Karyn D. Rode

Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change

Polar bears (PBs) are superbly adapted to the extreme Arctic environment and have become emblematic of the threat to biodiversity from global climate change. Their divergence from the lower-latitude brown bear provides a textbook example of rapid evolution of distinct phenotypes. However, limited mitochondrial and nuclear DNA evidence conflicts in the timing of PB origin as well as placement of the species within versus sister to the brown bear lineage. We gathered extensive genomic sequence data from contemporary polar, brown, and American black bear samples, in addition to a 130,000- to 110,000-y old PB, to examine this problem from a genome-wide perspective. Nuclear DNA markers reflect a species tree consistent with expectation, showing polar and brown bears to be sister species. However, for the enigmatic brown bears native to Alaskas Alexander Archipelago, we estimate that not only their mitochondrial genome, but also 5–10% of their nuclear genome, is most closely related to PBs, indicating ancient admixture between the two species. Explicit admixture analyses are consistent with ancient splits among PBs, brown bears and black bears that were later followed by occasional admixture. We also provide paleodemographic estimates that suggest bear evolution has tracked key climate events, and that PB in particular experienced a prolonged and dramatic decline in its effective population size during the last ca. 500,000 years. We demonstrate that brown bears and PBs have had sufficiently independent evolutionary histories over the last 4–5 million years to leave imprints in the PB nuclear genome that likely are associated with ecological adaptation to the Arctic environment.

Reduced body size and cub recruitment in polar bears associated with sea ice decline

Rates of reproduction and survival are dependent upon adequate body size and condition of individuals. Declines in size and condition have provided early indicators of population decline in polar bears (Ursus maritimus) near the southern extreme of their range. We tested whether patterns in body size, condition, and cub recruitment of polar bears in the southern Beaufort Sea of Alaska were related to the availability of preferred sea ice habitats and whether these measures and habitat availability exhibited trends over time, between 1982 and 2006. The mean skull size and body length of all polar bears over three years of age declined over time, corresponding with long-term declines in the spatial and temporal availability of sea ice habitat. Body size of young, growing bears declined over time and was smaller after years when sea ice availability was reduced. Reduced litter mass and numbers of yearlings per female following years with lower availability of optimal sea ice habitat, suggest reduced reproductive output and juvenile survival. These results, based on analysis of a long-term data set, suggest that declining sea ice is associated with nutritional limitations that reduced body size and reproduction in this population.

Variation in the nutritional value of primate foods: Among trees, time periods, and areas

The study of nutritional ecology has proven to be useful for understanding many aspects of primate behavior and ecology and is a valuable tool in primate conservation. However, to date this approach has had limited application since chemical analyses of food items is very time-consuming and collections of perishable food material are often made in remote field locations. Such logistic difficulties have led to plant material being collected in a variety of fashions, and it is not known how variation in collection method might influence our understanding of the chemical basis of dietary selection. A standardization of collection methods is greatly needed to allow for direct comparison among studies. To develop an appropriate standardized method and to evaluate past research, it is necessary to understand along what dimensions plant chemistry varies. We evaluated variation in nutritional value—protein, fiber, digestibility, alkaloids, saponins, cyanogenic glycocides, and minerals—of leaf material from species eaten by red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) of Kibale National Park, Uganda. We consider variation at 3-levels: among trees, time periods, and areas. While there was considerable variation among species with respect to protein, digestibility, and saponins, there was also variation among individuals of the same species; in fact, individuals may vary by as much as 20%. The average coefficients of variation (CV) among individuals of the same species are 13.4 for protein, 12 for digestibility, and 43 for saponins, while the average CV among species are 35, 31.3, and 82.4, respectively. No species showed a variable response with respect to testing for the presence or absence of cyanogenic glycocides, while 2 of 11 species tested for alkaloids showed a variable response. Over 2 years there was evidence of variation among time periods in the chemical composition of the same food items. The protein-to-fiber ratio of mature leaves of the same species collected from 4 sites separated by 12 km within Kibale was also variable and in some cases the variation among sites was greater than the differences among species. For example, while Funtumia latifolia had little variation in protein-to-fiber ratio at 3 sites (0.44 at all sites), the remaining site was 28% greater. Because temporal variation is less than variation among individuals, it is likely more important to sample from multiple trees at a single point in time than to sample across time. However, the most accurate assessment of nutrient intake is obtained by collecting plant material from the specific trees selected for consumption.

