Mammal communities of primeval forests as sentinels of global change.

Understanding the drivers and consequences of global environmental change is crucial to inform predictions of effects on ecosystems. We used the mammal community of Bialowieza Forest, the last lowland near-primeval forest in temperate Europe, as a sentinel of global change. We analyzed changes in stable carbon (δ13 C) and nitrogen (δ15 N) isotope values of hair in 687 specimens from 50 mammal species across seven decades (1946-2011). We classified mammals into four taxonomic-dietary groups (herbivores, carnivores, insectivores, and bats). We found a significant negative trend in hair δ15 N for the mammal community, particularly strong for herbivores. This trend is consistent with temporal patterns in nitrogen deposition from (15 N depleted) industrial fertilizers and fossil fuel emissions. It is also in line with global-scale declines in δ15 N reported in forests and other unfertilized, non-urban terrestrial ecosystems and with local decreases in N foliar concentrations. The global depletion of 13 C content in atmospheric CO2 due to fossil fuel burning (Suess effect) was detected in all groups. After correcting for this effect, the hair δ13 C trend became non-significant for both community and groups, except for bats, which showed a strong decline in δ13 C. This could be related to an increase in the relative abundance of freshwater insects taken by bats or increased use of methane-derived carbon in food webs used by bats. This work is the first broad-scale and long-term mammal isotope ecology study in a near-primeval forest in temperate Europe. Mammal communities from natural forests represent a unique benchmark in global change research; investigating their isotopic temporal variation can help identify patterns and early detections of ecosystem changes and provide more comprehensive and integrative assessments than single species approaches.

Spatial ecology of conflicts: unravelling patterns of wildlife damage at multiple scales.

Human encroachment into natural habitats is typically followed by conflicts derived from wildlife damage to agriculture and livestock. Spatial risk modelling is a useful tool to gain the understanding of wildlife damage and mitigate conflicts. Although resource selection is a hierarchical process operating at multiple scales, risk models usually fail to address more than one scale, which can result in the misidentification of the underlying processes. Here, we addressed the multi-scale nature of wildlife damage occurrence by considering ecological and management correlates interacting from household to landscape scales. We studied brown bear (Ursus arctos) damage to apiaries in the North-eastern Carpathians as our model system. Using generalized additive models, we found that brown bear tendency to avoid humans and the habitat preferences of bears and beekeepers determine the risk of bear damage at multiple scales. Damage risk at fine scales increased when the broad landscape context also favoured damage. Furthermore, integrated-scale risk maps resulted in more accurate predictions than single-scale models. Our results suggest that principles of resource selection by animals can be used to understand the occurrence of damage and help mitigate conflicts in a proactive and preventive manner.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

Metal(loid) exposure assessment and biomarker responses in captive and free-ranging European brown bear (Ursus arctos).

We investigated the level of five non-essential metal(loid)s (As, Cd, Hg, Tl, Pb) and nine essential metals (Mg, Ca, Mn, Fe, Co, Cu, Zn, Se, Mo) in hair and blood components of captive and free-ranging European brown bear populations in Croatia and Poland. Metal(loid) associations with biomarkers of oxidative stress (superoxide dismutase, SOD; glutathione-peroxidase, GSH-Px; malondialdehyde, MDA) and metal exposure (metallothionein, MT) were estimated in this top predatory mammal. Lead was the most abundant non-essential metal(loid) in both blood and hair, with 4 of 35 individuals having blood levels over 100 µg/L. A positive association was found between Pb level and SOD activity in blood. Free-ranging bears had higher blood SOD activity, Mn, Zn and Cd levels, hair Co, Cd, Tl and Pb compared to captive individuals, while the opposite was true for Mg and hair Ca thereby reflecting habitat and diet differences. With increasing age, animals showed lower levels of SOD activity and certain essential metals. Females had higher SOD activity and blood levels of some essential metals than males. Hair showed a higher Fe and Co level when sampled during the growth phase and was not predictive of non-essential metal(loid) blood levels. The established metal(loid) baseline values will enable future risk assessment in both captive and wild European brown bear populations.

Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale.

