Detection of pregnancy in a hibernator based on activity data

Pregnancy and parturition are often difficult to detect in wild-living animals, especially in species that give birth to altricial young in burrows or caves. Current methods to detect pregnancy and birth in hibernating animals often entail disturbances that can affect the animals' reproductive success. We developed a new method to confirm pregnancy and parturition in hibernating brown bears (Ursus arctos) using activity data recorded in dual-axis motion sensors mounted on GPS–GSM neck collars on 30 brown bears during 52 hibernation seasons in Sweden. We adjusted recorded activity to the individual basal activity level for each bear. Pregnant females showed characteristic activity patterns during the period of pregnancy, with significantly higher daily activity levels and frequency of active periods during pregnancy than nonpregnant bears. Pregnant females were active on average 2.20 times more often during the pregnancy period than during the postpartum period, compared with 0.97 times for nonpregnant females. A pregnancy index was defined as the average of the proportion of mean daily activity levels and the proportion of activity events during the pregnancy period compared with the postpartum period. It averaged 2.61?±?1.73 (SD) for pregnant females and 0.94?±?0.24 for nonpregnant females. Using this method, we evaluated a group of adult females that had an unverified reproductive status but were classified as not pregnant because no cubs had been observed after den emergence. The results suggested that 35 % of those females had, in fact, been pregnant.     

The effects of forest fires on polar bear maternity denning habitat in western Hudson Bay

The effects of forest fires on polar bear (Ursus maritimus) maternity denning habitat in western Hudson Bay were determined by comparing the physical characteristics of 48 burned and 101 unburned maternity den sites from September 2001 to October 2003. Fire significantly altered vegetation composition and increased the depth of the active layer, resulting in a decrease in the stability of den sites, the collapse of dens, and degradation of the surrounding habitat. Although bears investigated burned areas, analysis of mark and recapture data, satellite telemetry, radio-telemetry, and field observations all demonstrated that bears did not use burned areas for denning. While peat denning habitat is likely not limiting at this time, the re-use and occupancy of peat den sites during the summer may be an important means of energy conservation for pregnant female bears in western Hudson Bay. Increased energy expenditures in association with increased search times for suitable den sites and the excavation of new dens can potentially affect reproductive success. Predicted increases in forest fire activity as a result of climate change, along with the long-term recovery of denning habitat may reduce the amount of suitable denning habitat in the future. Resource managers need to be aware of the possibility of a shift in the distribution of denning bears and further loss of maternity denning habitat in western Hudson Bay.     

Seasonal activity budget of adult baltic ringed seals

Although ringed seals are important components in oceanic and fresh water ecosystems at high latitudes, little is known about how they exploit these harsh environments. Seasonal activity and diving behaviour of 19 adult Baltic ringed seals were studied by satellite telemetry. We elaborated an activity budget for ten months of the year, extending over the period from moult to the breeding season. Seals from three main regions showed explicit site fidelity and the distributions of animals tagged from different areas did not overlap, suggesting separate stocks. Both the mean duration and the mean depth of dives peaked in June and July. Seals spent 70% (females) to 85% (males) of their time diving in June and July which decreased to 50% in late autumn. Less than one percent of dives exceeded 10 min in females, while 10% of male dives lasted longer than 10 min in June to September. Less than one percent of dives lasted for more than 25 min. Both females and males were most active during day time and hauled out predominantly during the night. Activity patterns during the summer are suggested to be correlated to energy accumulation and prey availability. The information on seasonal activity budget is crucial for developing population energetic models where interactions between ringed seals and other trophic levels can be evaluated.     

