The Caribou Conservation Conundrum
By Arthur T. Bergerud, PhD
It is assumed that an undisturbed animal community lives in a certain harmony . . . the balance of nature. The picture has the advantage of being an intelligible and apparently logical result of natural selection in producing the best possible world for each species. It has the disadvantage of being untrue.
—Charles Elton
Fifty Years of Research
Caribou or reindeer (Rangifer tarandus) are an Arctic and Subarctic species of deer found all around the world’s northernmost regions. There are two general groups: the tundra caribou that live in the far north in comparatively barren tundra habitat, and the woodland caribou that reside in northern forests.
Woodland caribou (Rangifer tarandus caribou)—a subspecies that is found primarily today in Canada but once was found in the North American boreal forest from Alaska to Newfoundland and Labrador, and as far south as New England, Idaho, and Washington—are now listed as “threatened” with some herds listed as “endangered.”1
Based on well over fifty years of research on woodland caribou, I can only conclude that the primary reason for their decline is increased predation from expanding wolf numbers. To reduce wolves to lower densities, we need the support of the general public, especially the environmentalists that are most concerned about the caribou. However, there are two huge problems in gaining public support: for decades, biologists and naturalists have argued that habitat determines animal numbers and that caribou are wilderness animals that cannot coexist with logging and industrialization. Secondarily, environmentalists and some biologists and naturalists have accepted the pseudoscientific myth that there is a balance of nature, a stable equilibrium between prey and predators, which prevents extinctions in the absence of anthropogenic factors (of, relating to, or resulting from the influence of human beings on nature). They argue that, if caribou are declining, it must be anthropogenic factors such as logging and human disturbance that are causing these declines.2
Predator-Prey Relationship Misconceptions
Fundamental to understanding predator-prey interactions is the debate whether ecological systems are structured from top down (predator-driven) or bottom-up (food-limited). This question has been debated since at least 19603 and has been rekindled with the introduction of wolves to Yellowstone National Park and Idaho in 1995–96 and with the rapid decline in recent years of woodland caribou across Canada.
The decline in woodland caribou, however, has been in progress since the early 1900s.4 Common early explanations were that the decline was the result of the loss of boreal forests from logging and the loss of the lichen’s ranges from forest fires and early settlements. That argument continues today.
Based on years of research that began in the 1950s in Newfoundland and Labrador, in 1974, I published that the decline of both woodland and barren-ground caribou resulted from increased predation, primarily from wolves, and not from a decrease in lichen pastures by fire and overgrazing of terrestrial lichen.5 My 1974 paper is now generally quoted by young caribou biologists as showing that the proximate cause (an act from which an injury results as a natural, direct, uninterrupted consequence and without which the injury would not have occurred) for the decline of caribou is wolf predation with the implication that the real reasons are anthropogenic factors such as logging that have upset the “balance of nature.” Many older wolf biologists still believe in the balance of nature concept, have helped indoctrinate the general public to that view, and still do not support management intrusion into natural systems.
Research Findings
To resolve the question of top-down or ground-up, I selected two study areas following all the controversy of the 1974 paper. For the experimental area, we chose an insular caribou herd on the Slate Islands in Lake Superior near Pukaskwa National Park, Ontario. Those islands had no terrestrial ground lichens and also no natural predators of caribou—i.e., no wolves, bears, lynx, or wolverines.
As the control population, we selected the caribou in Pukaskwa National Park (PNP), fifty kilometers distant. In the Park, there was a normal boreal fauna of wolves, bears, lynx, moose, and caribou and little anthropogenic disturbance. We compared the demography to these two populations over thirty years (1974–2004). On the Slates and in the absence of wolves, the population persisted for thirty years with the highest density of caribou in North America, up to ten caribou/km2 with numbers varying from 150 to six hundred animals. Total numbers were regulated by starvation from a shortage of summer foods, not lichens.6 The animals went into the winter too weak to survive, regardless of the abundance of winter forage. This density was a hundred times greater than the control herd in PNP where the density was 0.06 caribou per km2—a hundred times less than the Slate Islands. This original low density was due to the predation of wolves existing at eleven wolves per 1,000 km2. As the study continued, the PNP herd declined, and by 2009, only four caribou were left. The herd may now be extinct. It was clearly regulated top-down by predation and was favorably critiqued in the prestigious textbook Ecology 6th Edition, 2009, by Emeritus Professor Charles Krebs.
