Viable populations of American black bears (Ursus americanus; hereafter, black bear) and grizzly bears (U. arctos) were extirpated from the interior mountain ranges of Nevada, USA, by the early1900s, in part as a result of predator removal efforts and landscape-scale habitat changes caused by deforestation in several mountain ranges across the state (Beckmann and Lackey 2008, Lackey et al. 2013). However, remnant populations of black bears occurred in the Sierra Nevada along the Nevada–California border near Lake Tahoe and these populations began to expand (Malaney et al. 2018). It is thought that this expansion was a result of a slow reforestation of Nevada's mountain ranges initiated by the nation's growing dependency on fossil fuels post–World War I, combined with changes in grazing practices and forestry practices, such as wildfire control (Nevada Forests Industries Committee 1963). By the early 1980s, black bear sightings, human–bear conflicts, and bear deaths from vehicles remained rare events in Nevada (LeCount 1979, Goodrich and Berger 1994). By the late 1980s, a population of black bears occupied western Nevada (Goodrich 1990) and by the mid-1990s, conflicts between humans and black bears began to rise sharply in the Lake Tahoe Basin and the western portion of the Great Basin Desert (Beckmann 2002; Beckmann and Berger 2003a,b). A 10-fold increase in the annual number of complaints and a 17-fold increase in bear mortalities, due to collisions with vehicles, were reported between the 1990s and early 2000s (Beckmann 2002; Beckmann and Berger 2003a,b). These increasing human–bear conflicts were the impetus for a long-term research and monitoring effort beginning in 1997 to understand black bear ecology and conservation in the region (Beckmann 2002; Beckmann and Berger 2003a,b; Lackey et al. 2013). Current estimates of the population are 500–700 individuals and the population is expanding in the Great Basin, including areas with increased human presence and activity (Lackey et al. 2013).

Black bears in western Nevada are exhibiting demographic and behavioral changes influenced by anthropogenic modification of the environment. These changes include shifts in home range size and location, activity patterns, denning chronology, fecundity, dietary changes, mass, and demography (Beckmann and Berger 2003a,b; Beckmann and Lackey 2008; Lackey et al. 2013; Johnson et al. 2015). Fully understanding the effects of human-modified landscapes on the individual bear and at the population level is important to help managers make management decisions to reduce human–black bear conflicts.

Continued expansion of the black bear population in Nevada may influence conservation and management planning efforts in areas heavily populated by humans. Areas that offer suitable bear habitat, despite anthropogenic modification, may be recolonized by bears in the future and should also be evaluated (Beckmann and Lackey 2008, Lackey et al. 2013). Given that Nevada is one of the fastest growing states in the United States with a human population about to reach 3 million (World Population Review 2016), and is a state in which most of the population resides in urban settings, the rapidly increasing human footprint in Nevada will bring challenges with the continued expansion of the bear population. Here we use hair samples collected from bears in the Sierra Nevada and western Great Basin from 2003 to 2010 and stable carbon and nitrogen isotope analysis to assess differences in biological, chronological, and spatial factors affecting use of anthropogenic foods. Stable isotopes can indicate greater use of human foods because the corn-based diet causes an enrichment of ¹³C and high meat content increases ¹⁵N. Our primary objective was to gain a better understanding of factors associated with bear use of human-derived foods. Such information is important to guide efficient and effective management of human–bear conflicts and to determine what type of data should be collected when a bear is handled as a result of a complaint or conflict.

Study area

The current distribution of black bears in Nevada is restricted to the Carson Range of the Sierra Nevada, Pine Nut Mountains, Pine Grove Hills, Sweetwater Range, Virginia Range, Aurora Hills, and the Wassuk Range in western Nevada (Beckmann and Berger 2003a,b; Lackey 2004). These mountain ranges and associated basins cover an area of approximately 12,000 km² and are characterized by steep topography with high granite peaks and deep canyons. Mountain ranges are separated by desert basins that range from 16 to 64 km across (Grayson 1993). These basins are often large expanses of unsuitable habitat (e.g., large areas of sagebrush [Artemisia spp.]) that bears do not use as primary habitat (Goodrich 1990, Beckmann and Berger 2003a). Black bears in this region are at the eastern edge of their current range in the Great Basin, with the closest Great Basin population being approximately 750 km to the east in Utah. However, recent evidence suggests the black bear population is expanding back into historical habitat in the central and eastern Great Basin (Lackey et al. 2013). The study area extends from the Carson Range of the Sierra Nevada eastward to the Virginia Range and Pine Nut Mountains, and from Reno south to the Aurora Hills. Many bears were captured in response to conflicts, but these captures occurred primarily at the wildland–urban interface of cities and towns within the study area and included developed areas in the Lake Tahoe Basin: Incline Village, Glenbrook, Cave Rock, Zephyr Cove, and Stateline, and the lower elevation urban centers of Reno, Carson City, Minden, and Gardnerville.