Selection of maternity dens by female polar bears in western Hudson Bay,Canada and the effects of human disturbance

We deployed 19 satellite radio collars on adult female polar bears (Ursus maritimus) in western Hudson Bay to study how pregnant females select maternity-den sites and the degree to which human disturbance might influence this process. To eliminate the possibility that being handled while pregnant might influence the final choice of a suitable site, the collars were attached 1 year before the females were expected to select dens. Our results indicated that pregnant females moved inland and selected an area to den shortly after coming ashore in the summer and remained there if not disturbed. We analyzed 24 years of consecutive data (1979–2002) to examine whether disturbance of pregnant females in the denning area in the autumn affected litter size or mass of cubs the following spring. We defined three levels of disturbance (none—bear not seen; low—bear seen but not handled; high—bear seen and handled), and found that disturbance had no effect on either litter size or the mass of male cubs. However, we did find that females handled in the autumn had significantly lighter female cubs than females that were not seen. Our disturbance of pregnant females occurred in August and September, which is only a few months prior to parturition; it is not known what the effects of disturbance might be in late October or early November, closer to the time when cubs are born.     

Individual Effects of Seasonal Changes,Visitor Density,and Concurrent Bear Behavior on Stereotypical Behaviors in Captive Polar Bears (Ursus maritimus)

Stereotypical behaviors in captive polar bears (Ursus maritimus) can be detrimental to their welfare. These behaviors can be reduced through enrichment programs but are often not completely eliminated, so identifying potential triggers is important. The present study investigated the influences of seasonal changes, visitor density, and concurrent bear activity on stereotypical behaviors exhibited by 3 captive polar bears at the Toronto Zoo. All bears exhibited these behaviors; however, individual differences were found in duration and form. The male exhibited less stereotypical behavior during spring, and the females exhibited less stereotypical behavior during winter. An increase in visitor density was associated with more stereotypical behavior in 1 female but less stereotypical behavior in the other 2 bears. All bears engaged in more stereotypical behaviors when the other bears were inactive, and 1 female engaged in more stereotypical behaviors when the other bears were out of sight. Further, when conspecifics were active, all bears engaged in less stereotypical behaviors. Given the variability among individual bears, future enrichment programs must be tailored to the needs of individuals to maximize efficacy.     

Physical growth of northern fur seals (Callorhinus ursinus): seasonal fluctuations and migratory influences

Growth curves are described for males, pregnant females, and non-pregnant females using morphometric measurements collected from over 18000 northern fur seals ( Callorhinus ursinus ) shot at sea between California and the Bering Sea from 1958 to 1974. Seals of all ages experience seasonal increases and decreases in body mass and length. Seasonal fluctuations of body length may be an artefact of mass displacement caused by seasonal changes in mass. Rapid growth and gain in mass occur during a brief one to three month period as the population migrates northward through the coastal waters of northern British Columbia and Alaska on their way to the Pribilof Islands. Body mass of females and immature males is gradually lost while fasting on land and wintering along the coasts of Washington, Oregon, and California. Pregnant females are both heavier and longer than non-pregnant females of the same age. Body mass in pregnant females levels off with age in contrast with the increasing mass of non-pregnant females. Growth of northern fur seals does not appear to stop at an upper asymptote, but continues throughout their life spans.     

Determinants of Home Range Size for Polar Bears (Ursus maritimus)

The mean home range size of female polar bears ( Ursus maritimus ; 125 100 km² ± 11 800; n  = 93) is substantially larger than the predicted value (514 km²) for a terrestrial carnivore of similar weight. To understand this difference, we correlated home range size and sea ice characteristics. Home range size was related to (i) the ratio of land vs. sea within a given home range (42% of explained variance), and (ii) seasonal variation in ice cover (24%). Thus, bears using land during the ice-free season had larger home ranges and bears living in areas of great seasonal variation in ice cover also had larger home ranges. In another analysis we investigated how variation in a bear's environment in space and time affects its choice of home range. We found that polar bears adjusted the size of their home range according to the amount of annual and seasonal variation within the centre of their home range. For example, polar bears experiencing unpredictable seasonal and annual ice tended to increase their home range size if increasing home range size resulted in reducing variation in seasonal and annual ice. Polar bears make trade-offs between alternate space-use strategies. Large home ranges occur when variable ice cover is associated with more seals but also a more unpredictable distribution of those seals.     