Understanding the distribution of biodiversity across the Earth is one of the most challenging questions in biology. Much research has been directed at explaining the species latitudinal pattern showing that communities are richer in tropical areas; however, despite decades of research, a general consensus has not yet emerged. In addition, global biodiversity patterns are being rapidly altered by human activities. Here, we aim to describe large-scale patterns of species richness and diversity in terrestrial vertebrate scavenger (carrion-consuming) assemblages, which provide key ecosystem functions and services. We used a worldwide dataset comprising 43 sites, where vertebrate scavenger assemblages were identified using 2,485 carcasses monitored between 1991 and 2018. First, we evaluated how scavenger richness (number of species) and diversity (Shannon diversity index) varied among seasons (cold vs. warm, wet vs. dry). Then, we studied the potential effects of human impact and a set of macroecological variables related to climatic conditions on the scavenger assemblages. Vertebrate scavenger richness ranged from species-poor to species rich assemblages (4-30 species). Both scavenger richness and diversity also showed some seasonal variation. However, in general, climatic variables did not drive latitudinal patterns, as scavenger richness and diversity were not affected by temperature or rainfall. Rainfall seasonality slightly increased the number of species in the community, but its effect was weak. Instead, the human impact index included in our study was the main predictor of scavenger richness. Scavenger assemblages in highly human-impacted areas sustained the smallest number of scavenger species, suggesting human activity may be overriding other macroecological processes in shaping scavenger communities. Our results highlight the effect of human impact at a global scale. As species-rich assemblages tend to be more functional, we warn about possible reductions in ecosystem functions and the services provided by scavengers in human-dominated landscapes in the Anthropocene.

Lessons from Bialowieza Forest on the history of protection and the world's first reintroduction of a large carnivore.

Understanding how the relationships between large carnivores and humans have evolved and have been managed through centuries can provide relevant insights for wildlife conservation. The management history of many large carnivores has followed a similar pattern, from game reserved for nobility, to persecuted pests, to conservation targets. We reconstructed the history of brown bear (Ursus arctos) management in Bialowieza Forest (Poland and Belarus) based on a detailed survey of historical literature and Russian archives. From the end of the Middle Ages to the end of 18th century, the brown bear was considered "animalia superiora" (i.e., game exclusively reserved for nobility and protected by law). Bears, also a source of public entertainment, were not regarded as a threat. Effective measures to prevent damages to traditional forest beekeeping were already in practice. In the beginning of 19th century, new game-management approaches allowed most forest officials to hunt bears, which became the primary target of hunters due to their valuable pelt. This, together with an effective anticarnivore policy enhanced by bounties, led to bear extirpation in 1879. Different approaches to scientific game management appeared (planned extermination of predators and hunting levels that would maintain stable populations), as did the first initiatives to protect bears from cruel treatment in captivity. Bear reintroduction in Bialowieza Forest began in 1937 and represented the world's first reintroduction of a large carnivore motivated by conservation goals. The outbreak of World War II spoiled what might have been a successful project; reproduction in the wild was documented for 8 years and bear presence for 13. Soft release of cubs born in captivity inside the forest but freely roaming with minimal human contact proved successful. Release of captive human-habituated bears, feeding of these bears, and a lack of involvement of local communities were weaknesses of the project. Large carnivores are key components of ecosystem-function restoration, and site-specific histories provide important lessons in how to preserve them for the future.

Seasonal species interactions minimize the impact of species turnover on the likelihood of community persistence.

Many of the observed species interactions embedded in ecological communities are not permanent, but are characterized by temporal changes that are observed along with abiotic and biotic variations. While work has been done describing and quantifying these changes, little is known about their consequences for species coexistence. Here, we investigate the extent to which changes of species composition impact the likelihood of persistence of the predator-prey community in the highly seasonal Bialowieza Primeval Forest (northeast Poland), and the extent to which seasonal changes of species interactions (predator diet) modulate the expected impact. This likelihood is estimated extending recent developments on the study of structural stability in ecological communities. We find that the observed species turnover strongly varies the likelihood of community persistence between summer and winter. Importantly, we demonstrate that the observed seasonal interaction changes minimize the variation in the likelihood of persistence associated with species turnover across the year. We find that these community dynamics can be explained as the coupling of individual species to their environment by minimizing both the variation in persistence conditions and the interaction changes between seasons. Our results provide a homeostatic explanation for seasonal species interactions and suggest that monitoring the association of interactions changes with the level of variation in community dynamics can provide a good indicator of the response of species to environmental pressures.

