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The cascading effects of human food on hibernation and cellular aging in free-ranging black bears

Authors:
  • U.S. Forest Service
  • USGS Alaska Science Center

Abstract and Figures

Human foods have become a pervasive subsidy in many landscapes, and can dramatically alter wildlife behavior, physiology, and demography. While such subsidies can enhance wildlife condition, they can also result in unintended negative consequences on individuals and populations. Seasonal hibernators possess a remarkable suite of adaptations that increase survival and longevity in the face of resource and energetic limitations. Recent work has suggested hibernation may also slow the process of senescence, or cellular aging. We investigated how use of human foods influences hibernation, and subsequently cellular aging, in a large-bodied hibernator, black bears (Ursus americanus). We quantified relative telomere length, a molecular marker for cellular age, and compared lengths in adult female bears longitudinally sampled over multiple seasons. We found that bears that foraged more on human foods hibernated for shorter periods of time. Furthermore, bears that hibernated for shorter periods of time experienced accelerated telomere attrition. Together these results suggest that although hibernation may ameliorate cellular aging, foraging on human food subsidies could counteract this process by shortening hibernation. Our findings highlight how human food subsidies can indirectly influence changes in aging at the molecular level.
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The cascading eects of human
food on hibernation and cellular
aging in free-ranging black bears
Rebecca Kirby
1, Heather E. Johnson
2,3, Mathew W. Alldredge4 & Jonathan N. Pauli1
Human foods have become a pervasive subsidy in many landscapes, and can dramatically alter wildlife
behavior, physiology, and demography. While such subsidies can enhance wildlife condition, they can
also result in unintended negative consequences on individuals and populations. Seasonal hibernators
possess a remarkable suite of adaptations that increase survival and longevity in the face of resource
and energetic limitations. Recent work has suggested hibernation may also slow the process of
senescence, or cellular aging. We investigated how use of human foods inuences hibernation, and
subsequently cellular aging, in a large-bodied hibernator, black bears (Ursus americanus). We quantied
relative telomere length, a molecular marker for cellular age, and compared lengths in adult female
bears longitudinally sampled over multiple seasons. We found that bears that foraged more on human
foods hibernated for shorter periods of time. Furthermore, bears that hibernated for shorter periods
of time experienced accelerated telomere attrition. Together these results suggest that although
hibernation may ameliorate cellular aging, foraging on human food subsidies could counteract this
process by shortening hibernation. Our ndings highlight how human food subsidies can indirectly
inuence changes in aging at the molecular level.
Human food subsidies, like garbage, crops, and livestock, are a ubiquitous consequence of human development13.
While such food subsidies can enhance nutritional condition and physiological performance of wildlife4, more
human food may not always be better. Easily accessible human foods may lack species-specific nutritional
requirements5,6, contain lethal toxicological compounds7, or enhance the spread of disease8. Consumption of
human foods can also alter animal behavior9, increasing the risk of injury or mortality in human-dominated land-
scapes10,11. In general though, the consequences of human food subsidies on the individual tness and longevity
of free-ranging animals remain largely unknown.
Torpor, a state of lowered metabolic demand, has evolved as an adaptive response to food limitations and
harsh environmental conditions. Although the degree and type of torpor range widely across animal groups, one
of the deepest and most extended forms is seasonal hibernation12, which is observed in eight groups of mammals.
By lowering body temperatures and reducing metabolic rates, hibernators accrue signicant energetic savings
and avoid predation, which increases overwinter and annual survival13, with direct implications for longevity14.
In particular, small-bodied mammals that can enter hibernation possess lifespans longer than expected from
their body size or metabolic rate15. is increased longevity appears to have coevolved with aspects of a relatively
slow life history strategy, including delayed onset of senescence13,16. Hibernation, then, not only conserves energy,
but may also be adaptive in slowing cellular aging14. Increasingly, researchers are utilizing telomeres – repetitive
DNA sequences on the ends of eukaryotic chromosomes17,18 that are lost during cellular replication and from
oxidative damage19 – as markers to quantify cellular aging, or aging distinct from chronology2022. Recent studies
have found that more time spent in torpor can decelerate telomere attrition, or reduce cellular aging, among
small hibernators2325. Although the exact mechanism of hibernation that slows cellular aging in small-bodied
mammals is unknown, it appears to be associated either with a reduction in cell turnover rates26 or a reduction
in oxidative stress24.
1Department of Forest and Wildlife Ecology, University of Wisconsin – Madison, 1630 Linden Dr., Madison, WI, 53706,
USA. 2Mammals Research Section, Colorado Parks and Wildlife, 415 Turner Dr., Durango, CO, 81303, USA. 3Present
address: USGS Alaska Science Center, 4210 University Dr., Anchorage, AK, 99508, USA. 4Mammals Research Section,
Colorado Parks and Wildlife, 317 W. Prospect Rd., Fort Collins, CO, 80526, USA. Correspondence and requests for
materials should be addressed to R.K. (email: kirbyr@gmail.com)
Received: 16 August 2018
Accepted: 15 January 2019
Published: xx xx xxxx
OPEN
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Changes to hibernation strategies and characteristics, then, are likely to have important implications for indi-
vidual tness. For example, warmer weather during the winter and spring due to climate change27 has altered the
timing of emergence, leading to phenological mismatches with food sources28 and reducing individual tness29.