The seasonal sensitivity of brown bear denning phenology in response to climatic variability

Background

For brown bears (Ursus arctos), hibernation is a critical part of the annual life cycle because energy savings during hibernation can be crucial for overwintering, and females give birth to cubs at that time. For hibernation to be a useful strategy, timing is critical. However, environmental conditions vary greatly, which might have a negative effect on the functionality of the evolved biological time-keeping. Here, we used a long-term dataset (69 years) on brown bear denning phenology recorded in 12 Russian protected areas and quantified the phenological responses to variation in temperature and snow depth. Previous studies analyzing the relationship between climate and denning behavior did not consider that the brown bear response to variation in climatic factors might vary through a period preceding den entry and exit. We hypothesized that there is a seasonal sensitivity pattern of bear denning phenology in response to variation in climatic conditions, such that the effect of climatic variability will be pronounced only when it occurs close to den exit and entry dates.

Results

We found that brown bears are most sensitive to climatic variations around the observed first den exit and last entry dates, such that an increase/decrease in temperature in the periods closer to the first den exit and last entry dates have a greater influence on the denning dates than in other periods.

Conclusions

Our study shows that climatic factors are modulating brown bear hibernation phenology and provide a further structuring of this modulation. The sensitivity of brown bears to changes in climatic factors during hibernation might affect their ability to cope with global climate change. Therefore, understanding these processes will be essential for informed management of biodiversity in a changing world.

     

Increased Arctic sea ice drift alters adult female polar bear movements and energetics

Recent reductions in thickness and extent have increased drift rates of Arctic sea ice. Increased ice drift could significantly affect the movements and the energy balance of polar bears (Ursus maritimus) which forage, nearly exclusively, on this substrate. We used radio‐tracking and ice drift data to quantify the influence of increased drift on bear movements, and we modeled the consequences for energy demands of adult females in the Beaufort and Chukchi seas during two periods with different sea ice characteristics. Westward and northward drift of the sea ice used by polar bears in both regions increased between 1987–1998 and 1999–2013. To remain within their home ranges, polar bears responded to the higher westward ice drift with greater eastward movements, while their movements north in the spring and south in fall were frequently aided by ice motion. To compensate for more rapid westward ice drift in recent years, polar bears covered greater daily distances either by increasing their time spent active (7.6%–9.6%) or by increasing their travel speed (8.5%–8.9%). This increased their calculated annual energy expenditure by 1.8%–3.6% (depending on region and reproductive status), a cost that could be met by capturing an additional 1–3 seals/year. Polar bears selected similar habitats in both periods, indicating that faster drift did not alter habitat preferences. Compounding reduced foraging opportunities that result from habitat loss; changes in ice drift, and associated activity increases, likely exacerbate the physiological stress experienced by polar bears in a warming Arctic.     

Polar bears (Ursus maritimus), the most evolutionary advanced hibernators, avoid significant bone loss during hibernation

Some hibernating animals are known to reduce muscle and bone loss associated with mechanical unloading during prolonged immobilisation,compared to humans. However, here we show that wild pregnant polar bears (Ursus maritimus) are the first known animals to avoid significant bone loss altogether, despite six months of continuous hibernation. Using serum biochemical markers of bone turnover, we showed that concentrations for bone resorption are not significantly increased as a consequence of hibernation in wild polar bears. This is in sharp contrast to previous studies on other hibernating species, where for example, black bears (Ursus americanus), show a 3-4 fold increase in serum bone resorption concentrations posthibernation,and must compensate for this loss through rapid bone recovery on remobilisation, to avoid the risk of fracture. In further contrast to black bears, serum concentrations of bone formation markers were highly significantly increased in pregnant female polar bears compared to non-pregnant,thus non-hibernating females both prior to and after hibernation. However, bone formation concentrations in new mothers were significantly reduced compared to pre-hibernation concentrations. The de-coupling of bone turnover in favour of bone formation prior to hibernation, suggests that wild polar bears may posses a unique physiological mechanism for building bone in protective preparation against expected osteopenia associated with disuse,starvation, and hormonal drives to mobilise calcium for reproduction, during hibernation. Understanding this physiological mechanism could have profound implications for a natural solution for the prevention of osteoporosis in animals subjected to captivity with inadequate space for exercise,humans subjected to prolonged bed rest while recovering from illness, or astronauts exposed to antigravity during spaceflight.? 2008 Elsevier Inc. All rights reserved.     