The challenge of implementing the European network of protected areas Natura 2000.

Established under the European Union (EU) Birds and Habitats Directives, Natura 2000 is one of the largest international networks of protected areas. With the spatial designation of sites by the EU member states almost finalized, the biggest challenge still lying ahead is the appropriate management of the sites. To evaluate the cross-scale functioning of Natura 2000 implementation, we analyzed 242 questionnaires completed by conservation scientists involved in the implementation of Natura 2000 in 24 EU member states. Respondents identified 7 key drivers of the quality of Natura 2000 implementation. Ordered in decreasing evaluation score, these drivers included: network design, use of external resources, legal frame, scientific input, procedural frame, social input, and national or local policy. Overall, conservation scientists were moderately satisfied with the implementation of Natura 2000. Tree modeling revealed that poor application of results of environmental impact assessments (EIA) was considered a major constraint. The main strengths of the network included the substantial increase of scientific knowledge of the sites, the contribution of nongovernmental organizations, the adequate network design in terms of area and representativeness, and the adequacy of the EU legal frame. The main weaknesses of Natura 2000 were the lack of political will from local and national governments toward effective implementation; the negative attitude of local stakeholders; the lack of background knowledge of local stakeholders, which prevented well-informed policy decisions; and the understaffing of Natura 2000 management authorities. Top suggestions to improve Natura 2000 implementation were increase public awareness, provide environmental education to local communities, involve high-quality conservation experts, strengthen quality control of EIA studies, and establish a specific Natura 2000 fund.

Mapping roadless areas in regions with contrasting human footprint.

In an increasingly human- and road-dominated world, the preservation of functional ecosystems has become highly relevant. While the negative ecological impacts of roads on ecosystems are numerous and well documented, roadless areas have been proposed as proxy for functional ecosystems. However, their potential remains underexplored, partly due to the incomplete mapping of roads. We assessed the accuracy of roadless areas identification using freely available road-data in two regions with contrasting levels of anthropogenic influence: boreal Canada and temperate Central Europe (Poland, Slovakia, Czechia, and Hungary). Within randomly selected circular plots (per region and country), we visually examined the completeness of road mapping using OpenStreetMap 2020 and assessed whether human influences affect mapping quality using four variables. In boreal Canada, roads were completely mapped in 3% of the plots, compared to 40% in Central Europe. Lower Human Footprint Index and road density values were related to greater incompleteness in road mapping. Roadless areas, defined as areas at least 1 km away from any road, covered 85% of the surface in boreal Canada (mean size ± s.d. = 272 ± 12,197 km2), compared to only 0.4% in temperate Central Europe (mean size ± s.d. = 0.6 ± 3.1 km2). By visually interpreting and manually adding unmapped roads in 30 randomly selected roadless areas from each study country, we observed a similar reduction in roadless surface in both Canada and Central Europe (27% vs 28%) when all roads were included. This study highlights the urgent need for improved road mapping techniques to support research on roadless areas as conservation targets and surrogates of functional ecosystems.

Testing foraging optimization models in brown bears: Time for a paradigm shift in nutritional ecology?

