1. Conservation Biology 55-437 Lecture 18 April 1, 2010 Case Study I

2. Black-footed ferret (Mustela nigripes) member of the weasel family 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.

3. 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 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.

4. Prairie dogs were targeted as pests because their burrows damaged farm implements and tractors. Historically, has been thought that burrows could harm livestock. Encroachment of development on habitat. Prairie dogs also appear to have suffered from introduction of diseases.

5. In 1964, small population discovered in S. Dakota Studied and in 1971 brought into captivity for captive rearing attempts. 1978 end of known ferret existence in wild. 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.

6. By 1985, black footed ferrets were limited to ~130 individuals in one population at Meteetsie, Wyoming. The other population (from South Dakota) had been placed in a captive breeding program without success. ( 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. 1985: Six additional ferrets captured from wild. Population low reached with N = 4 known wild survivors and 6 in captivity. During 1985-1986: No reproduction in captivity but 2 litters at Meeteetse. Decision made to capture all wild individuals bring them into captivity.

7. 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 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).

9. The population is growing and introductions of ferrets to sites in Wyoming (Shirley Basin – 228 ferrets over 1991-4), in South Dakota (90 ferrets) and one in southern Montana (78 ferrets) in 1994-5. In the Shirley Basin 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.

10. Since reintroductions in Wyoming and South Dakota, a number of additional 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.

11. 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) Location / Year introduced and population as of 2010

12. No ferrets have been observed in Canada since 1937. 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 reintroduction site, but are left unprotected should they move off site.

13. In 2007, Grenier et al. used demographic modeling to determine the keys to population persistence. They expected adult survivorship and long-term fertility were important. first year survival and early fertility were the keys. For conservation, that means long-term monitoring may not be necessary but need to maintain early survival and fertility. Dynamics of the Shirley Basin reintroduction:

14. African cheetah (Acinonyx jubatus): The cheetah was once found on 5 continents. At the turn of the 20 th century it occurred in both Africa and Asia). Today it is limited to Africa and a small population in Iran.

15. The historical distribution: The current distribution:

16. The cheetah population is estimated to have declined by 50% in abundance (to ~10,000 - 20,000) by the mid-1970s from the previous decade, largely as a result of habitat destruction and hunting by humans. Current population may now be between 1,500 and 25,000 individuals. There may be another contributing factor. In 1983, O‘Brien and colleagues reported that cheetahs had remarkably little genetic variation. 55 captive and wild-caught cheetahs derived from two separate populations were monomorphic at all 47 allozymes surveyed.

17. The cheetah had 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.

18. Patterns of low genetic diversity in cheetah are attributed to a severe population bottleneck (O’Brien 1983). This bottleneck may have followed decimation of the population by legal and illegal hunting by African cattle farmers about 100 cheetah generations ago. Merola (1994) compared the cheetah's genetic variability with that of other carnivores 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).

19. Could this low genetic diversity be affecting the population? Genetic theory predicts that inbreeding among members of small populations will reveal deleterious recessive alleles. Deleterious recessive alleles can manifest in: 1.High infant mortality 2.Lowered fecundity 3.Higher susceptibility to disease Are these effects witnessed in cheetahs?

20. Cheetah also experienced high infant mortality rates. O’Brien (1983) cited high infant mortality among captive individuals and noted that such mortality was consistent with effects of low genetic diversity. So, could this explain what is happening in the wild? High infant mortality

21. O’Brien et al. (1985) noted that infant mortality rates for inbred and non-inbred cheetah mating (in captivity) did not differ significantly, suggesting that inbreeding has no pronounced effect today (largely because strong effects were evident earlier) – i.e. genetic diversity was already low. High infant mortality

22. Kelley et al. (1998) radio-collared female cheetahs in the Serengeti and followed them as they traveled throughout their 800-km 2 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 High infant mortality

23. 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

24. 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 either sex is compromised. Lowered fecundity

25. Susceptibility to Disease O’Brien et al. (1985) cited a field study of disease sweeping through a successful felid breeding colony in Oregon. Within this colony, 60% of the captive cheetahs died from corona virus associated diseases. noted that this mortality rate was consistent with, but not proof positively a consequence of genetic uniformity.

