Joy Erlenbach

Macronutrient optimization and energy maximization determine diets of brown bears

Abstract Many animals consume mixed diets that maximize their fitness by optimizing macronutrient intake. We tested whether brown bears (Ursus arctos), generalist omnivores that hibernate, regulated their diet to a common nutrient target, achieved a nutrient target related to fitness, and selected a nutrient target that differed between seasons and from other species with differing life histories. When given unlimited access to 2 or 3 highly digestible foods containing primarily protein, carbohydrate, or lipid, brown bears selected mixed diets in which protein provided 17% ± 4% SD of the metabolizable energy and 22% ± 6% of the dry matter. This dietary protein content maximized the rate of gain per unit of energy consumed, is similar to the level preferred by other omnivores, and is less than that preferred by obligate carnivores. Between seasons, bears selected similar dietary protein levels, although the proportion of lipid was higher during the fall than during the spring. Bears strongly preferred lipids over carbohydrates, as did other carnivores, but they used lipids and carbohydrates with equal efficiency to produce a dietary protein content that maximized mass gain per unit of energy intake. Thus, dietary sources of lipids and carbohydrates play an interchangeable and important role in determining the productivity of bears that goes beyond their role in providing energy.

IMMOBILIZATION OF GRIZZLY BEARS (URSUS ARCTOS) WITH DEXMEDETOMIDINE, TILETAMINE, AND ZOLAZEPAM

Abstract Safe and effective immobilization of grizzly bears (Ursus arctos) is essential for research and management. Fast induction of anesthesia, maintenance of healthy vital rates, and predictable recoveries are priorities. From September 2010 to May 2012, we investigated these attributes in captive and wild grizzly bears anesthetized with a combination of a reversible &agr;2 agonist (dexmedetomidine [dexM], the dextrorotatory enantiomer of medetomidine) and a nonreversible N-methyl-d-aspartate (NMDA) agonist and tranquilizer (tiletamine and zolazepam [TZ], respectively). A smaller-than-expected dose of the combination (1.23 mg tiletamine, 1.23 mg zolazepam, and 6.04 µg dexmedetomidine per kg bear) produced reliable, fast ataxia (3.7±0.5 min, x̄±SE) and workable anesthesia (8.1±0.6 min) in captive adult grizzly bears. For wild bears darted from a helicopter, a dose of 2.06 mg tiletamine, 2.06 mg zolazepam, and 10.1 µg dexmedetomidine/kg produced ataxia in 2.5±0.3 min and anesthesia in 5.5±1.0 min. Contrary to published accounts of bear anesthesia with medetomidine, tiletamine, and zolazepam, this combination did not cause hypoxemia or hypoventilation, although mild bradycardia (<50 beats per min) occurred in most bears during the active season. With captive bears, effective dose rates during hibernation were approximately half those during the active season. The time to first signs of recovery after the initial injection of dexMTZ was influenced by heart rate (P<0.001) and drug dose (P<0.001). Intravenous (IV) injection of the reversal agent, atipamezole, significantly decreased recovery time (i.e., standing on all four feet and reacting to the surrounding environment) relative to intramuscular injection. Recovery times (25±8 min) following IV injections of the recommended dose of atipamezole (10 µg/µg of dexmedetomidine) and half that dose (5 µg/µg) did not differ. However, we recommend use of the full dose based on the appearance of a more complete recovery. Field trials confirmed that the dexMTZ + atipamezole protocol is safe, reliable, and predictable when administered to wild grizzly bears, especially during helicopter capture operations.

