Sustainability of the Grizzly Bear Hunt in British Columbia, Canada

The Journal of Wildlife Management; DOI: 10.1002/jwmg.21189 Research Article Sustainability of the Grizzly Bear Hunt in British Columbia, Canada BRUCE N. MCLELLAN, 1 British Columbia Ministry of Forests, Lands and Natural Resource Operations, P.O. Box 1732, D Arcy, BC V0N 1L0, Canada GARTH MOWAT, British Columbia Ministry of Forests, Lands and Natural Resource Operations, Suite 401 333 Victoria St. Nelson, BC V1L 4K3, Canada TONY HAMILTON, British Columbia Ministry of Environment, 2975 Jutland Road, Victoria, BC V8W 9M1, Canada IAN HATTER, British Columbia Ministry of Forests, Lands and Natural Resource Operations, 2975 Jutland Road, Victoria, BC V8W 9M8, Canada ABSTRACT The sustainability of the grizzly bear (Ursus arctos) hunt in British Columbia, Canada has been questioned and is a high profile issue, particularly in the media. To investigate the hypothesis that the hunt is unsustainable, we examined the sustainable human-caused mortality rate for grizzly bears using recent data on vital rates and population projection models and compare these to rates used by the management agency; examined the age and sex ratio of the kill and how the sex ratio changes with age for the entire province, each population unit, and cohorts born each year between 1977 and 1990; summarized population density estimates in hunted population units in British Columbia and compared these to unhunted areas in adjacent jurisdictions; and reviewed case studies of population units that have been highlighted as most likely to have had unsustainable kill levels. Because the natural mortality rate of adult grizzly bears is 1 2% and lower than was estimated when sustainable human-caused mortality targets were developed, estimated sustainable kill rates are 4 10%, and generally higher than the 4 6% used in British Columbia. We estimated that males have been 3 4 times more vulnerable to being killed by hunters than females, yet males dominate the kill at all ages and the proportion of males increased with age, which is opposite of what is predicted for a heavily hunted population. The average age of female and male grizzly bears killed by hunters increased from 7.1 years and 7.4 years, respectively, in the 1980s to 7.7 years and 8.7 years, respectively, in the 2000s. An average of 107.4 females and 204.9 males per cohort born between 1977 and 1990 were eventually killed by people and recorded, suggesting that many more females than males died for unknown reasons. There have been more population inventories of grizzly bears in British Columbia than in any other jurisdiction. The average density estimate of 21 inventories in hunted areas without salmon (Oncorhynchus spp.) in British Columbia (31.2 bears/1,000 km 2 ) was as high as or higher than nearby unhunted areas. The case studies had the highest kill densities or among the highest kill rates in the province and hunting targets were commonly exceeded and seasons closed or the hunter kill target reduced. Although population inventories in these areas found moderate or even high densities of bears, some are now in decline. Hunter kill data from declining populations had a high proportion of males and these were older, demonstrating that these indices of kill rates are sometimes unreliable. Although more population density, trend, and vital rate measurements would be beneficial, the hypothesis that the grizzly bear hunt has been unsustainable was not supported by our investigation of available information. Ó 2016 The Wildlife Society. KEY WORDS British Columbia, demography, grizzly bear, hunting, overkill, population model, sustainable harvest, Ursus arctos. There are many historical (Mattson and Merrill 2002) and recent examples (Hutchings and Myers 1994) reporting that human-caused mortality resulted in the collapse of animal populations. With social pressure to continue harvesting, it can be difficult to ensure that the take is sustainable (Ludwig et al. 1993). In British Columbia, Canada, managing the Received: 17 March 2016; Accepted: 12 September 2016 1 E-mail: bruce.mclellan@gov.bc.ca grizzly bear (Ursus arctos) hunt has been an ongoing challenge. Although demand for the hunt remains sufficient for elected officials to support its continuation, the sustainability of the kill continues to be a high-profile debate within and beyond the province. For several decades, some people have suggested that the grizzly bear hunt in British Columbia is unsustainable (Horejsi et al. 1998, Gilbert et al. 2004) and in 2002, the European Union banned the import of grizzly bears killed in British Columbia because of concerns over sustainability. Recently, Artelle et al. (2013) suggested that the procedure used by wildlife managers to McLellan et al. Sustainability of Grizzly Hunt 1

derive sustainable kill levels did not account for inherent uncertainty, which may frequently lead to excess mortality and population decline. Grizzly bears have a low reproductive rate compared to other terrestrial mammals in North America and consequently are sensitive to excessive mortality (Craighead et al. 1974). Indeed, intentional overkill was the major cause of the near extirpation of grizzly bears from the lower 48 states of the United States and the Canadian prairies in the 1800s and early 1900s. Is the ongoing legal kill of grizzly bears in British Columbia leading to their extirpation or is the kill sustainable? With the possibility of removing grizzly bears from the list of threatened species in portions of the lower 48 states, there will be pressure to hunt grizzly bears in those jurisdictions too (Miller et al. 2013). Those decisions will be controversial, and information regarding the sustainability of grizzly bear hunting may become important to managers in the lower 48 states. We evaluated the evidence for the overkill hypothesis using 3 independent sources of information. We first estimated sustainable kill rates of grizzly bears by using vital rate information from recent research (Garshelis et al. 2005, Schwartz et al. 2006, Mace et al. 2012, McLellan 2015) and compared these rates to those used by the management agency. If recent information suggested higher kill rates are sustainable, then there is less support for the overkill hypothesis. Next, we summarized indicators of unsustainable mortality from the age and sex of bears killed. The use of kill data to accurately estimate kill rate or to determine whether a small population is stable or beginning to decline because of excessive mortality is questionable because of inherently small sample sizes and statistical assumptions are unlikely to be met (Fraser 1984, Harris and