Biology of the Ringed Seal (Phoca hispida) in Alaska, 1960–2010

Final Report to: 

National Marine Fisheries Service 

Lori Quakenbush 

 John Citta 

and 

Justin Crawford

Arctic Marine Mammal Program

Alaska Department of Fish and Game

1300 College Road, Fairbanks, AK 99701 

March 2011 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

2 

EXECUTIVE SUMMARY

The Alaska Department of Fish and Game (ADF&G) has been monitoring the health and 

status of ringed seals (Phoca hispida) in Alaska since 1960 by collecting information and 

samples from the Alaska Native subsistence harvest. This monitoring program is especially 

important because agencies are unable to overcome the logistical and sampling constraints 

necessary to estimate seal abundance in remote, ice covered waters. As such, reliable estimates 

of ringed seal abundance or population trend are lacking. Retrospective data analyses from this 

monitoring program allow us to examine how parameters that affect population size and status 

may vary in time and how current conditions compare with past conditions. Parameters we 

monitor that are indicative of population health or status include growth rate, body condition, 

diet, age distribution, sex ratio, age of maturation, and pregnancy rate. Since 2000, ADF&G has 

also conducted surveys for local knowledge and hunter preferences and analyzed tissue samples 

for contaminants and disease. All of these collections rely on the cooperation of coastal 

subsistence communities. Villages that have participated in the sampling program span the 

region from Hooper Bay in the Bering Sea to Kaktovik in the Beaufort Sea, including islands in 

the Bering Sea; an area that encompasses most of the range of ringed seals in Alaska. 

Local knowledge—Hunter questionnaires are used to evaluate seal availability for harvest 

and hunter bias in the samples so that we can determine whether changes are due to hunter 

behavior or related to the seal population itself. Responses to hunter questionnaires from five 

participating villages did not indicate decreases in ringed seal numbers (availability) at any 

location. The majority of respondents from all villages reported that ringed seals were found in 

the same areas as in the past and hunting occurred at the same time as in the past.

Diet—Using stomach contents from 1,555 ringed seals collected between 1960 and 2009, 

we identified 155 different fish and invertebrate prey of which 99 were common. Using percent 

frequency of occurrence, fish were consumed significantly more frequently (4.1 times) during 

the 2000s than during the 1960s and 1970s. Too few data were available for analysis in the 

1980s and 1990s. The increase in general fish consumption over time was strongly correlated 

(Pearson correlation) with changes in the consumption of cod from the Family Gadidae (r = 

0.67), suggesting changes in the consumption of Arctic cod (Boreogadus saida), saffron cod 

(Eleginus gracilis), and to a lesser extent walleye Pollock (Theragra chalcogramma) were likely 

responsible for variations we observed among all fish. Ringed seals have also consumed 

significantly more Pacific herring (Clupea harangus), capelin (Mallotus villosus), Pacific sand 

lance (Ammodytes hexapterus), and prickleback (Stichaeidae), including eelblenny (Lumpenus

spp.) in the 2000s than in the 1960s and 1970s (P < 0.01). 

In general, invertebrates were consumed less frequently in the 2000s (66%) than during 

the 1960s and 1970s (89%; P < 0.01). Too few data were available for analysis in the 1980s and 

1990s. Although invertebrates were consumed less frequently in the 2000s, the diversity (D) of 

invertebrate species consumed recently was somewhat greater (D = 0.26) than during the 1960s 

and 1970s (D = 0.29), based on Simpson’s Diversity Index. The decrease in general invertebrate 

consumption over time was strongly correlated with crustacean (r = 0.96) and shrimp 

consumption (r = 0.58), suggesting decreases in their consumption were likely responsible for 

the decrease observed among all invertebrates. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

3 

Contaminants—Liver (n = 35) and kidney (n = 12) tissues from ringed seals collected 

during 2003 and 2007 were analyzed for concentrations of potentially toxic elements such as 

arsenic, cadmium, mercury, and lead. Concentrations of these elements in ringed seals in Alaska 

were lower than for ringed seals in Canada, Greenland, and Russia. Within Alaska, ringed seals 

had the second lowest concentrations of cadmium and mercury of the four species of ice seals in 

our studies (only spotted seals were lower) and lead levels were very low in all ringed seals 

analyzed. Blubber (n = 35) and liver (n = 26) tissues were analyzed for persistent organochlorine 

compounds and compared to bearded, spotted, and ribbon seals in Alaska, ringed seals had the 

lowest levels of total CHL (chlordanes), and the second lowest of HCH 

(hexachlorocyclohexane), DDT (dichlorodiphenyltrichloroethane), and PCB (polychlorinated 

biphenyls) in our studies. Ringed seals in our study also had lower levels of these compounds 

than ringed seals in Canada, Norway, and Russia. 

Disease—Antibodies for Brucella, phocine herpesvirus, phocine and canine distemper, 

Leptospira, and Toxoplasma, were detected in ringed seals at levels below or similar to the past. 

Screening for toxic algae detected domoic and saxitoxin at very low levels in four and six of 34 

individual ringed seals, respectively. 

Growth rates—We analyzed growth rate using length at age data for 1,610 seals ≥1 years 

old and 543 pups. Seals were identified as being longer or shorter than expected, given their age, 

and were then classified by birth year. For seals >1 year of age, individuals born after 1976 were 

larger than expected in 20 of 23 sample years. We fit von Bertalanffy growth curves to age-atlength data. Seals harvested before and after 1976 reached similar asymptotic (maximum) 

lengths; however, seals harvested after 1976 grew at a faster rate. For example, at age 1, seals 

born after 1976 were an average of 1.7 cm longer than seals born in 1976 or earlier. This affect 

was greatest at 6 years of age, when seals born after 1976 were an average of 6.2 cm longer. By 

age 25, the affect had diminished to an average of only 2.8 cm. Growth rates for pups were 

lowest in 1961 and 2005. Pups were shorter than expected, given their date of harvest, in six of 

ten (60%) sample years between 1960 and 1979. In contrast, pups were shorter than expected in 

only three of nine (33%) sample years between 2000 and 2009. Too few data were available for 

analysis in the 1980s and 1990s. 

Body condition—We examined patterns in sternal blubber thickness using linear models 

to control for covariates, such as time of year, for 147 pups, 215 subadults, and 189 adults 

collected between 1971 and 2010. Pups had less blubber than expected in 1971 and 1976; since 

2002, blubber thickness of pups has been average. Adults and subadults also had less blubber 

than expected in 1971, but more than expected in 1978. Since 2002, blubber thickness of adults 

and subadults has been average. 

Age distributions—We analyzed age at harvest for 528 ringed seals harvested in the 

1960s, 4,694 in the 1970s, and 727 in the 2000s. Too few data were available for analysis in the 

1980s and 1990s. A much greater proportion of pups were identified in the 2000s (56%) than in 

the 1960s (14%; P <0.01) and 1970s (23%; P <0.01). On average, ringed seals harvested in the 

1960s were older than those harvested in the 1970s, and seals harvested in the 1970s were older 

than those harvested in the 2000s. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

4 

Sex ratios—Sex ratios were generally male biased. However, the patterns were not 

consistent through time or by age class. The shifts in the sex ratios were driven by an increase in 

the proportion of adult males (ages 5 and older; P <0.01) harvested in the 1960s and 2000s. Too 

few data were available for analysis in the 1980s and 1990s. 

 Age at maturity and pregnancy rate—Sexual maturity was determined by examining 

reproductive tracts of 690 female ringed seals; 47 harvested between 1965 and 1975, 84 in 1976, 

196 in 1977, 162 in 1978, 81 between 1979 and 1984, and 120 between 1999 and 2010. The 

average age of maturity varied significantly in time. Average age of maturity was 5.3 years of 

age between 1965 and 1975 and increased to 6.4 in 1976 and 6.5 in 1977 (P <0.05). In 1978, the 

average age of maturity significantly decreased to 5.0 years of age (P <0.05). Age at maturity 

rose to 5.9 years from 1979 to 1984. Since 1999, however, the average age of maturity has been

the lowest observed (3.2 yrs), and is significantly lower than all other years (P <0.05). 

 

Female reproductive tracts were analyzed for percent pregnant at harvest. The decades 

with the lowest percentage was the 1960s (76.8%) and the 1980s (76.2%). The 1970s had the 

highest percentage at 89.1% and the 2000s were next highest at 79.5%. Too few data were 

available for analysis in the 1990s. 

Conclusions—These data span five decades and include time periods well before changes 

in sea ice or other factors attributed to global climate change were present. Our analyses show 

that ringed seals have been positively and negatively affected by past and current conditions. 

Currently, however, ringed seals are growing faster, have average blubber thickness, are 

maturing at the youngest age to date (indicating females are in a positive nutritional state 

allowing them to grow faster and become mature at an earlier age), and have the second highest 

pregnancy rate to date. Current environmental conditions have not had a negative effect on any 

of these factors. In addition, there are more pups in the harvest now. Because age ratios are 

proportional, a higher proportion of pups in the sample may indicate that adult survival is 

decreasing or that reproduction is increasing. Based upon other information, however, it is most 

likely that reproduction has increased. For example, growth rate, age of maturation, pregnancy 

rate, and blubber thickness are average or better than expected, and hunter responses to 

questionnaires indicate that ringed seal numbers have not decreased. The high proportion of 

pups in the harvest also indicates that pups are surviving long enough to be harvested (i.e., pups 

survive to weaning). Sex ratios are currently male biased; however, this is probably not a 

concern as it corresponds to a period with high pregnancy rates and increasing numbers of pups. 

Levels of contaminants in ringed seals harvested in Alaska are lower than levels reported in 

Canada, Europe, and Russia, and the prevalence of diseases has remained stable. 

The results from this long-term program demonstrate its ability to monitor and detect 

changes in parameters that are useful for monitoring population status when estimating the 

population size is not possible. Parameters that determine the status of the ringed seal population 

in the Bering, Chukchi, and Beaufort seas have been more favorable throughout the 2000s than 

during the 1960s and 1970s. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

5 

INTRODUCTION

In Alaska, the ringed seal (Phoca hispida or Pusa hispida) is one of four species of seals 

that are associated with sea ice during some portion of the year. The other ice-associated species 

are the bearded seal (Erignathus barbatus), the spotted seal (Phoca largha) and the ribbon seal 

(Histriophoca fasciata). Ringed seals have the widest distribution, which includes the Bering, 

Chukchi, and Beaufort seas near Alaska but they are also found throughout the Arctic, including 

Canada, Greenland, Svalbard, and Russia, and in freshwater lakes in Europe (Frost and Lowry 

1981). Ringed seals feed on a variety of fish and invertebrates in the water column. They are 

the most ice adapted of the arctic phocids and maintain breathing holes and subniviean lairs in 

shorefast ice where the adults breed and pups are born in March and April. Pups are weaned 

after 5–7 weeks (Frost and Lowry 1981). Although ringed seal distribution is strongly correlated 

with the presence of sea ice all year, during the open-water season, ringed seals occur in ice-free 

waters of the Beaufort, Chukchi, and Bering seas (Burns et al. 1981). 

Population estimates for ringed seals are difficult to obtain due to problems related to 

conducting surveys over large areas of ice-covered waters far from shore and the lack of 

correction factors for seals under the ice. Aerial surveys of nearshore areas in the 1980s (Frost et 

al. 1988) and 1990s (Moulton et al. 2002, Bengtson et al. 2005) resulted in several minimum 

estimates that indicated the population of ringed seals in Alaskan waters is more than one million

individuals and the population throughout the Arctic is on the order of several million. There are 

no current estimates of abundance or trend. 

Ringed seals are currently being considered for listing as threatened under the 

Endangered Species Act due to concerns that climate change may alter sea ice habitat (50 CFR 

223 Vol. 75, No. 237:77476–77495). Sea ice is changing in thickness, persistence, and 

distribution (Rigor and Wallace 2004, Comiso 2006, Serreze et al. 2007, Stroeve et al. 2008). 

Evidence also indicates that oceanographic conditions have been changing in the Bering and 

Chukchi seas (Niebauer 1980, 1983, 1988; Trenberth 1990; Ebbesmeyer et al. 1991; Grebmeier 

et al. 2006a; Bluhm and Gradinger 2008), which suggests changes in the ecosystem may be 

occurring as well. 

The Alaska Department of Fish and Game (ADF&G) has collected information and 

samples from the Alaska Native subsistence harvest of all ice seal species, including ringed seals, 

for more than 40 years in order to monitor the health and status of the population in the absence 

of reliable population estimates and trends. Retrospective analyses of these samples and 

measurements provide evidence of current population status by evaluating changes in population 

parameters, such as body condition, the growth rate of individuals, diet, age distribution and sex 

ratio of the harvest, age of maturation, and pregnancy rate. Since 2000, ADF&G has also used

surveys to collect information on local knowledge and assessed contaminant levels and disease 

rates. Participating villages span the region from Hooper Bay in the Bering Sea to Kaktovik in 

the Beaufort Sea, including islands in the Bering Sea (Fig. 1), thereby encompassing virtually the 

entire range of ringed seals in Alaska. 

In this report we analyze results from ringed seal measurements and samples collected 

between 1960 and 2010 in order to evaluate how growth rates, body condition, diet, age 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

6 

distribution, sex ratio, and productivity have changed over time. The purpose of this report is to 

make unpublished data, collected by ADF&G, available for researchers, managers, subsistence 

hunters, and others with an interest in the status of ringed seals in Alaska. 

Figure 1. Collection locations. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

7 

METHODS

Sampling years 

Ringed seals from the subsistence harvest were sampled between 1960 and 2010; 

however, sampling effort and opportunity were not consistent. The majority of ringed seals 

sampled were harvested during two time periods, 1960–1979 (1960s and 1970s) and 1998–2010 

(2000s; Fig. 2). Ringed seals were also collected on scientific cruises in 1968, 1972, and 1976–

1979 (n = 47) and were included in our analyses as appropriate. Age class distributions of ringed 

seals collected during cruises were significantly different from ringed seals harvested by 

subsistence hunters during the same decade (P = 0.02), therefore cruise data were included where 

age distribution was not important. Cruise data were included in analyses of diet, age at 

maturation, and pregnancy rate, but not in age at harvest. We were able to include data from 429 

ringed seals harvested near Point Hope as part of the Cape Thomson, Project Chariot study 

(1960–1961; Wilimovsky and Wolfe 1966). In addition to the summary information presented 

by Johnson et al. (1966) we acquired copies of original datasheets from that study, which 

included data collected using methods consistent with ours. For each analysis, the sample size 

of seals used differed slightly as not all measurements or samples were collected for each seal. 

Figure 2. Number of ringed seals sampled in Alaska, by year, for which ages were known, 1960–

2010. Sample sizes differed slightly for each analysis, as not all measurements or samples were 

collected for each seal. Although sample sizes differ by analysis, this figure illustrates the 

general distribution of samples by year. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

8 

Local knowledge 

Harvest data require careful interpretation, as hunters may not randomly sample seals 

throughout their range. For example, changing preferences of hunters may confound the 

interpretation of seal distribution or age structure. Hunters may also have local knowledge that 

corroborates or aids the interpretation of data from the biomonitoring program. Hence, 

discussions with hunters are critical for understanding how to interpret results of data collected 

from the harvest. In collaboration with the Subsistence Division at ADF&G, we developed a 

questionnaire to collect information from villages participating in the bio-monitoring project. 

Questions were designed to determine the importance of the different seal species, whether 

changes had occurred in seal numbers, seal distribution, seal health, harvest methods, harvest 

timing, and local conditions. We used the responses to help us understand seal hunting practices 

and to identify topics that may need further investigation. The results help us understand 

whether changes observed in our sample collections are due to changes in seal availability or 

changes in harvest methods or preferences. Results obtained from the questionnaires were not 

intended to be definitive as they do not represent all or even the majority of the hunters from 

each community; however, majority responses give us a reasonable indication of hunter activity 

and preferences. 

Collection and handling of specimens 

Biological information collected included location, date harvested, date sampled, species, 

sex, standard length, blubber thickness, and axillary girth. Standard length measured along a

straight line from nose to tip of tail with seals on their backs (American Society of 

Mammalogists 1967). Blubber thickness was measured through a small incision to the sternum 

midway between the front flippers and axillary girth was measured with a soft tape placed under 

the foreflippers at the level of the axillae (McLaren 1958). Samples collected included one of 

the mandibles, the female reproductive tract, the whole stomach, and liver, kidney, blubber, and 

skin tissue. Samples were frozen in the field and shipped to ADF&G in Fairbanks for 

processing. 

Age determination 

For specimens collected in the 1960s and 1970s, ages were determined by counting the 

number of growth bands or ridges on claws (McLaren 1958, Burns 1969) and by counting 

cementum layers within decalcified sections of canine teeth (Hewer 1960, Mansfield and Fisher 

1960, Burns 1969, Stewart et al. 1996). After 2000, all ages were determined by counting 

cementum layers within sectioned teeth. We refer to ages determined via claws as “claw ages” 

and ages determined via teeth as “tooth ages.” Ages determined with claws are known to be 

biased low for older age classes, because claws wear over time; however, McLaren (1958) found 

that seals could be reliably aged by counting growth bands on claws until seals were at least nine 

years of age. After age nine, claw wear removes growth bands and only minimum age can be 

determined. When both claws and teeth were sampled, we relied on tooth ages. Some analyses 

are expected to be sensitive to the proportion of older seals (e.g., growth rates and age 

distributions) so we repeated these analyses with and without claw ages to ensure that the 

inclusion of claw ages did not bias results. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

9 

Stomach content analysis

We investigated stomach contents of ringed seals from 1961–2009 to determine if the 

frequency of prey items has changed over time. Stomachs from ringed seals harvested by 

Alaskan Natives and during scientific cruises were collected, frozen, and shipped to ADF&G 

offices in Fairbanks. Stomach were thawed in the laboratory and the contents were rinsed with 

freshwater through two sieves with mesh sizes of 1.0 mm and 0.5 mm and prey items were 

indentified to the lowest taxonomic level and weighed to the nearest 0.1 g. 

