Case Studies I

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Case Studies I Black-footed ferret (Mustela
nigripes) This species is a member of the
weasel family that formerly occupied plains and
prairie habitat from Saskatchewan to Texas. It
was listed as threatened in the US in 1967 and
endangered in 1973. An initial recovery plan was
devised by the US Fish and Wildlife Service in
1978. By then, however, there were no known wild
black-footed ferrets.
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Decline of the species coincided with, and may
have been caused by, the tremendous decline
(90-95) in prairie dog abundance earlier this
century.  Prairie dogs are the primary (90) food
of black footed ferrets.  Prairie dogs were
targeted as pests because their burrows damaged
farm implements and tractors. Prairie dogs also
appear to have suffered from introduction of
Sylvatic plague and from canine distemper. These
diseases then affected ferrets.  
4

• Prairie Dogs are Considered Keystone Species
• are the primary (90) food of black footed
• ferrets, swift fox, the golden eagle, the
  badger,
• and the ferruginous hawk.
• species, such as the mountain plover and the
• burrowing owl rely on prairie dog burrows for
• nesting areas.
• grazing species such as bison, pronghorn and
• mule deer may prefer the vegetative conditions
  
• after prairie dogs have foraged through the
  area.

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In 1964, small population discovered in S.
Dakota. It was studied and brought into captivity
in 1971 for captive rearing attempts. Captive
breeding was a dismal failure. 1978 was the end
of known ferret existence in wild. The species
was re-discovered at a single site in Wyoming in
1981. A Species Survival Plan (SSP) was developed
based on captive propagation to eventually
re-release ferrets into the wild. A severe
decline in prairie dog abundance was evident by
1985, when ferrets were collected to begin the
captive propagation program.
6
By 1985, black footed ferrets were limited to
130 individuals in one population at Meteetsie,
Wyoming. Another re-discovered population (from
South Dakota) had been placed in a captive
breeding program without success. (this
population went extinct good conservation
biology?)  The Wyoming population was surveyed
but not captured. This population suffered after
plague was discovered among its prairie dog prey.
Six ferrets were captured for a captive breeding
program all died of canine distemper. Additional
collections of 6 and 12 animals were made for
captive breeding programs. 
7
The last known free-ranging individuals died from
distemper, resting the fate of the species in the
last 12 (eventually only 7) individuals in the
captive breeding program. Goals were quickly set
to maintain as much (90) genetic diversity as
possible for a minimum of 50 years.  Two litters
of kits were born in 1987. Since then 4800 kits
have been born in captivity (Grenier 2007). In
1988 the captive population was subdivided into
two isolated groups (to minimize chances of
catastrophic extinction of the species).
8
By the early 1990s the captive breeding program
was was producing gt100 kits annually at 6 captive
breeding sites (including the Toronto
zoo). Ferrets were reintroduced to southern
Wyoming in 1991 (228 ferrets over the period
1991-4). By 1992 some individuals (12) survived
the winter and reproduced successfully in the
wild.  Coyotes appeared to be the primary
predator and source of mortality, and survival
was only moderate (20-25 for 30 days).
9
The population is growing (slowly) and other
introductions of ferrets have also occurred (see
below). In the Shirley Basin (Wyoming) the
release was thought to be failing. By 1996 there
were lt25 ferrets remaining from the release, and
monitoring became sporadic. But then in 2003
there were 52, and continued increase found an
estimated 223 in 2007. In 2005 the estimated
ferret population in South Dakota was 400.
Verification of this estimate has not proved
easy.
10
Since reintroductions in Wyoming and South
Dakota, a number of successful reintroductions
have occurred 186 released beginning in 2001 in
northwest Colorado in January 2006 wild
reproduction found. Continuing releases in Aubrey
Valley, Arizona must have been successful. In
2005 14 ferrets were counted that must have been
born in the wild (no microchip marker). There are
four other active re-release sites (8, aiming for
10 in all) being monitored for success in the
U.S. and Mexico. The SSP calls for 10 populations
with 30 breeding adults in each. The species will
then be downgraded to threatened.
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Location / Year introduced and population as of
2010
1. Shirley Basin (1991 gt 30) 2. Conata
Basin/Badlands (1994 gt 30) 3. UL Bend Refuge
(1996 lt 30) 4. Aubrey Valley (1996 lt 30) 6.
Coyote Basin (2000 lt 30) 7. Cheyenne River
Reservation (2000 gt 30) 8. Wolf Creek (2000 lt
30) 9. 40-Complex (2000 lt 30) 10. Janos,
Chihuahua (2000 lt 30) 11. Rosebud Sioux
Reservation (2000 lt 30) 12. Lower Brule
Reservation (2006 lt 30) 13. Wind Cave National
Park (2007 lt 30) 14. Logan County (2007 lt 30)
15. Northern Cheyenne Reservation (2008 lt 30)
16. Espee Ranch (2008 lt 30)
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Dynamics of the Shirley Basin reintroduction
Grenier et al. used demographic modeling to
determine keys to observed growth. They expected,
as a mammal, adult survivorship and long-term
fertility were important. However, first year
survival and early fertility were the keys.
Success is indicated by an estimated ? 1.35.
Note the implication of this rapid growth for
bottleneck effects.
13
For conservation, that means long-term monitoring
may not be necessary. None have been observed in
Canada since 1937. The re-introduction sites are
a first example of the problem imposed by
political opposition. The re-introduced ferrets
are (in the language of the U.S. Endangered
Species legislation) a nonessential, experimental
population. Under this designation, the animals
are protected at the re-introduction site, but
are left unprotected should they move into a
farmer's field or a rancher's pastureland.
14
What are the genetic implications of
reintroduction? Among the possible effects on
re-introduced animals are disease exposure and
predation. In addition to the natural bottleneck
that led to reintroduction, the new population
can face a bottleneck, as well. The genetic
result of a bottleneck/re-introduction can
be founder effects genetic drift loss of
genetic variation ? inbreeding depression all
ele fixation decreased fitness ? increased
probability of local extinction
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• What tools/procedures can alleviate the genetic
  danger to black-footed ferrets?
• Translocation among isolated reintroduced
  populations.
• Augmentation (annually) of reintroduced
  populations that are not growing from captive
  breeding stocks. This is what was done.
• What evidence points to the need for one or both
  of these steps?
• Among the 3 reintroduced populations studied
  (South Dakota, Wyoming and Arizona), dynamics
  suggest that the Wyoming population was most in
  need (Wisely, et al. 2008).