Expanding human development and increased wildlife access to supplemental food has been linked to delayed
or shortened hibernation11,30,31, and even the loss of hibernation for a winter altogether32. Shortened hibernation
periods are likely to lead to similar mismatches with local food sources and increased interactions and conicts
with humans11,31. It is unknown what these consequences will have on individual physiology or tness traits,
but given that hibernation is modulated primarily by local food conditions11,12,30,33, natural food availability and
human subsidies could indirectly govern senescence by altering rates of cellular aging.
In this study, we investigated the relationship between food subsidies, hibernation, and cellular aging in the
American black bear (Ursus americanus). As large-bodied hibernators, bears are suciently long-lived to exhibit
senescence34,35, but unlike small hibernators, they remain near-euthermic during hibernation in spite of their
reduced metabolic rate36 and increased oxidative stress37. Preliminary research suggests that cellular aging in
black bears is driven principally by environmental conditions—such as natural food availability—found at dif-
ferent latitudes38. Bears generally hibernate for 4–6 months/year, and denning chronology is driven in part by
forage availability – individuals with access to more food tend to enter hibernation later and den for shorter peri-
ods11,30,39. Furthermore, black bears oen supplement their diet with human food subsidies, especially in years of
natural food shortages40,41. Bears that use areas of human development show decreased hibernation periods11,30,31.
is altered denning chronology is assumed to result from increased consumption of food subsidies, although
this link has not been directly explored. To assess the eects of food subsidies on hibernation and cellular aging,
we tracked and sampled a subset of female black bears through several summer and winter seasons as part of a
larger study in Durango, Colorado, USA11,40. We analyzed bear stable isotopic signatures (δ13C) as a measure of
consumption of human foods41,42, and determined the inuence of use of human food on hibernation lengths
across individuals. We then assessed the relationship between hibernation length and rates of telomere length
to test the role of hibernation in cellular aging. Finally, we examined whether the specic role of oxidative stress
associated with hibernation is a potential mechanism mediating telomere length change in bears.
Results
Female black bears (n = 30) averaged 8 years old at rst sampling (range: 2 to 24) and hibernation lengths over
the study averaged 170 days (range: 134 to 223). Summer sampled bears averaged 20.63 δ13C (range: 22.36 to
18.80). Bear serum exhibited average oxidative damage of 10.8 mg H2O2 dl1 (range: 4.5 to 18.8) and average
antioxidant capacity of 516 μmol HClO ml1 neutralized (range: 349 to 769). Age was positively correlated with
hibernation length (r = 0.73, P < 0.001); however, given the importance of age in determining bear physiology
and behavior11, and that the variance ination factor was only 1.47, we retained age as a covariate in subsequent
tests.
Bears enriched in δ13C during the summer (i.e., those that consumed more human foods), as well as younger
bears, hibernated for shorter periods the subsequent winter (Table1a, Fig.1A). Telomere lengths on average
decreased at a rate of 0.001 RTL/month (σ = 0.01) throughout the study period, but this pattern was inconsistent,
as almost half the bears showed increased telomere lengths. We found that the mean monthly rate of telomere
change was related to hibernation length; bears that hibernated longer on average experienced a slower rate of tel-
omere attrition or even telomere lengthening during the study (Table1b, Fig.1B). ere was limited support that
telomere length change was related to oxidative stress (antioxidant capacity/oxidative damage; Table1b; model
coecients are reported in Supplementary Table1).
Oxidative damage (ROM) was related to sampling season, breeding status, and age (Table2a). Bears exhibited
increased oxidative damage during hibernation compared to the summer, and bears that had newborn cubs
AICcΔAICcweight Adj. R2
(a) Hibernation length
δ13C 132.48 0.00 0.60 0.44
δ13C + Age 134.26 1.78 0.25 0.47
Age 135.57 3.09 0.13 0.32
Intercept only 139.19 6.71 0.02
(b) Telomere leng th change (per month)
Hibernation 176.08 0.00 0.39 0.12
Age 174.38 1.70 0.17 0.07
Intercept only 173.76 2.32 0.12
Hibernation + Oxidative stress 173.49 2.60 0.11 0.09
Hibernation + Age 173.49 2.60 0.11 0.09
Age + Oxidative stress 172.00 4.09 0.05 0.04
Oxidative stress 171.40 4.68 0.04 0.00
Hibernation + Age + Oxidative stress 170.70 5.38 0.03 0.06
Table 1. Models ranked by AICc to predict: (a) hibernation length over one winter, with age and δ13C signature
of bear hair sampled in the preceding summer as covariates (n = 15); (b) average monthly telomere length
change, with age, oxidative stress, and hibernation length over the study period as covariates (n = 30).
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exhibited reduced oxidative damage compared to those that were barren or had yearlings. We found minimal
dierences in antioxidant capacity among bears based on our covariates (model coecients are reported in
Supplementary Table2).
Discussion
Highly accessible and predictable food subsides can alter animal behavior9,43, change population dynamics44, and
restructure community assemblages and species interactions45,46. Our study demonstrates that such food subsi-
dies are also associated with cellular aging indirectly via altering hibernation length. Black bears with a greater
reliance on human food subsidies were associated with having shorter hibernation lengths, and these shortened
hibernation periods were associated with greater telomeric attrition. Consequently, bears that use more food
subsidies hibernate less and thereby appear to experience greater cellular aging.