Metzgar 1987a,b, Garshelis 1990). However, there are indicators that can suggest a relatively light kill rate as opposed to heavy, possibly unsustainable kill levels and the strength of inference is increased by examining multiple indices (Harris and Metzgar 1987b, Garshelis 1990). These indicators are based on males being more vulnerable than females to being killed by people. Most simply, both the proportion of the kill that are males and the average age of these males will decline as kill rates increase provided recruitment and other causes of mortality remain constant (Gilbert et al. 1978, Harris and Mezgar 1987b). These simple indicators have been used to monitor population status of black bears (Ursus americanus) in many jurisdictions in North America (Garshelis 1990). They are also used on grizzly bears in Alaska where the objective is for the kill to be > 60% males and these with an average age of >6.5 years (Harper 2009). In addition, the rate that the sex ratio of the kill changes with increasing age is another indicator of harvest levels (Paloheimo and Fraser 1981, Fraser et al. 1982, Fraser 1984, Beston and Mace 2012). If the grizzly bear hunter kill has been unsustainably high, then we expected a significant decline in the proportion of males in the harvest with increasing age. We then summarized recent inventories of grizzly bear populations that were based on mark-recapture methods. If hunting has been at an unsustainable rate, then population densities in areas that have been hunted for decades should be much lower than nearby, unhunted areas such as those in protected areas. Finally, we investigate case studies of grizzly bear population units (PUs) which our analyses, and those of Artelle et al. (2013), suggest are most likely to have had unsustainable kill levels. Our objective was to use available information on grizzly bears in British Columbia and beyond for evidence that the legal hunt has been unsustainable. In doing so, we hoped to assist managers refine kill levels to ensure hunting is not a major factor influencing population trajectories into the future. STUDY AREA The Province of British Columbia, Canada covers 944,735 km 2 of land and is bordered by the Pacific Ocean. Although British Columbia separates the states of Washington and Alaska in the United States by only 810 km in a straight line, the coast is highly fiorded among high, glaciated mountains so the actual coastline is 25,725 km long. The complexity of the coast is important for grizzly bear conservation because unlike the United States, it has not been roaded south to north. The Coastal Mountains are the most rugged range in the province, but many others, including the Rocky, Columbia, Cassiar, and Cariboo mountains, cover most of the landbase. This geographic complexity leads to ecological complexity. There are coastal and interior temperate rainforests, boreal and sub-boreal forests, deserts, and alpine tundra. In 2012, there were 4.6 million people in British Columbia, but 3.9 million lived in the extreme southwest corner of the province or the dry, southern interior where there are no grizzly bears. Most of the province is forested and grizzly bears are rarely observed except along salmon (Oncorhynchus spp.) spawning streams or in some less forested, alpine areas. But grizzly bears occur across approximately 800,000 km 2 of British Columbia and by far the majority are rarely seen by people. Populations of grizzly bears were never found on Vancouver Island, Haida Gwaii, and many smaller, coastal islands where black bears are common (Mattson et al. 2005). Most grizzly bears in British Columbia are listed as least concern by the International Union for Conservation of Nature (IUCN); however, some small, semi-isolated, or isolated populations along the southern fringe are listed as endangered or even critically endangered (IUCN 2016). A Summary of the British Columbia Grizzly Bear Harvest Procedure In British Columbia, harvest targets (i.e., Annual Allowable Harvest [AAH]) were based on estimates of grizzly bear population size and the sustainable rate of all human-caused mortality. Multiplying the estimated population size by this rate provided the number of bears that people could kill each year. There were 3 categories of bears killed by people. One category included bears killed for reasons other than legal hunting but were reported to the agency, such as defense of life or property, or road and train kills. The second category was the estimated number of bears that people kill that were 2 The Journal of Wildlife Management 9999()

not reported. The third category was the legal hunter kill. The management agency determined the AAH by subtracting the bears known to have been killed for non-hunting reasons and the estimated unreported kill from the allowable mortality estimate. In practice, the non-hunter kill is the mean annual kill over the previous 5 or more years and the unreported kill is predicted by a model based largely on results of McLellan et al. (1999). Estimating the size of grizzly bear populations across an area as large, diverse, and heavily forested as British Columbia is difficult but methods have improved over time. In the early 1990s, there were few reliable density measures of grizzly bears within or near British Columbia. In 1995, biologists in British Columbia developed a method of using hair traps to obtain DNA samples from bears across a systematic grid so capture-recapture models could be used to generate more reliable density estimates across larger areas (Woods et al. 1999). These methods improved population estimates and Mowat et al. (2013b) used these estimates (and others) in a multiple regression that enabled extrapolation, with measurable confidence, to areas that had not been inventoried. The management agency set the sustainable rate of all human-caused mortality at 4 6%, depending on the estimated habitat quality. This rate was based on demographic information available in the 1990s (Craighead et al. 1974, Knight and Eberhardt 1985, McLellan 1989a, b, c) and in particular the modeling work of Harris (1984, 1986) who suggested that a maximum kill rate of 6.35 6.6% should be sustainable. The unreported kill rate used in the British Columbia procedure ranged from 0.3% to 2.0% depending on the estimated relative abundance of people with firearms that spend time in bear habitat in the PU (Austin et al. 2004). For management purposes, the agency divided the distribution of grizzly bears in British Columbia into PUs in the 1990s. Five southern PUs contain small and somewhat isolated populations for which there is conservation concern and are not hunted. Ten other PUs had more bears and