Gut microbiome biogeography in reindeer supersedes millennia of ecological and evolutionary separation.

Ruminants are dependent on their gut microbiomes for nutrient extraction from plant diets. However, knowledge about the composition, diversity, function, and spatial structure of gut microbiomes, especially in wild ruminants, is limited, largely because analysis has been restricted to faeces or the rumen. In two geographically separated reindeer subspecies, 16S rRNA gene amplicon sequencing revealed strong spatial structuring, and pronounced differences in microbial diversity of at least 33 phyla across the stomach, small intestine, and large intestine (including faeces). The main structural feature was the Bacteroidota to Firmicutes ratio, which declined from the stomach to the large intestine, likely reflecting functional adaptation. Metagenome shotgun sequencing also revealed highly significant structuring in the relative occurrence of carbohydrate-active enzymes (CAZymes). CAZymes were enriched in the rumen relative to the small and large intestines. Interestingly, taxonomic diversity was highest in the large intestine, suggesting an important and understudied role for this organ. Despite the two study populations being separated by an ocean and six millennia of evolutionary history, gut microbiome structuring was remarkably consistent. Our study suggests a strong selection for gut microbiome biogeography along the gastrointestinal tract in reindeer subspecies.

Nutrient intake and its possible drivers in free-ranging European brown bears (Ursus arctos arctos).

The dietary nutrient profile has metabolic significance and possibly contributes to species' foraging behavior. The brown bear (Ursus arctos) was used as a model species for which dietary ingredient and nutrient concentrations as well as nutrient ratios were determined annually, seasonally and per reproductive class. Brown bears had a vertebrate- and ant-dominated diet in spring and early summer and a berry-dominated diet in fall, which translated into protein-rich and carbohydrate-rich diets, respectively. Fiber concentrations appeared constant over time and averaged at 25% of dry matter intake. Dietary ingredient proportions differed between reproductive classes; however, these differences did not translate into a difference in dietary nutrient concentrations, suggesting that bears manage to maintain similar nutrient profiles with selection of different ingredients. In terms of nutrient ratios, the dietary protein to non-protein ratio, considered optimal at around 0.2 (on metabolizable energy basis), averaged around 0.2 in this study in fall and around 0.8 in spring and summer. We introduced the minimal non-fat to fat ratio necessary for efficient maintenance metabolism. This ratio varied across seasons but never fell beneath the theoretically estimated minimum to ensure metabolic efficiency. This population thus managed to ingest diets that never exerted a lack of glucogenic substrate, suggesting that metabolic efficiency may either be a driver of active diet selection or that natural resources available to bears did not constitute a constraint in this respect. Given the considerable proportion of fiber in the diet of brown bears, the relevance of this nutrient and its role in foraging behavior might be underestimated.

Land cover type modulates the distribution of litter in a Nordic cultural landscape.

Litter pollution is a global environmental problem that occurs in virtually all ecosystems. Scientific research on anthropogenic litter and its environmental impacts focusses predominantly on plastics and the marine environment. Little empirical knowledge exists about the distribution and ecological impacts of litter in terrestrial environments, where most litter is produced. To start closing that knowledge gap, we investigated the distribution of litter in a cultural landscape in central Norway and in relation to land cover types. We registered and collected litter in 110 survey plots that were randomly stratified across various land cover types. Our results show that land cover type modulates the occurrence, abundance, fragments size, and that litter is most present and abundant in or near land cover types associated with high human activities. Plastic was by far the most common litter material type, although the litter community (in terms of materials type) was not independent from land cover type. This knowledge can help to inform and optimize litter management and clean-up activities in terrestrial landscapes. How and to what extent the spatial structure of the litter community mediates ecological effects across various land cover types remains unknown to a large extent and warrants further study.

Directed endozoochorous dispersal by scavengers facilitate sexual reproduction in otherwise clonal plants at cadaver sites.