Hibernation chronology is driven by individual energy balance47, which is strongly linked to local weather
conditions and food availability11,30. Recent work has shown that bears with access to more food, and bears exhib-
iting increased use of human development, den later and for a shorter period11,31. Our results demonstrate that
greater consumption of human foods is associated with shorter hibernation in black bears. Increased consump-
tion of human foods by bears has been associated with increased body weights and fecundity, but also reduced
survival (due to vehicle collisions, lethal management, etc.)10,48. As a result, it has been suggested that urban areas
may serve as an ecological trap10,41. is risk may be compounded by increased bear-human interactions result-
ing from shortened denning31, as well as have further consequences on tness, through altered hibernation and
accelerated telomere loss.
Bears display a remarkable suite of adaptations allowing them to remain immobile during hibernation, yet
avoid negative side eects such as bone loss49 and muscle atrophy50. An additional advantage of hibernation
appears to be slowed cellular aging; we found that bears with longer average hibernation lengths showed reduced
rates of telomere shortening over the study period. Our nding corroborates recent work in small hibernators
that eectively demonstrated that longer and deeper bouts of torpor slowed cellular aging2325. Because telomere
Figure 1. (A) Hibernation length for each bear (over one winter) regressed on the δ13C signature of bear hair
sampled in the preceding summer (n = 15), showing a relationship between increased enrichment in δ13C and
shorter hibernation lengths. (B) Average monthly telomere length (RTL) change regressed against hibernation
lengths (days) for each bear (n = 30), exhibiting a relationship between longer hibernation length and slower
rate of telomere shortening, and even telomere lengthening.
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dynamics reect accumulated life stress20 and can predict survival and longevity21, altering those dynamics
through shortened denning periods may have negative long-term consequences.
Some animals display adaptations to counteract telomeric shortening, such asunusually high levels of the
enzyme telomerase, which lengthens telomeres51,52. Although oxidative damage is typically an accelerant of tel-
omere attrition19,53,54, animals that increase their antioxidant capacity might be able to mitigate such eects55.
However, we found that although bears exhibited increased oxidative damage during hibernation compared to
the active season37, we did not detect a concurrent increased antioxidant capacity. According to these stress meas-
ures, it appears that hibernation ameliorates cellular aging in spite of increased oxidative damage, perhaps due
to reduced metabolic rate or enhanced somatic maintenance. is lack of a relationship between oxidative stress
and telomere attrition could, however, also be inuenced by our sampling - telomeres were not measured imme-
diately before and aer hibernation, and therefore may be more representative of stress experienced throughout
the study period, not only during hibernation.
In addition to seasonal dierences, oxidative damage diered among breeding status; females with cubs
showed less damage, corroborating a recent study in polar bears56. Reproduction, and lactation in particular, is
energetically expensive57,58, and resulting oxidative stress is typically regarded as a cost of reproduction59. e
relationship between reduced oxidative damage and reproduction in bears remains unclear; however, researchers
have speculated it could result from physiological changes during lactation that allow the o-loading of contam-
inants that otherwise induce oxidative stress56.
Our study of a free-ranging large hibernator suggests that increased reliance on human food subsidies reduces
hibernation lengths. Our study also supports previous work on small hibernators that a benet of hibernation is
decelerated telomere attrition23. us, bears consuming more human foods may lose some of the long-term t-
ness advantages associated with hibernating, in particular rates of cellular aging. erefore, the continued growth
in food subsidies to wildlife are likely to cascade into altered behavior, ultimately with potential molecular conse-
quences for rates of cellular aging.
Methods
Sample collection. Black bears were captured near Durango, Colorado, from summer 2011 through winter
2015. All captures and animal handling were performed in accordance with relevant guidelines and regulations
and approved by Colorado Parks and Wildlife [CPW], Fort Collins, CO (Animal Care and Use Protocol #01-
2011)11. Adult females were tted with GPS collars (Vectronics Globalstar) and subsequently relocated at their
winter dens. irty bears were included in this study that were sampled a minimum of twice during the study
period, twenty-six were sampled 3 times. Sampling occurred during initial capture in summer (mainly June –
August) and then again during winter den visits (mainly early February – mid-March) in subsequent years; 18 of
the bears were sampled in both the summer and winter within the same year.