Near the end of our Slate Island study, a natural experiment occurred in 1994 when Lake Superior froze and two wolves crossed to the Slate Islands. We lost nearly all the calves born in 1994 and 1995, and in those two years, the wolves caused sufficient mortality of adult females to change the sex ratio from the nominal sex ratio of one male to two females (approximately 35 percent males) to 55 percent males, a decline of a hundred animals, mostly females. This mortality was replicated in 2003 and 2004 when another duo of wolves reached the islands and, again, the wolves killed nearly all the calves on the island.
Caribou Decline
In the 1970s, I researched the demography of mountain caribou in northern British Columbia and published three peer-reviewed papers in 1984, 1986, and 1987.7 The 1984 paper documented that 90 percent of the calves were killed each spring before the age of six months mostly by wolves and bears. The 1986 paper documented that the decline of caribou in British Columbia occurred when the moose population increased, which brought higher wolf populations to northern British Columbia. Additionally, we compared the recruitment and adult mortality of caribou for all herds in North America where wolf abundance had been measured (a sample size of 750,000 caribou). The wolf density where caribou mortality and recruitment were balanced for caribou [the stabilizing density (rS)] was 6.5 wolves/1,000 km2 [finite rate of increase (λ) = (1 percent adult mortality)/ (1 percent recruitment)]. When wolf densities were higher, caribou declined. With caribou, the stabilizing recruitment of calves to balance adult mortality should be 15 percent of the population, or twenty-five calves per one hundred females measured, when calves are ten to twelve months of age. The pregnancy rate in caribou is normally greater than 80 percent (eighty-plus calves per one hundred females).8 To maintain caribou populations, wolf numbers need to be below the densities of eight or less wolves/1,000 km2.9 In multi-ungulate systems, wolf densities are commonly fifteen to twenty-five wolves/1,000 km2.10
In the l980s, I joined Dr. John Elliott, regional fish and wildlife biologist in British Columbia, in studying the demography of caribou, moose, elk, and Stone’s sheep in northeastern British Columbia. At that time, all four species were in decline. As in the case of the Ontario studies, we had control and experimental areas replicated in two separate regions: the Kechika region (18,400 km2) and the Muskwa region (19,000 km2). The two control replications were left undisturbed, and in the two experimental areas, we removed wolves—Kechika: 492 wolves in four years, and Muskwa: 505 wolves in three years. The grizzly bear and wolverine populations were left undisturbed. The study was ten years in duration.11
In the paper, we showed that in the areas where we reduced wolves, recruitment was greatly increased based on calves per one hundred females at six months to twelve months. For moose, recruitment averaged forty calves per one hundred females; elk, forty-nine per one hundred females; Stone’s sheep, forty-one per one hundred females; and caribou, thirty-nine per one hundred females. For those herds with no wolves removed, the recruitment was moose, eleven calves per one hundred females; sheep, twenty per one hundred; elk twenty-six per one hundred; and caribou, seven per one hundred. The elk and moose populations in this study that had wolf management increased from eighteen thousand to thirty-three thousand. In all removals, wolves were harvested in the spring before wolf denning, and in all years, young wolves were already dispersing into the removal area but insufficiently organized for denning so that the four prey species secured positive recruitment. At the end of the ten years, the wolf population was a healthy twenty-plus wolves per one thousand km2.
In the other areas in the North where wolves have been managed, the percentage of calves before and after wolf reductions were as follows: Nelchina herd, Alaska, 1960s, 24 percent vs. 40 percent; Forty Mile herd, Alaska, 1970s, 5 percent vs. 31 percent; Delta Herd, Alaska, 1 to 9 percent vs. 25 percent; and Beverly Herd, Northwest Territory, 1960s, 7 to 8 percent vs. 20 to 25 percent.12
The Predator Pit
The last study I wish to mention is the George River caribou herd in northern Quebec and Labrador. I counted the herd in 1958 at fifteen thousand animals. In 1958, there were no wolves; hunters that had been going in the country for decades had seen practically none on the land. The wolverine had also gone extinct. Starting in 1958, the herd increased yearly, reaching three hundred thousand by 1980.
In the 1970s, wolves reappeared and increased as the herd grew. By 1980, the wolves finally reached sufficient numbers that their predation halted the growth of the herd (recruitment equaled adult mortality). Then in 1981 and 1982, the wolves got rabies and declined by 80 percent. The caribou herd exploded with numbers reaching 537,000 by 1985 and 650,000 by 1987, the largest herd in the world at that time. The herd started to decline in 1988 when densities reached ten per km2, similar to the density that resulted in decline on the Slate Islands. However, unlike the Slate Islands, there was no winter starvation. In the George River herd, the females died in the summer from malnourishment with lactation problems and insect attacks with the result that pregnancy rates declined.13 In addition, wolf predation continued as did hunting, which was unabated. The herd reached seventy-four thousand in 2010, well within the carrying capacity of forage, but it is continuing to decline from heavy predation of calves and adults. The herd is now in what some biologists call “the predator pit,” which means that each time the herd starts to recover, the predation intensifies, and the herd remains limited.