 

To provide an overall description of ringed seal diet, we first calculated the frequency of 

occurrence (FO) for each prey taxa, i. FOi is calculated as the number of stomachs that contains 

prey taxa i, divided by the number of stomachs with contents (i.e., we did not include empty 

stomachs in the calculation). Because FOi is a proportion, it mediates the effect of large 

differences in samples size between collection periods (Sinclair et al. 2008). To make direct 

comparisons over time, prey items sampled were grouped by taxa and compared by decade. We 

used Pearson Correlation Coefficients in SAS (Version 9.2; PROC CORR, SAS Institute Inc., 

Cary, NC, USA) to examine correlations among annual FO values for all prey items across all 

time periods and within each time period. Due to biases in digestion time, volume measurements 

were not considered representative of the true volume of prey consumed and were not analyzed. 

In order to determine whether ringed seal diet had changed over time, we used logistic 

regression (Ramsey and Schafer 2002) to calculate odds ratios and test for differences in the 

presence (0 = absent, 1 = present) of prey species in stomachs containing prey. Variables of 

interest included time period (1961–1984 or 1998–2009), sex, region (Bering or Chukchi sea), 

season (winter: November–May; open water or summer: June–October), and age class (pup: <1, 

subadult: 1–4 or adult: ≥5). We used odds ratios to assess the strength of an association between 

an explanatory variable and the presence of a prey item. A prey item that occurred more 

frequently in the 2000s than during the 1960s and 1970s would have an OR >1.0; this change 

would be expressed as a multiplicative increase in the odds of occurrence from one time period 

to another (e.g., a prey item that occurred 2.5 times as often in the 2000s than during the 1960s 

and 1970s would have an odds ratio of 2.5). Models were fit using SAS software (PROC 

LOGISTIC) and the best model was selected using a backward elimination procedure that 

sequentially eliminated statistically non-significant variables (P >0.05) until only statistically 

significant variables remained (P >0.05). 

To examine the occurrence of prey items relative to other prey items, we also calculated 

their relative occurrence (RO). ROi is calculated as the number of stomachs that contains a prey 

taxa i (e.g., fish), divided by the cumulative number of fish taxa identified in all ringed seal 

stomachs. For example, assume five stomachs contained fish and that sculpin were found in all 

five stomachs and cod, sand lance, and flatfish were each found in only one stomach. Hence, 

there were eight fish occurrences of four fish taxa. Using RO, cod, sand lance, and flatfish were 

each one of eight fish occurrences (1/8 or 12.5%) and sculpin represented five of eight fish 

occurrences (5/8 or 62.5%). Whereas, using FO, cod, sand lance, and flatfish each occurred in 1 

of 5 (20%) stomachs and sculpin occurred in 5 of 5 (100%) stomachs. The use of RO allows us 

to assess the diversity of taxa consumed by ringed seals and does not treat each prey item in 

isolation. RO was calculated each time period for five fish taxa (rainbow smelt, cod, sculpin, 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

10 

flatfish, and sand lance) and we evaluated differences in RO ratios by decade using chi-squared 

statistics using SAS software (PROC FREQ). 

We also used the Simpson’s Diversity Index (D) to further evaluate the diversity of fish 

and invertebrate taxa identified in ringed seal diets for each time period (Simpson 1949). We 

calculated D in two ways: first using the total count of all fish identified (i.e. the sum of all fish 

identified from each fish group; range: 0–1,150), then using the occurrence of fish (i.e. only the 

presence of a fish taxa) in seal stomachs. The index is calculated as:

where:

S is the number of fish (or invertebrate) taxa considered, 

ni is the number of prey taxa i counted in all stomachs (totals) or the number of stomachs 

that contained prey taxa i (occurrences), and 

N is the sum of all individual prey items identified (total) or the cumulative number of 

prey taxa identified in all stomachs (occurrences).

 

For invertebrate prey, we only used counts of prey item occurrences due to our concern 

that digestion processes bias counts of invertebrate prey. We considered index values close to 

zero to represent more diverse or heterogeneous diets and values near 1 to be more 

homogeneous. 

Contaminants

Tissue preparation—Ringed seal samples collected in 2003–2007 were analyzed for 

contaminants. Liver and blubber tissue were clean-sampled at ADF&G following protocols 

established by the National Institute of Standards and Technology (Becker et al. 1991) and 

organochlorine contaminants were quantified by TDI – Brooks International, Inc., B&B 

Laboratories, Inc., College Station, TX. Subsamples of liver tissue analyzed for organochlorines 

were analyzed for trace metals by LET laboratories in Columbia, MI. Individual seals were 

selected for contaminants testing only if liver, kidney, and blubber tissue were available in 

quantities required for testing after clean sampling each tissue. A tooth was also required so that 

age could be related to results. 

Trace metals and other elements—Liver, kidney, and muscle tissues were analyzed for 

trace metals. Samples were homogenized with a meat grinder. An aliquot of approximately 100 

g was weighed and freeze-dried and then further homogenized using a blender prior to 

extraction. Percent moisture was calculated by comparing the weight of the wet sample with the 

weight of the dry samples before a 0.5 g sample was extracted and digested in a microwave wet 

ash procedure using, H2O2, and HCl. Microwave digestion was used for all metals except As 

and Se.

, )1(

)1(

1

−

−

=

∑=

NN

nn

D

S

i

ii
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

11 

Samples analyzed for As and Se were digested using magnesium dry ash digestion 

methods. This method uses methanol, HNO3, HCl, and heat for digestion. After digestion As 

and Se were analyzed using Hydride Generation AA. Calibration was done at 0, 1.0, 5.0, and 15.0 

ppb and the QC check was 10.0 and a known reference sample. The 5.00 ppb standard was checked 

every tenth sample and if the value differed by >5% from 5.00 the instrument was recalibrated. If 

the value was >10% different from 5.00 the last 10 samples were re-analyzed. Pb was analyzed 

using Graphite Furnace AA. Calibration was done at 0 and 1.0 ppb and then 3–5 standards were 

run to check the calibration. All other metals were analyzed using ICP on a Perkin-Elmer 4300 DV.

For total mercury, a 10 ml aliquot was removed immediately after dilution, HCl was added 

and concentrations were determined using Cold Vapor AA. Calibration was done at 0, 1.0, 5.0, and 

30.0 ppb and the QC checks were 10.0, 20.0, and a known reference sample. The 5.00 ppb standard 

was checked every tenth sample and if the value differed by >5% from 5.00 the instrument was 

recalibrated. If the value was >10% different from 5.00 the last 10 samples were rerun. 

For analysis of methyl mercury (MeHg), liver samples were delivered frozen to the 

University of Alaska Wildlife Toxicology Laboratory in Fairbanks. Samples were freeze-dried 

before extraction to eliminate water and aid in the extraction process. Extraction of MeHg was 

initiated by the addition of 10 g 25% KOH in methanol and left overnight at room temperature 

(25oC). The extraction procedure was continued over 24 hours with the addition of 15.6 g of 

methanol. The extraction process was complete when all tissues were solubilized in the KOH in 

methanol solution. Extracts were analyzed for MeHg using cold vapor atomic fluorescence 

spectrometry (CVAFS) using the BrooksRand Model III detection system (Seattle, WA) and 

following procedures modified from Woshner et al. (2001a and b), Dehn et al. (2005, 2006) and 

Method 1630 (EPA-821-R-01-020, 2001). In short, 0.05–1.00 mL of the extract was added to 

100 mL of ultrapure water, adjusted to pH 4-5 with acetic acid buffer. Methylated forms of 

mercury in the sample were ethylated with a solution of 1.0% sodium tetraethyl borate (NaBEt4) 

in 2% KOH in a closed bubbler for 20 minutes. Methyl ethyl mercury was subsequently 

separated from the solution by purging with nitrogen (N2) gas onto Tenax® speciation traps. 

The methyl ethyl mercury was thermally desorbed from the traps and traveled via inert argon gas 

through a gas chromatography (GC) column heated to 105oC that further isolated the mercury 

species of interest. Mercury forms were next heated to 750oC with a pyrolytic coil that converted 

all organic mercury to elemental forms (Hg II), which can be detected by CVAFS. Three peaks 

emerge during the detection run, with the second (representing methyl ethyl mercury forms) used 

for calculation of MeHg in the sample. The amount of MeHg in each sample was compared to a 

6 point calibration curve (calibration coefficient = 0.07; RSD = 14.3%), calculated using 

Mercury Guru software (version 3.0.48; BrooksRand, Seattle, WA), and converted to ppb wet 

weight (ww). All samples were performed in duplicate with a coefficient of variation <18%. The 

detection limit for the sample run was 25 pg and recovery of quality control samples ranged from 

88 to 136%. 

Organochlorines—Liver and blubber tissues were analyzed for organochlorines (e.g., 

PCBs and pesticides). Tissue samples were homogenized using a stainless steel blender with 

titanium blades. Aliquots of approximately 15 g of wet tissue were chemically dried using 

Hydromatix and extracted with 100% dichloromethane using a Dionex Accelerated Solvent 

Extractor (ASE200) operated at 100°C and 2,000 psi. The extracts were reduced to 3 mL by 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

12 

evaporative solvent reduction. A 100 μL aliquot is removed and weighed to determine lipid 

weight. The remaining sample portion was purified using alumina/silica gel column 

chromatography and gel permeation column (GPC)/high performance liquid chromatography 

(HPLC). After HPLC purification, the eluents were reduced to 0.5 mL and analyzed for PCBs 

and pesticides by either gas chromatography/mass spectrometry (GC/MS) or gas 

chromatography/electron capture detector (GC/ECD). 

A GC/ECD, coupled to two capillary columns, was used to resolve and detect chlorinated 

hydrocarbons (polychlorinated biphenyls and pesticides) in tissues. Samples were injected into a 

temperature-programmed GC/ECD, operated in splitless mode. The capillary columns were DB5 (30 m x 0.25 mm ID and 25 μm film thickness) and DB-17HT (30 m x 0.25 mm ID and 0.15 

μm film thickness). The DB-17HT column is used for analyte confirmation. A data acquisition 

system continuously acquired and stored all data for quantitation. This method is capable of 

producing data at parts-per billion and parts-per trillion concentrations. The surrogate spiking 

solution includes 4,4’-dibromooctaflurobiphenyl (DBOFB), 2,2’,4,5’,6 pentachlorobiphenyl 

(PCB 103), and 2,2’,3,3’,4,5,5’6 octachlorobiphenyl (PCB 198). Surrogate solution (100 μL) is 

added to all samples and quality control samples prior to extraction. Surrogate compounds are 

resolved from, but elute in close proximity to, the analytes of interest. The recovery of PCB 103 

is used to correct analyte concentrations. Spikes, duplicates, and blanks were analyzed for 

quality control with each batch of 20 samples or less. 

Disease

We collected blood from ringed seals harvested near Point Hope, Kotzebue, Shishmaref, 

and Little Diomede Island, between 1998 and 2010. We tested serum for antibodies to four 

diseases known to affect phocids; Brucella spp., phocine herpesvirus-1 (PhHV-1), phocine

herpesvirus-2 (PhHV-2), and phocine distemper virus (PDV). Brucella is known to cause 

reproductive problems in marine mammals, including placental infections and abortion (e.g., 

Miller et al.1999). Zarnke et al. (2006) identified Brucella in harbor seals, in Alaska. PhHV-1 

usually affects pups and immunocompromised or diseased adults (Zarnke et al.1997). In 

contrast to PhHV-1, PhHV-2 is not known to cause disease in phocids, however its antibodies 

have been detected in all the phocids within Alaskan waters (Zarnke et al.1997, Zarnke et 

al.2006). PDV is a morbillivirus known to cause large die-offs. PDV infected seals exhibit 

symptoms of respiratory distress and the most common post-mortem finding is pneumonia 

(Kennedy 1998). In Alaska, PDV has previously been identified in harbor seals (Zarnke et 

al.1997). 

 Blood collected from harvested seals was allowed to clot before being centrifuged and 

serum was transferred to sterile cryovials. The cryovials were stored at –20°C for several weeks 

and then at –40°C for several months before shipping to the Oklahoma Animal Disease 

Diagnostic Laboratory (OADDL) in Stillwater, OK for testing. For Brucella, serum was 

screened for antibodies by using the standard card agglutination test (SCA). Samples that tested 

positive were retested using SCA, particle concentration fluorescence immunoassay, Brucella

buffered antigen standard plate agglutination test, complement fixation test, standard plate test, 

and Rivanol test (MacMillan 1992). For PDV, PhHV-1, and -2, serum was tested for the 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

13 

presence of antibodies by using the microplate virus neutralization test (Saliki and Lehenbauer 

2001). Threshold titers of ≥8 were considered positive. 

In addition to testing blood for antibodies to bacteria, viruses, and parasitic protozoans, 

we also tested intestinal material for domoic acid and saxitoxin produced by the ingestion of 

toxic algae, and we tested tongue tissue for the nematode Trichinella. Digestion assays using 

PCR were used to isolate two species of Trichinella (T. nativa and T. spiralis). 

Morphometrics

Analysis of growth rates—We examined standard length (cm) of ringed seals between 

1961 and 2010 to determine if length varied by seal cohort. For seals >1 year of age, we first 

calculated the average length for each age class. Seals were classified into year classes for ages 

1 through 14. Because there are relatively few seals in each year class >15 years of age, we 

pooled seals older than 14 years of age into a single age class. We subtracted the seal’s age from 

the year of harvest to determine the birth year. For each birth year, we then calculated residual 

growth as the length of a seal minus the average length of seals given that year age. We then 

looked for years or strings of years associated with seals that were long (or short), given their age 

at harvest. 

By linking residual growth with the birth year of seals, this approach assumes the length 

of seals is more dependent upon events that occur early in life than later in life. For example, we 

are assuming that a year with poor foraging conditions or a short nursing period will affect pups 

and one year old seals more than eight or nine year old seals. We believe this is reasonable, as 

ringed seals attain approximately 50% of their body length within approximately the first three 

years of age (McLaren 1958, Frost and Lowry 1981). 

However, for seals that are harvested after their birth year (i.e., non-pups), discrete 

perturbations in growth will have an integrative effect. For example, consider a series of years 

characterized by good foraging conditions that were followed by a single poor year. Although, 

the effect of this poor year on growth would be most discernable in pups born within that year, 

we would also expect to see decreased growth in seals born prior to that year. As such, a year 

with poor foraging would cause the largest perturbation in pup growth, followed by smaller 

perturbations in older seals. 

Seals less than one year of age (pups) were analyzed separately. Methods for calculating 

the residual growth of pups were similar for that of seals >1 year of age, except pups were 

classified by harvest month instead of year age. Hence, when calculating residuals of pup length, 

we accounted for the month in which the pup was harvested and assumed that all seals were born 

on 1 April. Although we are standardizing residuals by month, a limitation of this approach is 

that parturition dates and growth rates are confounded. Hence, differences in the length of pups 

by year could be due to shifts in the average date of parturition and not changes in the actual 

growth rate of pups. For example, if parturition occurs late in a given year, this will result in 

pups that are short given their month age. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

14 

Asymptotic growth models—For seals >1 year of age, we also described growth with 

asymptotic growth curves. Age-at-length data was fit with a generalized von Bertalanffy growth 

curve (e.g., Schnute 1981, McLaren 1993). The model is: 

( )b xxa

x eLL )( 0 1 −−

∞ −= , 

where:

Lx is the standard length of harvested individuals, 

L∞ length at infinite age (i.e., asymptotic length), 

a and b are rate parameters that define the rate at which growth approaches asymptotic 

length, 

x is the empirical age of individuals, determined by teeth and/or claws, and 

x0 is an adjustment for where the curve crosses the x-axis. Because of prenatal growth, 

individuals are not length 0 at birth. 

Lx and x are vectors of empirical data, from harvested seals; Linf, a, and b are estimated 

parameters. McLaren (1993) recommends setting x0 to a constant, rather than estimating x0 from 

the growth curve. We follow McLaren’s (1993) recommendation for ringed seals from the 

Bering and Chukchi seas and use -0.61 years for x0. We also followed McLaren’s 

recommendation and only included seals one year of age or older. Seals less than one year of 

age are analyzed elsewhere in this document. To account for the time of year seals were 

sampled, we assumed that all seals were born on 1 April. Growth of seals is rapid during the 

first few years of age; by adjusting the seal age to account for a spring birth date, we account for 

the fact that seals nearing a birthday will generally have a length closer to that of the next year 

age than the last year age. 

