Transcript Case Studies I: ferrets, cheetahs, spotted owl

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.
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.
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.
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.
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.
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).
By the early 1990s the captive breeding program was
was producing >100 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).
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 <25 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.
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.
Location / Year introduced and
population as of 2010
1. Shirley Basin (1991; > 30)
2. Conata Basin/Badlands (1994; > 30)
3. UL Bend Refuge (1996; < 30)
4. Aubrey Valley (1996; < 30)
6. Coyote Basin (2000; < 30)
7. Cheyenne River Reservation (2000; > 30)
8. Wolf Creek (2000; < 30)
9. 40-Complex (2000; < 30)
10. Janos, Chihuahua (2000; < 30)
11. Rosebud Sioux Reservation (2000; < 30)
12. Lower Brule Reservation (2006; < 30)
13. Wind Cave National Park (2007; < 30)
14. Logan County (2007; < 30)
15. Northern Cheyenne Reservation (2008; < 30)
16. Espee Ranch (2008; < 30)
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.
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 reintroduced 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.
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
allele fixation
decreased fitness  increased probability of
local extinction
What tools/procedures can alleviate the genetic danger
to black-footed ferrets?
1.Translocation among isolated reintroduced
populations.
2.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).
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
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.
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.
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.
The historical distribution:
The current distribution:
Recent estimates (Selebatso, et al. 2008) place the
total population of cheetahs at <10,000 mature
individuals, with <1000 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, …
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.
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 noninbred cheetah mating had among the highest infant
mortality rates of all mammals surveyed.
As well, infant mortality rates for inbred and noninbred cheetah
mating did not differ
significantly,
suggesting that
inbreeding has no
pronounced effect
today (largely
because strong effects
were evident earlier).
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.
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.
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.
O’Brien and his collaborators have become involved
in controversy over their conclusions about cheetahs.
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).
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.
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
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.
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.
Demographically, 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.
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.
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 244:473-488
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.
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?
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.
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.
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).
In the USA, the northern spotted owl has pitted
environmentalists against loggers. The case was
resolved during summer 1995 by the conservativeleaning Supreme Court in favour of preservation of
essential lands for owl habitat. Habitat loss in the U.S.
has been extensive:
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.
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:
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:
1.Is the owl population growing (is  [finite rate of
growth] >1? Answer: No
2.Do owls differentiate among forests of different
ages or structures. Answer: Yes The owls prefer
habitats based with old-growth forest disproportionate to the abundance of this habitat type.
3.Habitat type selected by the owls has not changed
in abundance. Answer: No, it has decreased.
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.
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:
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).
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.
Those losses are most severe in the Washington
Cascades and in southern Oregon Coast Range
populations (Funk, et al. 2008).
Populations outlined in red are
those in which evidence of
genetic loss is most evident
from study of a number of
microsatellite loci.
The survey results even mention the threat of the
spotted owl entering an extinction vortex.
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 Service’s 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!
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. 246:45-56.
Bart, J. 1995. Amount of suitable habitat and viability of northern spotted
owls. Conservation Biology 9:943-946.
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 62:95-100.
Crooks, K.R., M.A. Sanjayan, D.F. Doaks. 1998. New insights on
cheetah conservation through demographic modeling. Conservation
Biology 12: 889-895.
Dunbar, D.L. et al. 1991. Status of Spotted Owl, Strix occidentalis, and
Barred Owl, Strix varia, in southwestern British Columbia. Canadian
Field Naturalist 105:464-468.
Durant, S.M. et al. 2007. Relating long-term studies to conservation
practice: the case of the Serengeti Cheetah project. Conservation
Biology 21:602-611.
Funk, W.C., E.D. Forsman, T.D. Mullins and S.M. Haig. 2008. Genetics
show currect decline and Pleistocene expansion in Northern Spotted
Owls. U.S. Geological Survey Open-File Report 2008-1239, 12 p.
Grenier, M.B., D.B. McDonald and S.W. Buskirk. Rapid population
growth of a critically endangered carnivore. Science 317:779.
Laurenson, M.K., N. Wielebnowski and T.M. Caro. 1995. Extrinsic
factors and juvenile mortality in cheetahs. Conservation Biology
9:1329-1331.
Lubben, J. et al. 2008. Management recommendations based on matrix
projection models: The importance of considering biological limits.
Biological Conservation 141:517-523.
Marker, L.L. et al. 2008. Molecular genetic insights on Cheetah
(Acinonyx jubatus) ecology and conservation in Namibia. J. Heredity
99:2-13.
May, R.M. 1995. The cheetah controversy. Nature 374:309-310.
Menotti-Raymond, M. and S.J. O'Brien. 1993. Dating of the genetic
bottleneck of the African cheetah. Proceedings of the National
Academy of Science 90:3172-3176.
Merola, M. 1994. A reassessment of homozygosity and the case for
inbreeding depression in the cheetah, Acinonyx jubatus: implications for
conservation. Conservation Biology 8:961-971.
Murphy, D.D. and B.R. Noon. 1992. Integrating scientific methods with
habitat conservation planning: reserve design for northern spotted owls.
Ecological Applications 2:3-17.
O'Brien, S.J., D. Wildt, D. Goldman, C. Merril and M. Bush. 1983. The
cheetah is depauperate in genetic variation. Science 221:469-462.
O'Brien, S.J. and 9 others. 1985. Genetic basis for species vulnerability
in the cheetah. Science 227:1428-1434.
O'Brien, S.J. and 7 others. 1987. East African cheetahs: evidence for
two population bottlenecks? Proceedings of the National Academy of
Science 84:508-511.
O'Brien, S.J. 1994. The cheetah's conservation controversy.
Conservation Biology 8:1153-1155.
Stokstad, E. 2008. Spotted owl recovery plan flawed, Review panel
finds. Science 320:594-5.
Wisely, S.M., R.M. Santymire, T.M. Livieri, S.A. Mueting and J.
Howard. Genetic and phenotypic consequences of reintroduction
history in the black-footed ferret (Mustela nigripes). Conservation
Genetics 9:389-399.