were not isolated but were not hunted because objectives were to increase bear numbers, sometimes to help recover adjacent PUs. Grizzly bears have been hunted for many decades in the remaining 41 PUs. Combined, there were an estimated 13,900 bears over an area of 630,000 km 2 in these hunted PUs in 2012 (http://www. env.gov.bc.ca/soe/indicators/plants-and-animals/grizzly-bears. html, accessed May 2016). No hunted PUs were genetically or demographically isolated (Proctor et al. 2012). Grizzly bears in British Columbia can be hunted by residents and non-residents of British Columbia. Nonresidents must hunt with a registered outfitter that has a territory with exclusive rights to guide non-resident hunters. Outfitters receive a grizzly bear quota for a 5-year period that can be as few as 1 bear. For residents of British Columbia, a limited number of permits are allocated by a lottery system for portions of PUs to distribute the kill. The number of resident permits is calculated by dividing the target resident kill by the average recent success rate. To enable adjustments accounting for actual success, the agency manages the hunt over a 5-year period where permit and quota numbers are adjusted to reflect recent kill. Because hunter success and non-hunter kills vary among years, killing more bears in 1 year than is the target is common, but the number of permits the following year may be decreased with the goal of meeting targets over the 5-year period. Additional hunting regulations include the protection of females and their offspring when together and a ban on baiting. Finally, a maximum of 30% of the total target kill (including nonhunter kills) can be females. Since 1976 all successful grizzly bear hunters have been required to bring the skull and hide to an agency office where employees recorded the location of kill and sex of the bear and removed a tooth aging (Matson s Laboratory LLC, Milltown, MT, USA). The agency also made an effort to record the location, cause of death, and sex, and remove a tooth from bears killed for other reasons. The compulsory inspection database includes the date, cause, and location of death plus the age and sex of most grizzly bears known to have been killed in British Columbia for >3 decades. METHODS Testing Parameters With Recent Information We compared recent estimates of grizzly bear vital rates (Garshelis et al. 2005, Schwartz et al. 2006, Mace et al. 2012, McLellan 2015) to those used by Harris (1986) on which the British Columbia procedure was based. These recent estimates were based on relatively large samples, were either in or close to British Columbia, and they varied greatly. Garshelis et al. (2005) worked in and near Banff National Park that borders southern British Columbia to the east in the Rocky Mountains. In this area, bears were not hunted and reproductive rates were the lowest recorded anywhere on the continent at the time, but the population was increasing with high adult survival. Schwartz et al. (2006) collected data on bears in the Greater Yellowstone Ecosystem (GYE) where the population was not hunted and had been increasing for several decades. Mace et al. (2012) worked in the Northern Continental Divide Ecosystem (NCDE) of Montana where grizzly bears were not hunted and the population was also increasing. McLellan (2015) collected data in the Flathead valley of British Columbia from 1979 to 2010 where the population was hunted but increased during the first 2 decades of study. After reaching a high density, however, the population declined during decade 3. In addition to the high density of bears, a decline in huckleberries (Vaccinium membranaceum), which were the most important summer and fall energy food in the area (McLellan 2011), was thought to have caused reproductive rates of the bears to drop to very low levels. These 5 datasets ranged from rapidly increasing populations that were below carrying capacity (i.e., Flathead decade 1, GYE) to 1 above carrying capacity and in decline with a very low reproductive rate (i.e., Flathead decade 3). These extremes likely represent the variation of demographic conditions found across British Columbia. To estimate the rate of increase using information from these 5 datasets with only natural (i.e., non-human caused) mortality, we used a life table approach (Caughley 1977) and performed calculations using the life table module of the McLellan et al. Sustainability of Grizzly Hunt 3

Microsoft Excel (Microsoft, Redmond, WA, USA) add-in program PopTools 3.0 (PopTools version 3.0; http://www. poptools.org, accessed Jun 2012). We set the age of primiparity to the closest age to the average estimated for each study (except NCDE, see results). To estimate the natural mortality rate of cubs and yearlings, we adjusted the reported rate by the proportion of deaths due to the mother being shot. We then increased the mortality rate of independent female bears (i.e., >2 yr old) until population change (l) equaled 1.00. This change in mortality is the proportion of independent female bears that humans could remove annually and have a stable population provided females with cubs or yearlings were not shot. We did not invoke density effects because they were already represented among the datasets (Schwartz et al. 2006, Mace et al. 2012, McLellan 2015). The British Columbia harvest procedure is not based on the mortality rate of independent female bears but the proportion of the entire population that people kill. We therefore used a deterministic sex and age structured population model based on life table metrics (Caughley 1977). Our primary goal was to test whether the 4 6% kill rates used in British Columbia were sustainable and sufficiently conservative to account for some uncertainly in population estimates as has been suggested (British Columbia Ministry of Environment, http://www. env.gov.bc.ca/fw/wildlife/management-issues/docs/grizzly_ bear_faq.pdf, accessed May 2014). The model used agespecific reproductive and natural survival rates of independent bears. We added human-caused mortality to the natural mortality. Cub and yearling survival rates were estimates from the original studies and included natural deaths plus those assumed to have died if their mother was killed. In the model, each sex and age class could have a different vulnerability of being killed by people. To include the possibility of selection for a trophy (i.e., large adult male), we added an age category of >10-year-old males. The model had 30 ages but females stopped reproducing at 25 years of age (Schwartz et al. 2003). The age and sex structure of the initial population in the model was based on a 50:50 sex ratio at birth and the stable