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Mitochondrial Diversity Offers Insight on Invasive European Starling Populations Worldwide

Blog written by Julia Zichello and Louise Bodt. Read the full manuscript here.

The European starling is one of the most wide-spread and successful invasive avian species in the world. Their native range extends across Europe and into Western Asia. Since the mid-1800’s, there have been multiple deliberate introductions of European starlings outside of their native range. Today, there are populations of starlings on every continent except Antarctica. Starlings are aggressive birds which travel sometimes in massive undulating flocks called murmurations. These birds are ubiquitous, industrious and downright hated. They destroy agricultural crops, spread diseases to livestock, fly into aircrafts and outcompete native birds. And yet, their outsized ability to establish and expand in novel environments, cannot — from an ecological or evolutionary perspective — be ignored.

Although there has been research investigating some of these invasive populations, our new dataset from North American starlings, combined with existing datasets from Australia, South Africa and the UK, allows us to compare mitochondrial diversity of starling populations across multiple continental distributions.

The story of the European starling in North America starts in 1890. Approximately 100 birds were brought to New York City’s Central Park between 1890 and 1891 by Eugene Schieffelin. This was part of an initiative by the American Acclimatization Society to bring all birds mentioned in Shakespeare to the US. The starling is mentioned only once in Shakespeare’s Henry IV. And over the last 130 years the starling population in North America has exceeded 200 million, over one-third of the global population. Several other introductions of starlings occurred in Australia and New Zealand in the mid-1800’s, in South Africa in the late 1800’s and in Venezuela and Argentina in the mid- to late-1900’s. These populations persist today and some continue to expand. These misguided introductions were undoubtedly ecologically destructive, and yet because of the scale, persistence, and repeatability they demonstrate, there is certainly a great deal to learn from these unfortunate experiments.

Starling specimens (Denis Finnin)

            Here, we have presented the most geographically widespread analysis of starling population genetics to date. Our sampling from the United States (tissue samples provided from the USDA) combined with the existing datasets from Australia and South Africa and the native range allow us to compare genetic diversity and population dynamics among continents. We found that the US population shows signs that it is currently expanding, but does not show signs of any population structure. The lack of population structure could be due to the flexible patterns of seasonal migration that are exhibited in the North American population.

            Additionally, the three invasive populations share only one mitochondrial haplotype with each other (see Venn diagram). This is consistent with three independent sub-samples of the mitochondrial diversity of the original native range. We also found that the mitochondrial diversity of the invasive populations in Australia, South Africa and the US are lower than that of the native range, as expected due to founder effects. However, this contributes to a broader understanding of how low genetic diversity is sometimes not an obstacle for evolutionary success (as has often been thought). Instead, perhaps behavioral and ecological plasticity are more primary factors in a species’ successful establishment in a new environment.

Invasive species offer a window into evolutionary processes over short timescales. The starling shows what can happen when a species is introduced to contrasting environments and independent populations are established from different founders. Because European starling invasions span multiple continents, comparisons of these populations can inform how subtle differences in founder populations and expansion rates affect present day patterns of diversity. The climatic variation across the different invasive regions here also provides another powerful variable to explore. Furthermore, studying a species with such a wide distribution across heterogenous environments (both ecologically and politically) has implications for conservation and invasive species management.

            Birdwatchers leave them off their lists, ornithologists and farmers scoff at them and they present intricate and costly ecological challenges wherever they go. But they are — for better or worse— here, there and almost everywhere. Our paper represents intriguing insights into what the multiple European starling invasions across the world reveal about evolution and adaptive changes, and we will be engaging in future research on this unique, troublesome and complex avian system. Because, what is it about European starlings that made them such successful invaders again and again and again? That, is the question. 

Is Smart Sexy? Testing female preferences for problem-solving males in zebra finches

Blog written by Clara Howell. Read the full paper here.

A huge and diverse taxonomic group of birds, from temperate crows to tropical birds-of-paradise, learn their songs by imitating adults of their species that they hear when young. Understanding the complicated genetic and cultural evolution of song is interesting not just in its own right, but also as a window into the mechanisms by which communication systems arise and persist. A large part of understanding how this occurs is learning what kind of information is exchanged via song, and how that information benefits both senders and receivers in order to make it a communication system worth investing in. We have known for many years, for instance, that male song can tell a female a lot about a male’s species, location, and willingness to mate. But with playback experiments, we are just beginning to understand the incredible nuance of song. Females of many species respond differently to songs that vary in geographic origin, age, and developmental conditions of the singer. These sorts of experiments indicate that a female is not only able to use song to find a mate of the right species, but also one from the same area, of the ideal age, and who had a healthy development.

