study and a complete resurvey. The resurvey was used to determine the magnitude of the bias of revisitation. In the revisitation study, we found an average loss of historical sites of plant species of 51.1% (SE = 3.4%). When sites newly observed in the resurvey were also considered and assumed to represent new colonizations, the average loss in sites declined to 26.8% (SE = 5.7%). However, if newly observed sites were treated as historically overlooked sites the loss of sites was only 45.7% (SE = 3.4%). Our results thus show that revisitation studies can overestimate local extinction, but that the corresponding bias depends on whether newly observed sites are considered as historically overlooked sites or as new colonizations. Revisitation studies using historical information from literature or museums to assess the rate of local extinction of species suffer from the bias that they can only find decline or stasis in the number of historical sites, while newly colonized sites are not detected. In a study also considering newly colonized sites we show that the bias of revisitation studies can be substantial.
Human life and other biotic organisms inhabiting Earth are endangered due to the vagaries of climate change, overexploitation and unsustainable use of natural resources like freshwater ecosystems, forests, genetic resources, wildlife and land use, etc. While emphasizing on the vitality of natural ecosystems and the goods and services accruing from them for human and other biotic organisms, focus is also reinforced on the conservation and sustainable use of natural resources to ward off adverse impacts of climate change and sustain the continuity of life cycle on Earth.
Cambridge Core - Natural Resource Management, Agriculture, Horticulture and forestry - Shepherding Nature - by J. Michael Scott
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Many plant species may already be functionally extinct
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This paper reviews what has been learned about Delta Smelt and its status since the publication of The State of Bay-Delta Science, 2008 (Healey et al. 2008). The Delta Smelt is endemic to the upper San Francisco Estuary. Much of its historic habitat is no longer available and remaining habitat is increasingly unable to sustain the population. As a listed species living in the central node of California's water supply system, Delta Smelt has been the focus of a large research effort to understand causes of decline and identify ways to recover the species. Since 2008, a remarkable record of innovative research on Delta Smelt has been achieved, which is summarized here. Unfortunately, research has not prevented the smelt's continued decline, which is the result of multiple, interacting factors. A major driver of decline is change to the Delta ecosystem from water exports, resulting in reduced outflows and high levels of entrainment in the large pumps of the South Delta. Invasions of alien species, encouraged by environmental change, have also played a contributing role in the decline. Severe drought effects have pushed Delta Smelt to record low levels in 2014-2015. The rapid decline of the species and failure of recovery efforts demonstrate an inability to manage the Delta for the "co-equal goals" of maintaining a healthy ecosystem and providing a reliable water supply for Californians. Diverse and substantial management actions are needed to preserve Delta Smelt.
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One of the most endangered vertebrates, the Devils Hole pupfish Cyprinodon diabolis, survives in a nearly impossible environment: a narrow subterranean fissure in the hottest desert on earth, Death Valley. This species became a conservation icon after a landmark 1976 US Supreme Court case affirming federal groundwater rights to its unique habitat. However, one outstanding question about this species remains unresolved: how long has diabolis persisted in this hellish environment? We used next-generation sequencing of over 13 000 loci to infer the demographic history of pupfishes in Death Valley. Instead of relicts isolated 2–3 Myr ago throughout repeated flooding of the entire region by inland seas as currently believed, we present evidence for frequent gene flow among Death Valley pupfish species and divergence after the most recent flooding 13 kyr ago. We estimate that Devils Hole was colonized by pupfish between 105 and 830 years ago, followed by genetic assimilation of pelvic fin loss and recent gene flow into neighbouring spring systems. Our results provide a new perspective on an iconic endangered species using the latest population genomic methods and support an emerging consensus that timescales for speciation are overestimated in many groups of rapidly evolving species. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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In the five years since we first reviewed the status of the world’s fishes (Moyle and Leidy 1992), there has been an explosion of new information on the conservation of aquatic organisms and their ecosystems. Notwithstanding this surge of interest, many aquatic ecosystems remain poorly understood because conservation biology remains primarily focused on the loss of biotic diversity in terrestrial environments. Loss of diversity in aquatic environments has received comparatively little attention, even though the physical, chemical, and biological degradation of aquatic environments is widely recognized as a major problem, usually in the context of the spread of human disease, loss of fisheries, or degraded water quality for drinking, irrigation, or recreation. Yet aquatic habitats support an extraordinary array of species, many of which are being lost as their habitats deteriorate.