The regeneration niche of many plant species involves spatially and temporally unpredictable disturbances, called recruitment windows of opportunity. However, even species with clear dispersal adaptations such as fleshy berries may not successfully reach such elusive regeneration microsites. Ericaceous, berry-producing species in the northern hemisphere demonstrate this dispersal limitation. They are said to display a reproductive paradox owing to their lack of regeneration in apparently suitable microsites despite considerable investment in producing large quantities of berries.Cadavers generate vegetation-denuded and nutrient-rich disturbances termed cadaver decomposition islands (CDIs). Cadavers attract facultative scavengers with considerable capacity for endozoochorous seed dispersal. We hypothesize that CDIs facilitate recruitment in berry-producing ericaceous species due to endozoochorous dispersal directed toward favorable microsites with low competition.We examined seedling establishment within a permanent, semi-regular 10 × 10 m grid across an ungulate mass die-off on the Hardangervidda plateau in southeastern Norway. Competing models regarding the relative importance of factors governing recruitment were evaluated, specifically cadaver location (elevated seed rain) and microsite conditions (competition).We found that CDIs did facilitate seedling establishment, as cadaver density was the best predictor of seedling distribution. Other important factors governing seedling establishment such as percentage cover of soil and vascular plants alone were inadequate to explain seedling establishment. Synthesis: This study provides a novel understanding of sexual reproduction in species with cryptic generative reproduction. The directed nature of endozoochorous dispersal combined with long-distance dispersal abilities of medium to large vertebrate scavengers toward cadavers allows plants to exploit the advantageous but ephemeral resource provided by CDIs.

Animal-borne video systems provide insight into the reproductive behavior of the Asian black bear.

Previous studies on the mating system of the Asian black bear (Ursus thibetanus) have been limited to observations of captive populations and estimations of multiple paternities. Hence, the mating system of wild bears remains poorly understood. Animal-borne camera systems (i.e., cameras mounted on animals) provide novel tools to study the behavior of elusive animals. Here, we used an animal-borne video system to record the activities of wild bears during the mating season. Video camera collars were attached to four adult Asian black bears (male "A" and "B," and female "A" and "B") captured in Tokyo, central Japan, in May and June 2018. The collars were retrieved in July 2018, after which the video data were downloaded and analyzed in terms of bear activity and mating behavior. All the bears were found to interact with other uniquely identifiable bears for some of the time (range 9-22 days) during the deployment period (range 36-45 days), and multiple mating in males was documented. Both males and females exhibited different behaviors on social days (i.e., days when the bear interacted with conspecifics) compared with solitary days (i.e., days with no observed interactions with conspecifics). Compared with solitary days, the bears spent a lower proportion of time on foraging activities and higher proportion of time on resting activities on social days. Our results suggest that Asian black bears have a polygamous mating system, as both sexes consort and potentially mate with multiple partners during a given mating season. Furthermore, bears appeared to reduce their foraging activities on social days and engaged more in social interactions.

Grading fecal consistency in an omnivorous carnivore, the brown bear: Abandoning the concept of uniform feces.

Grading the fecal consistency of carnivores is a frequently used tool for monitoring gut health and overall digestion. Several fecal consistency grading systems are available for mainly felids and canids. No such system exists for the brown bear (Ursus arctos Linnaeus, 1758). We aim at extending current fecal consistency grading systems with a scoring system for brown bears. The system was set up during a diet study with nine individuals fed a variety of diets including beef meat, rabbit, fruit, and grass-fruit-pellet mix in an incomplete crossover design. One additional individual was included opportunistically and was fed the typical zoo diet (vegetable-fruit-meat-pellet diet). All feces from the collection period were photographed, graded by "handling the feces" and visually inspected for dietary components. Based on a total of 446 feces, a six-point scale for uniform fecal consistencies was established. In 11% of all feces, two distinct consistencies could be distinguished, a feature that appears in other carnivore species as well. Hence, an additional grading system for dual consistencies was developed. The fecal consistency of brown bears is heavily dependent on the diet items processed before defecation with the general observation that the more vegetation or whole prey, the firmer the feces, and at certain proportions of the latter, the higher the chance for dual fecal consistencies to occur. The results indicate that in bears, diet may have a strong effect on fecal consistency, hampering animal health assessments without prior knowledge of the diet.

Heritability of head size in a hunted large carnivore, the brown bear (Ursus arctos).