The inspiration for our present study came from a larger body of research investigating the ways in which song—because it is learned during a sensitive period of development and vulnerable to disruption—can signal past developmental stress and allow females to choose healthier mates. In addition to song from developmentally robust males, female songbirds of many species are also known to prefer longer and more complex song, or in species in which males sing multiple song types, a larger repertoire. A 2008 study by Boogert and colleagues found a positive correlation between learning ability in zebra finch males and the complexity of their song, which neatly connected two related theories of bird song—that song serves as a signal of healthy brain development, and that females have sensory preferences that lead to the evolution of more complex song. If song complexity and brain function are connected in males, it could explain why female preference for less monotonous song have persisted—because only males with well-functioning brains can learn and produce complex song, and those well-functioning brains also help take care of more offspring.

As elegant as the theory was, it quickly fell apart. Not only were many “preferred” features of song found to have null or even inverse correlations with the time it took males to learn cognitive tasks, the entire concept of a general cognitive ability in birds also had mounting evidence against it. But we were still interested in the connection between brain function and song, despite the complicated and conflicting evidence for it. Maybe it is too broad to say that song complexity = general cognitive ability, but is it possible that song still contains information about some cognitive abilities? And is it possible that if that information is there, it is encoded in a way that does not map perfectly onto the ways that we as researchers often define song complexity, as numbers of motifs and unique notes?

We decided to test not whether song attractiveness was correlated with general cognitive abilities, but whether song attractiveness was correlated with performance on a specific task we thought most likely to affect parental care: the ability to gather food from a new source. And instead of measuring song complexity by looking at spectrograms and visually categorizing complexity, we decided to present the songs to a set of females to see whether they could determine a difference between high performers and low performers when given only their song.

We used zebra finches as our test subjects because this species had been used in many of the original studies looking at this topic. First we tested male learning ability in their “novel foraging” task—how quickly they would be able to learn to flip an object covering a food reward. We tested a large cohort of males and found two distinctive groups on either end of the spectrum—those who breezed through the task in the minimum number of trials, and those who were unable to learn even after weeks of prompting. Six males were selected from each group and their song recorded, which was then made into pairs of “quick-solver” and “non-solver” songs to present to females. It was critical that the females not know the males—we didn’t want them using song to identify a male that they knew already knew to be particularly attractive or unattractive. We instead used fifteen naïve females who had never been housed with the males in question, and thus could assess the males using only their song.

Examples of solver song (top) vs non-solver song (bottom)

We then tested females on multiple pairs of quick-solver vs. non-solver song. We did this by installing two perches in each female’s home cage that could trigger playback of a song when hopped on, and thus measure a female’s preference through number of hops. To ensure that females understood the perches and were triggering favored songs, we first compared female responses to the songs of zebra finches versus rufous-collared sparrow, knowing that they would prefer song from their own species. When females demonstrated proficiency with the perches, we moved on to quick-solver vs. non-solver. Remarkably—because there was no discernable difference between song types to us—we found that over thousands of hops, females were preferring quick-solver over non-solver songs about 60% of the time. To put this in context, they preferred zebra finch vs. sparrow song 70% of the time. We analyzed our data using three statistical approaches: (1) with a non-parametric Wilcoxon sign-rank test, which essentially determined whether there were more deviations from the null preference than you would expect, (2) with a mixed effects linear model, which also determined whether female preference deviated from the null and whether factors such as order of presentation, specific female, or specific stimulus song had any effect on the findings, and (3) with a hierarchical Bayesian model, which modeled a population-wide preference given individual female preferences for quick-solver songs. In each model, we found a significant (or in the case of the Bayesian model, non-overlapping credible intervals) result: females preferred the quick-solver song in every pair of stimulus songs.

This is an exciting finding because the females knew absolutely nothing about the males, yet were still more interested in the song of a male who had quickly performed a cognitive task over one who was never able to figure it out. There have recently been a few studies showing that females prefer “smarter” males when observing them figure out tasks, and our results added a new dimension: females were preferring the males who solved the task, and they were able to make that distinction based on song alone. Song, in other words, can contain information about problem-solving ability in addition to everything else we already know it encodes. It’s a remarkable communication system, from the males who are able to so accurately advertise various aspects of their brain and behavior, to the females who are so accurately able to decode it. And while there is still a lot more to understand about problem-solving ability and song, this finding indicated to us that while there might not be a straightforward connection between song complexity, female preference, and male brain function, this is still a rich area for further study and a valuable insight into how communication systems arise and persist.  