The herd could be turned around now and started back up if wolves were managed, but in Canada, there has been little or no wolf management in recent decades. The herd will continue down until the wolves go elsewhere; that was what happened in the decline in the 1890s, from a high of seven hundred thousand to the fifteen thousand I counted in 1958. If the herd was managed now at seventy-four thousand, it could increase rapidly as did the Western Arctic herd in the 1970s. That herd had declined from 242,000 in 1970 down to seventy-five thousand by 1976. Then Alaska Fish and Game took over, and the harvest was drastically curtailed with the natives fully cooperating, and predators were managed. With wolves managed, the herd was back to 113,000 by 1979 and continued higher.14
Support of the Population
The only wildlife agency in North America that manages wolf numbers as a standard practice is in Alaska. This management has the support of the majority of the population in a system where the populace commonly depends on moose and caribou as subsistence food.15 This dependence is protected under both state (state subsistence statue) and federal (Alaska National Interest Lands Conservation Act—ANILCA) and is in agreement with the National Research Council 1997 standards.16 There has been some sporadic management of wolves in Alberta and of coyotes and bears on the Gaspe Peninsula—150 animals are left at this time. Recently British Columbia had planned to manage wolves for their remaining endangered arboreal caribou (less than fourteen hundred), but environmental groups thought the high abundance of wolves was more valuable than the last remaining arboreal caribou and forced the government to cancel the management.17
Going Extinct
Species around the world are going extinct. In Africa, many endemic species are declining from poaching and predation, and population numbers of predators themselves are decreasing, especially the large cats (tigers, cheetahs, and lions).18 But in North America, wolves are prospering, spreading across the western United States from the Yellowstone and Idaho introductions and increasing in Canada as their prey base of moose and deer expand with climate change.
In 1992 or 1993, I received a questionnaire from a polling company apparently under contract to the US Fish and Wildlife Service (USFWS), asking how wolf introduction to Yellowstone Park would impact the other species and the vegetation in the Park. The participants of this poll became known as the Delphi Committee, which was made up of ungulate and wolf biologists. It was an anonymous committee. I still do not know who else took part, but I believe it was weighted to pro-wolf biologists.
Based on our research in northern British Columbia, I predicted a major decline in elk and moose if wolves were introduced. My major comment was that, if the introduction went ahead, the wolves would have to be managed in Yellowstone Park and prevented from spreading beyond the Park. Well of course, there was no intention to manage wolves; they have now reached California and Colorado, and Utah is trying to hold the line. The Northern Yellowstone elk herd in the Park is mostly gone—from twenty thousand in 1994 prior to the wolf relocation, to 4,635 in 2011—and elk hunters may have seen the end of their hunting in that area. Animal rights activists and anti-hunting organizations have won.
I couldn’t believe USFWS would introduce wolves to Idaho where the last caribou herd was classified as endangered (the Selkirk herd), but they did, and the wolves are now hunting these last caribou. An even more unethical act, the USFWS is adding an additional area of 152,000 hectares (61,538 acres) to the preserve surrounding the herd that is off-limits to the local residents. The caribou do not need this additional land grant. They need predator control of the mountain lions and now the introduced wolves, but there will be none by the USFWS. Lion predation has been a problem in the past.
Patrick Valkenburg, a caribou biologist, emailed me stating: “With 300 million people in the United States now, is it realistic to just let ‘wolves do their thing’? Wolves belong in the boreal forest, not the Great Plains and the Great Basin where there are no longer any buffalo. Perhaps the USFWS did not know.”
Some older wolf biologists—Dr. Victor Van Ballenberghe, Dr. James Peek, Dr. John Theberge, and Dr. Paul Paquet—are emotionally involved with wolves and do not want to see wolves managed. I can relate to an emotional involvement relative to caribou. There is nothing more heart rending than watching a female caribou that has had her calf so completely eaten by a wolf or bear that there is not even any scent left. She does not understand that her calf is dead, and will stand and look and then go back to the last undisturbed location where they were together, and then finally back to the birth site. I have seen a female travel up a long line of cows and calves, scenting each calf, seeking recognition of her lost progeny. Some cows will stay near the remains of their dead calves for many days, waiting for them to get up and guarding the carcass from the lynx that often monitor attack and kill sites.19 Such cows can be called close by imitating calf bleating.