How organisms obtain energy to survive and reproduce is fundamental to ecology, yet researchers use theoretical concepts represented by simplified models to estimate diet and predict community interactions. Such simplistic models can sometimes limit our understanding of ecological principles. We used a polyphagous species with a wide distribution, the brown bear (Ursus arctos), to illustrate how disparate theoretical frameworks in ecology can affect conclusions regarding ecological communities. We used stable isotope measurements (δ13 C, δ15 N) from hairs of individually monitored bears in Sweden and Bayesian mixing models to estimate dietary proportions of ants, moose, and three berry species to compare with other brown bear populations. We also developed three hypotheses based on predominant foraging literature, and then compared predicted diets to field estimates. Our three models assumed (1) bears forage to optimize caloric efficiency (optimum foraging model), predicting bears predominately eat berries (~70% of diet) and opportunistically feed on moose (Alces alces) and ants (Formica spp. and Camponotus spp; ~15% each); (2) bears maximize meat intake (maximizing fitness model), predicting a diet of 35%-50% moose, followed by ants (~30%), and berries (~15%); (3) bears forage to optimize macronutrient balance (macronutrient model), predicting a diet of ~22% (dry weight) or 17% metabolizable energy from proteins, with the rest made up of carbohydrates and lipids (~49% and 29% dry matter or 53% and 30% metabolizable energy, respectively). Bears primarily consumed bilberries (Vaccinium myrtillus; 50%-55%), followed by lingonberries (V. vitis-idaea; 22%-30%), crowberries (Empetrum nigrum; 8%-15%), ants (5%-8%), and moose (3%-4%). Dry matter dietary protein was lower than predicted by the maximizing fitness model and the macronutrient balancing model, but protein made up a larger proportion of the metabolizable energy than predicted. While diets most closely resembled predictions from optimal foraging theory, none of the foraging hypotheses fully described the relationship between foraging and ecological niches in brown bears. Acknowledging and broadening models based on foraging theories is more likely to foster novel discoveries and insights into the role of polyphagous species in ecosystems and we encourage this approach.

A range-wide synthesis and timeline for phylogeographic events in the red fox (Vulpes vulpes).

BACKGROUND: Many boreo-temperate mammals have a Pleistocene fossil record throughout Eurasia and North America, but only few have a contemporary distribution that spans this large area. Examples of Holarctic-distributed carnivores are the brown bear, grey wolf, and red fox, all three ecological generalists with large dispersal capacity and a high adaptive flexibility. While the two former have been examined extensively across their ranges, no phylogeographic study of the red fox has been conducted across its entire Holarctic range. Moreover, no study included samples from central Asia, leaving a large sampling gap in the middle of the Eurasian landmass. RESULTS: Here we provide the first mitochondrial DNA sequence data of red foxes from central Asia (Siberia), and new sequences from several European populations. In a range-wide synthesis of 729 red fox mitochondrial control region sequences, including 677 previously published and 52 newly obtained sequences, this manuscript describes the pattern and timing of major phylogeographic events in red foxes, using a Bayesian coalescence approach with multiple fossil tip and root calibration points. In a 335 bp alignment we found in total 175 unique haplotypes. All newly sequenced individuals belonged to the previously described Holarctic lineage. Our analyses confirmed the presence of three Nearctic- and two Japan-restricted lineages that were formed since the Mid/Late Pleistocene. CONCLUSIONS: The phylogeographic history of red foxes is highly similar to that previously described for grey wolves and brown bears, indicating that climatic fluctuations and habitat changes since the Pleistocene had similar effects on these highly mobile generalist species. All three species originally diversified in Eurasia and later colonized North America and Japan. North American lineages persisted through the last glacial maximum south of the ice sheets, meeting more recent colonizers from Beringia during postglacial expansion into the northern Nearctic. Both brown bears and red foxes colonized Japan's northern island Hokkaido at least three times, all lineages being most closely related to different mainland lineages. Red foxes, grey wolves, and brown bears thus represent an interesting case where species that occupy similar ecological niches also exhibit similar phylogeographic histories.

90Sr and stable element levels in bones of brown bears: long-term trends in bear populations from Croatia and Poland.

The aim of this study was to investigate the temporal trends and geographical differences in 90Sr and stable element (Ba, Ca, Mn, Sr, Pb, Zn) levels in the bones of Croatian and Polish brown bear (Ursus arctos) populations. Experimental data suggest that in the decades after nuclear weapon tests and the Chernobyl accident, 90Sr bone activity concentrations decreased from 352 to 11 Bq kg-1 in the Croatian bear population (period 1982-2015) and from 831 to 27 Bq kg-1 in Polish bears (period 1962-2020). Calculated effective and ecological half-lives were 9 and 13 years for Croatian bears, and 15 and 31 years for Polish bears, respectively. Different temporal trends were noted in levels of Ba, Mn, Pb and Zn between the two countries with majority of bones having lower Pb, Sr and Zn in Croatian than in Polish bears. Estimated values for the soil-to-bear transfer of 90Sr were the same order of magnitude in the studied populations. Contrary to this, the estimated transfer of stable Sr was an order of magnitude lower for the Croatian bear population compared to Polish bears. The observed differences in soil-to-bear transfer between stable Sr and 90Sr found for Croatian bears might suggest the need for careful consideration on the use of stable Sr data as an analogue for 90Sr. To our knowledge, this is the first study that analysed 90Sr activity in tissue of brown bears. As such, it provides insight into the fate and behaviour of one of the most relevant anthropogenic radionuclides at the top of the food chain.