age distribution generated by the mean reproduction, and cub and yearling survival rates from the 5 datasets but where the survival of independent male and female bears were equal and set where l ¼ 1.0. From this initial population, we modified parameters to investigate implications of various sex- and age-specific kill rates. We ran the population model for 50 years because by then age distributions stabilized and the model produced the same trend as the life table module of Poptools. Model outputs included l (N t50 /N t49 ), the overall human-caused kill rate (no. of bears killed at t 50 /N t50 ), proportion of bears killed that were males (for each age and overall), the average age of male and female bears killed, and the proportion of the living population of each sex at each age. We did not invoke stochasticity in our model because we were not interested in a variety of possible outcomes from a single, small population where inter-annual variation of survival may affect l but rather generic results from variation of a few parameters in large populations. We estimated the relative vulnerabilities of each age and sex class of grizzly bear to being killed by a hunter by matching, as close as possible, the age and sex of the kill in the model to bears actually killed by hunters in British Columbia since 1980. We first standardized the total number of bears killed in the model to match the total number of bears killed by hunters. We then used the optimization tool SOLVER in Excel to iteratively change the adult female (5 yr old) hunter kill rate and relative vulnerabilities (and thus kill rate) of subadult (2 4 yr old) females, subadult males, 5 9-yearold males, and 10-year-old males until the sum of the squared differences (Hilborn and Mangel 1997) between the actual hunter kill and the modeled kill was minimized. We used reproduction, cub and yearling survival, and natural mortality data from the 5 populations but only the actual kill data from British Columbia. Indicators of Unsustainable Kill From the Compulsory Inspection Database We suspect the recording of hunter kills may have been unreliable for the first few years after the system was introduced and recording non-hunter kills was even less reliable. Thus, we used only hunter kill data beginning in 1980. From this database, we calculated the average age of male and female bears and sex ratio of bears killed by hunters each year and each decade over the entire province and by each PU. We made comparisons between ages using randomization tests (bootstrapping) in PopTools 3.0. To investigate whether male-biased harvest was sufficient to influence the sex ratio of bears killed in older age classes (assuming rates of other types of mortality were similar for M as F), we used linear regression with the dependent variable being the proportion of hunter-killed bears that were male and the independent variable being age weighted by the number of bears killed at each age (Paloheimo and Fraser 1981, Fraser 1984). We used these regressions for all hunterkilled bears in the province since 1980 and for each decade to examine trends in the regression slope over time. Because bears can live for 30 years, we also used these regressions for single-birth cohorts to avoid possible implications of pooling individuals born many years apart. We used these cohortspecific regressions for bears born in 1977 (first killed by hunters in 1979 as 2-year-olds) through bears born in 1990 because most, if not all of these bears would now be dead. We also compared the number of male to female bears recorded from each of these cohorts. Because all bears in these cohorts are dead, the difference between the number of males and females recorded is equal to the difference in unrecorded deaths that are natural or unreported human kills (assuming an equal sex ratio at birth). Although sample size requirements for these weighted regressions are higher than for simple sex ratio or average age of the kill calculations, we examined regressions for each hunted PU using hunter kill data since 1980 to investigate whether there were any detectable depletions of males at older ages at the spatial scale managers set kill rates. We then pooled some of the smaller, adjacent and ecologically similar PUs to increase sample sizes and used data from 1990. For all 4 The Journal of Wildlife Management 9999()

Table 1. Natural survival rates (i.e., mortality not directly caused by people), reproductive characteristics, and rate of increase with only natural mortality of grizzly bears in Banff, Canada (Garshelis et al. 2005), the Greater Yellowstone Ecosystem (GYE; Schwartz et al. 2006), Northern Continental Divide Ecosystem (NCDE) of Montana (Mace et al. 2012), and the Flathead drainage of British Columbia, Canada during decade 1 and 3 of study (McLellan 2015). Natural survival a Reproduction a Study area F 2yr M 2 yr Cub Yearling Reproductive rate Age of primiparity Rate of increase (l) Banff 0.987 (134.5) a 0.983 (60.4) 0.79 (53) 0.91 (32) 0.240 (155) 8.4 (9, 8) b 1.06 GYE c 0.99 1.0 (285.0) 0.967 0.977 (214.1) 0.75 (137) 0.85 (73) 0.318 (327) 5.8 (22, 18) 1.10 NCDE 0.967 0.992 (122.7) 0.78 (60) 0.69 (34) 0.367 (95) 5.4 (10) d 1.08 Flathead e 0.983 (226.2) 0.989 (79.4) 0.74 0.86 (100) 0.87 (77) Decade 1: 0.374 (51) Decade 3: 0.192 (80) Decade 1: 6.6 (6, 4) Decade 3: 10.5 (4, 5) Decade 1: 1.11 Decade 3: 1.04 Total 0.983 0.991 (768.4) 0.975 0.980 (353.9) 0.76 0.80 (350) 0.84 (216) 0.297 (708) 6.64 (51, 35) a Bear-years of monitoring in parentheses. b For age of primiparity (no. of who had their first litter, no. of >4 yr old who were censored before having their first litter). c Includes research and management bears. d This estimate only included females that did have their first litters so will be biased low. e Survival estimates are for all 3 decades of study, whereas reproduction is limited to decade 1 and decade 3. regressions we examined the significance of the relationship, the slope of the line, the intercept, and the age when the number of males and females killed were equal (Fraser 1984). Population Inventories Using mark-recapture analyses of systematically distributed hair traps and DNA genotypes from hairs as permanent markers, biologists in British Columbia have done >30 inventories (Mowat et al. 2013b). Because grizzly bear conservation in the small, southern PUs is an ongoing challenge, many population estimates were in areas without a grizzly bear hunt, but several were in areas that have been hunted for many decades. Additionally, inventories were repeated in some areas to assess harvest sustainability or examine recovery. We summarized these inventories and compared densities in