We estimated Linf, a, and b within a Bayesian framework using Markov Chain Monte 

Carlo (MCMC) simulations and Gibbs sampling (Congdon 2003, Gelman et al. 2004) in 

WinBugs (Speigelhalter et al. 2003). Bayesian methods use simulations to describe the 

probability distribution of a parameter, such as Linf, given the data (Gelman et al. 2004). 

Typically, when using MCMC sampling, a set number of initial iterations are discarded (i.e., the 

‘burn-in’) to remove the effect of initial values on the posterior distribution. We used Raftery 

and Lewis’s diagnostic (Raftery and Lewis 1995), as calculated by Package CODA (available at: 

http://cran.r-project.org/web/packages/coda) in R, to estimate the required ‘burn-in’ and to 

determine how many iterations are required to completely describe the posterior distribution. 

Iterations had high levels of autocorrelation; this results in large number of iterations being 

necessary to accurately estimate the posterior distribution. In effect, more iterations are needed 

to ‘fill in’ the posterior distribution and yield consistent parameter estimates. We ran four 

simulations (i.e., ‘chains’) 200,000 iterations each and discarded the first 10,000 iterations of 

each chain for the ‘burn-in’. 

We compared four models that represented competing hypotheses for how growth rates 

of seals may have changed through time or by harvest location. We used the pattern of growth 

residuals to guide us in specifying time periods for comparison. The residual analysis indicated 

that seals harvested after 1977 were larger than those harvested prior to 1977 (see RESULTS). 

Hence, one model estimated growth curves specific to these two time periods (i.e., prior to 1977 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

15 

and after 1977). McLaren (1993) reported that ringed seals are longer in the Bering Sea 

(standard length = 137.1 cm) than in the Chukchi Sea (standard length = 120.9 cm). Hence, the 

second model assumed different growth parameters for the Bering and Chukchi seas. The third 

model partitioned growth parameters by sex (male or female). McLaren (1993) found that male 

ringed seals were larger than female ringed seals; however, this relationship was not statistically 

significant. The final model assumed that all growth parameters were constant. Since 1980, few 

older female seals have been harvested and this prevented fitting models where sex interacted 

with time or location. Furthermore, most seals sampled in the Bering Sea were sampled in the 

1970s, so we could not fit models where sampling location interacted with sex or time. 

Models were compared using Deviance Information Criterion (DIC; Spiegelhalter et al. 

2002). DIC is equal to the -2 log likelihood of the model, calculated with the posterior means of 

the model parameters, plus 2 times the effective number of parameters. DIC are used for model 

selection in a similar fashion as Akaike Information Criterion (Burnham and Anderson 2002); 

models greater than 4 DIC units from the best approximating model are considered to have little 

statistical support. 

Body condition—We used sternal blubber thickness as an index for body condition 

because we did not have enough ancillary data (e.g., axillary girth or standard length) to calculate 

indices of body condition that are more correlated with the true blubber content of a seal (e.g., 

Parsons 1977, Ryg et al. 1990a, Gales and Renouf 1994, Arnould 1995). We examined blubber 

thickness using linear models with covariates to account for known patterns of variability in 

blubber thickness. We focused on seals sampled in May, June, and July, as these months had 

samples in most years. Covariates were tested for significance using Type III sums of squares 

and dropped from the model, one-at-a-time, if significance was P >0.05. For seals >1 year of 

age, we examined the effect of month (May, June, or July), age class (subadult or adult), 

standard length (cm), standard length squared, and the interaction between age class and standard 

length. Subadults seals were 1 to 4 years of age; adults were 5 years of age and older. Month 

was included because seals are expected to gain and lose mass seasonally (Ryg et al. 1990b). An 

examination of blubber thickness for all months indicated that blubber thickness increased with 

standard length in spring and summer, but not in winter. We speculate that the cost of molting 

and breeding are largely fixed costs. If these costs are fixed, we would expect bigger seals, with 

longer standard length, to lose less blubber during the breeding season. Because we are 

comparing the months of May, June, and July, we included standard length as a covariate. To 

account for possible curvilinear effects, standard length squared was included. Subadults, most 

of which are not of breeding age, may require less blubber than adults seals during these months. 

Hence, we also included the interaction of age class and standard length to allow the relationship 

between standard length and blubber thickness to vary by age class. The residuals of this model 

were then grouped by time period to identify time periods during when seals had thicker than 

average blubber given their length, sex, age class, or harvest month. 

Similar methods were used for pups (<1 year of age). For pups, we examined the effect 

of month (May, June, or July) and standard length (cm). The length of pups generally increases 

by month while average blubber thickness decreases. For pups, we are assuming that length is 

related to parturition date or age; by controlling for length, we remove variability due to variation 

in parturition dates. If poor foraging conditions lead to seals that grow more slowly, but 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

16 

maintain constant blubber thickness, controlling for length may mask changes in blubber 

thickness. The residuals of this model were then grouped by time period to identify time periods 

when seals had thicker than average blubber given their length or harvest month. 

Population parameters 

Age distribution—If harvest is an unbiased sample of the population, we can approximate 

the age distribution of the population by calculating the proportion of the harvest that falls into 

age categories. We assigned seals to one of three age categories; pups were <1 year of age, 

subadults were 1 to 4 years of age, and adults were >5 years of age, and then calculated the 

proportion of the harvest that fell into each age class on an annual basis. Seals collected during 

research cruises in the 1970s (n = 47) were omitted from the analysis of age distributions because

their distribution of age classes included a higher proportion of adults and pups than the 

subsistence harvest (χ2 = 7.61; P = 0.02). 

Mean age of harvest—We estimated mean age of ringed seals harvested during 1960–

2010. To isolate the effect of including pups in our calculations, we estimated mean age both 

including and excluding pups. If hunters harvested ringed seals randomly with respect to age, 

differences in mean harvest ages may represent actual changes in the age structure of the ringed 

seal population. We tested mean age, including and excluding pups, for differences among 

decades using SAS software (PROC GENMOD). Data were modeled with a gamma error 

distribution and a log link to account for skewness in the data (Garlich-Miller et al. 2006). We 

considered variables statistically significant at the level of α = 0.05. 

Sex ratios—We evaluated differences in sex ratios of ringed seals harvested during 1960–

2010. Models were fit using PROC LOGISTIC in SAS. Data were modeled with a binomial 

error distribution and a logit link. Variables of interest included decade (1960s, 1970s, and 

2000s), sex, region (Bering and Chukchi seas), season (winter: November–May; open water: 

June–October), age class (pups: <1; subadults: 1–4; adults ≥5) and all two-way interactions. The 

best model was selected using a backward elimination procedure. In general, seal hunters do not 

target a specific sex of ringed seal, therefore the sex of each harvested seal should not be subject 

to hunter bias, and therefore a change in the sex ratio of ringed seals over time may represent a 

change in the population structure. However, hunters avoid adult male ringed seals in the spring 

when they are in rut because of their strong smell (Hardy et al. 1991, Ryg et al. 1992). While 

this is a form of hunter bias, we expect this behavior to be consistent over time. 

Age at maturity and pregnancy rate—Reproductive tracts collected in the 1960s, 1970s, 

and 2000s were evaluated for sexual maturity (i.e., whether ovulation had occurred) and 

reproductive condition (i.e., pregnant, not pregnant) by sectioning ovaries, identifying corpora 

lutea and corpora albicantia, and examining the condition of uterine horns (McLaren 1958, 

Johnson et al. 1966, Smith 1973). We defined age at sexual maturity as the age at which the first 

ovulation occurred (McLaren 1958, Tikhomirov 1966, Smith 1973). Due to the delay between 

conception and implantation in pinnipeds (Harrison and Kooyman 1968) there are several 

months where pregnancy cannot be determined by the presence of a fetus. The presence of a 

corpora lutea indicates that the female ovulated but pregnancy cannot be confirmed during this 

time period. We considered all females with a corpora lutea that were harvested from May to 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

17 

September to be pregnant. Because each ovulation does not result in a pregnancy, the pregnancy 

rate will be inflated. 

We estimated the average age of maturity as the age at which 50% of sampled seals are 

mature. Average age of maturity was estimated using a generalized linear model with a probit 

link function and a binomial error distribution (e.g., Trippel and Harvey 1991) using PROC 

PROBIT in SAS (SAS Institute Inc. 2009). Like logistic regression, probit regression is 

designed to analyze data limited to two outcomes (i.e., binomial) and these two methods yield 

very similar parameter estimates. Probit regression is commonly used to estimate lethal doses 

for medical or pesticide studies and the average lethal dose (LD50) is analogous to the average 

age of maturation in our analysis. We chose to work with probit regression as these methods for 

estimating and comparing lethal doses is well described (e.g., Trippel and Harvey 1991, Wheeler 

et al. 2006, Robertson et al. 2007). Seals that had not ovulated were classified as immature; 

seals that had ovulated at least once were classified as mature. The accuracy of estimating age at 

maturity is largely dependent upon how many seals are sampled within age classes of 

intermediate maturity status (e.g., DeMaster 1978), where the proportion of mature seals is 

greater than zero, but less than one. Within our sample, intermediate maturity status was 

generally observed between three and seven years of age. For analysis, we pooled years within 

which fewer than 20 seals were sampled within this age range (Table 1). As such, seals were 

pooled into one of six groups; 1965–1975, 1976, 1977, 1978, 1979–1984, and 1999–2010. For 

each time period, model fit was assessed using a log-likelihood chi-square test. Estimates of the 

average age of maturation were statistically compared using the ratio test of Robertson et al. 

(2007, pages 27–29) at the level of P = 0.05. 

RESULTS

Local knowledge 

A total of 176 questionnaires were analyzed from five Bering and Chukchi sea villages. 

Responses did not indicate decreases in ringed seal population abundance at any location except 

for Hooper Bay where just over half (53%) of the respondents thought there were fewer ringed 

seals now, 38% thought the population was the same, and 9% thought there were more now 

(Table 2). The majority of respondents from all villages reported that ringed seals were found in 

the same locations as in the past. The timing of hunting had not changed for ringed seals in any 

village. Although the majority of Point Hope, Gambell, and Hooper Bay hunters reported 

preferences for certain types of ringed seals their preferences were highly variable. Some 

preferred big seals for more meat and oil, others liked small seals for tender meat, ease of 

handling, and because they are less likely to smell (referring to adult males in rut). There were 

also preferences for males because they are bigger and have more meat and oil and preferences 

for females because they are more tender. The majority of hunters in Shishmaref and Diomede 

that did not target specific types of ringed seals did not have a preference because all seals are 

food and taste good. Others said that they catch what they see and that they cannot tell the 

difference.
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

18 

Table 1. Sample sizes (n) for female ringed seals between 3 and 8 years of age with complete 

reproductive data. Seals were pooled into 1 of 6 groups for analysis. Years with >20 seals 3–8 

years of age were analyzed without pooling. 

Year n (all seals) n (3–8 years of age) Pooling group 

1965 1 1 1965–1975

1966 1 0 1965–1975

1967 7 1 1965–1975

1968 2 1 1965–1975

1969 15 6 1965–1975

1970 1 1 1965–1975

1972 1 1 1965–1975

1973 3 1 1965–1975

1975 16 8 1965–1975

1976 84 26 1976

1977 196 49 1977

1978 162 38 1978

1979 35 10 1979–1984

1980 15 0 1979–1984

1981 7 0 1979–1984

1984 24 11 1979–1984

1999 2 1 1999–2010

2000 13 2 1999–2010

2002 5 1 1999–2010

2003 18 2 1999–2010

2004 4 0 1999–2010

2005 7 0 1999–2010

2006 9 0 1999–2010

2007 28 3 1999–2010

2008 22 1 1999–2010

2009 5 1 1999–2010

2010 7 2 1999–2010

Total 690 167
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

19 

Table 2. Summary of selected local knowledge questions regarding seal harvest. Numbers are the percentage of respondents 

answering in the affirmative to selected questions. Responses of “don’t know” are not included in this table. 

Location

Point Hope Diomede Shishmaref Gambell Hooper Bay

Species Question n = 16 n = 29 n = 14 n = 44 n = 73

Ringed Have numbers remained the same? 31 55 43 63 38

Have numbers decreased? 31 40 36 22 53

Have numbers increased? 13 5 7 14 9

Are seals found in the same areas? 73 87 85 84 60

Does the hunt occur at the same time? 71 89 71 88 79

Do you try for certain types of this seal? 86 44 36 56 61

What is the hunting season? Jan–Aug Sept–Jun Jun; Sept–Nov Aug–May Sept–May

Bearded Have numbers remained the same? 56 70 64 75 60

Have numbers decreased? 19 15 7 6 29

Have numbers increased? 13 15 21 19 11

Are seals found in the same areas? 100 74 92 83 56

Does the hunt occur at the same time? 100 97 71 98 84

Do you try for certain types of this seal? 56 42 50 43 70

What is the hunting season? May–Jun Sept–Jun May–Jun Year round Aug–Jun

Spotted Have numbers remained the same? 56 65 36 62 46

Have numbers decreased? 13 26 36 26 24

Have numbers increased? 0 9 21 12 30

Are seals found in the same areas? 100 92 85 75 69

Does the hunt occur at the same time? 94 100 100 98 83

Do you try for certain types of this seal? 44 26 31 55 62

What is the hunting season? May–Aug Year round Jun; Sept–Nov Year round Year round

Ribbon Have numbers remained the same? 15 50 40 67 25

Have numbers decreased? 23 33 0 21 70

Have numbers increased? 0 17 0 13 5

Are seals found in the same areas? 55 82 43 77 44

Does the hunt occur at the same time? 89 95 80 83 81

Do you try for certain types of this seal? 0 22 33 52 53

What is the hunting season? May–Jun Apr–Jun; Oct May–Jun; Oct–Nov May–Jun; Nov Year round
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

20 

Diet 

 In the 1960s, 1970s, and early 1980s, stomachs from 1,300 ringed seals were examined 

and 1,080 (83%) contained prey items (Fig. 3); 247 were from the Bering Sea and 834 were from 

the Chukchi Sea. Samples from the Bering Sea came from eight villages (219) and four research 

cruises (28). Samples from the Chukchi Sea were from ten villages, the most were from 

Shishmaref (449). Three stomachs were collected from Kivalina as part of the Project Chariot 

investigation (1960–1961) near Cape Thompson (Wilimovsky and Wolfe 1966). Stomachs were 

collected during the spring-summer (739) and fall (342) subsistence harvests. Between 1998 and 

2009, stomachs from 589 ringed seals were examined and 475 (81%) contained prey items (Fig. 

3); 266 were from five villages in the Bering Sea and 209 were from four villages in the Chukchi 

Sea. Stomachs were collected during the spring-summer (99) and fall (376) subsistence harvests. 

No ringed seal stomachs with contents were collected in 1962–1968, 1972, 1973, 1982, 1983 and 

1985–1997 (Fig. 3). 

We identified 155 different prey taxa in 1,556 ringed seals sampled. The most common 

prey taxa and their frequency of occurrence (%FO) are presented in Table 3. There was no 

significant difference in occurrence of prey in the diets of males and females; therefore, sexes 

were pooled for all diet analyses. 

Fishes— Fish prey were commonly consumed by ringed seals within both time periods 

(annual %FO range: 72–100%; Fig. 4), but more frequently during the 2000s (93%) than during 

the 1960s and 1970s (82%; Table 3). Specifically, ringed seals were 4.1 times more likely to 

consume fish in the 2000s than during the 1960s and 1970s. We were able to identify significant 

increases in occurrence for fifteen fish taxa (i.e., genera or species; Table 3). Fish were also 

consumed more frequently in the Chukchi Sea than the Bering Sea and in winter than summer 

(Table 4). The average number of fish consumed per ringed seal was also higher in the 2000s 

( x = 42.6; SE = 3.2; range: 0–619) than in the 1960s and 1970s ( x = 32.8; SE = 2.7; range: 0–

1,550; U = 181422.50; P < 0.01). Changes in general fish consumption over time were strongly 

correlated with changes in consumption of species from the Family Gadidae (r = 0.67), 

suggesting changes in cod consumption were likely responsible for differences we observed 

among all fish. 

Currently ringed seals are consuming a greater diversity of fish than they did in the 1960s 

and 1970s. In the 1960s and 1970s, the diet was dominated by three species or taxa: Arctic cod 

(Boreogadus saida; 42%), saffron cod (Eleginus glacialis; 37%), and sculpin spp. (Cottidae; 

13%). Whereas, in the 2000s, there are five dominant species or taxa; the original three: Arctic 

cod (61%), saffron cod (46%), and sculpin (15%); plus rainbow smelt (Osmerus mordax; 27%) 

and walleye pollock (Theragra chalcogramma; 15%). 

Of the dominant taxa in the 1960s, the occurrence of Arctic cod increased from 39 to 

59% in the Bering Sea and from 43 to 63% in the Chukchi Sea. In contrast, the occurrence of 

saffron cod has remained stable in the Bering Sea (35 and 31%), but increased from 38 to 65% in 

the Chukchi Sea. Walleye pollock was rarely consumed (<1%) in both the Bering and Chukchi 

seas, but has become commonly consumed in the Bering Sea (26%; Table 4). Sculpin from the 

Family Cottidae, were identified in <20% of stomachs from both time periods (Table 4; Fig. 4). 

Of sculpin, the genus Myoxocephalus was consumed most frequently; the occurrence of 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

21 

Myoxocephalus increased in the Bering Sea (P < 0.01), but remained constant in the Chukchi 

Sea (P = 0.68; Table 4).