Skull shape in an endangered marsupial: would northern quolls rather ship out than shape up?

Blog written by Pietro Viacava & Vera Weisbecker. Read the full paper here. Featured image: scientific illustration by Nellie Pease.

When a species is threatened by habitat loss and environmental change, it is important to understand how to best preserve its populations. This cannot be done without a solid understanding of how diverse populations are. For example, if each population is unique, it is best to manage separate conservation units. Conversely, if they are all similar, then individuals from one population can boost the numbers of other, smaller populations without losing much of the species diversity. These conservation management decisions are mostly based on the genetic diversity of populations. However, the genetic patterns used for current conservation aims do not necessarily capture the variation in form (“morphology”). Because genetic and form diversity are not necessarily the same thing, adaptations that might be essential for the survival of a morphologically distinct population might be ignored.

In Australia, marsupials (“pouched” mammals, most famously the kangaroos and koalas) are of particular conservation concern, leading the world in mammal extinctions. Members of this fascinating group give birth at very early developmental stages. Their neonates – called “pouch young” – need to climb towards the pouch and attach to the teat of their mother with strongly developed forelimbs and snouts. To survive their suckling phase, the oral apparatus needs to maintain a certain shape. It has long been suspected that this requirement might also reduce the ability of marsupials to adapt to changing environments, even in the presence of substantial genetic diversity.

We tested this suspicion using a threatened and particularly wide-ranging species of marsupial, the northern quoll. These marsupial carnivores are opportunistic foragers the size of a guinea pig. They are also the largest semelparous animal, where nearly all males die off in their first year after an intense breeding season. Until European invasion and possibly even well before, their distribution ranged across 5000 kilometres of the Northern Australian coast: from the western arid environments of the Pilbara to the humidity of the eastern tropical rainforests. Nowadays, its fragmented distribution consists of four genetically distinct mainland populations and several islands. A perfect scenario to test if these populations show matching morphological differences!

We scanned specimens from museum collections and specimens collected by the Wilson Lab from the field in Groote Eylandt.

We travelled to six museum collections in Australia and North America using a 3D surface scanner to digitally acquire the shape of 101 skulls. We covered these 3D skulls with a dense set of 900 reference points. This allowed us to test for size and shape variation among and within the four mainland populations and one island population, and additionally assess if we could discern morphological adaptations to local climatic conditions.

This portable 3D surface scanner travelled with us to the museum collections.

Unexpectedly, we found that there is little population structure in their skull shape variation and no strong evidence of discrete “morphotypes” according to either population or climate. However, we did observe that size is the strongest contributor to shape variation: smaller individuals tend to present proportionally larger braincases and narrower, less pronounced cheekbones, while larger individuals tended to have proportionally smaller braincases and wider cheekbones that are more pronounced. This results in some small variation between populations because, on average, Northern Territory and Queensland animals are bigger; Kimberley, Groote and Pilbara are smaller. However, because there were no other strong determinants of shape, similarly sized individuals even from distant populations mostly share the same shape.

Shape variation due to size variation (allometry). Spheres represent the reference points (landmarks). Vectors in black show the magnitude and direction of variation from small to big specimens. Most of the allometric shape variation concentrates on the braincase and the zygomatic arches. For example, bigger skulls display proportionally smaller braincases.

We were surprised by the lack of shape differentiation across the extensive distribution of northern quolls, particularly because other species of vertebrates with similar breaks in their distributions tend to show genetic and morphological differences. For example, other marsupials such as wallabies and kangaroos, but also other vertebrates such as lizards, amphibians and birds, reveal distinctions of lineages at the corresponding northern quoll population breaks. Thus, we asked: is there something that is holding the northern quolls back?

It is very possible that northern quoll skulls are just the perfect match for multiple situations and prey types. This “one-shape-fits-all” situation would mean that, depending on the size, the corresponding shape is well adapted to match a range of environmental scenarios and related prey items. Thus, short and rapid modifications of their environment may not require them to “shape up”.

On the other hand, the combination of a substantial effect of size and lack of strong environmental influences might also mean that northern quolls are simply not very adaptable beyond a very narrow, growth-related line of shape variation. One would expect this if a developmental constraint, arising from the need for a strongly developed oral apparatus at birth, prevented the northern quolls from adapting their shape.