During captures, bears were immobilized11, and guard hair and blood samples were collected for molecular
analyses. At rst capture, a premolar was removed to determine chronological age by counting cementum annuli
(Matsons Lab, Milltown, MT)60. Breeding status was also identied by the presence/absence of cubs (or lactation
during summer captures when cubs were not always visible) or yearlings, and adult females categorized as “with
yearlings”, “with cubs”, or “barren. Black bear cubs are born during hibernation, and nurse part of that rst year,
AICcΔAICcweight marginal R2conditional R2
(a) Oxidative damage
Age + Season + Breeding status 506.36 0.00 1.00 0.26 0.42
Age + Breeding status 519.39 13.03 0.00 0.15 0.41
Age + Season 519.54 13.18 0.00 0.13 0.34
Age 531.17 24.81 0.00 0.04 0.27
Season + Breeding status 554.39 48.03 0.00 0.21 0.33
Breeding status 567.09 60.74 0.00 0.10 0.31
Season 567.21 60.85 0.00 0.10 0.27
Intercept only 578.20 71.84 0.00
(b) Antioxidant capacity
Age + Season + Breeding status 1011.64 0.00 0.96 0.01 0.53
Age + Breeding status 1017.88 6.24 0.04 0.01 0.54
Age + Season 1025.29 13.65 0.00 0.00 0.53
Age 1031.29 19.66 0.00 0.00 0.53
Season + Breeding status 1115.15 103.52 0.00 0.01 0.54
Breeding status 1121.19 109.55 0.00 0.01 0.55
Season 1128.93 117.29 0.00 0.00 0.54
Intercept only 1137.79 126.16 0.00
Table 2. Models ranked by AICc to predict measures of: (a) oxidative damage (ROM) and (b) antioxidant
capacity in black bear serum (unique bears = 28 and samples = 84, with repeated bear samples accounted
for with a random eect. Fixed eects included age, season (active/summer or hibernation/winter), and
reproductive status at summer sampling (barren or with cubs, as yearlings had already dispersed).
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typically staying with their mother through the next winter season; at the start of the second summer, yearlings
will disperse.
We used collar activity sensor data to determine den entry and exit dates for each bear on an annual basis11. In
11 observations (out of 58 total), activity data were not available to estimate denning dates. In those cases, we used
hourly GPS locations to dene den entry as the rst day of a 6-day period when a bear was exclusively located
within 135 m of her den, and den emergence as the rst day of a 6-day period when a bear remained 135 m away
from her den61. Hibernation length was calculated as the number of days between den entrance and emergence.
Laboratory analyses. Blood samples for DNA extraction were stored in EDTA tubes; those for oxida-
tive stress analyses were kept in serum-separating tubes. All samples were stored at 20 °C until analyses. We
extracted DNA with standard procedures (QIAGEN DNeasy Blood and Tissue Extraction Kit; QIAGEN Inc.,
Valencia, CA). We quantied relative telomere lengths (RTL) using real-time quantitative polymerase chain reac-
tion (qPCR)62. We previously optimized this method using the HNRPF gene63 and telomere primers telg and
telc38,64 (Supplementary Material). We quantied relative telomere lengths from each sample. Because samples
were collected once in the summer, and following mid-winters, we accounted for dierences between sampling
times of individuals by calculating an overall telomere length change for each bear between their rst and last
capture, averaged over months (n = 30).
Hair samples were prepared for stable isotope analyses asdescribed in Pauli et al. 200965. Results are provided
as per mil (‰) ratios relative to international standard, with calibrated internal laboratory standards. Individual
foraging was represented by δ13C of hair samples; specically enrichment in δ13C signies increased human food
in bear diets41,66. Human foods are enriched in δ13C compared to temperate native vegetation because they are
dominated by corn and cane sugar derivatives67. Hair samples represent the assimilated diet during hair growth
from spring through fall68, though in black bears tend to be highly correlated with stable isotopes in bone colla-
gen, representing overall lifetime diet42.
We measured oxidative damage in bear serum samples, using the d-ROM test (Diacron International, Italy).
e d-ROM test measures oxidative damage via the concentration of hydroperoxide, a reactive oxygen metabolite
(ROM) that results from an attack of reactive oxygen species on organic substrates (e.g. nucleotides, proteins).
e oxy-adsorbent test measures the total antioxidant capacity of the sample by measuring the ability of the
serum to oppose the massive oxidative action of a hypochlorous acid (HClO) solution. Oxidative stress or status
of an individual sample can be considered the ratio of antioxidant capacity to oxidative damage55,69. We prepared
samples following the manufacturer’s protocol (Supplementary Material).
Data analyses. We tested three main hypotheses: (1) bear consumption of human foods reduces hiberna-
tion length; (2) reduced hibernation accelerates telomere attrition (i.e., the cellular aging process); (3) increased
oxidative stress is a mechanism mediating telomere attrition. To test whether foraging on human food subsidies
inuenced hibernation length, we used linear regression with hibernation length (days) as the response variable
and δ13C of bear hair (sampled in the preceding summer) as an explanatory variable. We also included age as a
covariate, to account for the fact that older bears hibernate longer11. We restricted our data to bears sampled in
summer and then again in the following winter (n = 15). To test our second and third hypotheses, we explored the
relationship between telomeres (rate of telomere change for each individual, standardized as change per month),
hibernation length (days within one season for each individual, averaged over multiple seasons), and oxidative
stress (ratio of antioxidant capacity to oxidative damage for each individual, averaged over the sampling period;
n = 30). Finally, because repeated oxidative stress samples from an individual bear uctuated throughout the
study period, we also examined factors associated with individual measures of oxidative stress (oxidative damage
and antioxidant capacity) during sampling, rather than averaged over the study. We examined separately how
oxidative damage or antioxidant capacity varied with age, sampling season (summer or winter), and breeding
status of bears with linear mixed models; repeated samples from the same bear were accounted for with a random
eect (unique bears = 28, samples = 84). For all analyses, we compared linear regression models using Akaike’s
Information Criteria corrected for small sample sizes (AICc). e datasets are available from the corresponding
author on reasonable request.