Isotopic Incorporation and the Effects of Fasting and Dietary Lipid Content on Isotopic Discrimination in Large Carnivorous Mammals

There has been considerable emphasis on understanding isotopic discrimination for diet estimation in omnivores. However, discrimination may differ for carnivores, particularly species that consume lipid-rich diets. Here, we examined the potential implications of several factors when using stable isotopes to estimate the diets of bears, which can consume lipid-rich diets and, alternatively, fast for weeks to months. We conducted feeding trials with captive brown bears (Ursus arctos) and polar bears (Ursus maritimus). As dietary lipid content increased to ∼90%, we observed increasing differences between blood plasma and diets that had not been lipid extracted (∆13Ctissue-bulk diet) and slightly decreasing differences between plasma δ13C and lipid-extracted diet. Plasma Δ15Ntissue-bulk diet increased with increasing protein content for the four polar bears in this study and data for other mammals from previous studies that were fed purely carnivorous diets. Four adult and four yearling brown bears that fasted 120 d had plasma δ15N values that changed by <±2‰. Fasting bears exhibited no trend in plasma δ13C. Isotopic incorporation in red blood cells and whole blood was ≥6 mo in subadult and adult bears, which is considerably longer than previously measured in younger and smaller black bears (Ursus americanus). Our results suggest that short-term fasting in carnivores has minimal effects on δ13C and δ15N discrimination between predators and their prey but that dietary lipid content is an important factor directly affecting δ13C discrimination and indirectly affecting δ15N discrimination via the inverse relationship with dietary protein content.

Phenological synchronization disrupts trophic interactions between Kodiak brown bears and salmon

Significance Climate change is altering the seasonal timing of biological events, effectively rescheduling the potential interactions among species. We know specialist consumers suffer when they fail to synchronize with their prey; however, little is known about how generalist consumers respond to phenological shifts across multiple food resources. This reshuffling may create novel temporal overlap between foods that were once separated in time. We examined how a generalist consumer, the Kodiak brown bear, responded when two key foods, red elderberry and sockeye salmon, became synchronized. Bears switched from eating salmon to elderberries, disrupting an ecological link that typically fertilizes terrestrial ecosystems and generates high mortality rates for salmon. These results demonstrate an underappreciated mechanism by which climate-altered phenologies can alter food webs. Climate change is altering the seasonal timing of life cycle events in organisms across the planet, but the magnitude of change often varies among taxa [Thackeray SJ, et al. (2016) Nature 535:241–245]. This can cause the temporal relationships among species to change, altering the strength of interaction. A large body of work has explored what happens when coevolved species shift out of sync, but virtually no studies have documented the effects of climate-induced synchronization, which could remove temporal barriers between species and create novel interactions. We explored how a predator, the Kodiak brown bear (Ursus arctos middendorffi), responded to asymmetric phenological shifts between its primary trophic resources, sockeye salmon (Oncorhynchus nerka) and red elderberry (Sambucus racemosa). In years with anomalously high spring air temperatures, elderberry fruited several weeks earlier and became available during the period when salmon spawned in tributary streams. Bears departed salmon spawning streams, where they typically kill 25–75% of the salmon [Quinn TP, Cunningham CJ, Wirsing AJ (2016) Oecologia 183:415–429], to forage on berries on adjacent hillsides. This prey switching behavior attenuated an iconic predator–prey interaction and likely altered the many ecological functions that result from bears foraging on salmon [Helfield JM, Naiman RJ (2006) Ecosystems 9:167–180]. We document how climate-induced shifts in resource phenology can alter food webs through a mechanism other than trophic mismatch. The current emphasis on singular consumer-resource interactions fails to capture how climate-altered phenologies reschedule resource availability and alter how energy flows through ecosystems.

Validation of mercury tip-switch and accelerometer activity sensors for identifying resting and active behavior in bears