Materials and methods

Variable classification

Body mass measurements alone do not account for the overall condition of a bear because of confounding effects of age and sex. To account for differences in body mass associated with age and sex, we constructed 3 categories using the mean mass (average) and 1 standard deviation above mean (above average) and 1 standard deviation below mean (below average) for the 6 combinations of age and sex from all recorded bears (Table 1). We also used sex and age classification as separate variables. We defined 3 age classes of independent bears as 1.5–3.0 years, 3.5–6.5 years, and ≥7.0 years for our analyses because nutritional requirements and experience using anthropogenic foods can vary by age (Beckmann and Berger 2003a). We used urban, wildland, and unknown classifications to assess any differences in food habits by access to human developments (see Sample collection section for description of classification system for urban–wildland).

Table 1.

Body mass categories^a accounting for sex and age group based on a 95% confidence interval for all American black bears (Ursus americanus) captured during this study in Nevada, USA, 2003–2010.

We handled bears year-round, so we used a season variable to examine any potential differences throughout the year. Season classifications are as follows: winter (1 Dec to 28 Feb), spring (1 Mar to 31 May), summer (1 Jun to 31 Aug), and autumn (1 Sep to 30 Nov). These season classifications are based on assessments of food availability throughout the year (Beckmann and Berger 2003a,b; Lackey et al. 2013). Typically, there are more natural foods available during the late-spring to autumn period than during the winter and early spring periods. We noted that, in our study area, anthropogenic food was available year-round, including during the winter when a lack of natural foods should lead to hibernation (generally from November to April–May; Johnson et al. 2018). As a result of this food availability, we documented bear activity throughout the year, and some bears gaining mass through the winter months because of availability of garbage. A better understanding of seasonal patterns can help target management efforts and resources to reduce potential human–bear conflicts.

We used an information-theoretic approach and developed an a priori suite of linear regression models to examine associations of sex, age class, body mass, molt, season, year, and urban versus wildland classification with stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values (Burnham and Anderson 2002). We constructed design variables for all categorical variables. We used package MuMin (Bartoń 2016), based on Burnham and Anderson (2002;  https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf, Accessed Mar 2017) in Program R (v3.3.1; R Core Team 2016) to conduct the linear regressions, and calculate Akaike's second-order information criterion (AIC_c) for small sample size for each model and model-averaging for each parameter. We examined which parameters were associated with variations of carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values during 2003–2010. We used adjusted R² values to evaluate the variation captured with our best model(s). We used regression diagnostics with slope (β) to evaluate the assumptions for linear regression. We used model-averaging to report slope values.

Results

We sampled 193 black bears from 24 October 2003 through 12 August 2010. We omitted 18 bears sampled in the month of July and 2 bears with unknown body mass. Of the remaining 173 bears, 107 (39 F, 68 M) were classified as urban bears, 24 (13 F, 11 M) as wildland bears, and 42 (15 F, 27 M) were of unknown status. Urban bears had a mean δ¹³C of –20.18‰ (SD = 1.49) and a mean δ¹⁵N of 5.51‰ (SD = 1.30), whereas wildland bears had a mean δ¹³C of –21.07‰ (SD = 1.49) and a mean δ¹⁵N of 4.68‰ (SD = 1.27). Bears of unknown status had a mean δ¹³C of –20.14‰ (SD = 1.79) and a mean δ¹⁵N of 5.47‰ (SD = 1.44).

Our top 3 models for δ¹³C had 85% of AIC_c model weights (w_i) and included biological (mass category, sex), timing (molt stage), and spatial (urban–wildland–unknown) variables (Table 2). These 3 models (C12, C11, and C8) had ΔAIC_c values ≤0.95. All other models had ΔAIC_c values ≥3.53 and w_i ≤ 0.06. Bears in the above-average mass category had enriched ¹³C compared with the reference class of below-average mass (β = 1.36, CI = 0.86–1.86; Table 3). Values for δ¹³C for bears of average mass were not different from those below-average mass (Table 3). Wildland bears had depleted ¹³C compared with the reference class of urban bears (β = –0.86, CI = –1.42 to –0.31). Stable isotope values for δ¹³C for bears of unknown status were not different from bears classified as urban. Finally, δ¹³C stable isotope values were depleted for hair samples collected postmolting compared with the premolting stage (Table 3).

Table 2.

Model-selection results based on second-order Akaike's Information Criteria (AIC_c) to test association of δ¹³C stable isotope values with various attributes of American black bears (Ursus americanus) in Nevada, USA, 2003–2010.