Wild animal populations experience selection pressures from both natural and anthropogenic sources. The availability of extensive pedigrees is increasing along with our ability to quantify the heritability and evolvability of phenotypic traits and thus the speed and potential for evolutionary change in wild populations. The environment may also affect gene expressions in individuals, which may in turn affect the potential of phenotypic traits to respond to selection. Knowledge about the relationship between the genetic and environmental components of phenotypic variation is particularly relevant, given ongoing anthropogenically driven global change. Using a quantitative genetic mixed model, we disentangled the genetic and environmental components of phenotypic variance in a large carnivore, the brown bear (Ursus arctos). We combined a pedigree covering ~1,500 individual bears over seven generations with location data from 413 bears, as well as data on bear density, habitat characteristics, and climatic conditions. We found a narrow-sense heritability of 0.24 (95% CrI: 0.06-0.38) for brown bear head size, showing that the trait can respond to selection at a moderate speed. The environment contributed substantially to phenotypic variation, and we partitioned this into birth year (5.9%), nonadditive among-individual genetic (15.0%), and residual (50.4%) environmental effects. Brown bear head circumference showed an evolvability of 0.2%, which can generate large changes in the trait mean over some hundreds of generations. Our study is among the first to quantify heritability of a trait in a hunted large carnivore population. Such knowledge about the degree to which species experiencing hunting can respond to selection is crucial for conservation and to make informed management decisions. We show that including important environmental variables when analyzing heritability is key to understanding the dynamics of the evolutionary potential of phenotypic traits.

Hunting promotes sexual conflict in brown bears.

The removal of individuals through hunting can destabilize social structure, potentially affecting population dynamics. Although previous studies have shown that hunting can indirectly reduce juvenile survival through increased sexually selected infanticide (SSI), very little is known about the spatiotemporal effects of male hunting on juvenile survival. Using detailed individual monitoring of a hunted population of brown bears (Ursus arctos) in Sweden (1991-2011), we assessed the spatiotemporal effect of male removal on cub survival. We modelled cub survival before, during and after the mating season. We used three proxies to evaluate spatial and temporal variation in male turnover; distance and timing of the closest male killed and number of males that died around a female's home range centre. Male removal decreased cub survival only during the mating season, as expected in seasonal breeders with SSI. Cub survival increased with distance to the closest male killed within the previous 1·5 years, and it was lower when the closest male killed was removed 1·5 instead of 0·5 year earlier. We did not detect an effect of the number of males killed. Our results support the hypothesis that social restructuring due to hunting can reduce recruitment and suggest that the distribution of the male deaths might be more important than the overall number of males that die. As the removal of individuals through hunting is typically not homogenously distributed across the landscape, spatial heterogeneity in hunting pressure may cause source-sink dynamics, with lower recruitment in areas of high human-induced mortality.

Temporal effects of hunting on foraging behavior of an apex predator: Do bears forego foraging when risk is high?

Avoiding predators most often entails a food cost. For the Scandinavian brown bear (Ursus arctos), the hunting season coincides with the period of hyperphagia. Hunting mortality risk is not uniformly distributed throughout the day, but peaks in the early morning hours. As bears must increase mass for winter survival, they should be sensitive to temporal allocation of antipredator responses to periods of highest risk. We expected bears to reduce foraging activity at the expense of food intake in the morning hours when risk was high, but not in the afternoon, when risk was low. We used fine-scale GPS-derived activity patterns during the 2 weeks before and after the onset of the annual bear hunting season. At locations of probable foraging, we assessed abundance and sugar content, of bilberry (Vaccinium myrtillus), the most important autumn food resource for bears in this area. Bears decreased their foraging activity in the morning hours of the hunting season. Likewise, they foraged less efficiently and on poorer quality berries in the morning. Neither of our foraging measures were affected by hunting in the afternoon foraging bout, indicating that bears did not allocate antipredator behavior to times of comparably lower risk. Bears effectively responded to variation in risk on the scale of hours. This entailed a measurable foraging cost. The additive effect of reduced foraging activity, reduced forage intake, and lower quality food may result in poorer body condition upon den entry and may ultimately reduce reproductive success.

Bears and berries: species-specific selective foraging on a patchily distributed food resource in a human-altered landscape.