hunted areas to densities in areas where bears were not hunted. RESULTS Grizzly Bear Vital Rates and Sustainable Human- Caused Mortality In the GYE, NCDE, and the Flathead (all 3 decades), 31.2%, 42.9%, and between 20.0% and 31.6% of cub mortalities, respectively, were because mothers were killed by people. When we adjusted cub survival by these proportions, their natural survival rate averaged between 0.76 and 0.80 (Table 1). Of these studies, only the GYE reported a yearling mortality that was directly caused by people and the adjusted yearling natural survival rate was 0.85 and near the average of 0.84 for these 4 studies (Table 1). The natural survival rates of grizzly bear cubs and yearlings used by Harris (1984, 1986) to estimate sustainable kill rates were, at 0.91, higher than recent estimates. Harris (1984, 1986) used a variety of natural survival (S) rates for 6 age classes of independent male and female bears that varied because of added stochasticity, but means were S 2 ¼ 0.88, S 3 ¼ 0.774, S 4 ¼ 0.90, S 5 12 ¼ 0.95, S 13 20 ¼ 0.90, and S 21 25 ¼ 0.75; all remaining bears died at 25. Recent data suggest natural survival of independent females was higher and between 0.967 and 1.0 (Table 1). In these recent studies, female bears were monitored for 768.4 bear-years and between 7 and 13 died of natural causes for an average rate of between 0.983 and 0.991, assuming equal monitoring over the year. The natural survival rate for independent males was similar to that of females (Table 1). Harris (1986) used a mean reproductive rate of 0.335 female cubs/adult female/year and a mean age of primiparity of 5.5 years. Unlike the survival rates measured in recent studies, reproductive rates varied greatly among areas and particularly within the Flathead over time (Table 1). The average reproductive rate (0.297) and age of primiparity (6.64) from the recent studies (Table 1) indicated lower reproduction than that used by Harris (1986). Using only natural mortality rates (cubs, yearlings, and older bears) and observed reproductive rates resulted in a l of 1.10 in the GYE, 1.08 in the NCDE, and 1.11 in the Flathead Valley during decade 1 but only 1.04 during decade 3 (Table 1). In Banff, l was 1.06 when only natural mortality rates were used. A population with no human-caused mortality and the mean vital rates used by Harris (1986) increased at l ¼ 1.05. The estimated sustainable kill rate varied depending on the vulnerability of male and female bears. If males and females 3 years of age were equally vulnerable and cub and yearling survival was reduced to account for people killing mother bears, as in the original data (usually non-hunting mortalities), then all populations except the Flathead during decade 3 could sustain a kill rate of between 5.1% and 8.1%. During decade 3, the Flathead could only sustain a 2.0% kill rate. A population with vital rates used by Harris (1986) could sustain a 3.6% kill rate (Table 2). When males were 2 4 times more vulnerable than females, then the sustainable kill rate increased (Table 2). Adjusting the relative vulnerabilities so the age and sex of bears killed in the model was as close as possible to the actual hunter kill recorded across the province suggested that >10- year-old males were the most vulnerable class followed by subadult males, and then 5 9-year-old males (Table 3). Subadult females were almost twice as vulnerable as adult females. Using these vulnerabilities in the model suggested the sustainable kill rate varied between 3.9% for the Flathead with decade 3 vital rates to 10.2% for the Flathead in decade McLellan et al. Sustainability of Grizzly Hunt 5

Table 2. Model estimates of the sustainable human-caused mortality rates (%) of grizzly bears 3 years of age when males are equally vulnerable and when males are 2, 3, and 4 times more vulnerable to being killed as females. Populations were in Banff, Canada (Garshelis et al. 2005), the Greater Yellowstone Ecosystem (GYE; Schwartz et al. 2006), Northern Continental Divide Ecosystem (NCDE) of Montana (Mace et al. 2012), and the Flathead drainage of British Columbia, Canada during decade 1 and 3 of study (McLellan 2015) and vital rate estimates used by Harris (1984, 1986). Vital rates in all models came from original studies and both natural and human caused mortality rates of cubs and yearlings (i.e., the mother was shot) are included. Sustainable human-caused mortality rates (%) Population M ¼ F M2 as vulnerable M3 as vulnerable M4 as vulnerable GYE 6.37 7.86 8.56 9.04 Banff 5.52 7.06 7.83 8.28 NCDE 5.07 6.41 7.03 7.34 Flathead decade 1 8.10 9.96 10.80 11.27 Flathead decade 3 1.99 2.83 3.42 3.81 Harris (1984, 1986) 3.55 4.69 5.30 5.61 1 (Table 3) and the average using vital rates of the 5 populations was 7.4%. With these marginally sustainably kill rates and vulnerabilities estimated from province-wide hunter kill statistics, bears killed from a population with Flathead decade 3 vital rates would be almost 70% males and these would average almost 10 years of age (Table 3). Bears killed from populations with vital rates the same as the other 4 populations would be 51 56% males with average ages of 5.6 6.7 years when the kill rate stabilized population growth. In all cases, the living adult population would consist of 20 31% males (Table 3) at maximum sustainable kill rates. These results suggest that a sustainable total kill rate for the average of the sample populations excluding the Flathead during decade 3 would be 1.4 2.1 times higher than the 4 6% used in the British Columbia Procedure. A population with recruitment similar to the Flathead in decade 3 would decline with a kill rate of >4%. Human-Caused Mortality of Grizzly Bears in British Columbia Between 1980 and 2011, 11,084 grizzly bear deaths were recorded in British Columbia. The sex was recorded for 10,870 and both age and sex for 10,379. Of all deaths recorded, 86.2% were of bears legally killed by hunters and 10% were due to defense of life or property (i.e., animal control). Of all mortalities where the sex was recorded, 64.9% were males. Of the bears legally killed by hunters, 65.6% were males, whereas 60.3% of all non-hunting mortalities were males. The average age of female and male bears killed by hunters was 7.3 (median ¼ 6.2) and 7.9 years (median ¼ 6.7), respectively; for non-hunting mortalities, females and males averaged 6.5 (median ¼ 4.9) and 5.8 (median ¼ 4.2) years, respectively. We estimated that between 1980 and 2011, the mean age of female (P ¼ 0.006) and male (P < 0.001) bears killed by hunters increased from 6.9 years each (median F ¼ 5.7, M ¼ 5.5) to 7.6 (median ¼ 6.8) years for females and 8.8 years (median ¼ 7.9) for males