What Animal Behavior Would Be Helpful In A Polar Environment

Ecol Evol. 2018 Aug; 8(16): 7790–7799.

Development of on‐shore behavior among polar bears (Ursus maritimus) in the southern Beaufort Sea: inherited or learned?

Kate M. Lillie

^one Department of Wildland Resources, Utah Land Academy, Logan, Utah,

Eric M. Gese

^two U.Southward. Department of Agronomics, Wild fauna Services, National Wild animals Research Center, Section of Wildland Resource, Utah Land University, Logan, Utah,

Todd C. Atwood

^three Alaska Science Eye, U.S. Geological Survey, Anchorage, Alaska,

Sarah A. Sonsthagen

³ Alaska Science Centre, U.S. Geological Survey, Anchorage, Alaska,

Received 2018 Feb xx; Revised 2018 Apr 16; Accepted 2018 Apr 20.

Abstract

Polar bears (Ursus maritimus) are experiencing rapid and substantial changes to their environs due to global climate change. Polar bears of the southern Beaufort Sea (SB) have historically spent nigh of the year on the sea ice. However, recent reports from Alaska indicate that the proportion of the SB subpopulation observed on‐shore during belatedly summer and early fall has increased. Our objective was to investigate whether this on‐shore behavior has adult through genetic inheritance, asocial learning, or through social learning. From 2010 to 2013, genetic data were nerveless from SB polar bears in the fall via hair snags and remote biopsy darting on‐shore and in the spring from captures and remote biopsy darting on the bounding main ice. Bears were categorized as either on‐shore or off‐shore individuals based on their presence on‐shore during the fall. Levels of genetic relatedness, first‐gild relatives, mother–offspring pairs, and father–offspring pairs were determined and compared inside and betwixt the two categories: on‐shore versus off‐shore. Results suggested transmission of on‐shore behavior through either genetic inheritance or social learning equally there was a higher than expected number of offset‐gild relatives exhibiting on‐shore behavior. Genetic relatedness and parentage data analyses were in concurrence with this finding, but further revealed mother–offspring social learning as the main mechanism responsible for the development of on‐shore behavior. Recognizing that on‐shore behavior amongst polar bears was predominantly transmitted via social learning from mothers to their offspring has implications for future direction and conservation equally sea ice continues to refuse.

Keywords: climate change, on‐shore behavior, polar deport, social learning, southern Beaufort Sea, Ursus maritimus

i. INTRODUCTION

The ability of a species to adapt is fundamental to existence resilient to ecology change. A species tin can biologically reply to change by extinction, shifting its distribution, or adapting to new environmental conditions (Raia, Passaro Fulgione, & Carotenuto, 2012; Teplitsky & Millien, 2014). Alterations in species distribution and abundance that follow shifting of climatic weather have been documented in several plant and animal species (Parmesan & Yohe, 2003; Root et al., 2003). Similarly, changes in species phenology in response to climate change have been reported (Boutin & Lane, 2014; Charmantier & Gienapp, 2014; Inouye, Barr, Armitage, & Inouye, 2000). Polar bears (Ursus maritimus) are experiencing disquisitional and rapid changes to their surroundings due to climatic warming (Stirling & Derocher, 2012). This ice‐dependent Chill marine mammal (Amstrup, 2003) was listed as "threatened" under the U.S. Endangered Species Act in 2008 (U.Due south. Fish and Wildlife Service 2008). The listing was primarily due to the observed and projected loss of ocean ice habitat, which puts polar bears at hazard of becoming endangered in the foreseeable future (i.e., by mid‐century). During 1979–2014, the spatial extent of Arctic body of water ice in September (when sea ice reaches its annual minima) has declined by 13.3% per decade due to warming temperatures (Serreze & Stroeve, 2015). Sea ice extent (and book) is expected to proceed to turn down and the southern Beaufort Ocean is predicted to become essentially seasonally ice‐free (i.e., <1.0 × 10^half-dozen kmⁱⁱ) during the summertime earlier the end of the 21st century (Stroeve et al., 2012). Hence, agreement the ecology and behavior of species dependent on ocean water ice is necessary for conservation and management deportment to ensure their population persistence.

Polar bears depend on sea ice for long‐distance movements, mating, access to their primary prey of ringed seal (Phoca hispida) and bearded seal (Erignathus barbatus), and some maternal denning (Amstrup, 2003). Numerous studies indicate that survival (Bromaghin et al., 2015; Regehr, Hunter, Caswell, Amstrup, & Stirling, 2010), reproduction, and body status (Rode, Amstrup, & Regehr, 2010) of the southern Beaufort Sea (SB) subpopulation are negatively afflicted past irresolute sea ice conditions. In addition, polar bears accept been observed swimming increasingly longer distances as bounding main ice has, on boilerplate, retracted farther from shore during summer (Pilfold, McCall, Derocher, Lunn, & Richardson, 2017), resulting in potentially higher energetic costs (Pagano, Durner, Amstrup, Simac, & York, 2012). Furthermore, the distribution of denning has shifted to include fewer denning sites on the pack ice and more sites on land in correspondence with a reduction in the availability and quality of pack ice serving as denning habitat (Fischbach, Amstrup, & Douglas, 2007).