ABSTRACT: When animals are faced with extraordinary energy-consuming events, like hibernation, finding abundant, energy-rich food resources becomes particularly important. The profitability of food resources can vary spatially, depending on occurrence, quality, and local abundance. Here, we used the brown bear (Ursus arctos) as a model species to quantify selective foraging on berries in different habitats during hyperphagia in autumn prior to hibernation. During the peak berry season in August and September, we sampled berry occurrence, abundance, and sugar content, a proxy for quality, at locations selected by bears for foraging and at random locations in the landscape. The factors determining selection of berries were species specific across the different habitats. Compared to random locations, bears selected locations with a higher probability of occurrence and higher abundance of bilberries (Vaccinium myrtillus) and a higher probability of occurrence, but not abundance, of lingonberries (Vaccinium vitis-idaea). Crowberries (Empetrum hermaphroditum) were least available and least used. Sugar content affected the selection of lingonberries, but not of bilberries. Abundance of bilberries at random locations decreased and abundance of lingonberries increased during fall, but bears did not adjust their foraging strategy by increasing selection for lingonberries. Forestry practices had a large effect on berry occurrence and abundance, and brown bears responded by foraging most selectively in mature forests and on clearcuts. This study shows that bears are successful in navigating human-shaped forest landscapes by using areas of higher than average berry abundance in a period when abundant food intake is particularly important to increase body mass prior to hibernation. SIGNIFICANCE STATEMENT: Food resources heterogeneity, caused by spatial and temporal variation of specific foods, poses a challenge to foragers, particularly when faced with extraordinary energy-demanding events, like hibernation. Brown bears in Sweden inhabit a landscape shaped by forestry practices. Bilberries and lingonberries, the bears' main food resources in autumn prior to hibernation, show different temporal and habitat-specific ripening patterns. We quantified the bears' selective foraging on these berry species on clearcuts, bogs, young, and mature forests compared to random locations. Despite a temporal decline of ripe bilberries, bears used locations with a greater occurrence and abundance of bilberries, but not lingonberries. We conclude that bears successfully navigated in this heavily human-shaped landscape by selectively foraging in high-return habitats for bilberries, but did not compensate for the decline in bilberries by eating more lingonberries.

Socio-ecological features other than sex affect habitat selection in the socially obligate monogamous Eurasian beaver.

Habitat selection is a context-dependent mechanism, in which both the internal state as well as external factors affect the behavior and decisions of an individual. This is well known for polygamous mammals, which are typically sexually dimorphic, and often express great variability in behavior and habitat selection between individuals as well between the sexes. Among monogamous mammals, however, variability in habitat selection should be explained by group characteristics and the presence of offspring rather than by sex. We evaluated this hypothesis in a socially monogamous rodent, the Eurasian beaver (Castor fiber), in a saturated Norwegian population. For the first time in this species we applied GPS tracking devices (N = 22 adult beavers, in 15 territories, 2009-2013), and used resource selection functions (i) to document population-wide habitat selection and the importance of 'territory' therein, and (ii) to evaluate which socio-ecological factors explained potential individual differences in habitat selection. We found that variation in habitat selection was stronger between territories than between years or individuals nested by territory. We identified that family size and the presence of kits, but not sex, explained individual variation in habitat selection. Adults with kits and/or larger families tended to exhibit low risk-taking behavior (avoiding human-related variables such as roads, buildings, and agricultural land), and stayed close to their main lodge (parental care). Our results show that habitat selection is a context-dependent mechanism even in a species which expresses very little behavioral and morphological dimorphism.

A "clearcut" case? Brown bear selection of coarse woody debris and carpenter ants on clearcuts.

Forest management alters habitat characteristics, resulting in various effects among and within species. It is crucial to understand how habitat alteration through forest management (e.g. clearcutting) affects animal populations, particularly with unknown future conditions (e.g. climate change). In Sweden, brown bears (Ursus arctos) forage on carpenter ants (Camponotus herculeanus) during summer, and may select for this food source within clearcuts. To assess carpenter ant occurrence and brown bear selection of carpenter ants, we sampled 6999 coarse woody debris (CWD) items within 1019 plots, of which 902 were within clearcuts (forests ⩽30 years of age) and 117 plots outside clearcuts (forests >30 years of age). We related various CWD and site characteristics to the presence or absence of carpenter ant galleries (nests) and bear foraging sign at three spatial scales: the CWD, plot, and clearcut scale. We tested whether both absolute and relative counts (the latter controlling for the number of CWD items) of galleries and bear sign in plots were higher inside or outside clearcuts. Absolute counts were higher inside than outside clearcuts for galleries (mean counts; inside: 1.8, outside: 0.8). CWD was also higher inside (mean: 6.8) than outside clearcuts (mean: 4.0). However, even after controlling for more CWD inside clearcuts, relative counts were higher inside than outside clearcuts for both galleries (mean counts; inside: 0.3, outside: 0.2) and bear sign (mean counts; inside: 0.03, outside: 0.01). Variables at the CWD scale best explained gallery and bear sign presence than variables at the plot or clearcut level, but bear selection was influenced by clearcut age. CWD circumference was important for both carpenter ant and bear sign presence. CWD hardness was most important for carpenter ant selection. However, the most important predictor for bear sign was the presence or absence of carpenter ant galleries. Bears had a high foraging "success" rate (⩾88%) in foraging CWD where galleries also occurred, which was assessed by summing CWD items with the concurrence of bear sign and galleries, divided by the sum of all CWD with bear sign. Clearcuts appeared to increase the occurrence of a relatively important summer food item, the carpenter ant, on Swedish managed forests for the brown bear. However, the potential benefit of this increase can only be determined from a better understanding of the seasonal and interannual variation of the availability and use of other important brown bear food items, berries (e.g. Vaccinium myrtillus and Empetrum spp.), as well as other primary needs for bears (e.g. secure habitat and denning habitat), within the landscape mosaic of managed forests.