There are some intriguing lessons for the diversity and conservation of northern quolls in our study. Firstly, based on our morphological results on the skull, similarly sized individuals from any population share the same shape; therefore, no adaptive variation would be lost in eventual population translocations. Secondly, distinguishing between a comfortable “one shape fits all” scenario and a scenario where northern quolls are incapable of adapting, is crucial for future research. If marsupial carnivores are locked into a particular shape, then they will need far more help to survive environmental change than we might expect. Alternatively, if the “one-shape-fits-all” holds true, we may rest more relaxed in knowing that their adaptive capabilities will equip them for a changing climate. We look forward to unravelling these questions in future work within other species of marsupial carnivores, and deciphering how fast are other species “shaping up”.

Space use by giant anteaters in a protected area within human‐modified landscape

Blog written by Alessandra Bertassoni. Read the full article here.

Shaggy, toothless, great snout and slow… These are common adjectives applied to the Giant Anteater – the largest anteater species in the Neotropic. This is a species that attracts curiosity, as well as having gaps in our knowledge of its ecology. Despite its large distribution (from Honduras to southern South America), it can be locally rare or very threatened in some areas (e.g. Central America and at the south of its distribution).

Numerous risks threaten the persistence of populations, such as wildfires, poaching, conflicts with dogs, road-kills, fragmentation, and habitat loss – these last two are the major threat to populations. To try to preserve natural habitats, countries have adopted the creation and maintenance of protected areas. On one hand, this is a good conservation strategy in times of huge changes to global systems – mostly driven by intensive human activities. On the other hand, some protected areas and their communities are immersed and isolated in human-modified landscapes. Large mammals require extended space, and the borders of the protected area are often bypassed.

This is the background of our study – “Space use by giant anteaters (Myrmecophaga tridactyla) in a protected area within the human‐modified landscape”. Our work took place in the Santa Bárbara Ecological Station (SBES), a protected Cerrado biome remnant (27 km²) surrounded by human-modified landscape in the State of São Paulo, Southeastern Brazil (Figure 1).

Figure 1: Santa Barbara Ecological Station (SBES, black polygon) and its surroundings in Southeastern Brazil. The green polygon is a Pinus sp. Plantation, the red traces are roads and Aguas de Santa Barbara municipality is represented as a light orange diamond.

This area is considered to have high biological importance due to its typical Cerrado vegetation. However, it is surrounded by pasture, sugarcane, exotic timber plantations (green dash line, Figure 1), and urban zones. It is also divided by a road network (red dash line, Figure 1). There is a resident population of giant anteaters within the SBES. We hypothesized that they would be highly dependent on the natural features of the protected Cerrado remnant because of their extreme specializations and habitat requirements. We also predicted that their home ranges will be primarily located within the SBES and the resources inside will be more used than the surroundings. Finally, we predicted that home ranges will overlap by more than 50% due to the small size of the protected area. This was a pioneer study of giant anteaters in a highly human-modified area.

To pursue these ideas it was necessary to track giant anteaters in the SBES and surrounding area. This species needs to be captured actively, as methods such as cage traps or baits are ineffective. Therefore, the team has to be in the field to search, find and catch giant anteaters.

In 2015, we spent three months in the SBES and its surrounding area. We covered approx. 12,000 km (three field campaigns) and we succeeded in capturing eight giant anteaters; four females (F) and four males (M). We fitted them with GPS-harnesses (see Figure 2).

Figure 2. A tracked giant anteater with GPS harness in the Santa Barbara Ecological Station, Southeastern Brazil.

For a few months (10 – 147 days, 91 on average), we were able to record 13,170 locations of the tracked individuals (Figure 3). This enabled us to record a great deal of interesting ecological data. Five giant anteaters (2 F and 3 M) remained almost exclusively inside the SBES and the other three (F1, M2, and M4) had more than 20% of their locations recorded outside of it. This gives us some indication that the SBES area and its requirements are not enough alone to accommodate this population. Residing outside of the protected area could be the best choice for individuals that require more space or are searching for specific resources which are too many exploited or limited within the SBES.

Another clue was the increasing trend in the home-range area of the two males (M2 and M4) to leave the SBES. From a conservation genetic perspective, individuals that leave a population to reach another can be considered propagules that contribute to the genetic pool. But, in a human-modified landscape, leaving protected areas is too risky, especially in a place that has more than one road.