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Descriptive genetic parameters for three
reintroduced populations of black-footed
ferrets Population n He SE
Ho SE A South Dakota 44 0.41
0.01 0.40 0.01 2.00 Wyoming
32 0.21 0.04 0.21 0.01 1.43
Arizona 31 0.34 0.02 0.28
0.01 2.14 Captive 78 0.37
0.01 0.38 0.01 2.00
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There was no evidence that either Arizona or
South Dakota populations had lost genetic
diversity. All alleles in the captive source
population were found present in the South Dakota
reintroduced population. The genetic diversity
was retained even after augmentation ended.
Exponential growth has apparently obviated any
bottleneck effects. Genetic diversity has been
retained in Arizona, as well. Apparently this is
due to continued augmentation, since growth has
been slow (minimal). A new mutant allele not
present in the source population has even
increased the mean number of alleles to be larger
than in the source.
18
Wyoming has apparently been subjected to an
extended (multiple generation) bottleneck. 4 of 7
loci studied have become fixed there. There was a
28 loss of allelic diversity. An extended period
at low numbers apparently led to drift, decreased
genetic diversity and increased inbreeding. There
was also morphological evidence of inbreeding
depression. Ferrets from Wyoming were
significantly smaller than those from either
Arizona or South Dakota, even though all
originated from the same captive source
population.
19
African cheetah (Acinonyx jubatus) The
cheetah was once found on 5 continents. At the
turn of the 20th century it occurred in both
Africa and Asia). Today it is limited to Africa
and a small population in Iran.
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The historical distribution
The current distribution
21
Recent estimates (Selebatso, et al. 2008) place
the total population of cheetahs at lt10,000
mature individuals, with lt1000 in each of the
extant subpopulations. The main prey for cheetahs
are impala, springbok, the young of large
antelopes, and only to a lesser extent farm
animals like goats and sheep. That has led to a
generally supportive atmosphere for cheetah
conservation, at least for the largest natural
population in Namibia. However,
22
The cheetah has the lowest frequency of
polymorphic loci (0.0) and lowest average
heterozygosity (0.0).  Overall, the cheetah had
between 10 and 100 times less genetic variability
than other mammals.
23
O'Brien attributed the patterns in cheetah to a
severe population bottleneck followed by
inbreeding.  The bottleneck would reduce genetic
diversity as a result of selection pressures and
genetic drift.  They attribute the bottleneck to
decimation of the population by legal and illegal
hunting by African cattle farmers about 100
cheetah generations ago. A low sperm count and
abnormal sperm is another evidence of a
bottleneck and inbreeding. In zoos non-inbred
cheetah mating had among the highest infant
mortality rates of all mammals surveyed.
24
As well, infant mortality rates for inbred and
non-inbred cheetah mating did not
differ significantly, suggesting that
inbreeding has no pronounced effect today
(largely because strong effects were evident
earlier).
25
Another evidence of the limited genetic diversity
among cheetahs comes from a study of skin grafts.
7 different skin grafts were performed on
non-inbred pairs of cheetahs (14 individuals).
Successful grafts depend on acceptance of 'donor'
tissue by the 'recipient' individual, which is
governed by a group of genes called the 'major
histocompatability complex' (MHC).  In all
vertebrates, the MHC is the most polymorphic
region of the genome, thus it should be most
useful in differentiating genetically different
individuals.  All of the grafts succeeded through
the typical stage of rejection, though control
grafts of house cat tissue were rejected.
26
A comparison of frequency of enzyme polymorphisms