Stress and reproductive hormones in hair associated with contaminant metal(loid)s of European brown bear (Ursus arctos).

Environmental contaminants like arsenic (As), cadmium (Cd), mercury (Hg) or lead (Pb) may disrupt hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes due to their endocrine toxicity potential. Resulting long-term physiological stress or adverse effects on wildlife reproduction and ontogeny may cause detrimental effects at the individual and population levels. However, data on environmental metal(loid)s' impact on reproductive and stress hormones in wildlife, especially large terrestrial carnivores, are scarce. Hair cortisol, progesterone and testosterone concentrations were quantified and modelled with hair As, Cd, total Hg, Pb, biological, environmental and sampling factors to test for potential effects in free-ranging brown bears (Ursus arctos) from Croatia (N = 46) and Poland (N = 27). Testosterone in males (N = 48) and females (N = 25) showed positive associations with Hg and an interaction between Cd and Pb, but a negative association with interaction between age and Pb. Higher testosterone was found in hair during its growth phase compared to quiescent phase. Body condition index was negatively associated with hair cortisol and positively associated with hair progesterone. Year and conditions of sampling were important for cortisol variation, while maturity stage for progesterone variation (lower concentrations in cubs and yearlings compared to subadult and adult bears). These findings suggest that environmental levels of Cd, Hg and Pb might influence the HPG axis in brown bears. Hair was shown to be a reliable non-invasive sample for investigating hormonal fluctuations in wildlife while addressing individual and sampling specificities.

Large carnivores and naturalness affect forest recreational value.

Recreation is a crucial contribution of nature to people, relevant for forest ecosystems. Large carnivores (LCs) are important components of forests, however, their contribution to forest recreational value has not yet been evaluated. Given the current expansion of LC populations, the ongoing forest conservation debate, and the increasing use of nature for recreational purposes, this is a timely study. We used discrete choice experiments and willingness-to-travel to determine people' preferences for both forest structural characteristics and presence of four LC species in Poland (N = 1097 respondents) and Norway (N = 1005). In both countries, two-thirds of the respondents (termed 'wildness-positive') perceived LCs as contributing positively to forest recreational value and preferred to visit old forests with trees of different species and ages and presence of dead wood (i.e. natural forests). Respondents with negative preferences towards LCs preferred more intensively managed forest ('wildness-negative'); their preferences were stronger than in wildness-positive respondents and in Norway. Preferences towards wild nature were highly polarized and there were hardly neutral people. Our results showed a strong link between preferences for LC presence and forest structure, and reflected the dualism of human-nature relationships. This study highlights the need to consider the contribution of forests and LCs to human recreation services in ecosystem management policies.

Stress associated with group living in a long-lived bird.

Many long-lived avian species adopt life strategies that involve a gregarious way of life at juvenile and sub-adult stages and territoriality during adulthood. However, the potential associated costs of these life styles, such as stress, are poorly understood. We examined the effects of group living, sex and parasite load on the baseline concentration of faecal stress hormone (corticosterone) metabolites in a wild population of common ravens (Corvus corax). Corticosterone concentrations were significantly higher in non-breeding gregarious ravens than in territorial adults. Among territorial birds, males showed higher stress levels than their mates. Parasite burdens did not affect hormone levels. Our results suggest a key role of the social context in the stress profiles of the two population fractions, and that group living may be more energetically demanding than maintaining a territory. These findings have implications for understanding hormonal mechanisms under different life styles and may inspire further research on the link between hormone levels and selective pressures modulating gregarious and territorial strategies in long-lived birds.

Roadless and Low-Traffic Areas as Conservation Targets in Europe.