Variation in the response of an Arctic top predator experiencing habitat loss: feeding and reproductive ecology of two polar bear populations

Polar bears (Ursus maritimus) have experienced substantial changes in the seasonal availability of sea ice habitat in parts of their range, including the Beaufort, Chukchi, and Bering Seas. In this study, we compared the body size, condition, and recruitment of polar bears captured in the Chukchi and Bering Seas (CS) between two periods (1986-1994 and 2008-2011) when declines in sea ice habitat occurred. In addition, we compared metrics for the CS population 2008-2011 with those of the adjacent southern Beaufort Sea (SB) population where loss in sea ice habitat has been associated with declines in body condition, size, recruitment, and survival. We evaluated how variation in body condition and recruitment were related to feeding ecology. Comparing habitat conditions between populations, there were twice as many reduced ice days over continental shelf waters per year during 2008-2011 in the SB than in the CS. CS polar bears were larger and in better condition, and appeared to have higher reproduction than SB bears. Although SB and CS bears had similar diets, twice as many bears were fasting in spring in the SB than in the CS. Between 1986-1994 and 2008-2011, body size, condition, and recruitment indices in the CS were not reduced despite a 44-day increase in the number of reduced ice days. Bears in the CS exhibited large body size, good body condition, and high indices of recruitment compared to most other populations measured to date. Higher biological productivity and prey availability in the CS relative to the SB, and a shorter recent history of reduced sea ice habitat, may explain the maintenance of condition and recruitment of CS bears. Geographic differences in the response of polar bears to climate change are relevant to range-wide forecasts for this and other ice-dependent species.

Sexual dimorphism, reproductive strategy, and human activities determine resource use by brown bears

Despite significant sexual dimorphism and differing reproductive strategies in carnivores, sexual segregation is rarely studied and is often overlooked in the management of wild populations. Potential nutritional constraints imposed by sexual dimorphism and differing reproductive strategies between the sexes have important implications, particularly when combined with differential effects of human activities on sex and age classes. We examined the effects of sexual dimorphism, reproductive strategies, and human activities (bear-viewing and hunting) on resource use by different sex and age classes of brown bears (Ursus arctos). Sexual segregation of habitat use and effects of experimental bear-viewing were quantified at a single site in south-central Alaska, U.S.A., by capturing, collaring, and observing brown bears at a salt marsh and salmon stream. Effects of salmon capture rate, availability of alternative salmon runs, harvest pressure, and numbers of annual visitors on sex and age class use were examined from data collected or previously published from 13 other sites. Bear-viewing sites on salmon streams where salmon capture rates were low (<4 salmon/hour) resulted in low use by adult males (<10% of all bears), except for sites with falls. However, maximum male use of viewing areas also depended on the availability of alternative salmon streams and harvest pressure. Use of habitats by females with dependent young was significantly related to the prevalence of adult males at the site. Thus, both sexual dimorphism and differing reproductive strategies led to sexual segregation in habitat use by bears. As a result of infanticide, females with young appear to prioritize avoidance of male bears over avoidance of humans when choosing habitats, in contrast to responses documented in herbivores. Because carnivores often exhibit both sexual dimorphism and infanticide, selection for sexual segregation is likely to be high. In these cases, the nutritional demands of large adult males, balanced with responses to human activity, drive dynamic temporal and spatial distributions of individuals in the population.