and heterozygosity levels in subspecies of the
cheetah, the south African form A. jubatus
jubatus and its east African relative A. jubatus
raineyi found the genetic distance between
subspecies was minimal (0.004), indicating that
the cheetah became genetically impoverished
before the subspecies diverged.  These genetic
patterns are most consistent with 2 bottlenecks
(one 10,000 years ago and another during the past
century) followed by inbreeding. Conservation
genetics has moved past enzyme polymorphism into
DNA analysis, using microsatellites and MtDNA.
27
Menotti-Raymond and O'Brien (1993) used
hypervariable minisatellite loci and
mitochondrial loci to time the bottleneck in the
cheetah population. Based on expected mutation
rates and current levels of diversity, they back
calculated the bottlenecks to between 3500 -
12,700 years and 28,000 - 36,000 years,
respectively, for mitochondria and minisatellite
techniques. These techniques also identified only
1 to 10 of DNA diversity found among other
out-crossed cat species. OBrien and his
collaborators have become involved in controversy
over their conclusions about cheetahs.
28
Merola (1994) compared the cheetah's genetic
variability with that of other carnivorous
vertebrates. Of 24 terrestrial carnivores
surveyed, 8 had no heterozygosity (H 0), while
the remaining ones averaged H 0.042 (vs. H
0.014 for the cheetah).
29
Merola concluded stated that the lack of breeding
success and high infant mortality rates were due
to poor captive breeding program procedures, and
that the feline virus that decimated the Oregon
cheetahs was effective because the cheetahs were
held at very high density. She argued that as
long as recessive alleles (deleterious) were
slowly purged from the population, the resulting
population could be relatively homozygous but
without inbreeding effects. The inbreeding
effects observed in cheetahs would thus be an
artifact of the artificial captive breeding
environment.
30
More recent molecular genetics (Marker et al.
2008) indicate that there is limited genetic
variability and differentiation among cheetah
populations from Namibia, but that there is
panmixis across large areas. The distance between
captures of close relatives indicates how far
cheetahs may move Relationship Mean Distance
between captures (km) Dam daughter 13 Dam
son 116.38 Sire daughter
93.50 Sire son 99.06 Sibs
121.00 Overall 90.66
31
For Namibian cheetahs, habitat conservation and
promotion of natural dispersal and gene flow is
critical to species conservation. Merola also
acknowledged that the cheetah is suffering. From
her perspective, similarly, it is from a loss of
habitat and other adverse human effects. For
example, habitat destruction has resulted in
population densities of one cheetah per 6 km2
rather than the old rate of 1 per 100 km2. High
densities facilitate transmission and spread of
disease and 'focusing' of cheetah predators in
the small reserves.
32
A recent addition to the debate was demographic
modeling contributed by Crooks et al. (1998)
using published data from the Serengeti. The
importance of elevated cub mortality was
relatively minor relative to the large effects
from variation in adult survivorship. Demographica
lly, the adults have high reproductive value and
cubs low value. Any change in the adult
survivorship schedule has a much larger impact
than an equal change in cub survivorship (for
cheetahs). They argue that focusing on cub
mortality could obscure the importance of factors
producing even a small increase in adult
mortality. 
33
This conclusion, based on modeling, is also
controversial. How does this conclusion compare
with the result of demographic modeling for
black-footed ferrets? Recent matrix models of
cheetah population dynamics (Lubben et al. 2008)
suggest instead that small changes in the
survivorship of cubs could greatly enhance the
likelihood of population and species survival.
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High infant mortality