However, such emotional views will not help us manage the moose-caribou-wolf system. Those wolf biologists that have elevated the wolf to icon status have done a disservice to wildlife management in fostering the balance of nature myth. In contrast, coyote biologists have remained unattached and objective, relating the damage to livestock and the dangers of these animals in cities to small children and pets.
Balance of Nature
Charles Elton—the father of ecology, who discovered the three- to four-year cycle and the ten-year cycle of mammals and who wrote the first ecology book, Animal Ecology and Evolution, in 1927—told us at the beginning:
It is assumed that an undisturbed animal community lives in a certain harmony . . . the balance of nature. The picture has the advantage of being an intelligible and apparently logical result of natural selection in producing the best possible world for each species. It has the disadvantage of being untrue.20
In recent years, three widely respected biologists in Canada have concluded that woodland caribou are endangered from the increasing wolf population triggered by the increase in the moose and deer prey base with climate warming: Professor Emeritus Charles J. Krebs, Professor Emeritus A. R. E. Sinclair, and Professor Emeritus Valerius Geist.21 These men are the leading ecologists in Canada.
The most respected wolf biologist in the world is Dr. L. David Mech. In his 1996 monograph The Wolves of Isle Royale, he used the words “stable equilibrium” to describe moose-wolf interactions (“stable equilibrium” is a synonym for the “balance of nature”).
In later years, the balance completely disappeared.22 Mech accepted this disproof, stating in 1998: “The Isle Royale moose and wolf populations have fluctuated greatly over time, and there is little correlation between wolf and moose numbers in any given year.”23
From 1986 to 1994, Mech and his students studied the Denali caribou herd in Alaska.24 In The Wolves of Denali, Mech states: “The Denali wolf-caribou relationship is a good illustration of the dynamics of populations and why stability or balance at a variety of levels should not be considered inherent in natural systems.”25
Good scientists try to disprove their own hypotheses, and this is what he has done. This is significant because Mech, with his decades of study and publications about wolves, unintentionally has contributed probably more than any other scientist to furthering the pseudoscientific myth—the balance of nature.
Woodland caribou survived the Pleistocene epoch, more commonly known as the Ice Age, in the Appalachian Mountains, spacing themselves away from the large predators of the megafauna living at lower elevations. These caribou lived with a completely different set of species than they do today; i.e., sloths, peccaries, tapers, and austral faunal elements. In Science, Graham and associates stated that the fossil mammal fauna of the Late Quaternary at 2,945 fossil sites supported the Gleasonian community model, which assumes that species respond to environmental changes in accordance to their individual tolerances with varying rates of range shift.26 They stated, “Modern community patterns emerged only in the last few thousand years, and many late Pleistocene communities do not have modern analogs.”27 Those who say caribou and wolves evolved together for hundreds of eons have not checked the fossil record.
Each species, through individual selection, evolves its own distinct behavior-habitat strategies to persist, but that does not guarantee continual survival. Each species walks its own road down through time—there is no magical balance of nature. An article by Elisa Beninca and associates28 in the prestigious journal Nature stated: “Advanced mathematical techniques proved indisputable presence of chaos in this food web; short-term prediction is possible, but long-term prediction is not.”
Critical Habitat
In Canada, when animal species are classified as “endangered,” the federal government requests that the provinces involved develop a management plan for the species in danger of extinction, and they require that critical habitat be identified. For barren ground caribou, it is generally accepted that the calving grounds are the critical habitat. However, some still do not recognize the key element of that habitat is reduced predation risk and not forage.29 The critical habitat for montane and boreal woodland is the areas where the cows calve and where there is reduced risk for newborns.30 The montane caribou calve on alpine peaks spaced away from moose and wolves at lower elevations, and the boreal caribou calve on the islands, shoreline, and muskegs of the boreal forest.31 The critical habitat is not the winter ranges where boreal woodland caribou seek lichens. They adapted long ago to rotating their winter ranges in response to lichen destructions by forest fires and over-utilization.32 However, for the montane caribou, the old-growth high alpine forests with their lichen loads and protective deep snow that serves as a barrier to wolves are the critical habitats. In British Columbia, 2.2 million hectares (890,688 acres) of old-growth forest are protected from industrial forestry activity, sufficient for the present low population of the remaining fourteen hundred animals.