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Acknowledgements
is work was funded by Colorado Parks and Wildlife, University of Wisconsin-Madison, and an American
Society of Mammologists Grant-in-Aid. We thank numerous field technicians that collected data with the
Durango bear project, as well as student lab technicians, especially Sonia Petty and Samantha Paddock. We also
thank David Lewis for assisting with eld data summaries.
Author Contributions
R.K. and J.N.P. wrote the manuscript and performed statistical analyses. H.E.J. and R.K. carried out eld and
laboratory analyses. R.K., H.E.J., M.W.A., and J.N.P. designed the study and reviewed the manuscript.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-019-38937-5.
Competing Interests: e authors declare no competing interests.
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Supplementary resource (1)

... (2) Not yet explored in ursids Although HPA-mediated stress has been measured using a wide array of methods in non-ursid, free-ranging vertebrates, not all approaches would be practical in bear-stress studies, primarily due to reliance on laboratory-based experimentation and the challenges of studying animals in the natural environment. However, techniques that can be applied to physiological studies of stress in free-ranging bears include evaluating relative telomere length (Kirby, Alldredge & Pauli, 2017;Kirby et al., 2019), leukocyte profiles determined from differential haematological indicators and regenerative anaemia (Charbonnel et al., 2008;Johnstone et al., 2012b;Kotrschal, Ilmonen & Penn, 2007). ...
... While using telomere indicators of chronic stress to identify environmental stressors is plausible, it has not been extensively investigated in ecophysiological studies (Johnstone et al., 2012a). Thus far, hibernation has been shown to play a key role in ameliorating telomere attrition (Kirby et al., 2017(Kirby et al., , 2019 and, in some cases, promoting telomere lengthening in edible dormice (Glis glis) (Hoelzl et al., 2016;Turbill et al., 2013). Although telomeres and accumulated stress are inextricably linked, applications in bears have been primarily focused on telomere dynamics, rather than environmental and/or anthropogenic stress as a central topic. ...
... Although telomeres and accumulated stress are inextricably linked, applications in bears have been primarily focused on telomere dynamics, rather than environmental and/or anthropogenic stress as a central topic. For example, environmental factors are more important than individual characteristics in the regulation of telomere length in American black bears (Kirby et al., 2017) and bears that hibernate for shorter periods due to increased anthropogenic food availability experienced accelerated telomere attrition (Kirby et al., 2019). Results from Kirby et al. (2019) suggest that whilst hibernation is likely to play a key role in ameliorating cellular ageing and telomere attrition, availability and consumption of anthropogenic food subsidies may counteract these mechanisms by shortening hibernation, because hibernatory behaviour is dependent on food limitation during the winter. ...
Article
Full-text available
Stress responses, which are mediated by the neurogenic system (NS) and hypothalamic-pituitary-adrenal (HPA) axis help vertebrates maintain physiological homeostasis. Fight-or-flight responses are activated by the NS, which releases norepinephrine/noradrenaline and epinephrine/adrenaline in response to immediate stressors, whilst the HPA axis releases glucocorticoid hormones (e.g. cortisol and corticosterone) to help mitigate allostatic load. There have been many studies on stress responses of captive animals, but they are not truly reflective of typical ranges or the types of stressors encountered by free-ranging wildlife, such as responses and adaptation to environmental change, which are particularly important from a conservation perspective. As stress can influence the composition of age and sex classes of free-ranging populations both directly and indirectly, ecological research must be prioritised towards more vulnerable taxa. Generally , large predators tend to be particularly at risk of anthropogenically driven population declines because they exhibit reduced behavioural plasticity required to adapt to changing landscapes and exist in reduced geographic ranges, have small population sizes, low fecundity rates, large spatial requirements and occupy high trophic positions. As a keystone species with a long history of coexistence with humans in highly anthropogenic landscapes, there has been growing concern about how humans influence bear behaviour and physiology, via numerous short-and long-term stressors. In this review, we synthesise research on the stress response in free-ranging bear populations and evaluate the effectiveness and limitations of current methodology in measuring stress in bears to identify the most effective metrics for future research. Particularly, we integrate research that utilised haematological variables, cardiac monitors and Global Positioning System (GPS) collars, serum/plasma and faecal glucocorticoid concentrations, hair cortisol levels, and morphological metrics (primarily skulls) to investigate the stress response in ursids in both short-and long-term contexts. We found that in free-ranging bears, food availability and consumption have the greatest influence on individual stress, with mixed responses to anthropogenic influences. Effects of sex and age on stress are also mixed, likely attributable to inconsistent methods. We recommend that methodology across all stress indicators used in free-ranging bears should be standardised to improve interpretation of results and that a wider range of species should be incorporated in future studies.
... The availability of these foods can alter natural nutritional landscapes with detrimental effects [24,46]. For example, hibernation in mammals is perturbed when human foods are consumed [47,48], and racoons feeding on human foods in urbanized areas have greater weight and blood sugar content [49]. In birds, American crow (Corvus brachyrhynchos) chicks are smaller [50], Canadian geese (Branta canadensis maxima) have higher rates of angel wing disorder in urbanized areas, probably as a result of nutrient deficiency [51], and Australian magpies (Gymnorhina tibicen) show alterations to blood chemistry following backyard provisioning [52]. ...
... Similarly, our finding that ground finches do not find bitter tastes aversive expands the increasing knowledge on variation in response to tastes among species. As the adoption of human foods into animals' diets can have cascading effects on health, reproduction and fitness [6,15,20,47,49], it remains of paramount importance to elucidate why some species integrate these foods while others do not. ...