Of the two fish taxa that became frequently consumed in the 2000s, rainbow smelt is 

being consumed more frequently in the Chukchi Sea than the Bering (Table 4), and more 

frequently in the winter than summer (Table 4). In contrast, walleye pollock, the other new taxa, 

is being consumed more frequently in the Bering Sea than the Chukchi Sea (Table 4). 

In general, fish were found more commonly in the stomachs of adults and subadults than 

pups. Across all taxa of fish, adults (88%; P = 0.01) and subadults (85%; P < 0.01) were ~2.4 

times more likely to consume fish than pups (77%); however here was no evidence that 

consumption of fish varied between adults and subadults (P = 0.17). This pattern was generally 

true for cod, sculpin, and flatfish. Interestingly, this pattern was different for rainbow smelt; 

subadults consumed more rainbow smelt (15%) than pups (10%; P < 0.01), which consumed 

more than adults (8%; P < 0.01). 

In addition to examining %FO, we investigated changes in diet by calculating Simpson’s 

Diversity Indexes for the total number of fish identified (i.e., the sum of individual fish prey 

items) and also for the occurrence of taxa (i.e., the cumulative sum of fish taxa identified in all 

stomachs). We also calculated the relative occurrence (RO), defined as the number of stomachs 

that contains a prey category i (e.g., fish), divided by the cumulative number of fish taxa 

identified in all ringed seal stomachs (See METHODS). Simpson’s Diversity Index showed that 

ringed seals consumed a greater diversity of fish species (total counts: D = 0.78; occurrences: D

= 0.31) in the 2000s than during the 1960s and 1970s (total counts: D = 0.89; occurrences: D = 

0.48). The diet of ringed seals was dominated by five fish taxa throughout both time periods 

(Fig. 5). The RO of rainbow smelt increased from 3% in the 1960s and 1970s to approximately 

19% in the 2000s (Fig. 6). Although cod and sculpin were consumed more frequently during the 

2000s than the 1960s and 1970s (Table 3), their relative occurrence decreased proportionally in 

response to the addition of rainbow smelt (walleye pollock is part of the cod proportion). 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

22 

Figure 3. Number of stomachs from ringed seals harvested in Alaska, 1961–1984 and 1998–

2009 that contained prey. No stomachs were analyzed in 1962–1968, 1972, 1973, 1982, and 

1983. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

23 

Table 3. Percent frequency of occurrence (%FOi) of prey identified from ringed seal stomachs 

collected in Alaska, 1961–2009. Highlighted rows are discussed in text. 

Time period 1961–1984 1998–2009

Prey (i) n 1,081 475

All Fish * 81.59 93.05

Pacific herring (Clupea pallasi) * 3.70 5.68

Smelt (Osmerus mordax) * 2.41 26.74

Capelin (Mallotus villosus) * 0.65 7.37

Eelpout (Lycodes spp.) 1.02 1.05

Pacific sand lance (Ammodytes hexapterus) * 5.09 9.47

All Cod (Gadidae) * 66.60 83.58

Arctic cod (Boreogadus saida) * 42.09 60.63

Saffron cod (Eleginus gracilis) * 37.00 46.11

Walleye pollock (Theragra chalcogramma) * 0.09 14.53

All Sculpin (Cottidae) * 12.67 14.95

Gymnocanthus spp. * 1.20 5.26

Arctic staghorn sculpin (Gymnocanthus tricuspis) * 0.00 5.26

Myoxocephalus spp. * 3.70 7.79

All Snailfish (Liparidae) 1.39 1.68

All Pricklebacks (Stichaeidae) * 1.11 4.00

Eelblenny (Lumpenus spp.) * 0.74 3.16

Slender eelblenny (Lumpenus fabricii) 0.09 1.89

Ninespine stickleback (Pungitius pungitius) 1.30 1.68

All Flatfish (Pleuronectidae) * 4.35 6.32

Yellowfin sole (Limanda aspera) * 0.09 2.74

Longhead dab (Limanda proboscidea) 0.00 1.47

Arctic flounder (Pleuronectes glacialis) 1.48 0.00

Alaska plaice (Pleuronectes quadrituberculatus) 0.37 0.84

All Invertebrates * 88.62 66.11

Polychaeta 2.31 1.89

All Mollusca * 1.02 8.42

Gastropoda * 0.37 2.53

Bivalvia * 0.56 6.74

Cephalopoda * 0.37 1.89

Squid 0.28 0.21

Octopus (Octopodia) 0.09 0.84

All Crustacean * 88.44 62.53

All Copepods 3.15 0.00

All Mysidacea * 47.09 12.63

Mysidae * 46.62 12.21

Mysis spp. * 20.35 1.26

Mysis littoralis * 11.84 0.00

Neomysis spp. * 32.93 10.32

Neomysis rayii * 32.38 9.26

Diastylis spp. (Cumacean) 0.46 0.42

All Isopoda 4.63 2.53

Saduria entomon 4.26 1.26

All Amphipoda * 54.49 30.95

Ampeliscidae * 9.62 5.89

Ampelisca spp. * 8.51 2.74

Ampelisca macrocephalus 2.13 0.00

Bybils spp. 1.20 1.47

Atylus spp. 2.04 0.84

Eusirus spp. 1.20 0.00
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

24 

Rhacotropis spp. 2.31 0.00

Melitidae * 0.56 2.53

Melita spp. 0.56 2.11

Gammaridae * 21.92 7.79

Gammarus spp. * 18.32 4.63

Gammarus wilkitzkii * 13.88 0.00

Gammaracanthus loricatus 1.39 0.00

Weyprechtia spp. * 2.13 0.21

Weyprechtia pinguis 1.76 0.00

Ischyroceridae 0.65 0.21

Anonyx spp. * 15.26 6.95

Anonyx nugax * 15.17 2.32

Onisimus spp. * 7.49 2.11

Oedicerotidae * 5.27 0.42

Acanthostepheia spp. * 5.18 0.21

Acanthostepheia behringiensis 1.39 0.00

Hyperiidae * 25.44 10.53

Parathemisto libellula * 23.22 10.53

All Euphausiidae * 9.07 8.42

Thysanoessa spp. * 7.77 3.79

Thysanoessa raschi 2.50 2.53

All Decapods * 66.51 45.05

All Shrimp * 66.42 44.42

Hippolytidae * 30.62 7.16

Spirontocaris spp. 1.57 0.21

Lebbeus spp. 1.30 0.42

Eualus spp. * 29.42 4.21

Eualus fabricii 2.87 0.00

Eualus gaimardi * 25.44 2.95

Pandalidae * 28.03 13.26

Pandalus spp. * 27.66 10.53

Pandalus goniurus * 25.53 6.74

Pandalus hypsinotus 2.31 0.21

Crangonidae * 37.65 18.95

Crangon spp. * 24.98 10.32

Crangon dalli 1.39 0.21

Crangon alaskensis * 20.81 7.37

Sclerocrangon boreas 2.68 0.21

Argis spp. * 11.01 2.53

Argis lar * 9.53 1.47

Sabinea septemcarinata 1.30 0.00

All Crab * 0.74 2.95

Paguridae 0.19 0.42

Brachyura 0.56 0.84

Hyas lyratus 0.28 0.42

Chionoecetes opilio 0.09 0.63

All Echiuridae * 7.96 7.16

All Echinodermata 0.37 0.21

All Urochordata 0.19 0.42

* Significant difference in the occurrence of the prey item among time periods (P < 0.05).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

25 

Table 4. Regional and seasonal differences in frequency of occurrence (%FOi) of fish prey identified from ringed seal stomachs 

collected in Alaska, 1961–2009. Highlighted rows are discussed in text. 

Region Season

Bering Chukchi Spring-Summer Fall-Winter

Time period 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009

Prey (i) n 247 266 834 209 739 99 342 376

All Fish ab 74.49 91.35 83.69 95.22 77.54 87.88 90.35 94.40

Pacific herring (Clupea pallasi) a 1.62 1.13 4.32 11.48 3.11 2.02 4.97 6.67

Smelt (Osmerus mordax) abc 5.26 19.55 1.56 35.89 0.95 12.12 5.56 30.67

Capelin (Mallotus villosus) bd 0.40 6.39 0.72 8.61 0.81 2.02 0.29 8.80

Eelpout (Lycodes spp.) - 1.88 1.32 - 0.54 - 2.05 1.33

Pacific sand lance (Ammodytes hexapterus) ac 3.24 12.03 5.64 6.22 4.33 9.09 6.73 9.60

All Cod (Gadidae) b 60.32 83.08 68.47 84.21 62.92 75.76 74.56 85.60

Arctic cod (Boreogadus saida) bd 38.46 58.65 43.17 63.16 30.18 58.59 67.84 61.07

Saffron cod (Eleginus glacialis) abc 35.22 31.20 37.53 65.07 43.30 25.25 23.39 51.73

Walleye pollock (Theragra chalcogramma) a 0.40 25.56 - 0.48 0.14 18.18 - 13.60

All Sculpin (Cottidae) abd 16.19 19.55 11.63 9.09 9.20 17.17 20.18 14.40

Gymnocanthus spp. a 2.43 8.65 0.84 0.96 0.81 6.06 2.05 5.07

Arctic staghorn sculpin (Gymnocanthus tricuspis) a - 8.65 - 0.96 - 6.06 - 5.07

Myoxocephalus spp. ac 3.24 10.90 3.84 3.83 3.92 9.09 3.22 7.47

All Snailfish (Liparidae) b 0.81 3.01 1.56 - 0.41 1.01 3.51 1.87

All Pricklebacks (Stichaeidae) 1.21 5.64 1.08 1.91 1.08 3.03 1.17 4.27

Eelblenny (Lumpenus spp.) 0.40 4.14 0.84 1.91 0.68 3.03 0.88 3.20

Slender eelblenny (Lumpenus fabricii) - 2.63 0.12 0.96 0.14 3.03 - 1.60

Ninespine stickleback (Pungitius pungitius) a 4.05 2.63 0.48 0.48 1.08 1.01 1.75 1.87

All Flatfish (Pleuronectidae) abd 0.40 4.89 5.52 8.13 6.09 4.04 0.58 6.93

Yellowfin sole (Limanda aspera) a - 0.75 0.12 5.26 0.14 1.01 - 3.20

Longhead dab (Limanda proboscidea) - 1.13 - 1.91 - 1.01 - 1.60

Arctic flounder (Pleuronectes glacialis) - - 1.92 - 2.17 - - -

Alaska plaice (Pleuronectes quadrituberculatus) - 1.50 0.48 - 0.54 1.01 - 0.80 a Significant difference in the occurrence of the prey item between regions (P < 0.05). b Significant difference in the occurrence of the prey item between seasons (P < 0.05). c Significant difference in the occurrence of the prey item between regions and time periods: Interaction Time period × Region (P < 0.05). d Significant difference in the occurrence of the prey item between seasons and time periods: Interaction Time period × Season (P < 0.05).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

26 

Figure 4. Yearly patterns in percent frequency of occurrence (%FOi) of primary fish prey 

identified from stomachs of ringed seals harvested in Alaska, 1974–1984 and 1998–2009. 

Stomachs sampled before 1974 were omitted because sample sizes were small (n <5). No 

stomachs were analyzed in 1982 and 1983. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

27 

Figure 5. Yearly patterns in relative occurrence (RO) of fish prey identified in the stomachs of 

ringed seals harvested in Alaska, 1974–1984 and 1998–2009. Sample sizes of seals sampled 

prior to 1974 were too small to include with this comparison. No stomachs were analyzed in 

1982 and 1983. 

Invertebrates—Invertebrate prey items were commonly consumed by ringed seals within 

both time periods (annual %FO range: 49–100%; Fig. 6.). However, we found more stomachs 

with invertebrates in the 1960s and 1970s (89%) than during the 2000s (66%; Table 3). We 

identified a total of 103 invertebrate taxa. Of 56 commonly identified taxa, 30 significantly 

declined between time periods (Table 3). Within the early time period, all invertebrates were 

consumed more frequently in the Chukchi Sea than in the Bering Sea; however, the opposite was 

true for the later period (Table 5). However, there were differences among specific invertebrate 

groups (Tables 6 and 7). 

Prey items predominantly came from three Orders of the Class Crustacea: Mysidacea, 

Amphipoda, and Decapoda. Decapods were the most dominant class accounting for 66% in the 

early time period and 44% recently. Predominant decapod prey items came from three families 

of shrimp (Hippolytidae, Pandalidae, and Crangonidae). Within Hippolytidae, the genus Eualus

was most common, declining from 29 to 4% between time periods (Table 3). For Pandalidae, 

the genus Pandalus was most common and declined from 28 to 11%. For Crangonidae, Crangon 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

28 

and Argis were the dominant genera, declining from 25 to 10% and 11 to 2%, respectively. All 

Shrimp were consumed more frequently in the Bering Sea than the Chukchi Sea during both time 

periods (Table 7). Changes in shrimp consumption over time were correlated with changes in 

consumption of shrimp from the Family Crangonidae (r = 0.56).

Amphipods were consumed by 54% of ringed seals in the early time period and 31% 

recently (Table 3; annual %FO range: 6–100%; Fig. 6). Predominant amphipod prey items came 

from the taxonomic suborders of Ampeliscidae, Gammaridae and Hyperiidae (Table 3). Within 

Ampeliscidae two genera, Ampelisca and Bybils, were represented. Occurrence in Ampelisca

declined from 9 to 3%, while the occurrence of Bybilis remained low in both time periods (1 and 

2%). Within Gammaridae two genera, Gammarus and Anonyx, were identified. Gammarus 

declined from 18 to 5% and Anonyx declined from 15 to 7%. Seals consumed amphipods of the 

genus Gammarus more frequently in the Chukchi Sea than in the Bering Sea during the early 

time period (Table 6), but amphipods of the genus Anonyx were consumed more frequently in the 

Bering Sea. The only species identified within the suborder Hyperiidae was Parathemisto 

libellula; this species declined from 23 to 10% (Table 3); however, P. libellua did not decline as 

much in the Chukchi Sea (15%) as in the Bering Sea (7%; Table 6). During both periods it was 

consumed more in the winter than summer. Overall amphipod consumption was correlated with 

changes in Parathemisto libellula consumption (r = 0.52). 

Mysids were commonly identified in ringed seal stomachs (annual %FO range: 0–100%; 

Fig. 6). Two genera, Mysis and Neomysis, were identified. Mysidacea were consumed more 

frequently in the 1960s and 1970s (47%) than during the 2000s (13%; Table 3). Seals consumed 

mysids more frequently in the Chukchi Sea than in the Bering Sea and more in summer than 

winter (Table 5). 

Consumption of crustaceans varied by seal age class. Adult and subadult seals consumed 

crustaceans ~2 times more frequently than pups, but there was no evidence that consumption of 

crustaceans varied between adults and subadults (P = 0.10). Changes in the occurrences of 

crustaceans over time were correlated with changes in shrimp consumption (r = 0.60) and 

changes in general invertebrate consumption over time were strongly correlated with changes in 

crustaceans (r = 0.96). 

Although mollusks were infrequently consumed by ringed seals (Table 3), they were one 

of the few invertebrate prey items consumed less frequently in the 1960s and 1970s (1%) than 

during the 2000s (8%). Changes in mollusk consumption over time were correlated with 

changes in gastropod (r = 0.55) and bivalve consumption (r = 0.86). Ringed seals consumed 

more clams in the 2000s (7%) than during the 1960s and 1970s (<1%; Table 3). Clams were 

also consumed more frequently in the Bering Sea than in the Chukchi Sea (Table 5).

In addition to examining %FO, we investigated changes in diet by calculating Simpson’s 

Diversity Indexes for the occurrence of taxa (i.e., the cumulative sum of invertebrate taxa 

identified in all stomachs; See METHODS). Although invertebrates were consumed less 

frequently in the 2000s, ringed seals consumed a similar diversity of invertebrate species in the 

2000s (D = 0.26) than during the 1960s and 1970s (D = 0.29) based on Simpson’s Diversity 

Index for occurrences of prey items. 

 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

29 

Figure 6. Yearly patterns in percent frequency of occurrence (%FOi) of primary invertebrate 

prey identified from stomachs of ringed seals harvested in Alaska, 1974–2009. Stomachs 

sampled before 1974 were omitted because sample sizes were small (n < 5). No stomachs were 

analyzed in 1982 and 1983. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

30 

Table 5. Regional and seasonal differences in frequency of occurrence (%FOi) of invertebrate (polychaetes, mollusks, cephalopods, 

copepods, and mysids) prey identified from ringed seal stomachs collected in Alaska, 1961–2009. Highlighted rows are discussed in 

text.