The Canadian Parks and Wilderness Society (CPAWS) in February 2012 delivered a petition of thirty-two thousand signatures to the Environmental Minister to save woodland caribou by protecting their boreal habitat from industrialization. The World Wildlife Fund’s solution to the caribou conservation conundrum is to create more parks.33 None of these efforts will save the caribou. The boreal ecosystem is structured from the top down by predation. The boreal forest can be logged if the calving habitat is left undisturbed and if the wolf population is managed to the same levels as in Alaska, fewer than 6.5 wolves per 1,000 km2.34
Mistaken Beliefs
Some believe that caribou are wilderness animals, cannot tolerate anthropogenic35 disturbance, and cannot tolerate the presence of man.36 These are mistaken beliefs. Two biologists who hold this belief—Schaeffer and Vors—are modelers with very little experience studying the behavior of caribou on the ground. I’ve been on the calving grounds studying calving behavior for thirty-three years in five provinces, as well as the Northwest Territory and Alaska. In addition, I’ve established thirteen herds and maintained a captive herd for several years. There are numerous examples of caribou adapting to the presence of man. For example, caribou have wintered at the Armstrong Airport in Ontario for the past thirty-seven years so they can avoid the presence of wolves. In Alaska, the caribou have calved for decades in the Prudhoe Bay oil field, the herd increasing from five to thirty thousand animals in the absence of wolves and bears.
Skeptics should Google “Slate Island caribou” and see pictures of the caribou, visiting occupied campgrounds and seeking handouts and the ashes in the fire pits. Caribou adapt well to the presence of benign humans and have been domesticated by the reindeer herders in Eurasia.
In contrast, the caribou are now extinct due to predation in the Canadian National Parks of Banff, Glacier, and Revelstoke, where there is no logging, and anthropogenic disturbances are minimal.37 The arboreal caribou in British Columbia are facing extinction from predation in the protected habitat set aside for them. Wittmer showed that old-growth forest with arboreal lichens was adequate for the herd.38 There are possibly only three or four caribou left in Pukaskwa National Park, and wolf predation is the cause that stark decline.39 The woodland caribou in Newfoundland from 1970 to 1996 increased from 7,000 to 96,000 animals.40 These were years of intense anthropogenic disturbance: logging near calving grounds, roads built across the caribou habitat, lakes and rivers dammed, and increased mining—yet the caribou were able to increase, despite all this disturbance, because wolves had been extinct for several decades in Newfoundland.41
The Caribou-Moose-Wolf System
Woodland caribou spent the Pleistocene42 south of the Laurentide ice sheet in the Appalachian Mountains, spaced away from the megafauna at lower elevations.43 They left the mountains 13,000 to 12,000 BCE and reached Ontario at 10,000 BCE, passing through deciduous forests. Fossils have been found near Udora, Ontario, 10,500 BCE,46 and near Atikokan, Ontario, 9,940 BCE.45 The caribou were blocked going farther north by the ice sheet and, through time, evolved the anti-predator tactics of using islands and shorelines to calve where they could escape wolves by swimming.
A second segment of the Appalachian caribou gene pool moved though Maine and New Brunswick following the shore around the ice at about 9,000 BCE and turned north in tundra where forests were delayed by the cold temperature of the Labrador current. They reached Indian House Lake at 7,000 BCE, as did the Paleo Indians.46 This population became the “barren ground” race, the George River Herd. Wolves must have followed these two separate lines, but fossils have not been found (the acid soils of the Canadian Shield erodes fossils).
Moose did not reach the boreal forest until the end of Little Ice Age, 1,850 to 10,000 years later than the caribou. The caribou had persisted in the boreal forest with the single wolf prey system for ten thousand years. However, the arrival of moose signaled the decline of caribou,47 as moose provided the biomass to sustain much higher population of wolves. Biologists like Fuller calculate wolf numbers based on the total ungulate prey biomass weighted as follows: moose at six, elk at five, caribou at three, and deer at two.48 Moose provided the biomass for many more wolves than were provided previously with the single-prey system of caribou. Switchover by predators between prey species is well recognized and researched in biology. In the boreal forest with a two-prey system of moose and caribou, wolves commonly switch over to the caribou that are easier to kill than moose, which may stand and fight, but the large biomass of the moose is what maintains the higher wolf population.49 This results in inverse density dependence mortality—the Allee Effect—50and this generally leads to extinction unless safe refuges exist, like islands.51
Now we have a warming climate and more moose and deer than ever that are expanding farther north.52 The increased predation from wolves is causing the extinction of caribou along the southern edge of their range. Moose have now reached the Arctic Ocean coast.
Caribou can only cope with wolves in densities of six to eight per one thousand km2—this then is a species diversity problem for caribou, which generally do not have a shortage of forage. If wolf populations were managed, we could have caribou densities of greater than two per km2, but because of the Allee Effect, caribou can only persist by being rare—densities commonly of only 0.06 per km2.53 The only reason caribou cannot exist in logged areas with their abundance of deciduous forage is the greater abundance of moose supporting more wolves. The sequence is
settlement + climate change
= more deciduous forage = more moose = more wolves = more predation on caribou = more extinctions
In Ontario, the extinction line north for caribou has only halted because of the safety of islands in several large lakes in two provincial parks and Lake Nipigon.