Article
Full-text available
Urbanization is rapidly changing ecological niches. On the inhabited Galapagos Islands, Darwin's finches consume human-introduced foods preferentially; however, it remains unclear why. Here we presented pastry with flavour profiles typical of human foods (oily, salty, sweet) to small and medium ground finches to test if latent taste preferences might drive selection of human foods. If human-food flavours were consumed more than a neutral or bitter control only at sites with human foods, then we predicted tastes were acquired after urbanisation; however, if no site-differences were found then this would indicate latent taste preferences. Contrary to both predictions, we found no evidence that human-food flavours were preferred compared to control flavours. Instead, medium ground finches consumed the bitter control pastry most and wiped their beaks more frequently after feeding on oily and sweet pastry (post-ingestion beak-wiping can indicate aversions). Small ground finches showed no differences in consumption but wiped their beaks most after feeding on sweet pastry. We found no evidence that medium and small ground finches found bitter-tasting food aversive. Furthermore, we found no evidence that taste preferences could have played a major role in Darwin's finches responding to the presence of human foods during increased urbanization.
... Regardless of the mechanism (i.e., reduced energy expenditure or predation risk), a 2011 meta-analysis found evidence that during the hibernation period, individuals benefit from improved monthly survivorship relative to the active season and, overall, hibernating species had higher annual survival rates as compared to non-hibernators (Turbill et al., 2011). Further, hibernation has been associated with increased longevity (Turbill et al., 2011), which may be the result of senescence being inhibited during hibernation (Lyman et al., 1981;Turbill et al., 2013;Kirby et al., 2019) and/or life history trade-offs that result from increased survival probability (Turbill et al., 2011). ...
Thesis
Full-text available
Hibernation is an energy-saving strategy employed by species to survive periods of low resource abundance and inclement weather. Due to the costs and benefits associated with the use of torpor and arousal during hibernation, individuals are predicted to hibernate according to their energetic state entering hibernation and their requirements following hibernation. The timing and quantity of energetic requirements following hibernation can vary between the sexes due to differences in selective pressures. Thus, there is potential for sexual variation in hibernation expression to exist. Species and/or populations that exhibit individual variation in hibernation expression lend themselves as an ideal species to test such predictions. Black-tailed prairie dogs (Cynomys ludovicianus) are a species that demonstrates tremendous variation in over-winter thermoregulatory strategies across their range. Prairie dogs within Canada comprise the northernmost population of this species and are the only population of black-tailed prairie dogs known to consistently hibernate over winter. Previous studies reveal variation in hibernation expression within this population. Yet, it is currently unknown what influences this variation, and in general, this unique aspect of their biology remains understudied. However, recent study indicates that males and females differ in their overwinter winter mass loss which may result from differences in hibernation expression. In this thesis, I investigated the role of sex and pre-hibernation body condition on hibernation expression and over-winter energy expenditure in a single colony of prairie dogs located in Grasslands National Park, SK, CA. First, I investigated whether males and females differed in their hibernation expression and energy expenditure by assessing the use of various hibernation traits and quantifying over-winter change in body condition. I found that females had longer hibernation periods, used more bouts of torpor, and overall spent a greater amount of time in torpor compared to males. However, males spent a greater proportion of their shorter hibernation period in torpor and used longer, colder bouts of torpor. Despite differences in hibernation expression, I did not find any evidence that males and females lost similar amounts of condition over winter, though males appeared to lose condition at a faster rate. However, results regarding over-winter changes in body condition should be interpreted with caution due to discrepancies between when male and female prairie dogs hibernated relative to when I recorded body condition measurements. I also conducted a supplemental feeding trial during a portion of the pre-hibernation fattening period of prairie dogs to expand variation in pre-hibernation body condition and combined this data with previously existing data to investigate the influence of pre-hibernation body condition on hibernation expression and over-winter change in body condition. I found that, relative to individuals in poor condition, individuals in better pre-hibernation body condition did not shorten the duration of the hibernation period but did reduce the proportion of the hibernation period spent torpid and increased the length of arousal bouts. Prairie dogs in good pre-hibernation body condition did experience a greater decrease in body condition over winter but still emerged from hibernation in better condition compared to individuals of a poorer condition. The work presented in this thesis increases our understanding of a relatively unknown aspect of black-tailed prairie dog biology - hibernation. Additionally, this thesis improves our understanding of the factors that influence hibernation expression and how individuals alter their use of hibernation with respect to their energetic condition. Future research investigating prairie dog body mass dynamics immediately after hibernation and the effects of sociality and predation on hibernation could be explored to further our understanding of hibernation use. Increasing our understanding of the factors that influence intraspecific variation in hibernation expression can lead to advances in understanding how hibernation evolved as well as aid us in our predictions of if and how populations will respond to changing environments.
... Our results, combined with recent literature on telomere dynamics in small (Criscuolo et al., 2020;Foley et al., 2018; and large mammals (Kirby et al., 2019;Lemaître et al., 2021), as well as in fishes (Panasiak et al., 2020) and birds (Spurgin et al., 2018), pinpoint that a much greater variety of telomere dynamics patterns may exist than previously reported, including withinindividual telomere elongation, and that these patterns likely correlate with pace of life. Proximal mechanisms explaining telomere elongation in chipmunks will have to be investigated in the future, but we can hypothesize that telomerase activity is involved (Smith et al., 2021). ...