Region Season

Bering Chukchi Spring-Summer Fall-Winter

Time period 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009

Prey (i) n 247 266 834 209 739 99 342 376

All Invertebrates abcd 84.62 71.05 89.81 59.81 91.47 67.68 82.46 65.87

Polychaeta 1.21 3.38 2.64 - 2.57 5.05 1.75 1.07

All Mollusca a 1.21 13.16 0.96 2.39 0.95 16.16 1.17 6.40

Gastropoda a 0.40 4.51 0.36 - 0.14 5.05 0.88 1.87

Bivalvia a 0.81 10.15 0.48 2.39 0.68 13.13 0.29 5.07

Cephalopoda bd - 3.38 0.48 - 0.14 5.05 0.88 1.07

Squid - 0.38 0.36 - 0.14 1.01 0.58 -

Octopus (Octopodia) - 1.50 0.12 - - 4.04 0.29 -

All Crustacean abcd 84.21 65.79 89.69 58.37 91.34 61.62 82.16 62.93

All Copepods 4.05 - 2.88 - 2.57 - 4.39 -

All Mysidacea ab 40.89 10.90 48.92 14.83 51.15 13.13 38.30 12.53

Mysidae ab 40.08 10.90 48.56 13.88 50.61 13.13 38.01 12.00

Mysis spp. b 21.05 1.88 20.14 0.48 22.19 3.03 16.37 0.80

Mysis littoralis b 14.98 - 10.91 - 15.56 - 3.80 -

Neomysis spp. ab 23.48 8.27 35.73 12.92 37.35 10.10 23.39 10.40

Neomysis rayii ab 22.67 7.52 35.25 11.48 36.67 9.09 23.10 9.33

Diastylis spp. (Cumacean) - 0.75 0.60 - 0.68 2.02 - -

All Isopoda ab - 4.14 6.00 0.48 6.36 7.07 0.88 1.33

Saduria entomon ab - 2.26 5.52 - 5.82 4.04 0.88 0.53 a Significant difference in the occurrence of the prey item between regions (P < 0.05). b Significant difference in the occurrence of the prey item between seasons (P < 0.05). c Significant difference in the occurrence of the prey item between regions and time periods: Interaction Time period × Region (P < 0.05). d Significant difference in the occurrence of the prey item between seasons and time periods: Interaction Time period × Season (P < 0.05).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

31 

Table 6. Regional and seasonal differences in frequency of occurrence (%FOi) of invertebrate (amphipods and euphausiids) prey 

identified from ringed seal stomachs collected in Alaska, 1961–2009. Highlighted rows are discussed in text. 

Region Season

Bering Chukchi Spring-Summer Fall-Winter

Time period 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009

Prey (i) n 247 266 834 209 739 99 342 376

All Amphipoda ac 53.44 35.34 54.80 25.36 53.04 27.27 57.60 32.00

Ampeliscidae ab 14.98 10.53 8.03 - 6.22 6.06 16.96 5.87

Ampelisca spp. ab 10.12 4.89 8.03 - 4.87 3.03 16.37 2.67

Ampelisca macrocephalus 2.43 - 2.04 - 1.49 - 3.51 -

Bybils spp. 5.26 2.63 - - 1.49 3.03 0.58 1.07

Atylus spp. 2.02 1.13 2.04 0.48 2.57 1.01 0.88 0.80

Eusirus spp. 2.02 - 0.96 - 0.54 - 2.63 -

Rhacotropis spp. a 7.69 - 0.72 - 2.44 - 2.05 -

Melitidae a 1.62 3.38 0.24 1.44 0.68 4.04 0.29 2.13

Melita spp. a 1.62 2.63 0.24 1.44 0.68 3.03 0.29 1.87

Gammaridae abcd 14.57 8.65 24.10 6.70 26.52 5.05 11.99 8.53

Gammarus spp. abcd 9.72 5.64 20.86 3.35 24.09 4.04 5.85 4.80

Gammarus wilkitzkii ab 6.88 - 15.95 - 18.54 - 3.80 -

Gammaracanthus loricatus - - 1.80 - 1.35 - 1.46 -

Weyprechtia spp. 2.02 0.38 2.16 - 2.30 1.01 1.75 -

Weyprechtia pinguis 2.02 - 1.68 - 2.17 - 0.88 -

Ischyroceridae a 2.02 0.38 0.24 - 0.81 1.01 0.29 -

Anonyx spp. ac 27.53 12.03 11.63 0.48 15.70 10.10 14.33 6.13

Anonyx nugax a 27.53 3.76 11.51 0.48 15.56 4.04 14.33 1.87

Onisimus spp. a 3.24 0.38 8.75 4.31 8.66 - 4.97 2.67

Oedicerotidae b 3.64 0.75 5.76 - 3.65 - 8.77 0.53

Acanthostepheia spp. b 3.64 0.38 5.64 - 3.52 - 8.77 0.27

Acanthostepheia behringiensis 1.21 - 1.44 - 1.49 - 1.17 -

Hyperiidae abc 28.34 7.14 24.58 14.83 19.62 2.02 38.01 12.80

Parathemisto libellula abc 26.72 7.14 22.18 14.83 16.78 2.02 37.13 12.80

All Euphausiidae abd 7.29 4.14 9.59 13.88 11.50 1.01 3.80 10.40

Thysanoessa spp. abc 6.07 1.13 8.27 7.18 10.15 - 2.63 4.80

Thysanoessa raschi ac 2.43 0.75 2.52 4.78 3.52 - 0.29 3.20 a Significant difference in the occurrence of the prey item between regions (P < 0.05). b Significant difference in the occurrence of the prey item between seasons (P < 0.05). c Significant difference in the occurrence of the prey item between regions and time periods: Interaction Time period × Region (P < 0.05). d Significant difference in the occurrence of the prey item between seasons and time periods: Interaction Time period × Season (P < 0.05).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

32 

Table 7. Regional and seasonal differences in frequency of occurrence (%FOi) of invertebrate (shrimp, crabs, echiurids, echinoderms, 

urochordates) prey identified from ringed seal stomachs collected in Alaska, 1961–2009. Highlighted rows are discussed in text. 

Region Season

Bering Chukchi Spring-Summer Fall-Winter

Time period 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009 1961–1984 1998–2009

Prey (i) n 247 266 834 209 739 99 342 376

All Decapods abd 72.47 46.62 64.75 43.06 74.29 46.46 49.71 44.80

All Shrimp abd 72.47 45.86 64.63 42.58 74.15 45.45 49.71 44.27

Hippolytidae abc 38.87 12.03 28.18 0.96 35.32 15.15 20.47 5.07

Spirontocaris spp. 2.83 0.38 1.20 - 1.62 - 1.46 0.27

Lebbeus spp. a 4.05 0.75 0.48 - 1.49 1.01 0.88 0.27

Eualus spp. ab 36.03 6.77 27.46 0.96 34.10 9.09 19.30 2.93

Eualus fabricii ab 9.72 - 0.84 - 3.25 - 2.05 -

Eualus gaimardi ab 29.15 5.26 24.34 - 30.99 8.08 13.45 1.60

Pandalidae b 30.36 15.04 27.34 11.00 32.07 15.15 19.30 12.80

Pandalus spp. b 29.96 12.03 26.98 8.61 31.80 13.13 18.71 9.87

Pandalus goniurus b 22.67 8.27 26.38 4.78 30.18 8.08 15.50 6.40

Pandalus hypsinotus ab 9.72 - 0.12 0.48 0.54 - 6.14 0.27

Crangonidae bd 30.77 16.17 39.69 22.49 43.03 14.14 26.02 20.27

Crangon spp. abd 9.72 7.14 29.50 14.35 32.88 10.10 7.89 10.40

Crangon dalli 0.81 0.38 1.56 - 1.49 1.01 1.17 -

Crangon alaskensis abd 6.07 5.26 25.18 10.05 28.69 7.07 3.80 7.47

Sclerocrangon boreas 2.83 0.38 2.64 - 2.84 - 2.34 0.27

Argis spp. a 15.79 4.14 9.59 0.48 9.20 1.01 14.91 2.93

Argis lar a 10.93 2.26 9.11 0.48 7.85 1.01 13.16 1.60

Sabinea septemcarinata 2.02 - 1.08 - 1.08 - 1.75 -

All Crab abd 2.02 4.51 0.36 0.96 0.68 9.09 0.88 1.33

Paguridae 0.81 0.38 - 0.48 0.14 1.01 0.29 0.27

Brachyura a 1.21 1.50 0.36 - 0.68 3.03 0.29 0.27

Hyas lyratus 1.21 0.75 - - 0.41 1.01 - 0.27

Chionoecetes opilio - 1.13 0.12 - 0.14 3.03 - -

All Echiuridae abcd 1.21 10.53 9.95 2.87 10.55 9.09 2.34 6.67

All Echinodermata - 0.38 0.48 - - 1.01 1.17 -

All Urochordata 0.81 0.38 - 0.48 0.27 1.01 - 0.27 a Significant difference in the occurrence of the prey item between regions (P < 0.05). b Significant difference in the occurrence of the prey item between seasons (P < 0.05). c Significant difference in the occurrence of the prey item between regions and time periods: Interaction Time period × Region (P < 0.05). d Significant difference in the occurrence of the prey item between seasons and time periods: Interaction Time period × Season (P < 0.05).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

33 

Contaminants

Metals and other elements—Concentrations of 19 trace elements were quantified in liver 

(n = 35) and kidney (n = 12) tissue of ringed seals. Some elements are essential nutrients (e.g., 

copper (Cu), iron, magnesium (Mg), manganese (Mn), selenium (Se), and zinc (Zn)), while 

others are potentially toxic at high levels (arsenic (As), cadmium (Cd), mercury (Hg), lead (Pb)). 

The highest concentrations of all elements were found in liver tissue, except for Cd with was 

highest in kidney tissue (Table 8). Geometric means for potentially toxic elements were 0.04 

ppm for Pb, 0.66 ppm for As, 1.62 ppm for Cd, and 1.32 ppm for total Hg. Liver had higher 

concentrations of all elements except for Cd, which was higher in kidney. 

In addition to total Hg (THg), a more toxic form called methyl mercury (MeHg) was 

analyzed in liver tissue of seven ringed seals (three females and four males) ranging in age from 

2–19 years old ( x = 9.29, SD = 5.91). When MeHg was expressed as a percentage of THg the 

values ranged from 2.9–14.3% (geometric mean = 6.88, arithmetic mean = 8.07, SD = 4.66). 

Females had higher geometric (8.96%) and arithmetic means (10.44%) than males (gmean = 

5.64%, amean = 6.30%). Females were also older on average (10.7 years) than males (8.3 

years). 

Organochlorines—Concentrations of organochlorines (OC) were summarized in the 

blubber (n = 35) and liver (n = 26) of ringed seals sampled during 2003–2007. We examined 

four compounds of hexachlorocyclohexane (HCH; Alpha-HCH, Beta-HCH, Delta-HCH, and 

Gamma-HCH ), seven compounds of chlordane (CHL; Heptachlor, Heptachlor-Epoxide, 

Oxychlordane, Alpha-Chlordane, Gamma-Chlordane, Trans-Nonachlor, and Cis-Nonachlor), six 

compounds of dichlorodiphenyltrichloroethane (DDT;2,4’-DDD; 4,4’-DDD; 2.4’-DDE; 4,4’-

DDE; 2,4’-DDT; and 4,4’-DDT), and 84 congener and congener groups of polychlorinated 

biphenyls (PCB) in both blubber and liver tissues. 

 

In general, OC concentrations in blubber tissue were an order of magnitude higher than in 

liver. The relationship among the compounds differed slightly between blubber and liver with 

ΣHCH < ΣCHL < ΣDDT < ΣPCB in blubber (Table 9). As with blubber tissue, the lowest levels 

of ΣHCH and the highest levels of ΣPCB were observed in liver tissue; however, ΣDDT was 

lower than ΣCHL (Table 9). 

 

Of the six compounds composing ΣDDT in blubber tissue, the most dominant compound 

detected was 4,4’ DDE (90.0%). The geometric mean sum of DDTs (ΣDDT = Σ2,4’- and 4,4’- 

DDD and DDE and DDT) was 126.3 ng/g wet wt. 

Of the 84 PCB congener and congener groups, four made up the more than half (54.7%) 

of the ΣPCBs in blubber (Table 10). They were, in decreasing dominance, 153/132 (21.1%), 

101/90 (12.8%), 138/160 (12.2%), and 99 (8.6%). In liver, the five compounds with the highest 

concentrations accounted for 39.7% of the ΣPCBs (Table 11). Congener 109/90 was dominant 

and accounted for 10.7% of the ΣPCBs. The other dominant compounds, in decreasing order, 

were 18 (7.8%), 138/160 (7.3%), 153/132 (7.2%), and 66 (6.7%). 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

34 

Table 8. Geometric mean (Gmean), arithmetic mean (Amean) and range of concentrations (μg/g wet wt = ppm) of selected elements 

in liver (n = 35) and kidney (n = 12) of ringed seals harvested in Alaska, 2003–2007. The tissue with the highest value for each 

element is in bold. Elements that were not detected during analysis are denoted by nd. Some essential elements and those where 

information is not available to biologically evaluate concentrations are not included. 

As Cd Cu THg Mg Mn Pb Se Zn

Liver 

Gmean 0.66 1.62 9.52 1.32 220.31 4.61 0.04 3.00 39.01

Amean 0.77 2.62 11.59 2.45 220.69 4.76 0.04 3.74 43.64

Range 0.10–1.85 0.17–20.80 2.89–60.33 0.14–12.88 185.6–255.3 2.62–7.72 0.03–0.12 0.95–12.64 0.48–67.39

Kidney

Gmean 0.46 3.75 5.65 0.28 148.27 1.28 nd 2.82 29.48

Amean 0.52 5.94 5.93 0.34 148.98 1.29 nd 2.86 29.84

Range 0.17–0.95 0.91–18.73 3.47–10.33 0.09–0.82 128.4–177.3 0.95–1.60 nd 2.24–3.50 21.61–39.75

Table 9. Geometric mean and range (ng/g or ppb wet wt) of concentrations for total organochlorines by chemical category in blubber

(n = 35) and liver (n = 26) from ringed seals harvested in Alaska, 2003–2007. Contaminants that were not detected during analysis are 

denoted by nd. 

Compound

∑ HCH ∑ CHL ∑ DDT ∑ PCB

Blubber

Gmean 51.47 98.02 126.28 273.66

Range (17.16–150.21) (23.50–341.82) (18.72–627.59) (61.10–908.28)

Liver

Gmean 1.04 4.46 2.49 10.72

Range (nd–12.02) (1.33–18.87) (0.53–13.42) (3.51–174.88)
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

35 

Table 10. Geometric mean and range (ng/g or ppb wet wt) of concentrations of dominant PCB congeners in blubber (n = 35) from 

ringed seals harvested in Alaska, 2003–2007. 

Dominant PCB Congeners

153/132 101/90 138/160 99

Blubber

Gmean 57.79 35.10 33.32 23.53

Range 9.61–330.08 6.12–131.15 11.06–118.72 5.23–79.77

% of total 21.12 12.83 12.18 8.60

Table 11. Arithmetic mean and range (ng/g or ppb wet wt) of concentrations of dominant PCB congeners in liver (n = 26) from ringed

seals harvested in Alaska, 2003–2007. Congeners that were not detected during analysis are denoted by nd.

Dominant PCB Congeners

101/90 18 138/160 153/132 66

Liver

Amean 2.05 1.50 1.40 1.37 1.28

Range nd–22.66 nd–29.55 nd–4.93 nd–3.66 nd–25.97

% of total 10.70 7.83 7.31 7.15 6.68
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

36 

Disease 

We identified Brucella antibodies (i.e., evidence of exposure but no infection) in 6.4% (3 

of 47) and PhHV-1 antibodies in 16.7% (14 of 84) of ringed seals that were sera tested (Table 

12). We found no antibodies for PhHV-2 in 5 individuals and no antibodies for CDV or PDV in 

82 individuals. We found antibodies to four of six Leptospira species we tested for. Leptospira 

bratislava had the highest prevalence at 27.8%, L. icterrohemorrhagiae was next at 20.8%, and 

L. grippotyphosa and L. hardjo each had a low prevalence at 1.4% (Table 12). We did identify 

Toxoplasma in 5.0% (4 of 80) ringed seals tested. Ringed seal tongue tissue was tested for the 

parasite Trichinella but none were found to be positive (n = 58). 

Stomach or intestinal contents of 34 ringed seals (three harvested in 2007, six in 2008, 

and 25 in 2009) were tested for toxic algae (domoic acid and saxitoxin). The ringed seals tested 

were harvested in Point Hope, Shishmaref, Diomede, Gambell, Savoonga, and Hooper Bay. 

Four ringed seals had levels of domoic acid above the detection limit of 4 ng/ml and six had 

levels of saxitoxin above the same detection limit. Domoic acid concentrations ranged from 4.1 

to 31.1 ng/ml and saxitoxin ranged from 5.2 to 13.8 ng/ml, which were all far below (by 500–

1000 times) the regulatory limit for domoic acid in shellfish tissue tested for human 

consumption. Only one ringed seal contained both toxins. The ringed seal with the highest level 

of domoic acid was from Diomede, as was the one with the highest level of saxitoxin. 

Table 12. Serum antibody prevalence for 12 disease agents in ringed seals harvested near Point 

Hope, Kotzebue, Little Diomede, and Shishmaref, Alaska, 2003–2010. 

Disease Agent Antibody prevalence

No. positive/No. tested (%) 

Brucella spp. 3/47 (6.4) 

Canine distemper virus 0/82 (0) 

Phocine distemper virus 0/82 (0) 

Phocine herpesvirus-1 14/84 (16.7) 

Phocine herpesvirus-2 0/5(0) 

Leptospira bratislava 20/72 (27.8) 

Leptospira canicola 0/72 (0) 

Leptospira grippotyphosa 1/72 (1.4) 

Leptospira hardjo 1/72 (1.4) 

Leptospira icterrohemorrhagiae 15/72 (20.8) 

Leptospira pomona 0/72 (0) 

Toxoplasma spp. 4/80 (5.0) 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

37 

Morphometrics 

Growth rates—Our analyses of standard length included 1,610 seals one year of age or 

older (Fig. 7) and 543 pups (Fig. 8). The birth year of these seals >1 year of age ranged from 

1933 to 2009 and the birth year of pups ranged from 1961 to 2010. 