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

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

Polar bears in a warming climate

Polar bears (Ursus maritimus) live throughout the ice-coveredwaters of the circumpolar Arctic, particularly in near shoreannual ice over the continental shelf where biological productivityis highest. However, to a large degree under scenarios predictedby climate change models, these preferred sea ice habitats willbe substantially altered. Spatial and temporal sea ice changeswill lead to shifts in trophic interactions involving polarbears through reduced availability and abundance of their mainprey: seals. In the short term, climatic warming may improvebear and seal habitats in higher latitudes over continentalshelves if currently thick multiyear ice is replaced by annualice with more leads, making it more suitable for seals. A cascadeof impacts beginning with reduced sea ice will be manifestedin reduced adipose stores leading to lowered reproductive ratesbecause females will have less fat to invest in cubs duringthe winter fast. Non-pregnant bears may have to fast on landor offshore on the remaining multiyear ice through progressivelylonger periods of open water while they await freeze-up anda return to hunting seals. As sea ice thins, and becomes morefractured and labile, it is likely to move more in responseto winds and currents so that polar bears will need to walkor swim more and thus use greater amounts of energy to maintaincontact with the remaining preferred habitats. The effects ofclimate change are likely to show large geographic, temporaland even individual differences and be highly variable, makingit difficult to develop adequate monitoring and research programs.All ursids show behavioural plasticity but given the rapid paceof ecological change in the Arctic, the long generation time,and the highly specialised nature of polar bears, it is unlikelythat polar bears will survive as a species if the sea ice disappearscompletely as has been predicted by some.     

The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway?

Little is known about the prevalence of the parasite Toxoplasma gondii in the arctic marine food chain of Svalbard, Norway. In this study, plasma samples were analyzed for T. gondii antibodies using a direct agglutination test. Antibody prevalence was 45.6% among polar bears (Ursus maritimus), 18.7% among ringed seals (Pusa hispida) and 66.7% among adult bearded seals (Erignathus barbatus) from Svalbard, but no sign of antibodies were found in bearded seal pups, harbour seals (Phoca vitulina), white whales (Delphinapterus leucas) or narwhals (Monodon monoceros) from the same area. Prevalence was significantly higher in male polar bears (52.3%) compared with females (39.3%), likely due to dietary differences between the sexes. Compared to an earlier study, T. gondii prevalence in polar bears has doubled in the past decade. Consistently, an earlier study on ringed seals did not detect T. gondii. The high recent prevalence in polar bears, ringed seals and bearded seals could be caused by an increase in the number or survivorship of oocysts being transported via the North Atlantic Current to Svalbard from southern latitudes. Warmer water temperatures have led to influxes of temperate marine invertebrate filter-feeders that could be vectors for oocysts and warmer water is also likely to favour higher survivorship of oocycts. However, a more diverse than normal array of migratory birds in the Archipelago recently, as well as a marked increase in cruise-ship and other human traffic are also potential sources of T. gondii.     

Factors Affecting Date of Implantation,Parturition, and Den Entry Estimated from Activity and Body Temperature in Free-Ranging Brown Bears

Knowledge of factors influencing the timing of reproduction is important for animal conservation and management. Brown bears (Ursus arctos) are able to vary the birth date of their cubs in response to their fat stores, but little information is available about the timing of implantation and parturition in free-ranging brown bears. Body temperature and activity of pregnant brown bears is higher during the gestation period than during the rest of hibernation and drops at parturition. We compared mean daily body temperature and activity levels of pregnant and nonpregnant females during preimplantation, gestation, and lactation. Additionally we tested whether age, litter size, primiparity, environmental conditions, and the start of hibernation influence the timing of parturition. The mean date of implantation was 1 December (SD = 12), the mean date of parturition was 26 January (SD = 12), and the mean duration of the gestation period was 56 days (SD = 2). The body temperature of pregnant females was higher during the gestation and lactation periods than that of nonpregnant bears. The body temperature of pregnant females decreased during the gestation period. Activity recordings were also used to determine the date of parturition. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50% of the females. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions which was unexpected. We suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by human.     