and the age of males likely increased more rapidly than females (P ¼ 0.013; Fig. 1). We also estimated that the proportion of the hunter kill that were males likely increased (P ¼ 0.037) from 64.6% to 68.3% over these years. Using all bears 2 year of age (i.e., independent bears) killed by hunters, there was a significant relationship (P < 0.001) between age and the proportion that were males, but the slope was positive (b ¼ 0.005) with an intercept at 62.2% males. This relationship was unexpected and showed an increasing, not decreasing proportion of males in older age classes being killed by hunters. The slope of the weighted regression was 0.003 (P ¼ 0.125) for bears killed by hunters in the 1980s, 0.003 (P ¼ 0.178) for those killed in the 1990s, and 0.008 (P < 0.001) for bears killed from 2000 to 2011 (Fig. 2). The slopes and intercepts were almost identical in the 1980s and 1990s, but the slope was steeper in the 2000s (P ¼ 0.024 and 0.035), suggesting the sex ratio of the hunter kill in older age classes was increasingly skewed towards males in the 2000s. We found the slope of the regression line of the proportion of males in the hunter kill against age was positive (an increasing proportion of males at older ages) for 10 of the 14 cohorts of bears born between 1977 and 1990 (P < 0.05 for 5) and none had a significantly (P < 0.05) negative slope. All members of these cohorts are now likely dead and an average of 107.4 14.4 (SD) females and 204.9 29.3 males (and 3.5 of unknown sex) per cohort were killed by people and recorded. Table 3. The vulnerability (times >adult females) of the various age and sex classes of bears to being killed by hunters as estimated by minimizing the squared difference between the actual grizzly bear kill data from across all of British Columbia, Canada, 1980 2011, and the bears predicted to be killed by the model using vital rates (natural survival and reproduction) from Banff, Canada (Garshelis et al. 2005), the Greater Yellowstone Ecosystem (GYE; Schwartz et al. 2006), Northern Continental Divide Ecosystem (NCDE) of Montana (Mace et al. 2012), and the Flathead drainage of British Columbia, Canada during decade 1 and 3 of study (McLellan 2015). Based on these vulnerabilities, the table also shows the sustainable kill rate (l ¼ 1.00), the percentage of males and average age of males in the kill, and the percentage of the living adults that are males when killed at this rate. Variable Banff GYE NCDE Flathead decade 1 Flathead decade 3 x Vulnerability 2 4 yr M 3.29 3.05 2.95 2.48 5.37 3.43 Vulnerability 2 4 yr F 1.81 1.64 1.63 1.37 2.98 1.88 Vulnerability 5 9 yr M 3.26 2.95 2.95 2.29 5.52 3.39 Vulnerability 10 30 yr M 3.56 3.39 3.25 2.29 5.52 3.68 Sustainable kill rate (%) 5 30 yr F 6.46 8.34 6.67 11.18 1.87 6.90 Population sustainable kill rate (%) 7.75 8.32 6.80 10.24 3.87 7.39 M in kill (%) 54.36 50.90 55.89 52.78 69.69 56.72 Age of M in kill (x) 6.31 5.55 6.68 5.54 9.82 6.78 % M of living adults 22.9 20.2 26.7 26.4 31.1 25.4 6 The Journal of Wildlife Management 9999()

Figure 1. The average age of female and male grizzly bears killed by hunters in British Columbia, Canada, 1980 2011. The solid line is for female ages and the dashed line is for male ages. Figure 2. The weighted regressions of the proportion of male grizzly bears in the hunter kill at each age for all bears killed by hunters in British Columbia, Canada, in the 1980s, the 1990s, and 2001 2011. Weighting was by the total number of bears killed (and aged) at each age. For hunter-killed bears between 1990 and 2011, we calculated the proportion that were male and the average age of these males in each of the 41 hunted population units. At 6.48 years, the Kwatna-Owikeno was the only PU with an average age of males killed by hunters under 6.5 years, but 3 others were under 7.0 years of age. Seven units had <60% males in the hunter kill, but the average age of males was >7.5 years in each of these units. To measure the slope of the weighted linear regression between bear age and the proportion that were male, we used data from 1980 to 2011 for 32 PUs where hunters had killed >100 bears. The slope was positive for 26 units (P < 0.05 for 3) and none had a significantly (P < 0.05) negative slope. Because of sample size constraints, we pooled 1990 2011 hunter kill data from smaller, adjacent, and ecologically similar units. The regression between the proportions of males in the kill with age found 16 of 20 pooled units had positive slopes (P < 0.05 for 6) and none with significantly negative slopes (Table S1, available online in Supporting Information). Population Inventories Mowat et al. (2013b) summarized 102 grizzly bear density estimates in North America. Of these, 40 were in British Columbia, 30 were in Alaska, and the remainder were in the 7 other jurisdictions with grizzly bears. Of the British Columbia populations, 28 were hunted and their average estimated density was 31.7 15.9 (SD) bears/1,000 km 2. The average density estimate from Alaska was higher (146.4 bears/1,000 km 2 ) because of the extremely high densities on the Alaska Peninsula and some Alaskan Islands where there is an abundance of spawning salmon available to bears. When only populations with limited or no access to salmon were compared, the hunted populations in British Columbia were higher (31.2 bears/1,000 km 2, n ¼ 21) than those in Alaska (23.8 bears/1,000 km 2, n ¼ 16) or the lower 48 states (28.3 bears/1,000 km 2, n ¼ 6). These differences in density were not significant (F 2,40 ¼ 1.318, P ¼ 0.279), but inventory locations were not located randomly within jurisdictions. Case Studies Several PUs were of particular concern because kill levels frequently exceeded targets, the kill had a relatively low proportion of males, the average age of males killed was relatively young, or the regression line of the proportion of males killed by hunters by age declined. Three case studies that covered 5 hunted PUs have been particularly challenging for managers and illustrated these concerns. Purcell Mountains. There were 3 small PUs in the southern Purcell Mountains of southeastern British Columbia called Yahk, South Purcell, and Central Purcell, but in 2012, the South and Central Purcell units were joined because they were small and connected. There has been high non-hunting mortality in the Yahk unit, near the international border with the United States, and it has been closed to hunting since 1976. The southern half of the former South Purcell unit was closed to hunting in 2008 and the remainder closed in 2012 because female kill, primarily nonhunting mortality, exceeded targets. Between 1990 and 2011 in the combined Purcell Unit, 65% of the hunter kills were McLellan et al. Sustainability of Grizzly Hunt 7