In the two years that we spent in the study area, we found giant anteaters, deer and other animals killed by collisions with traffic. We predicted a great deal of overlap between individuals due to the SBES size, and we reported that dyads of opposite sex presented larger area-overlap than same-sex dyads, using two space-sharing indexes. However, this is not breaking news. Much more elucidative data came from the analysis of combined trajectories. This revealed proximity events in five dyads of opposite sexes and a male-dyad.

Figure 3. Giant anteaters locations inside the SBES and surroundings, Southeastern Brazil. M = male and F = female.

.What does this mean? Proximity events could indicate higher levels of coexistence than previously reported for this species, or that the study site is too small, meaning the anteaters interact more often. In addition, proximity analysis highlights that low home-range overlap cannot be strongly interpreted as a lack of individual interaction. Proximity events could indicate reproductive behaviour.

However, we still do not know if there is reproductive seasonality for the species, and this needs further study to advance our knowledge of this species’ natural history. Despite giant anteaters being most well-studied anteater species, we still lack the basic knowledge to to ask the right questions. We need to apply much more effort to studies on human-modified areas, to reach the minimal information needed to understand population trends and to move conservation forward.

Denning in brown bears

Blog written by Enrique González-Bernardo. Read the full article here.

Hibernation represents an adaptation for coping with unfavorable environmental conditions. For brown bears (Ursus arctos), hibernation coincides with winter in seasonal environments generally associated with low temperatures and low food abundance during which pronounced temporal reductions in several physiological functions occur. It is a critical period because at that time: (a) pregnant females give birth and undergo lactation while in dens; (b) energy savings during hibernation can be substantial; and (c) premature exit can negatively affect energy conservation and cub survival.

Brown bears are widely distributed around the northern hemisphere, with populations of different characteristics inhabiting very diverse habitats. Thus, the management and conservation of this species requires detailed knowledge about denning ecology of different populations, identifying patterns or gradients of denning behavior throughout the distribution range of the species and highlighting possible differences between populations. It is reasonable to expect that: (1) den chronology may vary by sex and bear reproductive status; (2) the duration of hibernation also depends on environmental factors, i.e. snow, temperature and food availability; (3) a relationship may exist between denning period and latitude, longitude and altitude; and (4) although the choice of a den and den surroundings may be variable, some differences may still exist by class, age and sex.

There are differences between sexes and ages in relation to denning chronology, with pregnant females enter the den earlier and exit later than other bear classes to take care of new-born and males and subadults generally having shorter denning periods. Hibernation in brown bears is mostly governed by a trade-off between environmental conditions metabolic dietary-related and energy conservation needs, with the exception of pregnant females which ultimate reasons are reproductive needs. As a general rule, the duration of hibernation in different brown bear populations seems to be conditioned by both snowfall/snow depth and snowmelt in spring. Snowfall can act as a major impetus to begin hibernation, as well as the ambient temperature. Warmer winters seems to be associated with a decrease in the length of the hibernation period and the postponement of den entry, while low autumn temperatures may cause early den entry. Den emergence seems to be regulated in some way with an increase in temperature, but not depending on the exact ambient temperature on the day of emergence (probably because den emergence is a longer process), but by the temperature the previous weeks. However, the hibernation period is primarily affected by a decrease in food availability due to the snow cover, which guides den entry and exit. Continuous availability of food and mild climates may prompt individuals to spend the winter outside dens, with bears in more northern areas spending more time hibernating than bears in the southernmost latitudes. There is an evident gradient between den chronology and latitude, but it seems to affect primarily to adult bears. Similarly, altitude has been described as influencing denning dates, with bears denning at lower altitudes emerging earlier than those hibernating at higher altitudes. Den abandonment occurs naturally, but human activities, such as industrial and forestry activity, hunting, transit of people or even research activity have been reported as the main cause. It may have negative consequences for populations, such as increases in cub mortality. In some populations where there are natural food sources during the winter, part of the population may not hibernate. This phenomenon is especially intense where supplementary food is provided during winter, which may alter the chronology of hibernation or winter.