Seasonal variation in the metabolic rate and body composition of female grey seals: fat conservation prior to high-cost reproduction in a capital breeder?

Many animals rely on stored energy through periods of high energy demand or low energy availability or both. A variety of mechanisms may be employed to attain and conserve energy for such periods. Wild grey seals demonstrate seasonal patterns of energy storage and foraging behaviour that appear to maximize the allocation of energy to reproduction—a period characterized by both high energy demand and low food availability. We examined seasonal patterns in resting rates of oxygen consumption as a proxy for metabolic rate (RMR) and body composition in female grey seals (four adults and six juveniles), testing the hypothesis that adults would show seasonal changes in RMR related to the reproductive cycle but that juveniles would not. There was significant seasonal variation in rates of resting oxygen consumption of adult females, with rates being highest in the spring and declining through the summer months into autumn. This variation was not related to changes in water temperature. Adults increased in total body mass and in fat content during the same spring to autumn period that RMR declined. RMR of juveniles showed no clear seasonal patterns, but did increase with increasing mass. These data support the hypothesis that seasonal variation in RMR in female grey seals is related to the high costs of breeding.     

Multi‐temporal factors influence predation for polar bears in a changing climate

Predation is an ecological interaction influenced by abiotic and biotic factors acting on multiple temporal scales, yet multi‐temporal comparisons are rare in empirical studies. For polar bears Ursus maritimus, the physical configuration of the habitat and conditions in which seals are hunted may change on intra‐ and inter‐seasonal scales. Additionally, while the effects of climate change on polar bears have focused on linking reductions in sea ice to body condition and survival, the potential changes to on‐ice hunting conditions have not been examined. Employing observational counts of seals killed by polar bears between early‐April and late‐May 1985–2011 (n = 650), we modelled the likelihood of predation events in the Beaufort Sea, Canada at multi‐temporal scales. We used the top model to estimate the expected kill rate of seals in the springs of 1985–1986 and 2005–2006 and integrated the result with fasting rates derived from physiological markers in blood samples. A log‐likelihood ratio test suggested a multi‐temporal approach fit the seal kill data better than any single scale alone. Predation events were influenced by ringed seal Pusa hispida reproduction and haul‐out behaviour, regional sea ice concentration and the phase of climatic indices. The expected kill rate from the top predation model and the estimated mean biomass of seal kills were significant predictors of polar bear fasting rates. Results suggest that 50% less seal biomass was killed in 2005–2006 than in 1985–1986, which correlates with a significant increase in the frequency of polar bears in a fasting state. We propose that the documented changes in polar bear fasting rates between 1985–1986 and 2005–2006 are due to a complex set of abiotic and biotic factors including underlying prey dynamics, rather than a single‐scale environmental correlation.     

Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears

The adaptation of black and polar bears to their environments is proportional to the severity of climate and food restriction. Both black and polar bears mate during the spring, despite differences in their recent metabolic state. Reproductive activity in black bears follows 4 mo of torpor, whereas reproduction in polar bears occurs prior to torpor. The goals of this study were to measure the annual changes in serum sex steroids in male and female black and polar bears, and to determine if changes in serum levels of these steroids were associated with metabolic condition or photoperiod. Serum testosterone (T) concentrations were elevated during spring in black and polar bears. Moreover, this increase in serum T in polar bears during spring was correlated with age and testis size. Serum progesterone (P4) concentrations increased in pregnant polar bears in fall coincident with the time of expected implantation. No increases in serum P4 were observed in nonpregnant black and polar bears. Serum estradiol (E2) was elevated in nonpregnant and pregnant polar bears 2 mo prior to the time of expected implantation. We found that serum sex steroids measured in black and polar bears change independent of torpor. Therefore, our results suggest that photoperiod may be a more important regulator of serum steroid levels and reproduction than metabolic condition.     