Table 3.

Parameter estimates of δ¹³C using model-averaging for hair collected from American black bears (Ursus americanus) in Nevada, USA, 2003–2010.

For δ¹⁵N stable isotope values, 2 top models (model N7 and N12) carried 91% of AIC_c model weight and included the variables molt, sex, and mass category (Table 4). All other models had ΔAIC_c values ≥6.45. Males had substantially enriched δ¹⁵N compared with females (Table 5). For hair samples collected postmolting, δ¹⁵N stable isotope values were smaller compared with samples collected during the premolting stage (Table 5).

Table 4.

Model-selection results based on second-order Akaike's Information Criteria (AIC_c) to test association of δ¹⁵N stable isotope values with various attributes of American black bears (Ursus americanus) in Nevada, USA, 2003–2010.

Table 5.

Parameter estimates of δ¹⁵N using model-averaging for hair collected from American black bears (Ursus americanus) in Nevada, USA, 2003–2010.

Isotopic signatures of all bears except one fell within the mixing space of diet samples (Fig. 1) and convergence criteria were met. One 2-year-old male bear captured in August 2007 was out of the range of possible δ¹⁵N and δ¹³C, based on the food items used in the analysis (Fig. 1). Overall however, wildland bears had depleted ¹³C and ¹⁵N compared with urban bears as demonstrated by the mixing models (Fig. 1), indicating they were less likely to access human foods than urban bears. There was great variability in the range of food items used by all categories (Fig. 1), but generally, urban bears had a higher median percentage (increase of 3.8%) of human foods in their diet compared with wildland bears (Table 6). Therefore, location relative to human developments affected the use of anthropogenic food for some, but not all, bears.

Fig. 1.

Mixing space and stable isotope signatures of American black bear (Ursus americanus) hair samples and food samples from the Program R package MixSIAR (v.3.1; Stock and Semmens 2013). Hair samples were classified as fixed effects of urban, wildland, or unknown. Food samples were classified using 3 categories: plants (onsite collection), animals (Hobson et al. 2000), and human-derived foods (Jahren and Kraft 2008).

Table 6.

Mixing model analysis of the proportions of animal, human-derived, and plant foods in the diet of American black bears (Ursus americanus) in Nevada, USA, 2003–2010, using δ¹³C and δ¹⁵N. Animal values were from Hobson et al. (2000), human values from Jahren and Kraft (2008) for beef and chicken, and plant values were from samples collected in Nevada. Discrimination factor from a review by Teunissen van Manen et al. (2011). CI is credible interval.

Discussion

Based on the top 3 models, the primary factors associated with δ¹³C included biological (mass category, sex), timing (molt), and spatial (urban–wildland class) factors. Bears in the above-average mass category had more enriched ¹³C than those in the below-average mass category. For δ¹⁵N, the primary factors included sex and molt and, to a lesser degree, body mass category. Similar to the carbon isotope results, bears in the above-average mass category were more enriched with ¹⁵N than bears in the below-average mass category. Mass category and wildland–urban interface (WUI) may have not been as important in predicting enrichment of ¹⁵N as ¹³C because natural foods may vary greatly in protein and nitrogen stable isotopes, whereas enrichment of ¹³C would be primarily controlled by access to human foods. Access to deer and other wild game and insects could vary, regardless of mass category and WUI location and could greatly affect enrichment of ¹⁵N. Teunissen van Manen et al. (2014) also found large variability in δ¹⁵N based on natural food availability (specifically hard mast production). In comparison, Hopkins et al. (2012) found only that stable isotopes of nitrogen were useful in predicting food-conditioned bears in Yosemite National Park, California, where there was less human development.

Based on our data, we do not know if heavier bears were more likely to use anthropogenic foods in the form of garbage, or if bears at the WUI were heavier because they use these anthropogenic food sources. We suggest that both explanations contributed. The mixing-space results supported this idea—33% of urban bears were in the above-average mass category and only 7% of wild bears were in the above-average mass category.

We did not consider sex an important variable for δ¹³C because the confidence interval of the beta value included 0. However, several studies, including previous work from Nevada (Beckmann et al. 2003a,b), indicate that male bears tend to have increased access to anthropogenic foods and other sources of food with more protein, and thus would have enriched ¹⁵N (e.g., Merkle et al. 2011, Johnson et al. 2015). Molt was included in the top model for δ¹³C and δ¹⁵N, with negative parameter estimates for postmolt hair samples (representative of late spring–early summer diet) relative to premolt hair samples (representative of late summer–early autumn diet) and may reflect greater use of anthropogenic foods in the late summer and early autumn, when bears are typically entering hyperphagia.