With increasing road encroachment, habitat fragmentation by transport infrastructures has been a serious threat for European biodiversity. Areas with no roads or little traffic ("roadless and low-traffic areas") represent relatively undisturbed natural habitats and functioning ecosystems. They provide many benefits for biodiversity and human societies (e.g., landscape connectivity, barrier against pests and invasions, ecosystem services). Roadless and low-traffic areas, with a lower level of anthropogenic disturbances, are of special relevance in Europe because of their rarity and, in the context of climate change, because of their contribution to higher resilience and buffering capacity within landscape ecosystems. An analysis of European legal instruments illustrates that, although most laws aimed at protecting targets which are inherent to fragmentation, like connectivity, ecosystem processes or integrity, roadless areas are widely neglected as a legal target. A case study in Germany underlines this finding. Although the Natura 2000 network covers a significant proportion of the country (16%), Natura 2000 sites are highly fragmented and most low-traffic areas (75%) lie unprotected outside this network. This proportion is even higher for the old Federal States (western Germany), where only 20% of the low-traffic areas are protected. We propose that the few remaining roadless and low-traffic areas in Europe should be an important focus of conservation efforts; they should be urgently inventoried, included more explicitly in the law and accounted for in transport and urban planning. Considering them as complementary conservation targets would represent a concrete step towards the strengthening and adaptation of the Natura 2000 network to climate change.

The role of the brown bear Ursus arctos as a legitimate megafaunal seed disperser.

Megafaunal frugivores can consume large amounts of fruits whose seeds may be dispersed over long distances, thus, affecting plant regeneration processes and ecosystem functioning. We investigated the role of brown bears (Ursus arctos) as legitimate megafaunal seed dispersers. We assessed the quantity component of seed dispersal by brown bears across its entire distribution based on information about both the relative frequency of occurrence and species composition of fleshy fruits in the diet of brown bears extracted from the literature. We assessed the quality component of seed dispersal based on germination experiments for 11 fleshy-fruited plant species common in temperate and boreal regions and frequently eaten by brown bears. Across its distribution, fleshy fruits, on average, represented 24% of the bear food items and 26% of the total volume consumed. Brown bears consumed seeds from at least 101 fleshy-fruited plant species belonging to 24 families and 42 genera, of which Rubus (Rosaceae) and Vaccinium (Ericaceae) were most commonly eaten. Brown bears inhabiting Mediterranean forests relied the most on fleshy fruits and consumed the largest number of species per study area. Seeds ingested by bears germinated at higher percentages than those from whole fruits, and at similar percentages than manually depulped seeds. We conclude that brown bears are legitimate seed dispersers as they consume large quantities of seeds that remain viable after gut passage. The decline of these megafaunal frugivores may compromise seed dispersal services and plant regeneration processes.

Brown bear communication hubs: patterns and correlates of tree rubbing and pedal marking at a long-term marking site.

Chemical communication is important for many species of mammals. Male brown bears, Ursus arctos, mark trees with a secretion from glands located on their back. The recent discovery of pedal glands and pedal-marking at a site used for tree-rubbing led us to hypothesize that both types of marking form part of a more complex communication system. We describe the patterns of chemical communication used by different age and sex classes, including differences in the roles of these classes as information providers or receivers over four years at a long-term marking site. Using video recordings from a camera trap, we registered a total of 285 bear-visits and 419 behavioral events associated with chemical communication. Bears visited the site more frequently during the mating season, during which communication behaviors were more frequent. A typical visit by male bears consisted of sniffing the depressions where animals pedal mark, performing pedal-marking, sniffing the tree, and, finally, rubbing against the trunk of the tree. Adult males performed most pedal- and tree-marking (95% and 66% of the cases, respectively). Males pedal-marked and tree-rubbed in 81% and 48% of their visits and sniffed the pedal marks and the tree in 23% and 59% of visits, respectively. Adult females never pedal marked, and juveniles did so at very low frequencies. Females rubbed against the tree in just 9% of their visits; they sniffed the tree and the pedal marks in 51% and 21% of their visits, respectively. All sex and age classes performed pedal- and tree-sniffing. There were significant associations between behaviors indicating that different behaviors tended to occur during the same visit and were more likely if another individual had recently visited. These associations leading to repeated marking of the site can promote the establishment of long-term marking sites. Marking sites defined by trees and the trails leading to them seem to act as communication hubs that brown bears use to share and obtain important information at population level.