Some ringed seals were aged by counting claw annuli. Claw annuli wear away over time, 

leading to a count of age that is biased low in seals >9 years old (McLaren 1958). To avoid a 

negative bias in estimated age, researches generally used claws to only age younger seals. Fortyfour of 396 seals were aged using claws in the 1960s, 386 of 881 in the 1970s, and 16 of 97 in 

the 1980s. All 188 seals sampled in the 2000s were aged with teeth. In general, length-at-age 

was similar for seals aged with teeth and claws (Figs. 9a and 9b) so we included claw ages in our 

analyses. 

Birth year

193019401950196019701980199020002010

Sample size

0

20

40

60

80

100

Figure 7. Distribution of ringed seals >1 year of age by birth year. A total of 1,610 seals were 

used to analyze growth rates. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

38 

Birth year

196019701980199020002010

Sample size

0

20

40

60

80

Figure 8. Distribution of 543 ringed seal pups plotted by birth year that were used to analyze 

growth rates. 

For seals >1 year of age, averaged residuals ranged from -6.2 cm in 1961 to 19.3 in 2005. 

In general, seals born after 1977 tended to be larger (i.e., have positive residuals) than seals born 

before 1977 (Fig. 10). Larger standard errors were present after 1980; this is partially due to 

smaller sample sizes, but may also be due to more sampling error or greater environmental 

variability. Two abrupt declines in residuals are apparent. One occurred in 1961 and was 

preceded by a gradual decline in residual values. The other occurred between 1974 and 1976 

and forms an abrupt 3-year decline in residual values. Because of the integrative nature of 

assigning growth to the birth year, it is likely that the perturbation occurred sometime between 

1974 and 1977, but the timing and duration of this event is uncertain. 

The best approximating model of seal growth indicated that seals grew differently 

between 1977 and 2009 than between 1940 and 1976. This model was 38 DIC units better than 

the model that partitioned growth rate parameters by sex, 62.9 DIC units better than the model 

that portioned growth rate parameters by sampling location (Bering vs. Chukchi), and 80.1 DIC 

units better than a model that assumed growth rate parameters were constant.

 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

39 

b

Age (yr)

0 5 10 15 20 25 30

Standard Length (cm)

40

60

80

100

120

140

160

Male Claw Age

Male Tooth Age

a

Age (yr)

0 5 10 15 20 25 30

Standard Length (cm)

60

70

80

90

100

110

120

130

140

Female Claw Age

Female Tooth Age

Figure 9. Standard length (cm) of (a) male ringed seals and (b) female ringed seals by age, as 

determined by counting claw annuli (triangles) or counting dentine/cementum layers in teeth 

(circles).
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

40 

Figure 10. Residual growth of ringed seals >1 year of age by birth year. 

The best approximating model indicated that asymptotic length was slightly less in seals 

born prior to 1977 (asymptotic length = 121.8 cm; 95% CL = 119.4–124.9) than seals born on or 

after 1977 (asymptotic length = 123.6 cm; 95% CL = 120.1–128.0; Fig. 11a). However, the 

major difference in growth was not in asymptotic length, but how fast seals reached asymptotic 

length (Fig. 11b). At age 1, seals born on or after 1977 were an average of 1.7 cm longer than 

seals born prior to 1977. This affect was greatest at 6 years of age, when seals born on or after 

1977 were an average of 6.2 cm longer. By age 25, the affect had diminished to an average of 

only 2.8 cm. 

Although the models with sex-specific or location-specific growth rate parameters were 

not supported, the estimates from these models are of biological interest. Asymptotic length was 

estimated to be virtually identical for both males (121.4 cm, SD = 1.2) and females (121.5 cm, 

SD = 3.4). Likewise, asymptotic length of ringed seals was almost identical for seals harvested 

in the Bering (119.8 cm, SD = 2.3) and Chukchi (121.1, SD = 1.3) seas. 

 

For pups, averaged residual growth ranged from -9.5 cm in 1961 to 11.4 cm in 2004 (Fig. 

12). The longest string of years with negative residuals occurred from 1975 to 1978 (4 years). 

However, the two years with the lowest growth rates occurred in 1961 and 2005. Six of ten 

(60%) sample years have negative residuals between 1960 and 1979. In contrast, only three of 

nine (33%) sample years have negative residuals between 2000 and 2009. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

41 

Figure 11. (a) Growth curves for ringed seals born prior to 1977 (solid line) and ringed seals 

born in 1977 and later (dotted line). (b) Average difference in standard length (cm) between the 

two time periods. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

42 

Figure 12. Residual growth of ringed seal pups by birth year. Negative residuals indicate that 

seals are shorter than average, given the month of harvest. 

In general, years associated with shorter than average pups also had shorter than average 

seals >1 year of age. As with seals >1 year of age, pups born in 1961 were short given their age. 

Seals >1 year of age also had less growth if they were born between 1974 and 1976; averaging 

3.8 cm shorter than expected if they were born in 1974, 3.4 cm in 1975, and 3.6 in 1976. Pups 

followed the same pattern for 1975 (3.3 cm shorter than expected) and 1976 (4.9 cm shorter than 

expected), but not for 1974 (11.0 cm longer than expected). The largest discrepancy between 

pups and older seals occurred in 2005 and 2007; in these years pups were short given the date of 

harvest, 8.2 cm shorter than expected in 2005 and 4.9 cm shorter than expected in 2007 (Fig. 12). 

However, seals >1 year of age had the highest growth rates we observed; 19.3 cm longer than 

expected in 2005 and 15.9 cm longer than expected in 2007 (Fig. 10).

Body condition—Average blubber thickness of subadult and adult ringed seals varied 

seasonally (Fig. 13). Maximum blubber thickness occurs in January or February and declines 

until July. The months we compared (May, June, and July) correspond to the time when blubber 

thickness is declining at the highest rate. Sternal blubber thickness was compared in 147 pups, 

215 subadults (1–4 years of age), 189 adults (>5 years of age; Table 13). 

For subadult and adult ringed seals, month and length were significant predictors of 

blubber thickness (P < 0.05). Standard length squared (P = 0.57), the interaction of standard 

length and age class (P = 0.56), age class (P = 0.45), and sex (P = 0.19) were dropped from the 

model. Average blubber thickness declined from 3.5 cm (SD = 0.87) in May to 2.7 cm (SD = 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

43 

0.88) in July. Longer seals generally had thicker blubber (Fig. 14). The residuals of this model 

indicated that adult and subadult ringed seals had thinner blubber than expected in 1971 and 

thicker blubber than expected in 1978. Since 2002, blubber thickness has been average (Fig. 15). 

For pups, both month (P < 0.01) and length (P < 0.01) were significant predictors of 

blubber thickness. Average blubber thickness declined from 2.8 cm (SD = 0.99) in May to 1.8 

cm (SD = 0.77) in July (Fig. 16). Longer seal pups generally had thicker blubber (Fig. 17). The 

residuals of this model indicated that pups had less blubber than expected in 1971 and 1976 (Fig. 

18). Since 2002, blubber thickness has been average (Fig. 18).

Figure 13. Seasonal variability in mean sternal blubber thickness of subadult and adult ringed 

seals, all years combined. Error bars represent 95% confidence limits. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

44 

Table 13. Sample sizes by year of ringed seals harvested in May, June, or July, which have data 

on sex, age, standard length, and sternal blubber thickness. 

 

Period Pups Subadults Adults

1971 19 46 18

1974 13 32 3

1975 8 49 29

1976 8 8 27

1977 32 23 29

1978 38 29 32

1979 6 7 21

1984 - 11 19

2002-2010 23 10 11

Total 147 215 189

Standard length (cm)

60 80 100 120 140

Sternal blubber 

thickness (cm)

0

1

2

3

4

5

6 May

June

July

Figure 14. Relationship between standard length and sternal blubber thickness from the fitted 

model for subadult and adult ringed seals. Residuals of this model were used to identify years 

when seals had sternal blubber that was thicker or thinner than expected given their length and 

month of harvest. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

45 

Figure 15. Residuals of sternal blubber thickness by time period for subadult and adult seals. 

Error bars are 95% confidence limits; statistically significant differences have error bars that do 

not overlap a residual of zero. Sample sizes are presented above error bars. Time periods with 

negative residuals had seals with less sternal blubber than expected, given their length and 

month of harvest. Time periods with positive residuals had seals with more sternal blubber than 

expected, given their length and month of harvest. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

46 

Figure 16. Average sternal blubber thickness by month for ringed seal pups. Error bars are 1 

SD.

Standard length (cm)

60 70 80 90 100 110

Sternal blubber 

thickness (cm)

0

1

2

3

4

5

6

May

June

July

Figure 17. Relationship between standard length and sternal blubber thickness from the fitted 

model. Residuals of this model were used to identify years when seal pups had sternal blubber 

that was thicker or thinner than expected given their length and month of harvest. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

47 

1971197419751976197719781979

2002-2010

Residual of sternal

blubber thickness (cm)

-2.5

-2.0

-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

19

13

8

8

32

38

6

23

Figure 18. Residuals of sternal blubber thickness by time period for ringed seal pups. Error 

bars are 95% confidence limits; statistically significant differences have error bars that do not 

overlap a residual of zero. Sample sizes are presented above error bars. Time periods with 

negative residuals had seals with less sternal blubber than expected, given their length and 

month of harvest. Time periods with positive residuals had seals with more sternal blubber than 

expected, given their length and month of harvest. 

Population parameters 

Age distributions—We analyzed age-at-harvest for 528 ringed seals harvested in the 

1960s, 4,694 in the 1970s, and 727 in the 2000s. During the 1970s, seven years had lower pup 

proportions than the study average ( x = 26%; Fig. 19). Pup proportions were lowest in 1972 

(12.5%; n = 106) and during the Bering Sea regime shift (Miller et al. 1994) in 1976 (6.4%; n = 

676). A greater proportion of pups were identified in the 2000s (56%) than in the 1960s (14%; P 

<0.01) and 1970s (23%; P <0.01). 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

48 

Figure 19. Proportion of ringed seals by age category (pup: <1 yr; subadult: 1–4 yr; adult: ≥5 

yr) that were harvested in Alaska, 1960–2010. 

Mean age at harvest—Overall, the mean age within the harvest declined from 7.4 years 

(95% CL = 6.8–8.1) in the 1960s, to 4.6 years (95% CL = 4.5–4.8) in the 1970s, and then 

declined further to 3.4 years (95% CL = 3.1–3.7) in the 2000s. Excluding pups from the 

calculation of mean age resulted in a mean ages of 8.5 (95% CL = 7.9–9.1) in the 1960s, 6.0 

(95% CL = 5.8–6.1) in the 1970s, and 6.8 (95% CL = 6.3–7.4) in the 2000s. Differences among 

all decades with and without pups were significant (P <0.01). 

 

Sex ratios— Sex ratios were generally male biased (Figs. 20 and 21). The proportion of 

males in the harvest varied significantly by decade, region, and season (P <0.01 for all 

parameters). For adults and subadults in the Bering Sea, sex ratios were somewhat female biased 

in the 1960s (36% male) but shifted to male biased in the 1970s (56%) and 2000s (69%; Fig. 20). 

In the Chukchi Sea, sex ratios were more heavily skewed toward males in the 1960s (73%) than 

in the 1970s (57%) and 2000s (61%). 

 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

49 

For pups in the Bering Sea, sex ratios were near unity in the 1960s (48% male) and 1970s 

(48%), and male biased in the 2000s (61%; Fig. 21). Pups in the Chukchi Sea showed the same 

pattern as those in the Bering Sea, increasing from 45% males in the 1960s, to 54% in the 1970s, 

and 58% in the 2000s. 

Seasonal effects were stronger for adults and subadults than for pups. On average, the 

harvest of adults and subadults was 10% more male biased during the winter. However, the 

effect was not uniform in that the proportion of males in the winter ranged from 36 (i.e., a female 

bias) to 80%. On average, the harvest of pups was 5% more male biased during winter. As with 

adults and subadults, the seasonal effects were not uniform in that the proportion of males pups 

in the winter ranged from 36 (i.e., a female bias) to 64%. 

Figure 20. Proportions of adult (≥5 years) and subadult (1–4 years) male ringed seals, 

harvested in the Bering and Chukchi seas during three decades in Alaska, 1960–2010. Error 

bars depict 95% confidence intervals. Dotted line depicts equal male:female sex ratio. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

50 

Figure 21. Proportions of pup (<1 year) male ringed seals harvested in the Bering and Chukchi 

seas during three decades in Alaska, 1960–2010. Error bars depict 95% confidence intervals. 

Dotted line depicts equal male:female sex ratio. 

Age at maturity and pregnancy rate—Maturity status was determined for 690 ringed 

seals; 47 harvested between 1965 and 1975, 84 in 1976, 196 in 1977, 162 in 1978, 81 between 

1979 and 1984, and 120 between 1999 and 2010 (Table 1). Probit regression adequately fit the 

data for all time periods (P >0.1). Average age of maturity was 5.3 years of age between 1965 

and 1975, then increased to 6.4 in 1976, and 6.5 in 1977 (P <0.05; Fig. 22). In 1978, the average 

age of maturity significantly decreased by 1.5 years (P <0.05) to 5.0 years of age. Age at 

maturity was again higher from 1979–1984 (5.9 years). However, there were few intermediate 

age seals in this time period and variance could not be estimated as all seals <6 years of age were 

immature and all seals >6 were mature. Since 1999, the average age of maturity was the lowest 

observed (3.2 yrs), significantly lower than all other years (P <0.05 for all comparisons). 

1960s. For the 1960s, data from both ADF&G and Project Chariot were available for calculation 

of pregnancy rates. Of the 41 reproductive tracts analyzed for sexual maturity from ADF&G 

data, nine (21.9%) were immature, 12 had ovulated once, 17 had ovulated more than once, and 

three were mature, however the number of ovulations was unknown. Of 32 sexually mature 

females, 32 (100%) were pregnant in the year they were harvested. Of the 696 reproductive 

tracts analyzed for sexual maturity from the Project Chariot data, 383 (55.0%) were immature, 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

51 

Figure 22. Mean age at maturity and 95% confidence limits for ringed seals sampled within 

each time period. Numbers above error bars represent sample sizes. Shared letters above time 

periods indicate periods that are not statistically significant at P >0.05. For example, “bc” is 

significantly different from periods with an “a” or “d” but similar to periods with a “b” or “c.” 

Statistical contrasts show that seals sampled since 1999 have a younger age of maturation than 

seals sampled in all other time periods. Error bars are not shown for 1979–1984 as there was 

no overlap in years between mature and immature seals and, therefore, no error. Specifically, 

all seals <6 years of age were immature and all seals >6 years of age were mature. 

 

but no data on the number of ovulations were available. Of 313 sexually mature females, 240 

(76.7%) were pregnant in the year they were harvested. When the two datasets were combined, 

272 of 354 (76.8%; 95% CL = 72–81%) mature females were pregnant when harvested.

 

1970s. Of the 527 reproductive tracts analyzed from the 1970s, 251 (47.6%) were immature, 68 

had ovulated once, 204 had ovulated more than once, and four were mature but the number of 

ovulations was unknown. Of 276 mature females, 246 (89.1%; 95% CL = 85–93%) were 

pregnant when harvested. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

52 

1980s. Of the 47 reproductive tracts analyzed from the 1980s, 26 (55.3%) were immature, three 

had ovulated once, and 18 had ovulated more than once. Of 21 mature females, 16 (76.2%; 95% 

CL = 58–94%) were pregnant when harvested. 

2000s. Of the 163 reproductive tracts analyzed from the 2000s, 119 (73%) were immature, 22 

had ovulated once, 12 had ovulated more than once, and 10 were mature but the number of 

ovulations was unknown. Of 44 mature females, 35 (79.5%; 95% CL = 67–92%) were pregnant 

when harvested.

DISCUSSION

Local knowledge 

We recognize that there is bias in hunter collected samples. Hunter questionnaires allow 

us to understand the bias so that we can evaluate whether changes in our results can be 

interpreted as changes in the population or if they are a result of changes in hunter behavior. 

Some hunters have preferences for certain types of seals, but those preferences are varied and 

include big, small, male, female, old, and young. Many hunters do not know what type of seal 

they are pursuing until after they retrieve it, and other hunters pursue any seal they observe. 

Only adult males in the spring are consistently avoided. Adult males in breeding condition can 

sometimes be identified by their black faces. Although the harvest was composed of a larger 

proportion of adult males than females, the proportion of males in the sample was 10% higher in 

the winter than in the spring. 

Hooper Bay was the only location of our sample of five villages where more than half of 

the hunters who responded thought ringed seals numbers have declined. We hesitate to interpret 

the population as declining at Hooper Bay, as 47% of respondents thought the population was 

stable or increasing. Even though the ice forms later and leaves earlier, the majority of 

respondents from all villages report that ringed seals are found in the same areas and they hunt 

them in the same months as in the past. 