Previous studies, including those from western Nevada, have demonstrated that black bears form commensal relationships with humans at the WUI through the use of anthropogenic foods, mostly in the form of garbage (Beckmann and Berger 2003a,b; Beckmann and Lackey 2004, 2008; Merkle et al. 2011, 2013; Lackey et al. 2013; Johnson et al. 2015; Lewis et al. 2015). The result that bears use anthropogenic food sources is not surprising, but the use of δ¹³C and δ¹⁵N allowed us to examine the relative prevalence in the diet of these sources of foods compared with naturally occurring wild foods for bears that we had classified behaviorally as urban or wildland. Based on δ¹³C and δ¹⁵N analyses, urban bears in western Nevada used both natural and anthropogenic foods, whereas the food habits of wildland bears fell into a tighter mixture space with a greater contribution of natural foods, particularly plants. Bears of unknown classification occupied the entire mixing space of diet samples, suggesting that both urban and wildland bears were included in the unknown classification category.

Johnson et al. (2015) found that bears in drier systems, including western Nevada, selected for areas of human development and anthropogenic foods more consistently than did bears in higher quality habitats. Our results from stable isotope analyses suggested that bears (both those classified as urban and wildland) in the Lake Tahoe Basin and western Nevada had isotope signatures representing elevated ¹⁵N and ¹³C in their diets compared with other more natural areas with American black bear (Hopkins et al. 2012, Teunissen van Manen et al. 2014) or grizzly bear populations (Bentzen et al. 2014) in North America studied in a similar manner.

From a purely physiological perspective, garbage represents an ideal food source for bears; it is predictable in space and time (i.e., garbage is set out the same day of the week, week after week); it is replenished after use (i.e., a bear can eat all the calories out of dumpster and come back the next week and new calories are available, which is not generally possible with wild sources of food); and the discrepancy between the caloric value in dumpsters compared with natural foods in the Great Basin (the driest system in North America where bears are native) probably makes this food source more likely to be used in this xeric environment then in other systems.

The idea that garbage may be the ultimate resource for bears from a physiological perspective has been well-demonstrated in our Lake Tahoe Basin and western Nevada study site, where it has earlier been shown that 1) bears that utilize garbage have increased body mass (a good correlate of fitness [cub production] in bears) compared with wildland counterparts; 2) females utilizing garbage have lower age at first reproduction compared with wildland females; 3) females utilizing garbage have larger mean litter sizes compared with wildland conspecifics; 4) bears foraging on garbage spend less time acquiring food resources on a daily basis compared with wildland conspecifics; and 5) bears foraging on garbage have smaller home ranges (Beckmann and Berger 2003a,b; Beckmann and Lackey 2008). All of these lines of evidence suggest that garbage is a good resource from a physiological perspective because ultimately it leads to high levels of fitness and it is a more reliable resource than natural foods. This is especially true in arid climates that undergo frequent drought cycles, such as our study system. However, even though females utilizing garbage saw an increase in fecundity, their realized reproductive output was actually lower than the number of cubs they produced because most of those cubs were eventually killed in collisions with cars before the age of dispersal (Beckmann and Lackey 2008).

However, not all bears use human foods at high levels, even though they are living near human developments. Just because an individual bear is living in, or adjacent to, the wildland–urban interface does not preclude that bear from foraging on wild foods found within the region in addition to anthropogenic foods. One would expect individual variation to occur in the level of utilization of wild and anthropogenic foods across bears, even within the wildland–urban interface. Bentzen et al. (2014) found that some grizzly bears were considered food-conditioned and some used natural foods, based on their diet from an oilfield region of the Arctic Coastal Plain in Alaska. Individual variation in diet had great management implications because nonlethal methods were not effective in controlling human–bear conflicts for food-conditioned grizzly bears.

We acknowledge that we may have missed some potential wild and anthropogenic food items used by these bears, which could have biased the proportions of anthropogenic, animal, and plant foods identified in our analysis (Phillips et al. 2014). However, taken in totality, the model results for both δ¹³C and δ¹⁵N isotopes suggested that bears in western Nevada exhibit higher and more consistent levels of use for anthropogenic foods in the form of garbage than other systems in North America where stable isotope analyses have been completed (Hopkins et al. 2012, Bentzen et al. 2014, Teunissen van Manen et al. 2014). In addition, our models supported the idea that large male bears tended to use anthropogenic sources of food most often and may have limited use by other sex and age classes. The great variability of human food use by urban and unknown bears was probably indicative that proximity to humans is not always related to actual use of anthropogenic food sources. Our results indicated that, in this xeric system, limiting access to anthropogenic food sources will be critical in reducing human–bear conflict and enhancing coexistence. Future work should further evaluate individual variation and characteristics of bears in urban settings to gain insight into the level at which they use anthropogenic foods.