males and these had the second youngest average age (6.6 yr) in the province. Additionally, the regression of the proportion of males in the hunter kill with age had the steepest declining slope of any PU in the province during 1980 2011 with females becoming dominant in the kill at 19.9 years of age. The hunter kill data suggested high mortality levels of both males and females. Inventory data for all 3 of the Purcell units are based on 6 DNA-based, mark-recapture surveys conducted between 2004 and 2009 in portions of these units (Proctor et al. 2007). Densities were then extrapolated across entire units based on habitat and human features using multi-scale resource selection functions. Density estimates of these inventories ranged from 10.4 bears/1,000 km 2 in a portion of the Yahk PU to 36.2/1,000 km 2 in a portion of the Central Purcell PU. The PU boundaries, however, were often in wide valleys that were settled by people and grizzly bears were uncommon. Extrapolating the spatial density models across the entire PUs resulted in reduced densities of 7.2/1,000 km 2 in the Yahk, 12.7/1,000 km 2 in the South Purcell and 18.3/ 1,000 km 2 in the Central Purcell. Rocky. During the 1980s and 1990s, this PU had the second highest estimated hunter kill rate in the province (5.8%) and although 64.5% of the hunter kill were males, their average age was only 6.0 and the average age of females was 5.8 years. These statistics suggested a high kill rate but in 1996 the kill was greatly reduced from an average of 34.7 bears/year to 11.2 bears/year. Even then this PU had the sixth highest estimated kill rate in the province and was highlighted by Artelle et al. (2013) as 1 of the 3 that had 3 over mortality periods between 2001 and 2011. Between 2000 and 2011, however, the average age of female bears killed by hunters had increased to 6.3 years and the average age of males increased to 9.1 years. The slope of the weighted regression of proportion of males in the hunter kill since 1990 against age was positive (b ¼ 0.011; P ¼ 0.017). A population inventory conducted in 1998 in a 3,114-km 2 portion of the Rocky unit, 2 years after the hunter kill rate was reduced, resulted in an estimate of 22.5 bears/1,000 km 2 (95% CI ¼ 20 29; Mowat et al. 2005). This density estimate was higher than the 12 15 bears/1,000 km 2 in Banff Park, an unhunted population also on the east slopes of the Rocky Mountains (Sawaya et al. 2012) nor was it an outlier in the modeling exercise by Mowat et al. (2013b). Southern Rockies and Flathead. These adjacent units are between Glacier National Park, Montana, and Banff National Park, Alberta. At 1.8 and 1.7 bears/1,000 km 2 / year, the South Rockies and the Flathead had the 2 highest recorded kill densities in the province. In the South Rockies, the rate of recorded non-hunter kills was the highest in the province and 4.5 times the average and more females than males were killed for these non-hunting causes. Despite heavy hunting, the population in the southern Flathead increased (l ¼ 1.07) from 1979 to 1998 but then declined from 1999 to 2010 primarily because of the high density of bears plus a decade-long huckleberry failure, which led to greatly reduced reproductive rates (McLellan 2015). Data from 2010 to 2015 suggest this decreasing trend has abated (B.N. McLellan and G. Mowat, British Columbia Ministry of Forests, Lands and Natural Resource Operations, unpublished data). Two DNA-based mark-recapture inventories occurred across the entire Flathead PU and density estimates were 40.5/1,000 km 2 in 1997 and 31.7/1,000 km 2 in 2007 (Mowat et al. 2013a). An ongoing DNA-based inventory also suggested a decline from 2007 (first year of measurement) to 2010 and then an increase (Mowat and Lamb 2016). Because of excessive female kill, the hunt in the South Rockies was closed in 2011 but was partially reopened in 2013 because a spatially explicit mark-recapture analysis of DNA-based hair trapping data suggested a relatively high density of 37.7 bears/1,000 km 2. But recent trend analysis suggested that, like the Flathead, the South Rockies population has been in decline since 2006 and by 2013 was estimated to have a density of only 20.7 bears/1,000 km 2 (Mowat and Lamb 2016). The age and sex of hunter kill data for these units may be initially viewed to be at odds with the telemetry monitoring of individuals (McLellan 2015) and ongoing DNA-based trend monitoring (Mowat and Lamb 2016). Between 1980 and 1999, when the populations were thought to be generally increasing, 66.7% of hunter kills in these 2 units were males and their average age was 7.1 years. Between 2000 and 2014, when the population was thought to be in decline, 70.8% of hunter kill were males, but their average age had increased to 9.5 years. The slope of the proportion of males in the hunter kill since 2000, when the populations were in decline, was positive but not significantly different from zero (b ¼ 0.009, P ¼ 0.21). DISCUSSION Our analyses provide evidence that, at least at broad spatial and temporal scales, the legal hunting of grizzly bears has been sustainable in British Columbia and the overkill hypothesis is not supported. The British Columbia Procedure used to determine the target number of grizzly bears that can be sustainably killed by hunters was based primarily on modeling work by Harris (1984, 1986). Empirical studies within British Columbia and in neighboring jurisdictions reported natural mortality rates of grizzly bears >2 years of age to be lower than those used by Harris (1984, 1986). With less natural mortality, populations can sustain more human-caused mortality. The 4 6% target rate for all human-caused mortality used in British Columbia appears to be conservative and in most cases, could accommodate some of the uncertainty in population estimates. Our estimates of the sustainable mortality rates of adult female bears fall between the 16% for populations with high recruitment and 1% for populations with very low recruitment (Eberhardt 1990). Specifically for bears in the GYE, Harris et al. (2006) estimated that, depending on the level of inter-annual variation, independent females (2 yr old) could support a 9 10% total mortality rate and likely maintain a stable or increasing population. Consistent with the more complex, stochastic models used by Harris et al. (2006), our results suggest independent females could sustain an 8.3% human-caused kill rate in addition to the 1% natural mortality for a total mortality rate of 9.3%. 8 The Journal of Wildlife Management 9999()