Monitoring the wild black bear's reaction to human and environmental stressors

Background

Bears are among the most physiologically remarkable mammals. They spend half their life in an active state and the other half in a state of dormancy without food or water, and without urinating, defecating, or physical activity, yet can rouse and defend themselves when disturbed. Although important data have been obtained in both captive and wild bears, long-term physiological monitoring of bears has not been possible until the recent advancement of implantable devices.

Results

Insertable cardiac monitors that were developed for use in human heart patients (Reveal® XT, Medtronic, Inc) were implanted in 15 hibernating bears. Data were recovered from 8, including 2 that were legally shot by hunters. Devices recorded low heart rates (pauses of over 14 seconds) and low respiration rates (1.5 breaths/min) during hibernation, dramatic respiratory sinus arrhythmias in the fall and winter months, and elevated heart rates in summer (up to 214 beats/min (bpm)) and during interactions with hunters (exceeding 250 bpm). The devices documented the first and last day of denning, a period of quiescence in two parturient females after birthing, and extraordinary variation in the amount of activity/day, ranging from 0 (winter) to 1084 minutes (summer). Data showed a transition toward greater nocturnal activity in the fall, preceding hibernation. The data-loggers also provided evidence of the physiological and behavioral responses of bears to our den visits to retrieve the data.

Conclusions

Annual variations in heart rate and activity have been documented for the first time in wild black bears. This technique has broad applications to wildlife management and physiological research, enabling the impact of environmental stressors from humans, changing seasons, climate change, social interactions and predation to be directly monitored over multiple years.     

Polar bear responses to the underwater vocalizations of ringed seals

Summary Two captive polar bears were exposed to six different marine mammal vocalizations, in an attempt to determine if polar bears would selectively respond to the underwater vocalization of their primary prey, ringed seals. Vocalizations were played to each bear for a total of eight minutes while their behavioral responses were observed. An analysis of activity indicated that the bears displayed a significantly stronger response to ringed seals' vocalizations. It is theorized that the ability to recognize the underwater vocalizations of their primary prey would increase a bear's probability of a successful capture when a ringed seal rises to breath at an ice bound breathing hole.     

Non-invasive detection of candidate pregnancy protein biomarkers in the feces of captive polar bears (Ursus maritimus)

Currently, there is no method of accurately and non-invasively diagnosing pregnancy in polar bears. Specific proteins may exhibit altered profiles in the feces of pregnant bears, but predicting appropriate candidate proteins to investigate is speculative at best. The objective of this study was to identify potential pregnancy biomarker proteins based on their increased abundance in the feces of pregnant polar bears compared to pseudopregnant females (controls) using two-dimensional in-gel electrophoresis (2D-DIGE) and mass spectrometry (MS). Three 2D-DIGE gels were performed to evaluate fecal protein profiles from controls (n = 3) and pregnant polar bears (n = 3). There were 2224.67 ± 52.39 (mean ± SEM) spots resolved per gel. Of these, only five proteins were elevated in the pregnant group (P < 0.05), and seven additional spots tended to be higher (0.05 < P < 0.10). All 12 were submitted for MS analysis and the identities of 11 were ascertained with a >99.9% confidence interval. The 11 spots represented seven distinct proteins, five of which were significantly more abundant in the pregnant group: IgGFc-binding protein, filamin-C, carboxypeptidase B, transthyretin, and immunoglobulin heavy chain variable region. To our knowledge, this was the first study that employed 2D-DIGE to identify differentially expressed proteins in fecal samples to characterize a physiological condition other than those related to gastrointestinal disorders. These promising results provided a strong foundation for ensuing efforts to develop a non-invasive pregnancy assay for use in both captive and wild polar bears.