26. Susceptibility to Disease Heeney et al. (1990) sampled captive and wild cheetah and found ~20 to 60% tested seropositive for a number of infectious agents. Shows variability in cheetah response to disease – some individuals can mount a response to exposure.

27. Merola (1994) concluded that the lack of breeding success and high infant mortality rates were due to poor captive breeding program procedures but may still be linked to homozygosity (maternal neglect, cannabalism: Simberloff 1988). 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. So, is low genetic diversity not a problem ?

28. 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 & daughter13 Dam & son 116.38 Sire & daughter 93.50 Sire & son 99.06 Sibs 121.00 Overall 90.66

29. May be a problem for some populations but are trumped by environmental and demographic problems. Genetic considerations typically impact on a slower time scale. For Namibian cheetahs, habitat conservation and promotion of natural dispersal and gene flow is critical to species conservation. habitat destruction has resulted in population densities of one cheetah per 6 km 2 rather than the old rate of 1 per 100 km 2 High densities facilitate transmission and spread of disease and 'focusing' of cheetah predators in the small reserves.

30. Northern Spotted Owl (S. occidentalis caurina): 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).

31. “If we have learned one thing about the influence of the Spotted Owl on wildlife conservation, it is that the solution to conserving a threatened species that is still relatively widespread is exceedingly complex.” --- Gutiérrez et al. 1995 --- Gutiérrez, R. J., A. B. Franklin and W. S. Lahaye. 1995. Spotted Owl (Strix occidentalis), The Birds of North America.

32. 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: The result of the conflict was the development of the Northwest Forest Plan to conserve diversity in northwest forests in general, as well as to protect the spotted owl.

33. Origins of 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.

34. Origins of Conflict Logging industry estimated that ~ 150,000 jobs would be lost because of logging reductions. In fact, the logging industry had been dwindling significantly due to loss of old-growth forest and protective legislation. Listing was implemented on June 23, 1990. Logging in national forests was stopped by court order in 1991.

35. 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/km 2, breeding pairs/km 2, young fledged/km 2, young fledged/km 2, and adult survival.

36. 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 lambda [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 dispropor- tionate to the abundance of this habitat type. 3.Habitat type selected by the owls has not changed in abundance. Answer: No, it has decreased.

37. 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.

38. 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:

39. A specific Northern Spotted Owl Recovery Plan was developed in 1992 by team of nonscientists. Plan specified de-listing criteria and formalized recovery strategies. The U.S. Federal Government took no action. Followed by series of alternative plans. -1994 Clinton’s Northwest Forest Plan Presently, ecosystem plan on federal lands being implemented. More Recent

40. What additional problems remain? 2007 USFWS considered owl still threatened but suggested that the cause had changed – invasion of habitat by barred owls. 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 resulted in a 44% reduction in the probability of spotted owl habitat loss. Owl populations continue to decline at ~ 4% / year.

41. What have we learned? Despite continued losses (~ 4% decline/year) Spotted Owl issue has been instrumental in facilitating additional learning in fields of: population genetics population dynamics metapopulation dynamics reserve design extinction and viability analyses

42. 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.

43. 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. Grenier, M.B. et al. Rapid population growth of a critically endangered carnivore. Science 317:779. Heeney, J.L. et al. 1990. Prevalence and implications of Feline Coronavirus infections of captive and free-ranging Cheetahs. Journal of Virology 64:1964-1972. Laurenson, M.K. et al. 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.

44. 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. et al. 1983. The cheetah is depauperate in genetic variation. Science 221:469-462. O'Brien, S.J. et al. 1985. Genetic basis for species vulnerability in the cheetah. Science 227:1428-1434. O'Brien, S.J. et al. 1987. East African cheetahs: evidence for two population bottlenecks? Proceedings of the National Academy of Science 84:508-511.

45. O'Brien, S.J. 1994. The cheetah's conservation controversy. Conservation Biology 8:1153-1155.