... Our results, combined with recent literature on telomere dynamics in small (Criscuolo et al., 2020;Foley et al., 2018; and large mammals (Kirby et al., 2019;Lemaître et al., 2021), as well as in fishes (Panasiak et al., 2020) and birds (Spurgin et al., 2018), pinpoint that a much greater variety of telomere dynamics patterns may exist than previously reported, including withinindividual telomere elongation, and that these patterns likely correlate with pace of life. Proximal mechanisms explaining telomere elongation in chipmunks will have to be investigated in the future, but we can hypothesize that telomerase activity is involved (Smith et al., 2021). ...
Article
Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus co-evolved with early reproduction, proactive behaviour and reduced lifespan, i.e. a fast Pace-of-Life Syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anti-cancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age (n = 204 and n = 20) and do not limit lifespan in this species (n = 51). Furthermore, short telomeres correlated with a slow POLS in a sex-specific way (n = 37). Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, while we found no differences in males. Our findings support most predictions adapted from the anti-cancer hypothesis, but none of those from the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade-offs shape the diversity of telomere length in adult somatic cells and the relationships between telomere length and life-histories.
... Our results also support the idea that a shorter growing season can improve maternal survival as mortality risk is lower during the hibernation period (e.g., reduced predation and reduced cellular aging) (Bieber et al., 2014;Kirby et al., 2019;Turbill et al., 2011). Reproductive females in particular must meet the energetic demands of reproduction by increasing the amount of time they spend foraging (Macwhirter, 1991). ...
Article
Full-text available
Maternal characteristics, social dynamics, and environmental factors can all influence reproduction and survival and shape trade-offs that might arise between these components of fitness. Short-lived mammals like the golden-mantled ground squirrel (GMGS; Callospermophilus lateralis) tend to maximize effort toward current reproduction at the expense of survival but may be complicated by other aspects of the species' life history and environment. Here, we use 25 years of data (1995-2020) collected from a population of GMGS at the Rocky Mountain Biological Research Laboratory in Gothic, Colorado, to test the effect of several maternal characteristics (e.g., age, experience, and timing of litter emergence), social context (e.g., litter sex ratio and kin density), and environmental context (e.g., date of bare ground and length of vegetative growing season) on survival of reproductive female GMGS using Cox proportional hazard models. Our results indicated that social dynamics (i.e., density) and environmental conditions (i.e., standardized first day of permanent snow cover and length of growing season) explained significant variation in annual maternal survival, while maternal characteristics did not. A higher density of related breeding females and the total number of females (both related and unrelated to the focal mother) were associated with an increase in the mortality hazard. A later standardized date of the first day of permanent snow cover and a shorter growing season both reduced the maternal mortality hazard. Together, our results suggest that factors extrinsic to the squirrels affect maternal survival and thus may also influence local population growth and dynamics in GMGS and other short-lived, territorial mammal species.
... The seasonal trends observed in marmot ageing probably occur in other species because molecular and physiological changes during hibernation are similar among mammals 36,41,47,70 . Some indications that hibernation slows ageing exist: Turkish hamsters (Mesocricetus brandti) that spent more time hibernating lived longer 71 ; black bears with shorter hibernation length had higher telomere attrition 72 and Djungarian hamsters (Phodopus sungorus) frequently using daily torpor had longer relative telomere length (RTL) 49 . RTL was shorter in edible 48 and garden 73 dormice (Glis glis and Eliomys quercinus) that spent more time euthermic during hibernation. ...
Article
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Species that hibernate generally live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor–arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause ageing suppression. Metabolic rate is also a known correlate of longevity; we thus proposed the ‘hibernation–ageing hypothesis’ whereby ageing is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots ( Marmota flaviventer ), which spend 7–8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females was modelled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic ageing over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (two years old). With respect to circannual patterns, the epigenetic age increased during the active season and essentially stalled during the hibernation period. Taken together, our results are consistent with the hibernation–ageing hypothesis and may explain the enhanced longevity in hibernators.
... While wildlife agencies consider hunting to be an important source of funding and a useful tool for maintaining target population sizes, access to human-provisioned foods can shift wildlife behavior (Newsome et al. 2015), influence cellular aging by shortening black bear hibernation length (Kirby et al. 2019), and affect both species interactions (Rodewald et al. 2011) and population dynamics (Fedriani et al. 2001). We showed that long-term consumption of human-provisioned foods by black bears can drive changes in microbial niche space in the black bear gut. ...
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Technical Report
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Aging negatively affects individual survival and reproduction; consequently, characterizing the factors behind aging can enhance our understanding of fitness in wild populations. The drivers of biological age are diverse, but often related to factors like chronological age or sex of the individual. Recently, however, environmental factors have been shown to strongly influence biological age. To explore the relative importance of these influences on biological aging in a free-ranging and long-lived vertebrate, we quantified the length of telomeres—highly conserved DNA sequences that cap the ends of eukaryotic chromosomes and a useful molecular marker of biological age—for black bears sampled throughout Colorado, and measured a variety of environmental variables (habitat productivity, human development, latitude, elevation) and individual characteristics (age, sex, body size, genetic relatedness). Our extensive sampling of bears (n = 245) revealed no relationships between telomere length and any individual characteristics. Instead, we found a broad-scale latitudinal pattern in telomere length, with bears in northern Colorado possessing shorter telomeres. Our results suggest that environmental characteristics overwhelm individual ones in determining biological aging for this large carnivore.