Important theoretical concepts tend to resist satisfactory definition (cf. Stigler 1957). Such concepts are in the service of the expansive ambitions of the theories in which they occur, and must accordingly respond flexibly to the changing requirements for maintaining order in a changing intellectual empire. The term ‘evolution’ – obviously important in biology, but also in the physical and social sciences – provides a good illustration of this principle. A prominent biologist and author of a highly expansive treatise on biological evolution had the following to offer in his glossary:
The Devils Hole pupfish (Cyprinodon diabolis; DHP) is an icon of conservation biology. Isolated in a 50 m(2) pool (Devils Hole), DHP is one of the rarest vertebrate species known and an evolutionary anomaly, having survived in complete isolation for thousands of years. However, recent findings suggest DHP might be younger than commonly thought, potentially introduced to Devils Hole by humans in the past thousand years. As a result, the significance of DHP from an evolutionary and conservation perspective has been questioned. Here we present a high-resolution genomic analysis of DHP and two closely related species, with the goal of thoroughly examining the temporal divergence of DHP. To this end, we inferred the evolutionary history of DHP from multiple random genomic subsets and evaluated four historical scenarios using the multi-species coalescent. Our results provide substantial information regarding the evolutionary history of DHP. Genomic patterns of secondary contact present strong evidence that DHP were isolated in Devils Hole prior to 20 - 10 ka and the model best supported by geological history and known mutation rates predicts DHP diverged around 60 ka, approximately the same time Devils Hole opened to the surface. We make the novel prediction that DHP colonized and have survived in Devils Hole since the cavern opened and the two events (colonization and collapse of the cavern's roof) were caused by a common geologic event. Our results emphasize the power of evolutionary theory as a predictive framework and reaffirm DHP as an important evolutionary novelty, worthy of continued conservation and exploration. This article is protected by copyright. All rights reserved.
Resource competition between animals is influenced by a number of factors including the species, size and relative abundance of competing individuals. Stream-dwelling animals often experience variably available food resources, and some employ territorial behaviors to increase their access to food. We investigated the factors that affect dominance between resident, non-native brook trout and recolonizing juvenile coho salmon in the Elwha River, WA, USA, to see if brook trout are likely to disrupt coho salmon recolonization via interference competition. During dyadic laboratory feeding trials, we hypothesized that fish size, not species, would determine which individuals consumed the most food items, and that species would have no effect. We found that species, not size, played a significant role in dominance; coho salmon won 95% of trials, even when only 52% the length of their brook trout competitors. As the pairs of competing fish spent more time together during a trial sequence, coho salmon began to consume more food, and brook trout began to lose more, suggesting that the results of early trials influenced fish performance later. In group trials, we hypothesized that group composition and species would not influence fish foraging success. In single species groups, coho salmon consumed more than brook trout, but the ranges overlapped. Brook trout consumption remained constant through all treatments, but coho salmon consumed more food in treatments with fewer coho salmon, suggesting that coho salmon experienced more intra- than inter-specific competition and that brook trout do not pose a substantial challenge. Based on our results, we think it is unlikely that competition from brook trout will disrupt Elwha River recolonization by coho salmon.
For purposes of the Endangered Species Act (ESA), a "species' is defined to include "any distinct population segment of any species of vertebrates fish or wildlife which interbreeds when mature'. Federal agencies charged with carrying out the provisions of the ESA have struggled to develop a consistent approach for interpreting the term "distinct population segment'. This paper outlines such an approach and explains how it can be applied to ESA evaluations of anadromous Pacific salmonids. The following definition is proposed: a population (or group of populations) will be considered "distinct" (and hence a "species') for purposes of the ESA if it represents an evolutionarily significant unit (ESU) of the biological species. A population must satisfy two criteria to be considered an ESU: 1) it must be substantially reproductively isolated from other conspecific population units, and 2) it must represent an important component in the evolutionary legacy of the species. -from Author