Conclusion
Environmentalists are contributing more to the extinction of caribou than anyone else is. Fish and game departments are not going to manage wolves without the support of the public, especially the vocal environmentalists. Environmentalists, as well as some biologists, are always blaming anthropogenic factors for declines in caribou like roads, seismic lines, pipelines, logging, etc. They say that such disruptions actually assist wolves in locating caribou. To the contrary, caribou have gone extinct in national parks, large parks that have not been logged, and where roads are minimal, due to predation. The supposed anthropogenic disturbances are absent, and the supposed effect persistence is also absent—the cause is not necessary.54 Caribou have persisted since the Ice Age in a simple one-prey primary predator system and continue to persist with climate change and increased species diversity. The bottom line is that wolves or the alternate prey species (moose and deer) will have to be managed if caribou are to survive.
1. COSEWIC (Committee on the Status of Endangered Wildlife in Canada) Report, 2002. [COSEWIC is a committee of experts that assesses and designates which wildlife species are in some danger of disappearing from Canada.]
2. Schaefer, J.A., “Long Term Recession and Persistence of Caribou in the Taiga,” Conservation Biology, 2003, 17: 1435–1439; Vors, L.S., J.A. Schaefer, B.A. Pond, A.R. Rodgers, and B.R. Patterson, “Woodland Caribou Extirpation and Anthropogenic Landscape Disturbance in Ontario,” Journal of Wildlife Management, 2007, 71:1249–1256.
3. Hairston, N.G., F.E. Smith, and L.B. Slobodkin, “Community Structure, Population Control and Competition,” American Naturalist, 1960, 194:421–425.
4. Cringan, A.T., “Some Aspects of the Biology of Caribou and a Study of the Woodland Caribou Range on the Slate Islands, Lake Superior, Ontario,” Master’s Thesis, 1957, University of Toronto, Toronto, Ontario, Canada.
5. Bergerud, A.T, “The Decline of Caribou in North America Following Settlement,” Journal of Wildlife Management, 1974, 38: 757–770.
6. Bergerud, A.T., W.J. Dalton, H.E. Butler, L. Camps, and R. Ferguson, “Woodland Caribou Persistence and Extirpation in Relic Populations on Lake Superior,” Rangifer, Special Issue, 2007, 17: 57–78.
7. Bergerud, A.T., H.E. Butler, and D.R. Miller, “Anti-Predator Tactics of Calving Caribou: Dispersion in Mountains,” Canadian Journal of Zoology, 1984, 62:566–575; Bergerud, A.T. and J.P. Elliott, “Dynamics of Caribou and Wolves in Northern British Columbia,” Canadian Journal of Zoology, 1986, 64: 1515–1529; Bergerud, A.T. and R.E. Page, “Displacement and Dispersion of Parturient Caribou as Calving Tactics,” Canadian Journal of Zoology, 1987, 65: 1597–1606.
8. Bergerud, A.T., “A Review of the Population Dynamics of Caribou and Wild Reindeer in North America,” 1980, pp. 556–581 (in “Proceedings of 22nd International Reindeer/Caribou Symposium,” Edited by E. Reimers, E. Gaare, and S. Skjenneberg, Roros, Norway, 17–21 September, 1980).
9. Bergerud, A.T. and J.P. Elliott, “Dynamics of Caribou and Wolves in Northern British Columbia,” Canadian Journal of Zoology, 1986, 64: 1515–1529; Thomas, D.C., 1995. “A Review of Wolf-Caribou Relationships and Conservation Implications in Canada,” pp. 261–273 (in L.N. Carbyn, S.H. Fritts, and D.R. Seip, editors, Ecology and Conservation of Wolves in a Changing World, Canadian Circumpolar Institute, Edmonton, Alberta, Canada); Lessard, R.B., “Conservation of Woodland Caribou in West-Central Alberta: A Simulation Analysis of Multi-Species Predator-Prey Systems,” Ph.D. Thesis, 2005, University of Alberta, Edmonton, Alberta, Canada.
10. Messier, F., “Ungulate Population Models with Predation: A Case Study with the North American Moose,” Ecology, 1994, 75: 478–488.
11. Bergerud, A.T. and J.P. Elliott, “Wolf Predation in a Multiple-Ungulate System in Northern British Columbia,” Canadian Journal of Zoology, 1998, 76: 1,51–1,569.
12. Bergerud, A.T. and J.P. Elliott, “Dynamics of Caribou and Wolves in Northern British Columbia,” Canadian Journal of Zoology, 1986, 64: 1515–1529.