In contrast, models used by McLoughlin (2003) suggested that most grizzly bear populations in North America could only tolerate a 3 5% human-caused kill rate. McLoughlin (2003), however, used survival rates that already included human-caused mortality (including hunting) as base rates upon which additional harvest was applied. Harris et al. (2006) suggested that if McLoughlin (2003) had used the actual natural mortality rates, then he would have estimated the sustainable mortality rate for independent females in the GYE to be 9.2%, which is almost identical to our result for this population. Drawing firm conclusions from the age and sex of hunter kill is notoriously difficult (Garshelis 1990) and, without additional information, will likely raise more intriguing questions than clear answers. This equivocal outcome was upheld by our analyses. Our modeling exercise suggested that if as few as 51 56% of the kill were males and their average age was as young as 5.5 6.7 years, then the overall kill rate should be marginally sustainable provided reproductive rates, and both juvenile and adult natural survival rates were similar to those documented in Banff, the GYE, NCDE, or Flathead during decade 1. The increasing average age of hunter-killed bears (particularly males) and increasing proportion of males in the hunter kill across the province over time, suggests a light harvest (Gilbert et al. 1978, Harris and Metzger 1987b, Garshelis 1990) and likely an expanding population. At the finer scale of the South Rockies and Flathead PUs, however, concluding that the populations were expanding because the proportion of males and the average age of the males in the kill was increasing, would have been incorrect. These results are almost identical to those predicted by our harvest model when we used vital rates from the Flathead during this time period (i.e., decade 3), vulnerabilities based on province-wide hunter kill statistics, and the hunter kill set to where l ¼ 1.0 (Table 3). The decline in reproduction of this population (McLellan 2015) would have resulted in few young bears being recruited and thus available to hunters so the average age of males killed increased. The regression of the proportion of the hunter kill that were males by age also failed to detect a decline. The insensitivity of this indicator was likely because the longevity of bears (25 30 yr) masked the rapid changes in vital rates and thus population trends. Our results highlight a problem with using age and sex of kill as indicators of sustainable harvest without monitoring the assumed constant recruitment. The Flathead and South Rockies PUs are in the extreme southeastern corner of British Columbia and cover <2% of hunted grizzly bear distribution. Although it is unlikely that such a trend is synchronized over an area as large and diverse as the distribution of grizzly bears in British Columbia, the spatial extent of this decline and how common similar declines are should be a concern for managers. We find the most intriguing question generated by our province-wide analyses of the kill data is what happened to the females? If there was simply no decline in the proportion of males killed by hunters as age increased then a light harvest with negligible effect on the sex ratio of the living bears would have been suggested. But we found a significant increase in the proportion of males with increasing age. We also found the death of almost twice as many males as females were reported. There are 3 reasons why fewer female deaths were reported than males: an unequal sex ratio at birth, reporting errors (Schliebe et al. 1999), or females have higher natural and unreported human-caused mortality rates. All of these factors may contribute, but it is unlikely that the first 2 account for the difference; identifying sex using DNA of 220 previously checked kills suggested <2% error rate and no systematic bias (G. Mowat, unpublished data). It is probable that, unlike the results of the telemetry studies that show similar natural mortality rates for males and females but higher non-hunting kill rates for males, that females across most of British Columbia have higher unrecorded mortality rates, both natural and human-caused. All 4 studies we relied upon to measure survival rates were in areas with considerable human-bear interface and yet all populations were generally increasing. In all 4 studies, human-caused mortality accounted for >80% of the deaths of radio-collared bears 2 years of age. Across most of British Columbia there is far less human-bear interface than in these study areas and perhaps female bears, all of which must die eventually, do so of natural causes more commonly. Although sample sizes were small, 2 of 2 deaths of female bears monitored in the mountains of central British Columbia by Ciarniello et al. (2009) and 3 of 3 female bears in the mountains of southwestern British Columbia (McLellan and McLellan 2015) died of natural causes. It is also possible that, because of their protective behavior when with cubs, more females than males are killed by ungulate hunters and not reported (Mace et al. 2012, McLellan 2015). Even in an area without human settlement and the highest density of hunter-killed bears in British Columbia, McLellan (2015) reported more radio-collared females were killed by people for reasons other than bear hunting than were by bear hunters. For people concerned with grizzly bear conservation, we believe that the population inventories are the most reassuring confirmation that decades of hunting has not led to population collapse. Although bear densities on the Alaskan Peninsula, Kodiak Island, and islands in southeastern Alaska, where there are numerous salmon spawning streams, are much higher than anywhere in British Columbia, there are no areas in British Columbia with comparable habitat conditions. The DNA-based markrecapture density estimates in 2 areas from mainland coastal Alaska just north of British Columbia were 34.6 and 64.2/ 1,000 km 2 when corrected for non-bear habitat (i.e., rock and ice) by Mowat et al. (2013b). These estimates are comparable to the corrected densities of 39.3, 46.6, and 57.5/1,000 km 2 in coastal British Columbia. For other non-coastal areas with similar habitat, the inventories suggest hunted populations in British Columbia had bear densities at least as high as in jurisdictions where there was no hunting. For example, the average density estimate of the 21 inventories reported in British Columbia where bears were hunted but there were no or limited amounts of salmon (31.2 bears/1,000 km 2 )was similar to the 30.0/1,000 km 2 Kendall et al. (2008) estimated for Glacier National Park, Montana and adjacent areas even McLellan et al. Sustainability of Grizzly Hunt 9