Litter loss triggers estrus in a nonsocial seasonal breeder.

Sexually selected infanticide (SSI) is often presumed to be rare among seasonal breeders, because it would require a near immediate return to estrus after the loss of an entire litter during the mating season. We evaluated changes in reproductive strategies and the reproductive fate of females that experienced litter loss during the mating season in a seasonal breeder with strong evidence for SSI, the brown bear. First, we used a long-term demographic dataset (1986-2011) to document that a large majority of females (>91%) that lose their entire litter during the mating season in fact do enter estrus, mate, and give birth during the subsequent birthing season. Second, we used high-resolution movement data (2005-2011) to evaluate how females changed reproductive strategies after losing their entire litter during the mating season. We hypothesized that females would shift from the sedentary lifestyle typical for females with cubs-of-the-year to a roam-to-mate behavior typical for receptive females in no more than a few (∼3) days after litter loss. We found that females with cubs-of-the-year moved at about 1/3 of the rate and in a less bimodal diurnal pattern than receptive females during the mating season. The probability of litter loss was positively related with movement rate, suggesting that being elusive and sedentary is a strategy to enhance cub survival rather than a relic of cub mobility itself. The movement patterns of receptive females and females after litter loss were indistinguishable within 1-2 days after the litter loss, and we illustrate that SSI can significantly reduce the female interbirth interval (50-85%). Our results suggest that SSI can also be advantageous for males in seasonally breeding mammals. We propose that infanticide as a male reproductive strategy is more prevalent among mammals with reproductive seasonality than observed or reported.

Male reproductive strategy explains spatiotemporal segregation in brown bears.

Spatiotemporal segregation is often explained by the risk for offspring predation or by differences in physiology, predation risk vulnerability or competitive abilities related to size dimorphism. Most large carnivores are size dimorphic and offspring predation is often intraspecific and related to nonparental infanticide (NPI). NPI can be a foraging strategy, a strategy to reduce competition, or a male reproductive strategy. Spatiotemporal segregation is widespread among large carnivores, but its nature remains poorly understood. We evaluated three hypotheses to explain spatiotemporal segregation in the brown bear, a size-dimorphic large carnivore in which NPI is common; the 'NPI - foraging/competition hypothesis', i.e. NPI as a foraging strategy or a strategy to reduce competition, the 'NPI - sexual selection hypothesis', i.e. infanticide as a male reproductive strategy and the 'body size hypothesis', i.e. body-size-related differences in physiology, predation risk vulnerability or competitive ability causes spatiotemporal segregation. To test these hypotheses, we quantified spatiotemporal segregation among adult males, lone adult females and females with cubs-of-the-year, based on GPS-relocation data (2006-2010) and resource selection functions in a Scandinavian population. We found that spatiotemporal segregation was strongest between females with cubs-of-the-year and adult males during the mating season. During the mating season, females with cubs-of-the-year selected their resources, in contrast to adult males, in less rugged landscapes in relative close proximity to certain human-related variables, and in more open habitat types. After the mating season, females with cubs-of-the-year markedly shifted their resource selection towards a pattern more similar to that of their conspecifics. No strong spatiotemporal segregation was apparent between females with cubs-of-the-year and conspecifics during the mating and the postmating season. The 'NPI - sexual selection hypothesis' best explained spatiotemporal segregation in our study system. We suggest that females with cubs-of-the-year alter their resource selection to avoid infanticidal males. In species exhibiting NPI as a male reproductive strategy, female avoidance of infanticidal males is probably more common than observed or reported, and may come with a fitness cost if females trade safety for optimal resources.