Polar bears of the SB accept historically spent most of the twelvemonth on the sea ice with the exception of denning (Amstrup, Durner, Stirling, Lunn, & Messier, 2000). Yet, recent research in Alaska indicates that polar bears of the SB subpopulation are becoming increasingly reliant on land during tardily summertime and autumn, when body of water ice is no longer present over the biologically productive, shallow h2o of the continental shelf (Atwood et al., 2016; Gleason & Rode, 2009; Schliebe et al., 2008). The estimated proportion of radio‐collared bears from the SB subpopulation observed on‐shore increased from 5.8% during 1986–1999 to 20.0% during 2000–2014, reaching a elevation of 37.0% in 2013 (Atwood et al., 2016).

The number of bears observed on‐shore has been shown to increase when sea ice retracts further from the shore post-obit the summer melt season (Schliebe et al., 2008). In addition, the spatial distribution of on‐shore bears appears to be linked to the accessibility of ringed seals in off‐shore waters and the availability of subsistence‐harvested bowhead whale (Balaena mysticetus) carcasses (Atwood et al., 2016; Schliebe et al., 2008). Coastal Iñupiat communities of Alaska annually hunt bowhead whales and eolith the unused remains at localized "bone piles" on‐shore that consist of trimmed blab, meat, and bones (Ashjian et al., 2010), thereby attracting polar bears and other wildlife. On‐shore bears could be at a higher risk of human–bear conflicts with local residents, tourists, and industrial activities (Laforge et al., 2017; Wilder et al., 2017), besides as increased exposure to certain pathogens (Atwood et al., 2017) and pollutants (Amstrup, Gardner, Myers, & Oehme, 1989). Despite this marked increase of bears exhibiting on‐shore behavior, there remains a lack of inquiry on how this behavior developed.

Recognizing how animals learn different behavioral strategies is necessary for both basic and applied scientific disciplines such as wild animals management and conservation biology. Animal behavioral traits can be obtained through genetic inheritance (Arnold, 1981), but often the conquering of a behavior occurs via learning (Heyes, 1994; Heyes & Galef, 1996). Learning incorporates circuitous ontogenetic processes allowing animals to learn, store, and use information about the environment (Galef & Laland, 2005). Learning can occur socially or asocially, whereby social learning refers to knowledge acquired from the observation of others, typically a conspecific or the products of their activities, and asocial learning refers to learning where no social interaction is required (Heyes, 1994).

Recent studies have investigated the transmission of foraging behavior from mother to offspring in complimentary‐ranging black bears (U. americanus) using observational and genetic techniques (Breck et al., 2008; Hopkins, 2013; Mazur & Seher, 2008). Similarly, studies on grizzly bears (U. arctos) examined the manual of habitat selection and conflict behavior from female parent to offspring (Morehouse, Graves, Mikle, & Boyce, 2016; Nielsen, Shafer, Boyce, & Stenhouse, 2013). Bears are proficient candidates for studying whether particular behaviors are transmitted from mother to offspring considering bears are highly intelligent and lone with the exception of a prolonged mother–offspring association (Gilbert, 1999). Polar acquit offspring typically remain with their mother upwards until 2.3 years of age (Ramsay & Stirling, 1988). Therefore, it is feasible to determine that a deport is learning socially from its mother if bears brandish the aforementioned behavioral patterns as adults.

In calorie-free of the pronounced increase in the number of polar bears coming on‐shore and its potential to accept both ecological and management implications, our objective was to elucidate how this behavior adult. We collected genetic and behavioral data from bears that come on‐shore (future "on‐shore") and those that remain on the pack water ice (futurity "off‐shore") during the fall flavor. Specifically, we addressed the following question: Was on‐shore behavior for polar bears in the SB subpopulation acquired via asocial learning, social learning, or genetic inheritance?