The choice of a den and its surroundings may affect individual fitness, for example, loss of offspring and excessive energy consumption. Den selection is the result of broad- and fine-scale habitat selection, mainly linked to den insulation, remoteness, and availability of food in the surroundings of the den location. The most common den types are those excavated in the ground or located inside natural caves, but other types of dens such as depressions under rock shelters, nest dens and tree cavities have been reported. The typical conformation of a den consists of an entrance, a tunnel and the chamber where the bear builds the nest. Brown bears select sunny slopes and sites with deeper snowpack, which have insulating properties that help maintain a constant temperature protection. Other selected features are the slope of the hillside (simpler digging, stability, solar radiation and protection) and the distance and altitude (more permanent snow cover and further from human disturbances). Differences have been described in terms of sex, with pregnant females hibernating higher because they have a longer hibernation and need more isolation, while adult males hibernate in lower areas, which would provide them with greater food availability at den emergence, rapidly increase body mass and thus improve breeding success.

Brown bears hibernate for several months during which they do not eat, drink, defecate or urinate. This huge metabolic challenge has demanded a series of physiological adaptations in tissues and organs, many of them unique, enabling bears to survive under nutritional deprivation and to overcome anuria, hyperlipidaemia and immobilization, preserve muscles and bones avoiding osteoporosis or sarcopenia and prevent diseases such as metabolic syndrome, diabetes and cardiovascular pathologies. During hyperphagia, brown bears becoming temporary insensible to leptin which allows a constant appetite. Bears exhibit an increase in body mass of around 40% during the pre-hibernation hyperphagia, mainly fat. During hibernation, the mass loss could reach 4 kg per day. The metabolic rate drops to a quarter of the active state level and the temperature drop is about 3-5 °C, starting days before the den entrance. As a result, heart rate begins to decrease up to 80%. During hibernation, brown bears exhibit blood parameters that would be indicators of pathology in humans and as a consequence of fat-based metabolism, maintaining concentrations of phospholipids, cholesterol and free fatty acids much higher than healthy human values. However, atherosclerosis, fatty streaks, foam cell infiltration and inflammation have not been reported in hibernating bears. The bladder becomes permeable and both water and nitrogenous substances re-enter the blood. This and other adaptation, such as a reduction of urea synthesis and reincorporating urea into skeletal muscle and other proteins, allow recycling of nitrogenous substances and prevent renal complications or azotemia. Organs involved in digestive, metabolic and excretion processes, such as the liver and kidneys, have their activity decreased compared to the active period decrease in function. Brown bears do not appear to suffer from skeletal muscle and bone dysfunction or bone loss during hibernation, despite immobilization and lack of food. Brown bears are able to maintain both muscle and bone mass and function by reducing catabolic processes and maintaining a certain level of mechanical activity, such as shivering. Brown bears give birth during hibernation, around January-February, when there is no intake of food and water. Pregnant females appear to have delayed implantation of the embryo. In older females, as well as in females with high body fat content, den entry dates and birth dates tend to be earlier and the lactation period may be longer than in other females. In addition, in females with a higher percentage of fat and lean mass, implant embryos and cub birth occur earlier and the mortality of their cubs during the first summer is lower than in other females.

Concerning the hibernation of brown bears it is important to correctly distinguish between actual drivers of hibernation (temperature, snow, food availability) and their correlates (physiological changes). We suspect that the correlates of proximate factors might fluctuate according to current environmental variations. Predicted variations in air temperatures generally point towards an increase in temperature and precipitation variability has already affected biological systems by altering the phenology. Inter-annual fluctuations in hibernation chronology are expected to occur due to inter-annual variations in climate, extreme climatic events and temperature anomalies resulting from climate change. These fluctuations are probably unpredictable for many organisms, including bears. It has been reported how brown bears advance the den exit by increasing spring temperature, and how the total duration of hibernation is reduced. Brown bears have been reported showing a noticeable plasticity when hibernating, adapting their denning behavior to environmental factors, availability of food during hyperphagia or changing snow conditions during the winter. Despite this, energy demands of hibernating mammals would increase with higher winter temperature, and mismatches could be expected between the den exit dates and food resources, in addition to a reduction in their abundance or availability. Altering hibernation conditions could have a negative effect on reproductive success and cub survival. Such increased mismatches might also increase the likelihood of bear-human conflicts if bears emerge earlier. It is important to highlight here the potential effect of anthropogenic food, and especially supplementary feeding (provided with hunting, eco-tourism and the mitigation of human-bear conflicts purposes), on the chronology of hibernation, being able to halve the denning period or increase den abandonments. For all this, future research is important to know how changes in climatic factors might affect the ability of bears to face global climate change and the human-mediated changes in food availability. In addition to this, a better understanding of how hyperphagia, predenning and denning periods, including for those populations in which bears do not hibernate every year, and how to approach the study of bear denning merging insights from different perspectives, that is, physiology, ecology, and behavior.

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