Diet

Frequency of occurrence in stomach contents is an imperfect measure of ecological 

change. First, frequency of occurrence is a binomial variable; which does not include the 

volume of prey but simply records if a prey item occurred. As such, using occurrence can mask 

changes in prey volume until a prey item completely disappears from the diet. Second, dietary 

preference may ameliorate changes in prey abundance. If a preferred prey item decreases in 

availability, seals may still preferentially seek and consume that prey item, thus frequency of 

occurrence may not reflect the availability of prey in the environment. While these factors must 

be considered, changes in seal diet are still likely to reflect broad ecological changes. As long as 

dietary preferences of seals are static over time, changes in the frequency of occurrence of 

common prey items can be interpreted as changes in prey availability. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

53 

We found that the diet of ringed seals shifted between the 1961–1984 time period and the 

2000s (i.e., 1998–2009). In general, seals still eat the same prey (i.e., cod, amphipods, and 

shrimp). However, the proportion of fish in the diet has increased between the 1960s and 1970s, 

and the 2000s, while the proportion of invertebrates decreased. Specifically, the frequency of 

occurrence of fish increased from 75 to 91% in the Being Sea and from 84 to 95% in the 

Chukchi Sea (Table 4). 

Ringed seals are also consuming a greater diversity of fish than they did in the 1960s and 

1970s. For example, diet was dominated by Arctic cod (42%), saffron cod (37%), and sculpin 

(13%) in the 1960s and 1970s. In the 2000s, the most common fish species consumed by ringed 

seals were Arctic cod (61%), saffron cod (46%), smelt (27%), sculpin (15%), and walleye 

pollock (15%). 

In contrast to fish, the frequency of occurrence of invertebrates decreased from 85 to 71% 

in the Bering Sea and from 90 to 60% in the Chukchi Sea during the same time periods (Table 

3). We identified 103 invertebrate taxa and 30 of these significantly declined between time 

periods (Table 3). Prey items predominantly came from three Orders of the Class Crustacea: 

Mysidacea, Amphipoda, and Decapoda. Decapods were the most dominant class accounting for 

66% in the early time period and 44% recently. Changes in the occurrences of crustaceans over 

time were correlated with changes in shrimp consumption (r = 0.60) and changes in general 

invertebrate consumption over time were strongly correlated with changes in crustaceans (r = 

0.96). 

Some authors have speculated that a longer open water period (i.e., fewer months with 

sea ice) will cause the Bering and Chukchi seas to shift from predominantly benthic systems to 

pelagic ones and some studies have detected declines in benthic biomass within the northern 

Bering Sea (e.g., Moore et al. 2003, Grebmeier et al. 2006b, Mueter and Litzow 2008). As such, 

we would expect to see more pelagic fishes (such as cod) and less benthic prey (such as, sculpin 

or molluscs) in the diet of ringed seals. Although the occurrence of cod has increased, patterns 

are not as clear for benthic species. For example, while the occurrence of sculpin decreased in 

the Chukchi Sea, it actually increased in the Bering Sea. If benthic prey is becoming less 

common, perhaps the magnitude of change is not yet great enough to override seal preference or 

be detected by occurrence statistics. 

 

Inferences into how dietary changes affect ringed seals must be made with caution. We 

observed changes in the occurrence of prey, not the quantity of prey consumed and we do not 

know what quantity of prey items is necessary to meet caloric requirements. Ringed seals have a 

more general diet that includes both pelagic and benthic species than spotted seals (pelagic 

specialists) and bearded seals (benthic specialists). As such, ringed seals may be less vulnerable 

to changes in prey populations. Interestingly, the lowest frequency of occurrence of all cod,

especially Arctic cod, occurred in 1975 (Fig. 4). Seals born in 1975 and 1976 had low growth 

rates (Figs. 10 and 12); few pups were harvested in 1976 (Fig. 19), and those that were had poor 

body condition (Fig. 18). By 1977, growth rates and body condition rebounded. Hence, 

environmental conditions quickly improved or seals quickly adjusted to new conditions. 

Currently, it is unlikely that their diet is unfavorable; high growth rates, an early age at 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

54 

maturation, high pregnancy rates, and good body condition all indicate ringed seals are finding 

sufficient prey to meet their caloric requirements, whatever those might be. 

Our analyses have shown that even using frequency of occurrence our methods were 

robust enough to see differences by time, region, age, and season. In future analyses, we may be 

able to include number and size of fish eaten and combine ringed, bearded, and spotted seal diet 

data to better describe ecological changes in the pelagic and benthic systems.

Contaminants 

Metals and other elements—Metals and other elements occur naturally in the marine 

environment and levels can vary widely in Alaska depending upon regional geology. The 

normal range of variation for metals is poorly understood in marine mammals and high 

concentrations of metals may not be toxic. For example, Cd and Hg are commonly present at 

high concentrations in liver and kidney tissue of marine mammals. While Cd can be toxic at 

elevated levels, in marine mammal kidney and liver it tends to bind with metallothionein, which 

makes it less bioavailable and therefore less toxic (Groten et al. 1990, Goyer 1991). Marine 

mammals are also known for their ability to use Se to detoxify Hg and elevated Hg levels are 

usually accompanied by elevated Se levels (Koeman et al. 1975). Most studies indicate that 

element concentrations generally increase with age (see review in Northern Contaminants 

Program 2003), yet few studies have sufficient samples to analyze for the affects of age. 

Alternatively, the concentrations of some elements may decline with age and some relationships 

may be non-linear (Dehn et al. 2005). 

Ringed seals had the second lowest concentration of Cd, and Hg of the four species of ice 

seals in our studies (Table 14) with spotted seals having the lowest and ribbon seals having the 

highest. Pb levels were barely above detection limits in any species (Table 14). Our 

concentrations of total Hg in liver were lower than that of ringed seals in Canada (Dehn et al. 

2005, Riget et al. 2005,), Greenland, and Russia, but similar to seals in Norway (Riget et al. 

2005). Our Cd concentrations were lower than all the above countries including Norway (Dehn 

et al. 2005, Riget et al. 2005). 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

55 

Table 14. Geometric mean concentration, geometric standard deviations (SD), and ranges (μg/g 

or ppm wet wt) for potential metals of concern in liver from ice seals harvested in Alaska 2003–

2007. The highest concentration for each metal is in bold. 

Metal Species

Ringed Bearded Spotted Ribbon 

n 32 42 17 9

Cd Mean 1.59 2.55 0.38 3.64

SD 2.86 6.19 3.98 3.65

Range (0.17–20.80) (0.01–39.93) (0.02–6.40) (0.42–15.21)

Hg Mean 1.21 2.13 0.88 2.10

SD 3.20 4.26 4.16 4.10

Range (0.14–12.88) (0.13–28.31) (0.03–5.61) (0.41–18.06)

Pb Mean 0.04 0.04 0.04 0.04

SD 1.57 0.05 1.67 1.68

Range (0.03–0.12) (0.03–0.48) (0.03–0.22) (0.03–0.13)

Organochlorines—Compared to other ice seals species in our studies, ringed seals had 

the lowest geometric mean concentrations of ΣCHL (96.5 ng/g lipid wt), and the second lowest 

of ΣHCH levels (51.8 ng/g lipid wt), ΣDDT (129.3 ng/g lipid wt), and ΣPCB (278.7 ng/g lipid 

wt) in blubber tissue (Quakenbush and Citta 2008a, Quakenbush et al. 2009; Table 15).

Our ΣHCH, ΣCHL, ΣDDT, and ΣPCB concentrations were much lower than ringed seals 

in Canada, Norway (Weis and Muir 1997), and Russia (Nakata et al. 1997). However, direct 

comparisons can be confounded by the analysis of different OC congeners. Concentrations may 

also depend both on sex or age, so differences in mean concentrations may have more to do with 

the sex ratio or age of the seals sampled than with the location or time period. 

 Other contaminants— Polybrominated diphenyl ethers (PBDEs) have been analyzed in 

the blubber of ringed seals (Quakenbush 2007). PBDEs are chemicals widely used as flame 

retardant additives in carpets and upholstery, and in plastics used in electrical appliances, 

televisions, and computers. It is thought that PBDEs enter the food chain by being released 

slowly into the air through the life of the products that contain them (Strandberg et al. 2001). 

Although little is known about the toxicology of PBDEs, PBDEs and their congeners are 

structurally similar to PCBs and thyroid hormones. Lab studies indicate that PBDEs may disrupt 

thyroid function and neurodevelopment (Darnerud 2003, Viberg et al. 2004). Ribbon seals had 

the highest mean level of total PBDEs (16.5 ng/g wet wt) followed by spotted seals (12.4 ng/g 

wet wt) and ringed seals (5.9 ng/g wet wt); bearded seals had the lowest (3.4 ng/g wet wt) of the 

Alaska ice seal species, but all had lower levels compared to seals from other regions of the 

Arctic (Quakenbush 2007). 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

56 

Perfluorinated contaminants (PFCs) have been analyzed in the liver of ringed seals 

(Quakenbush and Citta 2008b). PFCs affect cellular function and intercellular communication; 

however, the concentrations at which PFCs become toxic to seals are unknown. PFCs are not 

lipophilic like OCs, instead they are lipophobic, and the way they are acquired and how they 

bioaccumulate are not known. Perfluorooctane sulfonate (PFOS), perfluorononanoic acid 

(PFNA), perfluorodecanoic acid (PFDA), and perfluoroundecanoic acid (PFUnDA) were 

detected in most samples (Quakenbush and Citta 2008b). When compared to other Alaskan ice 

seals, ringed seals had the highest concentrations of PFOS, PFNA, PFDA, and the second highest 

concentration of PFUnDA (Quakenbush and Citta 2008b). PFOS has been identified as the 

predominant PFC in wildlife. Studies of ringed seals in Canada (Martin et al. 2004) and 

Greenland (Bossi et al. 2005) generally find levels of PFOS twice as high as what was observed 

in ringed seals (Quakenbush and Citta 2008b). However, our mean levels of PFNA were higher. 

Because little is known about the transport mechanism, the way the different compounds are 

acquired, and how they affect seals we have no explanation for why concentrations are different 

in Alaskan ice seals or whether they are harmful.

Table 15. Geometric mean concentration, geometric standard deviations (SD), and ranges (ng/g 

or ppb wet wt) for total organochlorines in blubber from ice seals harvested in Alaska 2003–

2006. The highest concentration for each compound is in bold. 

Compound Species

Ringed Bearded Spotted Ribbon 

n 32 33 17 9 

∑ HCH Mean 51.8 14.5 104.8 93.9

SD 1.65 1.55 1.56 1.64

Range (17–150) (3–28) (35–313) (53–228)

∑ CHL Mean 96.5 104.2 193.6 338.6

SD 2.12 1.60 1.96 2.10

Range (24–342) (51–415) (38–580) (199–1979)

∑ DDT Mean 129.3 91.2 199.5 456.5

SD 1.85 1.95 2.19 2.06

Range (39–628) (26–605) (30–695) (168–1382)

∑ PCB Mean 278.7 193.0 404.1 552.0

SD 1.71 1.76 1.97 1.94

Range (92–908) (69–943) (99–1256) (231–1467)
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

57 

Disease

Brucella—In general, low prevelence of Brucella antibodies have been found in Arctic 

seal species. We identified a lower prevalence of Brucella antibodies in ringed seals in this 

study (6.4%, 3 of 47) than we did in spotted seals (16.2%, 6 of 37; Quakenbush et al. 2009) and 

ribbon seals (14.3%, 2 of 14; Quakenbush and Citta 2008a). Nielsen et al. (1996) identified 

Brucella antibodies in 4.0% (10 of 248) of ringed seals in the Canadian Arctic and Tryland et al. 

(2001) identified Brucella antibodies in 5.4% (16 of 297) of polar bears near Svalbard. In 

contrast, Zarnke et al. (2006) found a high incidence, 46.0% (46 of 100), of Brucella antibodies 

in harbor seals from the Gulf of Alaska, similar to incidence rates, 49.0% (147 of 300), observed 

in harbor seals from Scotland (Foster et al. 2002). Harbor seals experience closer contact with 

one another on their terrestrial haulouts than ringed seals, or polar bears do on sea ice and this 

may explain the higher prevalence in them. Spotted seals are closely related to harbor seals and 

use terrestrial haulouts in summer, which may bring them in closer contact with one another than 

occurs with other ice seal species, although, they did not show a higher exposure. 

Neither mortality, nor reproductive disorders were noted in any of the studies cited above 

and it is believed that Brucellosis is not a significant source of reproductive failure in seals. 

However, Foster et al. (2002) notes there is little or no data on abortion rates, so Brucellosis may 

be more important than what is currently assumed. 

PhHV-1 and -2—Our findings of 16.7% (14 of 84) for PhHV-1 antibodies and no 

antibodies for PhHV-2 (0%, 0 of 5) in ringed seals were much lower than 50% (2 of 4) for each

reported by Zarnke et al. (1997). Our sample size was much larger (84 vs. 4) for PhHV-1, which 

may explain the different results, although the sample sizes for PhHV-2 (5 vs. 4) were similar. 

Our previous study of spotted seals also reported a lower prevalence of PhHV-1 (33.3%, 12 of 

36; Quakenbush et al. 2009) than that found by Zarnke et al. (1997) who identified antibodies in 

72% (23 of 32) and antibodies of PhHV-2 in 16% (5 of 32) of spotted seals sampled near 

southeastern Kamchatka and in the Bering and Chukchi seas. 

Our findings for ribbon seals also contrasted with Zarnke et al. (1997) in that we found 

no antibodies of either PhHV-1 or 2 (Quakenbush and Citta 2008a), whereas he found antibodies 

for both in 29.2% (7 of 24) of ribbon seals sampled in the Bering Sea. More disease screening is 

necessary to verify the prevalence of PhHV-1 and -2 in ringed seals. PhHV-1 was first identified 

in 1984, when it caused the deaths of 11 harbor seal pups in the Netherlands (Osterhaus et 

al.1985). Symptoms include fever, vomiting, and diarrhea (Visser et al. 1991). Colegrove et al. 

(2005) sampled live stranded harbor seals in California and found that 3–6% of live strandings 

were primarily or secondarily attributable to PhHV-1, although in some years PhHV-1 was 

responsible for 10–20% of strandings. PhHV-2 has been detected in harbor seals from the North 

Atlantic (Harder et al. 1996) and the North Sea (Lebich et al. 1994). 

PDV and CDV— We found no antibodies for PDV (n = 82) or CDV (n = 82) in ringed 

seals (this study). We also did not find PDV or CDV antibodies in spotted seals (n = 37, n = 22), 

respectively from the Bering and Chukchi seas (Quakenbush et al. 2009). 

It is thought that PDV is circulating within Arctic species (e.g., Barrett et al. 1995, 

Duignan et al. 1997, Härkönen et al. 2006) and that harp seals (Phoca groenlandica) may be the 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

58 

major reservoir for PDV in the Arctic (Barrett et al. 1995, Duignan et al. 1997). Harp seals have 

a high prevalence of PDV antibodies (83%; 130 of 157; Duignan et al. 1997) and exhibit 

attributes conducive for maintaining a virus, such as a large population size and dense 

aggregations. In contrast to our findings, Duignan et al. (1997) found that ringed seals had a 

high prevalence rate (41%; 106 of 259), which is surprising given their dispersed population 

structure. The prevalence of antibodies was highest where ringed seal and harp seals overlap in 

range, supporting the idea that harp seals might serve as a reservoir. Harp seals are also believed 

to be the source of the 1998 PDV outbreak in the northern Europe (Heide-Jørgensen et al. 1992, 

Härkönen et al. 2006). Migrating harp seals have been observed in the North Atlantic and they 

are believed to have transferred PDV to grey seals (Halichoerus grypus), which are largely 

immune (Heide-Jørgensen et al. 1992, Barrett et al. 1995, Härkönen et al. 2006). PDV has been 

documented as persisting within grey seal populations (Barrett et al. 1995, Hammond et al. 

2005) and both the 1988 and 2002 outbreaks of PDV in harbor seals have been traced to a single 

haulout on the island of Anholt, Denmark. This haulout is notable in that both grey and harbor 

seals haul out together and mix (Härkönen et al. 2006). 

An outbreak of CDV killed thousands of Baikal seals (Phoca sibirica) in 1988 (Grachev 

et al.1989, Mamaev et al. 1995) and over 10,000 Caspian seals (Phoca caspica) in 2000 

(Kennedy et al. 2000). Both epizootics are believed to have been caused by seals coming into 

contact with terrestrial carnivores that were disease vectors. Given that ringed seals in Alaska 

rarely haul out on land, they are less likely to contact terrestrial carnivores. CDV is the dominant 

morbillivirus in polar bears making polar bears a potential vector for ringed seals hauled out on 

pack ice. Follmann et al. (1996) found morbillivirus antibodies in 35% (68 of 191) of polar 

bears from Alaska and Russia; these antibodies were later identified as antibodies for CDV 

(Garner et al. 2000). 