To answer this question, we tested hypotheses to determine how on‐shore beliefs developed via three analyses: (a) genetic relatedness (i.east., quantitative estimate of the proportion of genes shared betwixt the genomes of any two individuals); (b) get-go‐order relatives (i.east., parent–offspring or sibling pairs); (c) and parentage (i.e., mother–offspring and begetter–offspring pairs) within and betwixt polar bears categorized as on‐shore and off‐shore bears. We included transmission (i.due east., the behavior was transmitted via social learning or genetic inheritance) as an additional hypothesis because not all analyses that we conducted could differentiate betwixt social learning and genetic inheritance. It is important to annotation that these hypotheses are not mutually sectional, thus evidence for ane hypothesis does not bespeak other mechanisms are not occurring simply that the most supported hypothesis is more predominant.

one.i. Hypothesis i: On‐shore behavior for polar bears adult via asocial learning

The asocial learning hypothesis from the genetic relatedness analyses predicts that female bears that exhibit on‐shore behavior do not accept college levels of genetic relatedness relative to the entire sampled population. Asocial learning of on‐shore and off‐shore behavior from the parentage analysis would be axiomatic if there was no association between the parent's beliefs and the offspring'southward behavior.

1.ii. Hypothesis ii: On‐shore behavior for polar bears developed via social learning

The transmission via social learning hypothesis from the genetic relatedness analyses predicts that female bears but not male person bears that exhibit on‐shore behavior have college levels of genetic relatedness relative to the sampled population. Furthermore, an association between the mother'south behavior and her offspring'southward behavior, but no association between the father's beliefs and his offspring's behavior (as male bears do not rear cubs), from the parentage analyses would be indicative of social learning for on‐shore and off‐shore behavior.

1.three. Hypothesis 3: On‐shore behavior for polar bears developed via genetic inheritance

The transmission via genetic inheritance hypothesis from the genetic relatedness analyses predicts that both female person and male bears that brandish on‐shore behavior accept higher levels of genetic relatedness than the sampled population. In improver, a scenario of genetic inheritance of on‐shore and off‐shore beliefs from the parentage analyses would be if at that place was an association between both the mother'due south behavior and her offspring's behavior and the father'southward beliefs and his offspring's behavior.

i.iv. Hypothesis 4: On‐shore beliefs for polar bears developed via transmission (i.e., social learning or genetic inheritance)

The transmission hypothesis from the genetic relatedness analyses predicts that female person bears that exhibit on‐shore beliefs accept a higher genetic relatedness than the sampled population. Secondly, a higher than expected number of first‐order relatives that display on‐shore beliefs would provide show of manual for this behavior.

two. MATERIAL AND METHODS

two.1. Study area

The SB polar deport subpopulation inhabits a region encompassing areas along the north coast of Alaska and Canada from Icy Cape, USA, (lxx.three°N, 161.9°W) in the west, to Tuktoyaktuk, Canada (69.four°N, 133.0°W), in the east; following IUCN (Polar Bear Specialist Grouping; http://pbsg.npolar.no/en/). The southern Beaufort Sea has a narrow continental shelf with a steep shelf‐break that plunges to some of the deepest waters of the Arctic Ocean (Jakobsson et al., 2008). The SB is typically ice covered from October to June, and sea water ice retreats to its minimum in the summertime and fall seasons from July to September. In recent years in that location has been a trend in the SB of earlier melt onset, reduced summer body of water ice extent, a lengthening of the open up‐water flavor (i.due east., ocean ice retreats toward the pole during the annual sea ice minimum), and subsequently freeze‐up (Stroeve, Markus, Boisvert, Miller, & Barrett, 2014).

2.2. Collection of genetic material

We collected genetic material from SB polar bears from 2010 to 2013 (Effigy1) via direct polar bear captures, remote biopsy darting, and hair snags. We used the gimmicky genetic data in conjunction with a long‐term information ready of SB polar bears captured virtually every spring since the mid‐1980s. We captured polar bears in coastal areas (e.grand., within 150 km of the declension) of the SB from Utqiagvik, Alaska (~157°W) to the U.Due south.–Canada border (~141°West). Nosotros conducted captures over the body of water ice during the leap season from March to early May over the written report. We encountered adults and subadults opportunistically while flying in a helicopter and immobilized them with tiletamine hydrochloride plus zolazepam hydrochloride (Telazol^®, Fort Contrivance and Warner‐Lambert Co.) using a projectile syringe fired from a dart gun. We collected blood and tissue samples for genetic identification. In addition, we fitted an Argos or global positioning organisation (GPS) platform transmitter terminal (PTT) satellite radio‐collars to a subset of adult female polar bears to collect motility and spatial information (Durner et al., 2009).