13. Bergerud, A.T., S.N. Luttich, and L. Camps, The Return of Caribou to Ungava, 2008, McGill and Queens University Press, Montreal, Quebec, Canada.
14. Davis, J.L., P. Valenburg, and H.V. Reynolds, “Population Dynamics of Alaska’s Western Arctic Caribou Herd,” in “Proceedings of 22nd International Reindeer/Caribou Symposium,” Edited by E. Reimers, E. Gaare, and S. Skjenneberg, Roros, Norway, 17–21 September, 1980.
15. Titus, K., “Intensive Management of Wolves and Ungulates in Alaska,” 72nd North American Wildlife and Natural Resources Conference, 2007, pp. 366–377.
16. Regelin, W.L., P. Valkenburg, and R.D. Boertje, “Management of Large Predators in Alaska,” Wildlife Biology in Practice, 2005, 1: 77–85.
17. Wittmer, H.U., A.R.E. Sinclair, and B.N. McLellan, “The Role of Predation in the Decline and Extirpation of Woodland Caribou,” Oecologia, 2005, 144: 257–267.
18. Sinclair, A.R., E. Pech, R.P. Dickman, C.R. Hik, S. Hik, P. Mahon, and A.E. Newsome, “Predicting Effects of Predation on Conservation of Endangered Prey,” Conservation Biology, 1998, 12: 564–574.
19. Bergerud, A.T., “The Population Dynamics of Newfoundland Caribou,” Wildlife Monograph, 1971, 25.
20. Elton, C., Animal Ecology, Macmillan, London, Sidgwick, and Jackson, 1927.
21. Krebs, Charles J., Professor Emeritus, Ecology: 6th edition, 2009, pp. 197–198; Sinclair, A.R.E., Professor Emeritus, co-author (with H.U. Wittmer and B.N. McLellan), “The Role of Predation in the Decline and Extirpation of Woodland Caribou,” Oecologia, 2005, 144: 257–267; Geist, Valerius, Professor Emeritus, The Deer of the World: Their Evolution, Behavior and Ecology, Mechanicsburg, Pennsylvania: Stackpole Books, 1998.
22. Peterson, R.O., “Wolf Ecology and Prey Relationship on Isle Royale,” Science Monograph Series No. 11, US National Park Service, 1977; McLaren, B.E., and R.O. Peterson, “Wolves, Moose, and Tree Rings on Isle Royale,” Science 266, 1994, 1,555–1,558.
23. Mech, L.D., L.C. Adams, T.J. Meier, J.W. Burch, and D. Dale, The Wolves of Denali, Minneapolis, Minnesota: University of Minnesota Press, 1998.
24. Ibid.
25. Pimm, S.L., The Balance of Nature: Ecological Issues in the Conservation of Species and Communities (Chicago: University Chicago Press) 1991.
26. Graham, R.W. et al., “Spatial Response of Mammals to Late Quaternary Environmental Fluctuations.” Science 272, 1996, 601–606.
27. Past 0.5 to 1.0 million years.
28. Benincà, Elisa, et al., “Chaos in a Long-Term Experiment with a Plankton Community,” Nature, February 14, 2008.
29. Bergerud, A.T., S.N. Luttich, and L. Camps, The Return of Caribou to Ungava, McGill and Queens University Press, Montreal, Quebec, Canada, 2008.
30. Montane means of mountains and other high-elevation regions; Boreal means of or relating to the forest areas of the Northern Temperate Zone.
31. Simkin, D.W., “A Preliminary Report of the Woodland Caribou Study in Ontario,” Department of Lands and Forest, Section Report No. 59, 1965; Shoesmith, M.W. and D.R. Storey, “Movements and Associated Behavior of Woodland Caribou in Central Manitoba,” Proceedings of International Congress of Game Biologists, 1977, 13: 51–65; Hatler, D.F., “Studies of Radio-Collared Caribou in the Spatsizi Wilderness Park Area,” Smithers: British Columbia Spatsizi Association for Biological Research, 1986; Edmonds, E, J., “Population Status, Distribution, and Movements of Woodland Caribou in West-Central Alberta,” Canadian Journal of Zoology, 1988, 66: 817–826.
32. Bergerud, A.T, “The Decline of Caribou in North America Following Settlement,” Journal of Wildlife Management, 1974, 38: 757–770.
33. Petersen, B., A. Iaconbelli, and E.E. Kushny, “The Caribou Conundrum: Conservation of Woodland Caribou and Designing Protected Areas,” World Wildlife Fund, Toronto Poster Presentation, 1998, 8th North American Conference, Whitehorse, Yukon.