• Kelley et al. (1998) radio-collared female
  cheetahs in the Serengeti and followed them as
  they traveled throughout their 800-km2 home
  ranges. Identified birthing sites (lairs).
• Entered lairs when adults were away and counted
  young. Regular monitoring showed that young
  suffered from high mortality rates (80 ).
• Most mortality was predation related not
  genetic defects.

Kelley et al. 1998. Journal of Zoology
244473-488
35
Durant et al. (2007) reviewed information that
suggests cheetah behaviour and interaction with
lions explains demography in Serengeti
populations and is critical in their conservation
status. Cheetah males live in small social groups
(coalitions) that move over small defended
territories, while females move with cubs over
larger areas. They hunt away from the cubs for
short periods. The relative movements create
hotspots of cheetah population density. Cheetah
cub (and adult) survival is negatively correlated
with local lion density. Cheetah populations
undergo dangerous declines when they are in
high local density and in the vicinity of lions. 
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Lowered fecundity

• Reproduction in captivity is low as of 1986,
  only 17 of 108 females and 12 of 85 males had
  bred in zoos
• ( 84 of captive cheetah do not breed)
• Does this mirror natural conditions?

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Lowered fecundity

• Wild cheetahs are polyestrus, cycling every 12
  days with a gestation period of 93 days.
• For wild cheetahs, high numbers of females
  breeding and rapid rates of litter production
  suggest that the reproductive physiology of
  neither sex is compromised.

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Survival in an area (even the entire Serengeti,
an IUCN category II park including 14,000 km2, is
too small to maintain a minimum viable population
of cheetahs) is dependent on movement among
population groups (and so that populations may
grow in areas with low lion numbers) and access
to the antelopes they hunt outside the
Serengeti. Humans were also indicated as
important in cheetah declines. However, Durant et
al. report survey results that suggest the
farmers consider cheetahs far less important than
other large predators. It seems they are not
likely important to the declines in cheetahs.
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Northern Spotted Owl (S. occidentalis caurina)  
Northern Spotted Owls occur in the southwest
region of British Columbia and in Oregon and
Washington.  In all instances, the owl is rare
(low abundance) even in the best of habitats. 
In southwestern B.C., the owl was found at 14
sites, with a total population of as few as 100
individuals (Dunbar et al. 1991). They
attributed its rarity to habitat destruction
(logging, fires, development) and to Barred Owls
which live in the same old-growth habitat and
which respond aggressively to spotted owl calls
(thus potentially limiting its habitat
availability).
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In the USA, the northern spotted owl has pitted
environmentalists against loggers. The case was
resolved during summer 1995 by the
conservative- leaning Supreme Court  in favour of
preservation of essential lands for owl
habitat. Habitat loss in the U.S. has been
extensive
42
The result of the conflict was the development of
the Northwest Forest Plan Here is the history of
the conflict

• Historical practice of clearcut logging in
  Pacific Northwest.
• U.S.F.W.S. reviewed the status of the Northern
  Spotted Owl in 1982 and 1987 - concluded it did
  not warrant listing as threatened or endangered.
• Reviews in 1989 and 1990 proposed listing as a
  threatened species under the ESA. Loss of
  old-growth habitat was cited as the primary
  threat.
• Listing was implemented on June 23, 1990.
• Logging in national forests was stopped by court
  order in 1991.