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Written report area forth the Beaufort Sea declension from Utqiagvik, Alaska to the Canadian edge

During the spring, we conducted remote biopsy darting from a helicopter to collect tissue samples from developed and subadult bears within approximately 150 km of the coast between Utqiagvik, Alaska, and the U.S.–Canada border. In improver, we conducted remote biopsy darting in the autumn forth the coastline, barrier islands, and inland areas within approximately thirty km of the coast (Pagano, Peacock, & McKinney, 2014). The remote biopsies nerveless skin tissue samples for genetic identification. We implemented hair snags in Utqiagvik, Alaska in the fall season of 2011 and Kaktovik, Alaska (~143°Westward), in the fall seasons of 2012 and 2013 to collect hair samples for genetic identification (encounter [Herreman & Peacock, 2013] for details).

2.three. Genetic identification

We genotyped claret, tissue, and hair samples at 20 microsatellite loci and a ZFX/ZFY sexual practice identification marker past Wildlife Genetics International (Nelson, British Columbia, Canada). The Deoxyribonucleic acid was extracted using a Qiagen DNeasy kit (QIAGEN Inc., Valencia, CA, USA). The DNA was extracted from hair samples using a minimum of 10 guard pilus roots, if available, or up to xxx whole underfur hairs if needed to supplement guard hairs. The Deoxyribonucleic acid was extracted from the dry claret and tissue samples using a clipped piece ~3 mm² from the end of a Q‐tip or ear punch. The DNA extracts were initially amplified at 11 hypervariable microsatellite markers to identify individuals: G1A, G10B, G10C, CX110, G1D, G10L, G10M, MU59, G10P (Paetkau & Strobeck, 1994; Proctor, McLellan, & Strobeck, 2002; Taberlet et al., 1997); and G10H and G10J (GenBank accretion numbers {"type":"entrez-nucleotide","attrs":{"text":"U22086.1","term_id":"775113","term_text":"U22086.1"}}U22086.one and {"type":"entrez-nucleotide","attrs":{"text":"U22087.ane","term_id":"775114","term_text":"U22087.ane"}}U22087.1, respectively). Whatever DNA extracts that were amplified at <11 loci were considered unsuccessful and excluded from further analyses. Later individuals were identified, each individual was amplified at nine additional markers including a sex‐linked locus: MSUT‐two, CPH9, CXX20, MU50, MU51, G10X, CXX173 (Kitahara, Isagi, Ishibashi, & Saitoh, 2000; Molecular Ecology Resources Primer Development Consortium, 2010; Ostrander, Sprague, & Rine, 1993; Paetkau, Calvert, Stirling, & Strobeck, 1995; Proctor et al., 2002; Taberlet et al., 1997); and 14RENP07 and G10U (GenBank accession numbers {"type":"entrez-nucleotide","attrs":{"text":"AJ411284","term_id":"15912914","term_text":"AJ411284"}}AJ411284, and {"type":"entrez-nucleotide","attrs":{"text":"U22092.1","term_id":"775119","term_text":"U22092.one"}}U22092.1, respectively).

two.iv. On‐shore and off‐shore bears

We categorized polar bears based on their behavior equally on‐shore or off‐shore individuals both pooled over the duration of the study and on an annual footing. For the pooled information set, nosotros considered bears as on‐shore individuals if they were identified on‐shore during the study. Nosotros identified bears on‐shore during the fall season using information from the remote biopsy, pilus snag, or GPS locations (run into [Atwood et al., 2016] for details). We restricted the fall season to July i to October 31 as this was when the sea ice was not contiguous to the coast. We categorized bears as off‐shore individuals if they were identified on the bounding main ice during the spring remote biopsy or direct capture and were not observed on‐shore at any time during the study. For the annual information prepare, we considered bears as on‐shore individuals if they were identified on‐shore for a given twelvemonth from the fall season remote biopsy, pilus snag, or GPS locations. We categorized bears as off‐shore individuals if they were not identified on‐shore for that corresponding year. We conducted the annual categorization because some bears switched behavioral strategies during the 4 years of sampling. Nosotros conducted identical analyses on the pooled and the annual data sets to ascertain if comparable results would exist obtained.

We estimated the age of individual bears from analysis of cementum annuli (Calvert & Ramsay, 1998), or they were classed as a known historic period bear if they were originally captured every bit dependent young with their mother (Ramsay & Stirling, 1988). We conducted 3 separate analyses to determine how on‐shore beliefs was caused: genetic relatedness, start‐society relatives, and parentage (Breck et al., 2008; Hopkins, 2013). We conducted all statistical tests using α = 0.05 in R (R Core Team 2016). We included an individual bear just once in all analyses after it was categorized as an on‐shore or off‐shore conduct. In add-on, we included just bears considered contained in all analyses considering dependent young had no choice but to remain with their mother. We considered bears equally independent if they were ≥2 years old or if they were observed without their mother when captured.