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The influence of climate change on the fitness of wild populations is often studied in the context of the spring onset of the reproductive season. This focus is relevant for climate influences on reproductive success, but neglects other fitness-relevant periods (e.g., autumn preparation for overwintering). We examined variation in climate variables (temperature, rainfall, snowfall, and snowpack) across the full annual cycle of Columbian ground squirrels (Urocitellus columbianus) for 21 years. We investigated seasonal climate variables that were associated with fitness variables, climate variables that exhibited directional changes across the study period, and finally observed declines in fitness (−0.03 units/year; total decline = 37%) that were associated with directional changes in climate variables. Annual fitness of adult female ground squirrels was positively associated with spring temperature (r = 0.69) and early summer rainfall (r = 0.56) and negatively associated with spring snow conditions (r = −0.44 to −0.66). Across the 21 years, spring snowmelt has become significantly delayed (r = 0.48) and summer rainfall became significantly reduced (r = −0.53). Using a standardized partial regression model, we found that directional changes in the timing of spring snowmelt and early summer rainfall (i.e., progressively drier summers) had moderate influences on annual fitness, with the latter statistically significant (ρ = −0.314 and 0.437, respectively). The summer period corresponds to prehibernation fattening of young and adult ground squirrels. Had we focused on a single point in time (viz. the onset of the breeding season), we would have underestimated the influences of climate change on our population. Rather, we obtained a comprehensive understanding of the influences of climate change on individual fitness by investigating the full lifecycle.
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Expanding human development and climate change are dramatically altering habitat conditions for wildlife. While the initial response of wildlife to changing environmental conditions is typically a shift in behaviour, little is known about the effects of these stressors on hibernation behaviour, an important life-history trait that can subsequently affect animal physiology, demography, interspecific interactions and human-wildlife interactions. Given future trajectories of land use and climate change, it is important that wildlife professionals understand how animals that hibernate are adapting to altered landscape conditions so that management activities can be appropriately tailored. We investigated the influence of human development and weather on hibernation in black bears (Ursus americanus), a species of high management concern, whose behaviour is strongly tied to natural food availability, anthropogenic foods around development and variation in annual weather conditions. Using GPS collar data from 131 den events of adult female bears (n = 51), we employed fine-scale, animal-specific habitat information to evaluate the relative and cumulative influence of natural food availability, anthropogenic food and weather on the start, duration and end of hibernation. We found that weather and food availability (both natural and human) additively shaped black bear hibernation behaviour. Of the habitat variables we examined, warmer temperatures were most strongly associated with denning chronology, reducing the duration of hibernation and expediting emergence in the spring. Bears appeared to respond to natural and anthropogenic foods similarly, as more natural foods, and greater use of human foods around development, both postponed hibernation in the fall and decreased its duration. Synthesis and applications. Warmer temperatures and use of anthropogenic food subsides additively reduced black bear hibernation, suggesting that future changes in climate and land use may further alter bear behaviour and increase the length of their active season. We speculate that longer active periods for bears will result in subsequent increases in human–bear conflicts and human-caused bear mortalities. These metrics are commonly used by wildlife agencies to index trends in bear populations, but have the potential to be misleading when bear behaviour dynamically adapts to changing environmental conditions, and should be substituted with reliable demographic methods.
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It has long been presumed impossible to measure telomeres in vertebrate DNA by PCR amplification with oligonucleotide primers designed to hybridize to the TTAGGG and CCCTAA repeats, because only primer dimer-derived products are expected. Here we present a primer pair that eliminates this problem, allowing simple and rapid measurement of telomeres in a closed tube, fluorescence-based assay. This assay will facilitate investigations of the biology of telomeres and the roles they play in the molecular pathophysiology of diseases and aging.
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Food subsidies have become a widely available and predictable resource in human-modified landscapes for many vertebrate species. Such resources can alter individual foraging behavior of animals, and induce population-wide changes. Yet, little consensus exists about the relative influence of the availabilities of native and human food subsidies to wildlife foraging throughout altered landscapes. We explored this unresolved question by analyzing the effects of landscape factors on American black bear (Ursus americanus) diet across the state of Colorado, USA. We estimated assimilated diet using stable isotope analysis of harvested black bear tissues to determine the contribution of human-derived foods to bear diets throughout Colorado, as well as how increasing reliance on human-derived food subsidies increases the risk of conflict. We found that bears (n = 296) showed strong regional diet variability, but substantial use of human-derived food subsidies in eastern Colorado (> 30% assimilated diet). The age-sex class of the bear and housing density of its harvest location were the most influential predictors of 13C enrichment (a tracer of human food subsidies). Furthermore, foraging on subsidies increased risk of conflict; the odds of being a nuisance bear increased by 60% for each ~ 1‰ increase in δ13C. Our study confirms the efficacy of δ13C as a proxy for human activity, and indicates that while demographic differences play a clear role in the foraging ecology of bears, availability of subsidies coincident with varying levels of human activity appears to be a major driver in predicting black bear diet throughout the western United States.