Abstract Activity sensors are often included in wildlife transmitters and can provide information on the behavior and activity patterns of animals remotely. However, interpreting activity-sensor data relative to animal behavior can be difficult if animals cannot be continuously observed. In this study, we examined the performance of a mercury tip-switch and a tri-axial accelerometer housed in collars to determine whether sensor data can be accurately classified as resting and active behaviors and whether data are comparable for the 2 sensor types. Five captive bears (3 polar [Ursus maritimus] and 2 brown [U. arctos horribilis]) were fitted with a collar specially designed to internally house the sensors. The bears’ behaviors were recorded, classified, and then compared with sensor readings. A separate tri-axial accelerometer that sampled continuously at a higher frequency and provided raw acceleration values from 3 axes was also mounted on the collar to compare with the lower resolution sensors. Both accelerometers more accurately identified resting and active behaviors at time intervals ranging from 1 minute to 1 hour (≥91.1% accuracy) compared with the mercury tip-switch (range = 75.5–86.3%). However, mercury tip-switch accuracy improved when sampled at longer intervals (e.g., 30–60 min). Data from the lower resolution accelerometer, but not the mercury tip-switch, accurately predicted the percentage of time spent resting during an hour. Although the number of bears available for this study was small, our results suggest that these activity sensors can remotely identify resting versus active behaviors across most time intervals. We recommend that investigators consider both study objectives and the variation in accuracy of classifying resting and active behaviors reported here when determining sampling interval.

The quantification of reproductive hormones in the hair of captive adult brown bears and their application as indicators of sex and reproductive state

We used enzyme immunoassays to measure testosterone, progesterone, estradiol and cortisol concentrations in serial hair samples collected from captive adult brown bears. Reproductive hormone levels changed throughout the year in step with different reproductive events underscoring the strong potential for these measurement to be used to augment non-invasive genetic sampling.

Phenological tracking associated with increased salmon consumption by brown bears

There is growing interest in the ecological significance of phenological diversity, particularly in how spatially variable resource phenologies (i.e. resource waves) prolong foraging opportunities for mobile consumers. While there is accumulating evidence of consumers moving across landscapes to surf resource waves, there is little data quantifying how phenological tracking influences resource consumption due to the challenge of documenting all the components of this ecological phenomenon (i.e., phenological variation, consumer movement, resource consumption, and consumer fitness). We examined the space use of GPS collared female brown bears to quantify the exploitation of a salmon resource wave by individual bears. We then estimated salmon consumption levels in the same individuals using stable isotope and mercury analyses of hair. We found strong positive relationships between time spent on salmon streams and percent salmon in assimilated diets (R2 = 0.70) and salmon mass consumed (R2 = 0.49). Salmon abundance varied 2.5-fold between study years, yet accounting for salmon abundance did not improve salmon consumption models. Resource abundance generally is viewed as the key variable controlling consumption levels and food web dynamics. However, our results suggest that in intact watersheds of coastal Alaska with abundant salmon runs, interannual variation in salmon abundance likely has less effect on salmon consumption than individual variation in bear foraging behavior. The results complement previous work to demonstrate the importance of phenological variation on bear foraging behavior and fitness.

Plasticity in physiological condition of female brown bears across diverse ecosystems

Variation in life history strategies facilitates the near global distribution of mammals by expanding realized niche width. We investigated physiological plasticity in the spring body composition of adult female brown bears (Ursus arctos) across 4 diverse Alaskan ecosystems. Brown bears are a highly intelligent omnivore with a historic range spanning much of North America, Europe, and Asia. We hypothesized that body mass, fat mass, lean mass, and total caloric content would increase across populations with increasing food resource availability. Throughout their range, brown bears enter a period of torpor during winter months, decreasing their metabolic rate as an adaptation to this period of reduced food availability. They also give birth to and nourish offspring during this time. Due to this specific life history strategy, we further hypothesized that proportional body fat and the proportion of total calories derived from fat would be consistent across populations. Our results supported our first hypothesis: body, fat, and lean masses, and caloric content of bears across populations increased with the quality and abundance of available food. However, the proportional body fat content and proportion of calories from fat differed across populations indicating population-specific strategies to meet the demands of reduced seasonal food availability, offspring production and rearing, and climate as well as some plasticity to respond to environmental change or ecosystem perturbations. Investigations of body condition and energetics benefit from combined assessments of absolute, proportional, and caloric metrics to understand the nuances of brown bear physiological dynamics across and within populations.