2.5. Genetic relatedness

We calculated pairwise relatedness (Queller & Goodnight, 1989) betwixt all possible pairings of individuals using Genalex (Peakall & Smouse, 2006, 2012). Theoretical values of relatedness range from −1 to ane, with negative values indicating the gene frequencies of the two compared individuals differ from the population mean in opposite directions, aught representing random associations betwixt individuals, and increasing values corresponding to increased relatedness. Relatedness values are afflicted past genetic structure, as these values measure genetic differences in overall allelic frequencies (Queller & Goodnight, 1989). Polar bears are weakly structured throughout their circumpolar distribution (Peacock et al., 2015). No differentiation observed at microsatellite loci amid southern Beaufort and next (northern Beaufort and Chukchi Bounding main) subpopulations was observed; therefore, nosotros conducted analyses among bears across all sampled sites.

We used bootstrap resampling for the genetic relatedness analysis because the relatedness distributions were non‐normal and each behavioral grouping was a subset of the entire sampled population (Hopkins, 2013). The behavioral groups tested were on‐shore/on‐shore, on‐shore/off‐shore, and off‐shore/off‐shore with mean relatedness determined for the unabridged sampled population, and females and males, separately. We randomly selected a subset of bears for each behavioral group from the sampled population matrix x,000 times and calculated relatedness. Nosotros then used every relatedness value to generate the bootstrap distribution of the sample hateful. We calculated the p‐value past the number of times the bootstrap relatedness estimate was greater than or equal to the mean relatedness for the entire sampled population.

2.half dozen. Parentage

Nosotros identified mother–offspring and father–offspring pairs (Breck et al., 2008) using Cervus 3.0 (Marshall, Slate, Kruuk, & Pemberton, 1998). We considered bears equally mothers or fathers if they were estimated to be ≥3 years older than the bear presumed to be the offspring, there were no genotype inconsistencies between parent–offspring pairs, and if parentage assignments were made with ≥80% confidence. We used either a chi‐square goodness‐of‐fit test or a Fisher's verbal examination (when sample size in at least 1 category was ≤v) to test the nix hypothesis that there was no association between the parent'south behavior and the offspring's behavior.

two.seven. Beginning‐order relatives

We used the pairwise relatedness values to identify individual pairs that were first‐lodge relatives (Breck et al., 2008). Based on relatedness values from known female parent–offspring (northward=27) and sibling (n=6) pairs, we used a value of relatedness ≥0.42 to betoken pairs related at the level of commencement‐social club relatives. We categorized first‐order relatives into the aforementioned on‐shore/on‐shore, on‐shore/off‐shore, and off‐shore/off‐shore behavioral groups examined previously. Nosotros used either a chi‐square goodness‐of‐fit test or an exact test for multinomial (when sample size in at least ane category was ≤5) to determine if the number of observed related pairs differed from the number of expected for each behavioral group. We calculated the expected numbers by multiplying the observed number of bears for each behavioral group past the proportion of all possible pairings within a behavioral group.

3. RESULTS

A total of 231 independent (i.east., ≥2 years old or if they were observed without their mother when captured) polar bears for the pooled data ready were successfully genotyped at a number of loci sufficient to provide private identity (11) and could exist categorized as on‐shore or off‐shore individuals from the behavioral data; of these 123 bears were categorized as off‐shore (59 females and 64 males) and 108 bears were categorized equally on‐shore (58 females and fifty males). Over the elapsing of the study, 12.6% (n=29/231) of the identified bears switched behaviors among the years. Nosotros conducted an annual analysis solely for 2011, because sample size for independent bears was the highest (2010: n=81, 2011: northward=103, 2012: north=97, 2013: due north=57) and we had sufficient data for mother–offspring and father–offspring pairs to acquit the Fisher's verbal test. In 2011, there were 103 identified independent bears with behavioral data; we categorized 47 bears as off‐shore (24 females and 23 males) and 56 bears equally on‐shore (28 females and 28 males).

Female person on‐shore/on‐shore pairs had the highest hateful relatedness of all behavioral groups (Tablei), which was significantly higher than the mean relatedness of the unabridged sampled population. Male person on‐shore/on‐shore pairs did not have a significantly higher mean relatedness than the hateful relatedness of the entire sampled population, which provided evidence of social learning of on‐shore behavior given that the female on‐shore/on‐shore pairs had significantly college relatedness than the sampled population. A similar blueprint was observed for the 2011 almanac analysis. Among the 2011 analyses, only female on‐shore/on‐shore pairs had significantly higher mean relatedness than the hateful relatedness for the entire sampled population (and the highest mean relatedness of all behavioral groups). In contrast, male on‐shore/on‐shore pairs did not have a significantly higher mean relatedness than the mean relatedness of the entire sampled population.