43
Bart and Forsman (1992) and Bart (1995) looked at
spotted owl density and breeding success in
habitats of differing quality in Washington and
Oregon.  In sum, the higher the percentage of
old growth forest (good habitat), the higher the
owls/km2, breeding pairs/km2, young fledged/km2,
and adult survival. Figures showing you that
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• To provide clear answers to key questions about
  the spotted owl populations, Murphy and Noon
  (1992) formulated a number of important, testable
  hypotheses regarding the owl
• Is the owl population growing (is ? finite rate
  of growth gt1?  Answer No
• Do owls differentiate among forests of different
  ages or structures.  Answer Yes  The owls prefer
  habitats based  with old-growth forest
  dispropor-tionate to the abundance of  this
  habitat type.
• Habitat type selected by the owls has not changed
  in abundance.  Answer No, it has decreased.

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4. The probability of persistence is not related
to the extent of its geographic distribution. 
Answer It is. 5. There is a relationship between
HCA (habitat conservation area) size and its owl
carrying capacity. Answer Yes. 6. A relationship
exists between habitat fragmentation and
persistence likelihood of species using that
habitat landscape.  Answer Yes 7. Distance
between habitat patches has a bearing on
dispersal success of juvenile owls. Answer  Yes,
there is a very strong relationship.
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Probability of successful owl dispersal versus
distance between suitable habitat patches
Based on these answers, a map of suitable habitat
patches for spotted owl conservation was
constructed for Oregon and Washington
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What additional problems remain? Habitat
destruction is clearly key not just logging,
but forest fires. The late successional forest
areas most important to spotted owls also have
fuel conditions that make fires likely. Ager et
al. (2007) showed via modeling that treatment of
fuel conditions on relatively small proportions
(20) of old growth forest areas had a
disproportionate effect in reducing forest fire
likelihood (a 44 reduction).
50
In the last two years the draft management plan
that resulted has been criticized from all fronts
(Stokstad 2008). The forestry industry wants to
see less forest protected. They claim that the
barred owl is a much more serious
threat. Environmentalists claim not enough is
being protected. In the U.S. the spotted owl
population continues to decline by 3.7 per
year. A recent genetic analysis by the U.S.
Geological Survey suggests that there is now
evidence of loss of genetic variability
(decreased Ne) and inbreeding depression even
beyond the numerical decline.
51
Those losses are most severe in the Washington
Cascades and in southern Oregon Coast Range
populations (Funk, et al. 2008). The
survey results even mention the threat of the
spotted owl entering an extinction vortex.
Populations outlined in red are those in which
evidence of genetic loss is most evident from
study of a number of microsatellite loci.
52
Some suggest that the threat of forest fires is
so dire that forests need to be thinned to reduce
the risk of catastrophic damage. Politics
continues to play a major role. Many important
scientists refuse to take part in the Fish
Wildlife Services development of a final
management plan due to interference from the
Dept. of the Interior and Bureau of Land
Management. They forced inclusion of an option
2. That option reduced land set aside as spotted
owl habitat and increased flexibility in
permitting logging (particularly in Oregon). It
appears this conflict is headed back into the
courts!
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References Ager, A.A. et al. (2007) Modeling
wildfire risk to northern spotted owl (Strix
occidentalis caurina) habitat in Central Oregon,
U.S.A. Forest Ecol. Manag. 24645-56. Bart, J.
1995. Amount of suitable habitat and viability of
northern spotted owls. Conservation Biology
9943-946. Bart, J. and E.D. Forsman. 1992.
Dependence of northern spotted owls (Strix
occidentalis caurina), on old-growth forests in
the western USA. Biological Conservation
6295-100. Crooks, K.R., M.A. Sanjayan, D.F.
Doaks. 1998. New insights on cheetah conservation
through demographic modeling.  Conservation
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Status of Spotted Owl, Strix occidentalis, and
Barred Owl, Strix varia, in southwestern British
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Durant, S.M. et al. 2007. Relating long-term
studies to conservation practice the case of the
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May, R.M. 1995. The cheetah controversy. Nature
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O'Brien, S.J. 1994. The cheetah's conservation
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