Mineral Resource Availability and Consumption by Colobus in Kibale National Park, Uganda

Very little information exists on mineral nutrition of tropical, forest-dwelling species, yet minerals are critical to growth, reproduction, and survival. We examined the mineral resources available to and consumed by colobus in Kibale National Park, Uganda. We combined behavioral data on black-and-white (Colobus guereza) and red colobus (Piliocolobus tephrosceles) in a section of unlogged forest, a heavily logged area, and a forest fragment with mineral analysis of their foods to estimate the proportion of the diet containing specific minerals (mineral content). We compared mineral content of colobus foods (natural and crops) across plant parts and among plant species. Additionally, we estimated mineral intake of frugivorous primates in Kibale from published dietary data and our estimates of mineral content of foods. Dietary mineral content for all colobus groups and frugivorous species is similar despite significant differences in the mineral content of foods. Ripe and unripe fruits are lower in mineral content than most foods. Foods rarely consumed, such as bark, petioles, and caterpillars have high levels of some minerals. The mineral content of crops is low in comparison to that ofnatural foods. For all colobus groups of both species, sodium content of foods was extremely low and iron content was generally low, suggesting that intake isbelow suggested requirements, though current suggested iron requirements may overestimate physiological needs. Copper content was marginal and deficient seasonally for most colobus groups. Despite a sodium-limiting environment, only one of 8 colobus groups appeared to select sodium; however, this may be due to a lack of variation in sodium content among plant species and a positive correlation between high plant sodium content and secondary compounds. Despite the lack of selection for sodium by colobines, some behaviors point to a potential sodium deficiency, including urine drinking, consumption of high-sodium swamp plants, and use of mud-puddles.

Effects of sea ice extent and food availability on spatial and temporal distribution of polar bears during the fall open-water period in the Southern Beaufort Sea

We investigated the relationship between sea ice conditions, food availability, and the fall distribution of polar bears (Ursus maritimus) in terrestrial habitats of the Southern Beaufort Sea via weekly aerial surveys in 2000–2005. Aerial surveys were conducted weekly during September and October along the Southern Beaufort Sea coastline and barrier islands between Barrow and the Canadian border to determine polar bear density on land. The number of bears on land both within and among years increased when sea-ice was retreated furthest from the shore. However, spatial distribution also appeared to be related to the availability of subsistence-harvested bowhead whale (Balaena mysticetus) carcasses and the density of ringed seals (Phoca hispida) in offshore waters. Our results suggest that long-term reductions in sea-ice could result in an increasing proportion of the Southern Beaufort Sea polar bear population coming on land during the fall open-water period and an increase in the amount of time individual bears spend on land.

Variation in the Diets of Cercopithecus Species: Differences within Forests, among Forests, and across Species

Dietary data have been used to address numerous theoretical issues, yet we have little understanding of dietary flexibility in primates. Previous comparative research has either explicitly or implicitly assumed that the closer the phylogenetic proximity between two taxa, or the spatial proximity between two populations of the same taxon, the more similar their diets will be. We examine such assumptions by making dietary comparisons among arboreal Cercopithecus species at the intergroup, interdemic, interpopulational, and interspecific levels. Our analyses reveal considerable variation and sometimes the magnitude of the variation of particular contrasts is unexpected. We conclude that dietary flexibility blurs our traditional trophic assessment of primate species. Thus, a study of the diet of a single group, in a specific habitat, at one point in time may not be representative of the species as a whole. This flexibility suggests that a profitable avenue of future research is quantifying the degree of flexibility that different primate lineages have in their digestive strategies.

Nutritional ecology of elephants in Kibale National Park, Uganda, and its relationship with crop-raiding behaviour

This study investigated the nutritional ecology of forest elephants in Kibale National Park, Uganda relative to crop-raiding behaviour, and examined nutritional differences between crops and food consumed by wild elephants. An index of dietary nutrient concentration was determined by quantifying the species and parts of plants consumed along feeding trails, collecting food items, and analysing foods for energy, fibre, protein, minerals and secondary compounds. Frequency of crop raiding was quantified over 13 mo. Energy and protein concentration was within suggested levels, but concentrations of several minerals, particularly sodium, were low relative to requirements based on captive elephants and values reported for other wild populations. The very low sodium concentrations of Kibale elephant diets and low availability of alternative sodium sources, such as soil or water, suggest that sodium drive is very likely in this population. Crops consumed by Kibale elephants had higher Na concentrations and lower concentrations of fibre and secondary compounds than wild diets. The known attraction of elephants to mineral sources throughout their range and the low mineral concentration of leaves, fruits, bark, and stems consumed by forest elephant in this study suggest that mineral nutrition is likely to be an important factor driving elephant behaviour and patterns of habitat use.

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.