Table one

Mean relatedness and corresponding p‐values of behavioral groups past category for polar bears of the southern Beaufort Sea, pooled for 2010–2013 and annually for 2011. The p‐value was calculated by the number of times the bootstrap relatedness guess for each behavioral category was greater than or equal to the mean relatedness for the entire sampled population

Behavioral groups	n	Hateful relatedness	p‐value
Pooled
Sampled population	231	−0.0043
On‐shore/on‐shore		0.0066	0.082
On‐shore/off‐shore		−0.0075	0.726
Off‐shore/off‐shore		−0.0072	0.648
Female person bears	117
On‐shore/on‐shore		0.0151	0.039
On‐shore/off‐shore		−0.0005	0.298
Off‐shore/off‐shore		−0.0020	0.406
Male bears	114
On‐shore/on‐shore		−0.0018	0.406
On‐shore/off‐shore		−0.0141	0.904
Off‐shore/off‐shore		−0.0147	0.849
2011
Sampled population	103	−0.0098
On‐shore/on‐shore		−0.0007	0.192
On‐shore/off‐shore		−0.0129	0.657
Off‐shore/off‐shore		−0.0151	0.678
Female bears	52
On‐shore/on‐shore		0.0110	0.089
On‐shore/off‐shore		−0.0196	0.810
Off‐shore/off‐shore		−0.0109	0.524
Male bears	51
On‐shore/on‐shore		−0.0083	0.459
On‐shore/off‐shore		−0.0241	0.894
Off‐shore/off‐shore		−0.0079	0.458

There was prove of an association between a mother's beliefs and her offspring'south behavior (Table2). The numbers of on‐shore/on‐shore and off‐shore/off‐shore mother–offspring pairs were college than expected. The number of on‐shore/off‐shore mother–offspring pairs was lower than expected consequent with the pattern of offspring retaining the behavioral strategy of their female parent. The same blueprint was observed for the 2011 data set, though the signal was not equally strong. The number of on‐shore/on‐shore and off‐shore/off‐shore mother–offspring pairs was college than expected, while the number of on‐shore/off‐shore female parent–offspring pairs was lower than expected. In that location was no significant association between a male parent's beliefs and his offspring's beliefs (Table3) for the pooled data prepare or for the 2011 information set; though the sample size was low for 2011 and may limit the power of the test. Collectively, the parentage findings provide evidence for female parent–offspring social learning of on‐shore behavior.

Table 2

Observed and expected mother–offspring pairs by behavioral group for polar bears of the southern Beaufort Ocean, pooled for 2010–2013 and annually for 2011. A chi‐square goodness‐of‐fit test or a Fisher's exact test (when sample size in at least one category was ≤5) was used to test the zippo hypothesis that at that place is no association between the parent'southward behavior and the offspring's behavior

Human relationship	Observed	Expected	p‐value
Pooled
Mother–offspring
On‐shore/on‐shore	32	28	0.004
Off‐shore/on‐shore	4	8
On‐shore/off‐shore	half dozen	x
Off‐shore/off‐shore	7	3
2011
Mother–offspring
On‐shore/on‐shore	fourteen	13	0.056
Off‐shore/on‐shore	one	iii
On‐shore/off‐shore	1	3
Off‐shore/off‐shore	2	1

Tabular array iii

Observed and expected begetter–offspring pairs by behavioral group for polar bears of the southern Beaufort Body of water, pooled for 2010–2013 and annually for 2011. A chi‐square goodness‐of‐fit examination or a Fisher's verbal test (when sample size in at least 1 category was ≤v) was used to exam the zip hypothesis that there is no association betwixt the parent's beliefs and the offspring'due south behavior

Relationship	Observed	Expected	χ²	p‐value
Pooled
Father–offspring
On‐shore/on‐shore	17	15	0.8755	0.349
Off‐shore/on‐shore	seven	9
On‐shore/off‐shore	7	9
Off‐shore/off‐shore	7	5
2011
Begetter–offspring
On‐shore/on‐shore	3	2	0.0521	0.400
Off‐shore/on‐shore	0	1
On‐shore/off‐shore	1	two
Off‐shore/off‐shore	1	0

The observed number of first‐society relatives deviated from the expectation for both the pooled and 2011 information sets (Tablefour). The number of on‐shore/on‐shore first‐club relatives was higher than expected, which provided evidence for manual via genetic inheritance or social learning of on‐shore behavior. Conversely, the number of on‐shore/off‐shore and off‐shore/off‐shore first‐order relatives was lower than expected.