34. Bergerud, A.T. and J.P. Elliott, “Dynamics of Caribou and Wolves in Northern British Columbia,” Canadian Journal of Zoology, 1986, 64: 1515–1529; Bergerud, A.T., “The Need for the Management of Wolves,” an open letter, Rangifer, Special Issue, 2007, 17: 39–50.
35. Of, relating to, or resulting from the influence of human beings on nature.
36. Schaefer, J.A, “Long-Term Recession and Persistence of Caribou in the Taiga,” Conservation Biology, 2003, 17: 1435–1439; Vors, L.S., J.A. Schaefer, B.A. Pond, A.R. Rodgers, and B.R. Patterson, “Woodland Caribou Extirpation and Anthropogenic Landscape Disturbance in Ontario.” Journal of Wildlife Management, 2007, 71: 1249–1256.
37. Serrouya, R. and H.U. Wittmar, “Imminent Local Extinctions of Woodland Caribou from National Parks,” Conservation Biology, 2010, 24: 363–364; Hebblewhite, M., C. White, and M. Musiani, “Revisiting Extinction in National Parks: Mountain Caribou in Banff,” Conservation Biology, 2010, 24: 341–344.
38. Wittmer, H.U., A.R.E. Sinclair, and B.N. McLellan, “The Role of Predation in the Decline and Extirpation of Woodland Caribou,” Oecologia, 2005, 144: 257–267; Wittmer, H.U., R.N.M. Ahrens, and B.N. McLellan, “Viability of Mountain Caribou in British Columbia, Canada: Effects of Habitat Change and Population Density,” Biological Conservation, 2010, 143: 86–93.
39. Bergerud, A.T., W.J. Dalton, H.E. Butler, L. Camps, and R. Ferguson, “Woodland Caribou Persistence and Extirpation in Relic Populations on Lake Superior,” Rangifer, Special Issue, 2007, 17: 57–78.
40. Wildlife Division Newsletter, June 6, 2009.
41. Bergerud, A.T., H.E. Butler, and D.R. Miller, “Anti-Predator Tactics of Calving Caribou: Dispersion in Mountains,” Canadian Journal of Zoology, 1984, 62: 566–575.
42. Geological epoch that lasted from about 2,588,000 to 11,700 years ago.
43. This ice sheet was the primary feature of the Pleistocene epoch in North America, commonly referred to as the Ice Age. The ice sheet was up to two miles thick in Quebec, Canada, but much thinner at its edges.
44. Storck, P.L. and A.E. Spiess. 1994 “The Significance of a New Faunal Identification Attributed to an Early PaleoIndian Occupation at the Udora Site, Ontario, Canada,” American Antiquity, 59: 121–142.
45. Jackson, L.J. 1989. “First Ontario C-14 Date for Late Pleistocene Caribou,” Archeology, 89: 4–5.
46. Bergerud, A.T., S.N. Luttich, and L. Camps, The Return of Caribou to Ungava (McGill and Queens University Press, Montreal, Quebec, Canada, 2008).
47. deVos, A., and R.L. Peterson. 1951 “A Review of the Status of Woodland Caribou in Ontario,” Journal of Mammalogy, 322: 337.
48. Fuller, T.K., “Population Dynamics of Wolves in North-Central Minnesota,” Wildlife Monograph 105, 1989.
49. Simkin, D.W., “A Preliminary Report of the Woodland Caribou Study in Ontario,” Department of Lands and Forest, Section Report No. 59, 1965.
50. Allee Effect: Mortality accelerates as prey numbers decline.
51. Wittmer, H.U., A.R.E. Sinclair, and B.N. McLellan, “The Role of Predation in the Decline and Extirpation of Woodland Caribou,” Oecologia, 2005, 144: 257–267; Bergerud, A.T., W.J. Dalton, H.E. Butler, L. Camps, and R. Ferguson, “Woodland Caribou Persistence and Extirpation in Relic Populations on Lake Superior,” Rangifer, Special Issue, 2007, 17: 57–78.
52. Latham, A.D.M., M.C. Latham, N.N.A. McCutchen, and S. Boutin, “Invading White-Tailed Deer Change Wolf-Caribou Dynamics in Northeastern Alberta,” Journal of Wildlife Management, 2010, 75: 204–212.
53. Bergerud, A.T., “Rareness as an Anti-Predator Risk for Moose and Caribou,” Wildlife 2001 Populations, editors D.R. McCullough and R. H. Barrett, New York: Elsevier Applied Science, 1992, pp. 1008–1021.
54. Hempel, C.G., Philosophy of Natural Science, Englewood Cliffs, N.J., 1966.
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