Table 4

Observed and expected first‐social club relatives by behavioral group for polar bears of the southern Beaufort Sea, pooled for 2010–2013 and annually for 2011. A chi‐square goodness‐of‐fit test or an exact test for multinomial (when sample size in at least 1 category was ≤5) was used to determine whether the number of observed related pairs differed from the number of expected for each behavioral group

Behavioral groups	Observed	Expected	χ²	p‐value
Pooled
On‐shore/on‐shore	64	25	80.8917	<0.001
On‐shore/off‐shore	30	57
Off‐shore/off‐shore	19	32
2011
On‐shore/on‐shore	21	eight	33.2949	<0.001
On‐shore/off‐shore	three	13
Off‐shore/off‐shore	two	five

4. DISCUSSION

Analyses testing relationships based on genetic relatedness and parentage estimates revealed that social learning was the primary mechanism responsible for on‐shore behavior. This was revealed by the finding that the female on‐shore/on‐shore behavioral category had a significantly higher hateful relatedness than the entire sampled population, while the male on‐shore/on‐shore behavioral category did non (Table1). Thus, female person polar bears exhibiting on‐shore beliefs had higher relatedness; while on‐shore males were non more related than the full general population. Furthermore, a pregnant association between a mother's behavior and her offspring's beliefs was observed (Tableii), while no association between a begetter's behavior and his offspring'southward behavior was found (Table3). In combination, the parentage results indicated that the manual of on‐shore and off‐shore beliefs was through female parent–offspring social learning because contained offspring generally continued to follow the aforementioned behavioral strategy of their female parent.

All three analyses from both the pooled and almanac data sets suggested manual, via social learning or genetic inheritance, of on‐shore behavior for the SB polar behave subpopulation. The pooled and annual information sets had concordant results indicating that bears switching behavior amongst the years did not modify the overall conclusions. Assay based on get-go‐club relatives revealed higher than expected on‐shore/on‐shore first‐guild relatives and lower than expected on‐shore/off‐shore and off‐shore/off‐shore first‐club relatives (Table4). Close relatives exhibiting the same behavior indicated transmission of on‐shore beliefs because closely related individuals were likely socially learning from each other or there was a genetic basis for on‐shore behavior.

A loftier proportion of male polar bears leaving the study area could have resulted in like patterns in our genetic relatedness analysis; thereby erroneously producing a signature of social learning. For example, male grizzly bears travel widely during breeding season (Ciarniello, Boyce, Seip, & Heard, 2007) and more often than not have longer natal dispersal distances than females (McLellan & Hovey, 2001; Proctor, McLellan, Strobeck, & Barclay, 2004), which would likely result in a higher level of genetic relatedness amongst female bears in a region. By and large, movements of male and female polar bears do not differ profoundly (Amstrup, Durner, McDonald, Mulcahy, & Garner, 2001) simply female polar bears can take larger breeding range sizes than males (Laidre et al., 2013); whereas Zeyl, Aars, Ehrich, and Wiig (2009) found that polar bears of the Barents Sea exhibit male‐biased natal dispersal. Thus, because dispersal distance is sex‐biased in polar bears, the scenario of higher genetic relatedness amongst female person bears exhibiting on‐shore behavior could exist a effect of greater male dispersal. Notwithstanding, the mother–offspring findings provided show of social learning despite the uncertainty regarding the genetic relatedness results because offspring mostly followed the same behavioral strategy as their mother.

Lower survival of off‐shore polar bears could as well generate equivalent results. That is, if on‐shore bears have college survival, and therefore on‐shore females have a higher recruitment rate of cubs than off‐shore bears, and so college genetic relatedness among on‐shore bears, a higher proportion of on‐shore/on‐shore commencement‐gild relatives, and more on‐shore/on‐shore mother–offspring pairs would be observed. Thus far, no studies accept been conducted on survival and recruitment comparing on‐shore and off‐shore polar bear subpopulations. However, enquiry on SB polar bears constitute similar activity patterns and physiological condition for on‐shore and off‐shore bears, which suggests that neither the on‐shore or off‐shore grouping realizes a greater benefit than the other (Whiteman et al., 2015). While the mother–offspring data propose on‐shore behavior was acquired through social learning, we cannot rule out the possibility that off‐shore mothers experienced a high incidence of reproductive failure, which then contributed to the clustering of relatives on‐shore.

Behavioral or physiological modifications in response to climate‐driven changes in their environment have been observed in other species (Bradshaw & Holzapfel, 2006) with both positive and negative fitness consequences (Both, Bouwhuis, Lessells, & Visser, 2006; Halupka, Dyrcz, & Borowiec, 2008; Réale, McAdam, Boutin, & Berteaux, 2003). The increase in SB polar bears coming on‐shore (Atwood et al., 2016) and the transmission of this behavior via female parent–offspring social learning may be a behavioral modification in response to climatic change and suggests that some SB polar bears are altering their behavior in response to a changing climate. Furthermore, some bears were observed switching behaviors over the duration of the study revealing that these behaviors are dynamic. Bears may alter their behavior for a multitude of reasons, such as annual sea ice conditions, food availability, and reproductive status. Plasticity in on‐shore/off‐shore behavior may provide an avenue for polar bears to respond to changing bounding main ice atmospheric condition on an annual ground.

On‐shore bears may be exposed to additional risks, including a greater potential for human being–comport conflicts and increased exposure to contaminants and diseases (Stirling & Derocher, 2012). At that place are several villages along the north coast of Alaska and an industrial footprint associated with oil exploration and extraction, all of which tin occur in relatively close proximity to on‐shore bears. Likewise in shut proximity to human settlements are the remains of subsistence‐harvested bowhead whale carcasses, which are deposited on country and attract large aggregations of bears (Herreman & Peacock, 2013). Therefore, human–acquit conflicts will probable increase as the sea water ice continues to decline and more than bears come aground. Human being–wildlife conflicts tin have wide effects: negatively impacting wildlife populations, irresolute the structure of ecosystems (Woodroffe, Thirgood, & Rabinowitz, 2005), and endangering public condom (Thirgood, Woodroffe, & Rabinowitz, 2005). Other polar carry populations, such every bit the Western Hudson Bay population, take experienced increases in the number of problem bears correlated with delayed body of water ice formation and changes in polar bear distribution and declining body condition. In addition, polar bears that were highly motivated to obtain food appeared more than willing to risk interacting with humans (Towns, Derocher, Stirling, Lunn, & Hedman, 2009).

The proportion of SB polar bears exhibiting on‐shore behavior during the fall flavour has increased over time (Atwood et al., 2016; Pongracz & Derocher, 2016). Furthermore, trends of earlier arrival on‐shore, increased length of stay, and afterwards divergence back to the sea water ice have been detected, which are all related to declines in the availability of sea ice habitat over the continental shelf and changes to ocean ice phenology. The Arctic is expected to continue to warm given the current trends in global greenhouse emissions (Larsen et al., 2014). Thus, SB polar bears will probable proceed to experience changes to their environment resulting in more bears coming on‐shore. Therefore, it will be important to monitor the population‐level consequences of extended country utilise. Properly managing polar bear mother–offspring pairs, when viable, will exist of import to ensure their continued persistence in a rapidly changing environment and mitigate human–deport conflicts for this apex predator in the irresolute Chill.

Conflict OF Involvement

None declared.

AUTHORS' CONTRIBUTIONS

All authors conceived and designed the report. T.A. carried out field studies. K.L. then analyzed the data and drafted the manuscript, with all authors contributing to revisions.

ACKNOWLEDGMENTS

Nosotros thank E. Peacock, J. Herreman, and the Northward Slope Borough Department of Wild animals Management for establishing the sampling try at Utqiagvik. We give thanks C. Simms, A. Smith III, and J. Smith for maintaining the sampling effort at Kaktovik. We appreciate the logistical support provided by the Chill National Wild animals Refuge and U.South. Air Force. We wish to express our gratitude to the residents of Kaktovik for allowing us to work in their community. This paper was reviewed and approved past USGS nether their Cardinal Science Practices policy (http://www.usgs.gov/fsp). Whatsoever employ of trade, production, or firm names is for descriptive purposes but and does not imply endorsement past the US Government. This research was canonical under the Marine Mammal Protection Act and Endangered Species Act with U.S. Fish and Wildlife Service (USFWS) let number MA690038. Capture protocols were canonical past the U.Southward. Geological Survey (USGS) Institutional Animal Care and Use Committee. Special cheers to J. Stevens, L. Aubry, and S. Watson for reviews of the manuscript.

Notes

Lillie KM, Gese EM, Atwood TC, Sonsthagen SA. Development of on‐shore beliefs among polar bears (Ursus maritimus) in the southern Beaufort Sea: inherited or learned? Ecol Evol. 2018;viii:7790–7799. 10.1002/ece3.4233 [CrossRef] [Google Scholar]

Funding information

This work was supported past the Graduate Enquiry Fellowship Programme from the National Science Foundation (Grant No. 1147384 to Thou.K.L.), U.Due south. Geological Survey‐Alaska Science Center, Utah State Academy, and USDA‐Wildlife Services‐National Wild fauna Research Center. Any stance, findings, and conclusions or recommendations expressed in this cloth are those of the author(south) and do non necessarily reflect the views of the National Science Foundation. Funding to the U.S. Geological Survey‐Alaska Science Center was provided through the Irresolute Arctic Ecosystems Initiative and the Wildlife Program of the Ecosystems Mission Area and the Bureau of Land Direction.

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