Zarnke et al. (2006) found a 1% (2 of 160) prevalence rate of PDV antibodies in harbor 

seals within the Gulf of Alaska. Recently, antibodies to PDV were detected in 40% (30 of 77) of 

sea otters in the eastern Aleutian Islands, Alaska Peninsula, and Kodiak Archipelago (Goldstein 

et al. 2009). However, exposure does not guarantee an epizootic. Although PDV results in high 

mortality rates in harbor seals (an outbreak of PDV in northern Europe killed over 23,000 harbor 

seals in 1998 and 30,000 in 2002; Härkönen et al. 2006), other phocids are largely immune to 

PDV. For example, grey seals are much less susceptible to PDV (Barrett et al. 1995, Härkönen 

et al. 2006) than harbor seals, only one harp seal has shown clinical disease attributed to PDV 

(Daoust et al. 1993), and there are no cases of clinical disease in ringed seals. Transmission rates 

are also affected by seal behavior, which changes seasonally. Ringed seals, however, are not 

very social and do not haul out in numbers during any time of year, thus they are not as likely to 

be susceptible to an epizootic as spotted seals, which may haul out together on gravel shoals or 

islands in summer.

Morphometrics

 Growth rate—Examination of growth rates indicated significant variability in the length 

of ringed seals over time. Seals varied from 6.2 cm shorter than expected to 19.3 cm longer than 

expected, depending upon the year in which they were born (Fig. 10). In general, seals >1 year 

of age have been growing larger since 1977. Most of the difference is in the rate of growth, not 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

59 

asymptotic length. In other words, while seals are growing longer, the main difference between 

growth curves is that seals are currently growing faster and attaining asymptotic length more 

quickly (Fig. 11). Given their age at harvest, seals >1 year of age have grown from 2.4 to 19.3 

cm longer than expected since 2000. 

As with seals >1 year of age, there are no indications that the growth of pups in recent 

years is reduced in comparison with past years (Fig. 12). Between 2000 and 2009, six of nine 

breeding seasons had pups that were larger than expected, based upon their harvest date. 

However, we must be cautious when interpreting pup growth, as changes in parturition date may 

confound measurements of length. For example, pups born in 2005 and 2007 were short given 

the date of harvest; 8.2 cm shorter than expected in 2005 and 4.9 cm shorter than expected in 

2007. However, seals >1 year of age had the highest growth rates we observed; 19.3 cm longer 

than expected in 2005 and 15.9 cm longer than expected in 2007. Furthermore, the proportion of 

pups in the harvest was over 50% in both 2005 and 2007, indicating that many pups were born 

and survived to be harvested (Fig. 19). Perhaps parturition date was delayed in 2005 and 2007, 

leading to pups that were shorter at harvest. Likewise, years with longer than average pups may 

have earlier parturition dates. 

However, some years characterized by poor growth of seals >1 year of age were also 

characterized by poor growth of pups. For example, the lowest growth rates we observed was 

for seals born in 1961, this was true for both pups and seals >1 year of age (compare Figs. 10 and 

12). All the seals sampled in 1961 were from Point Hope, in the Chukchi Sea. As such, all the 

data from pups came from Point Hope and we have no information on pup growth for the Bering 

Sea. However, none of the seals >1 year of age that were born in 1961 were sampled at Point 

Hope; hence, it is likely that 1961 was a poor year for ringed seals throughout the Bering and 

Chukchi seas. Other years included seals sampled in both the Bering and Chukchi seas and 

differences by region were undetectable. 

Seals grow rapidly for the first two or three years of age (Fig. 11) and we expect 

unfavorable conditions to affect pups and yearlings more than older seals. Hence, years with 

unfavorable conditions may affect seals born in prior years, but to a lesser extent than seals born 

in the current year. As an example, consider 1974 to 1976, a string of three years with shorter 

than expected growth (Fig. 10). Seals >1 year of age averaged 3.8 cm shorter than expected if 

they were born in 1974, 3.4 cm in 1975, and 3.6 in 1976. During this same time, pups were 11.0 

cm longer than expected in 1974, 3.3 cm shorter than expected 1975, and 4.9 cm shorter than 

expected in 1976 (Fig. 12). The proportion of pups in the harvest also decreased from 35% in 

1974, to 20% in 1975, and then to 6% in 1976, the second lowest proportion of pup ever 

observed in the harvest (Fig. 19). Hence, it is likely that low growth rates observed in seals born 

between 1974 and 1976 was mostly due to an environmental perturbation that started in 1975 

and peaked in 1976. 

It is unclear what environmental effects may lead to poor growth. Low growth rates in 

1975 and 1976 may correspond with the regime shift thought to occur in the Bering Sea in 1977 

(Miller et al. 1994). The frequency of occurrence of fish in the mid 1970s was low relative to 

other time periods, especially for Arctic cod (Fig. 4). Stirling (2002) noted years of poor ringed 

seal recruitment were associated with heavy ice conditions. During cold years, sea ice retreats 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

60 

late in spring and arrives early in fall, shortening the open water season and lowering primary 

productivity. Hence, years with heavy ice may affect the availability of prey for ringed seals. 

Growth was more variable for seals >1 year of age sampled after 1980 (Fig. 10). Some 

of the variability may be due to sampling error, as biologists worked more directly with fewer 

native seal hunters in the 1960s and 1970s. However, it is unlikely that mean growth rates would 

be consistently higher due to sampling error. 

We cannot adequately address the possibility that ringed seals consist of multiple, distinct

morphological types. A number of authors have noted that ringed seals breeding in landfast ice 

are larger and mature more slowly than seals breeding in drifting pack ice (e.g., Finley et al. 

1983, Fedoseev 2000). However, the seals in our sample are mostly harvested during open water 

periods, when distinct morphological types, if present, would be mixed. If the sample were 

clearly delineated into distinct morphological types, we would expect to see posterior 

distributions that were bimodal in our Bayesian analysis. However, the posterior distributions of 

growth parameters were unimodal, indicating that there was only one population of seals. 

Hence, if different morphological types are present, they are either rare or, perhaps there is 

substantial overlap in the growth parameters of the different morphological types. 

Body condition—In general, growth rates and body condition are expected to be 

correlated. Good conditions likely lead to longer, fatter seals. As such, using regression to 

control for length could mask changes in foraging conditions that affect both growth and blubber 

thickness simultaneously. For older seals, such simultaneous changes are not likely. Most 

growth occurs within the first few years of life, so short-term changes in prey availability (and 

blubber thickness) cannot be perfectly correlated with growth. 

For pups, we assumed that controlling for length removes variability in blubber thickness 

due to parturition date. This implicitly assumes longer pups were born earlier in the season and 

that nutritional stress leads to skinnier pups. If pups that are nutritionally stressed grow more 

slowly, but maintain constant blubber thickness, controlling for length may mask changes in 

blubber thickness by time period. 

However, after controlling for length, residual blubber thickness was not constant 

through time. Hence, it is reasonable to assume that length and blubber thickness are decoupled 

enough to identify years where foraging conditions were particularly good or bad. 

Sternal blubber thickness was less than expected in 1971 for both pups and seals >1 year 

of age. However, the perturbation associated with 1976 only affected pups. Interestingly, pups 

were extremely skinny in 1976 (Fig. 18), but adults had average blubber thickness (Fig. 15). As 

described elsewhere in this report, few pups were harvested that year, indicating that recruitment 

rates were low. The growth rate of seals born in 1976 was also lower than expected. However, 

it appears that whatever happened in 1976 primarily affected pups, not adults.

 

Comparisons with other studies are limited as most researchers examined other indices of 

body condition. Holst and Stirling (2002) examined blubber thickness in two populations of 

ringed seals in Baffin Bay, between May and July. Blubber thickness for pups was 4.4 (SD = 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

61 

1.1) in Grise Fiord and 2.4 (SD = 1.5) in Qaanaaq. Our mean, all years combined, declined from 

3.5 cm (SD = 0.87) in May to 2.7 cm (SD = 0.88) in July (Fig. 18). For seals >1 year of age, the 

average blubber thickness ranged from 3.7 to 4.4 in Baffin Bay (Holst and Stirling 2002). In our 

study, average blubber thickness declined from 3.5 cm (SD = 0.87) in May to 2.7 cm (SD = 0.88) 

in July (Fig. 13). 

Population parameters 

 

Age distribution—In general, the demographic characteristics of ringed seals in the 

Bering and Chukchi seas have changed over the last four decades. The proportion of pups in the 

harvest of ringed seals was significantly greater during the 2000s (56%) than the 1960s (14%) 

and 1970s (23%; P <0.01) and was also greater than would be expected (30%) based on previous 

observations of ringed seals throughout the Arctic (McLaren 1958, Fedoseev 1965, Smith 1973, 

Smith 1987, Holst et al. 1999, Holst and Stirling 2002, Stirling 2005). Because age ratios are 

proportional, a higher proportion of pups in the sample may indicate that adult survival 

decreased or that reproduction increased. Based upon other information, however, it is most 

likely that reproduction has increased. For example, growth rate, age of maturation, pregnancy 

rate, and blubber thickness are average or better than expected, and hunter responses to 

questionnaires indicate that ringed seal numbers have not decreased. The high proportion of 

pups in the harvest also indicates that pups survive long enough to be harvested (i.e., pups 

survive to weaning). 

Likewise, a low proportion of pups in the harvest may indicate years when reproduction 

or pup survival was low. For example, few pups were harvested in 1961, 1976, and 1984 (Fig. 

19). We also observed low growth rates for seals born in 1961 and 1976 (Figs. 10 and 12; no 

comparable data for 1984). Blubber thickness of pups (Fig. 18) and average age of maturation 

was also older in 1976 (Fig. 22; no comparable data for 1961 or 1984). As such, it appears that 

the proportion of pups in the harvest is a useful indicator of environmental conditions. However, 

we cannot determine if declines in harvested pups are due to pup production or survival. Studies 

suggest low pup production is related to heavy ice conditions (e.g., Harwood et al. 2000, Stirling 

2005) or ecosystem productivity (Holst and Stirling 2002). Pup survival may be related to snow 

depth (Ferguson et al. 2005) or rain on snow events, which increase predation pressure (Hammill 

and Smith 1991). 

Mean age of harvest—The mean age of seals in the harvest declined with time, largely 

reflecting the increasing proportion of pups. Mean age at harvest is currently lower in our study 

than what is observed elsewhere. Currently, including pups, mean age for males is 5.0 years and 

mean age for females is 4.5 years. Holst et al. (1999) examined mean ages of ringed seals in 

Hudson Bay between 1991 and 1992. In spring, the mean age was 13.9 and 14.9 years for males 

and females, respectively. In fall, the mean age declined to 9.1 and 8.7 years for males and 

females, respectively, presumably because more pups were available for harvest. At Svalbard, 

Lydersen and Gjertz (1987) found males and females had mean ages of 14.3 and 14.9 years, 

respectively, and thought younger age classes, including pups, were underrepresented in their 

sample because harvest occurred during breeding and pupping. They suspected that territorial 

males were forcing younger seals farther into marginal ice habitat, where they were harder to 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

62 

hunt. Also, pups were largely unavailable because they were in lairs and that females with pups 

are were more wary. 

Sex ratios—The sex ratio of the harvest was generally male biased for subadults and 

adult ringed seals. This was not expected, as sex ratios are more commonly near unity (e.g., 

Holst et al. 1999, Holst and Stirling 2002), or have a female bias (e.g., Lydersen and Gjertz 

1987). Most studies suggest the cost of maintaining territories reduces survival of adult males, 

thereby creating a female bias in sex ratio. Because sex ratio was calculated from harvested 

individuals, perhaps hunter bias accounts for a bias in males. However, we think this unlikely. 

Adult males and females had similar asymptotic lengths in our study. As such, hunters cannot 

target males by targeting large seals. The only time hunters can reliably distinguish males is 

during the spring, when males have darkened faces, but are likely avoided due to their “gasoline” 

smell. We did, in fact, see a decrease in the number of males harvested in spring. As such, it is 

likely that females have lower survival rates than males. We doubt this is of concern, as most 

other parameters we quantified are currently positive (e.g., high growth rates, high proportion of 

pups, high pregnancy rates) or neutral (e.g., average blubber thickness). 

We also found male bias in the number of pups harvested, albeit much smaller than that 

for subadults and adults. The male bias only existed in the 2000s, as the harvest in the 1960s 

was female biased and the harvest in the 1970s was near unity. 

Age at maturity and pregnancy rate—The average age of maturity varied significantly in 

time. The average age of maturity was highest in 1976 and 1977, 6.4 and 6.5 years of age, 

respectively (Fig. 22). In 1978, the average age of maturity significantly decreased to 5.0 years 

of age. Since 1999, the average age of maturity has been the lowest observed (3.2 years). 

We expect the average age of maturity to increase when environmental conditions are 

unfavorable or limiting and decrease when environmental conditions are favorable or not 

limiting. In effect, we expect healthy seals with unlimited resources to grow faster and larger, 

and to mature younger. As such, 1976 and 1977 were likely unfavorable years. This generally 

agrees with other analyses that indicate seals born in 1976 had lower growth rates and less 

sternal blubber. Although adults had average blubber thickness in 1976, individuals did not 

begin breeding until they were a year older on average. Since 1999, environmental conditions 

have been favorable and seals are breeding at a young age.

Female reproductive tracts were analyzed for percent pregnant at harvest. The decades 

with the lowest percentage was the 1960s (76.8%) and the 1980s (76.2%). The 1970s had the 

highest percentage at 89.1% and the 2000s were next highest at 79.5%. We have yet to examine 

annual patterns in pregnancy rate. However, pregnancy rate is currently similar to or higher than 

what was observed in past years. 

Conclusions

Our analyses show that ringed seals have been positively and negatively affected by past 

and current conditions. Currently, ringed seals are growing faster, have average blubber 

thickness, are maturing at the youngest age to date (indicating females are in a positive 

nutritional state allowing them to grow faster and become mature at an earlier age), and have the 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

63 

second highest pregnancy rate to date. These factors indicate that environmental conditions are 

currently as favorable (or better) than they were in the 1960s or 1970s. We have little data from 

the 1980s and 1990s, and cannot comment on those decades. In addition, there are more pups in 

the harvest now. Because age ratios are proportional, a higher proportion of pups in the sample 

may indicate that adult survival decreased or that reproduction increased. Based upon other 

information, however, it is most likely that reproduction has increased. For example, growth 

rate, age of maturation, pregnancy rate, and blubber thickness are average or better than 

expected, and hunter responses to questionnaires indicate that ringed seal numbers have not 

decreased. The high proportion of pups in the harvest also indicates that pups survive long 

enough to be harvested (i.e., pups survive to weaning). Sex ratios are currently male biased; 

however, this is probably not a concern as it corresponds to a period with high pregnancy rates 

and increasing numbers of pups. Levels of contaminants in ringed seals harvested in Alaska are 

lower than levels reported in Canada, Europe, and Russia, and the prevalence of diseases has 

remained stable. 

A major consideration is how these indices relate to abundance. Most of the indices we 

quantified relate to the physiology of individuals (e.g., body length or blubber thickness). While 

we can conclude that individuals are in good health, determining how individual health relates to 

population growth or abundance is more difficult. For example, individuals may exhibit high 

growth rates, early maturation, and high body condition in a low density population if 

demographics are density dependent. Clearly, inferences must be made with caution. 

In some situations, however, responsible population-level inferences can be made. The 

physiology of individuals in our sample is representative of the population and we have decades 

of data for comparison. For example, we know that the reproduction of ringed seals is currently 

robust. Pregnancy rates are high, pups are surviving to be harvested, and pups compose a large 

proportion of the harvest. Hence, ringed seals are reproducing as well as or better than they have 

since the 1960s. Blubber thickness is currently similar to what was observed in the 1970s, but 

ringed seals are growing faster and maturing younger. Hence, it is likely that they are finding 

enough food. Using these physiologically based data, the likelihood that the population is 

declining due to poor reproduction, pup survival, or starvation is very low. However, detecting 

changes in survival that affect all age classes in a similar fashion will be problematic. For 

example, if predation or overharvest decreases the abundance of all age classes equally, the 

proportion of individuals in each age class will remain the same over time and a population 

decline would go undetected. Because hunter questionnaires generally indicate that the 

availability of ringed seals has not changed over time, it is unlikely that large changes in 

abundance have occurred. At a coarse scale, we can certainly conclude that ringed seals are still 

harvested annually throughout the Bering and Chukchi seas. Smaller, more gradual changes in 

abundance will be difficult to detect with questionnaires. 

We have also provided baseline information for ringed seals and shown how indices vary 

over time. While we are primarily interested in current conditions, understanding past conditions 

allows us to put current conditions in context and make comparisons. Ringed seals were 

petitioned to be listed under the Endangered Species Act due to concerns that changing ice 

conditions may threaten population persistence. Although sea ice is declining now, the most 

significant declines in ringed seal physiological parameters to date occurred around 1961 and 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

64 

1976. We do not know what caused the perturbation in 1961, but the perturbation in 1976 may 

have been related to a regime shift in the Bering Sea, believed to occur in 1977. Following this 

shift, demersal and benthic fishes decreased, while the production of zooplankton and pelagic 

fish increased (See review in Benson and Trites 2002). Most of the information on the 1977 

regime shift comes from commercial fisheries data in the southern and central Bering Sea, which 

only partially overlaps the range of ringed seals in Alaska. While the regime shift is poorly 

understood in the northern Bering and Chukchi seas, we found evidence of physiological stress 

in ringed seals in 1976. Depressed physiological parameters rebounded in 1978, suggesting that 

conditions either improved or ringed seals quickly adapted. 

We think it reasonable to assume that changing ice conditions will affect the status of 

ringed seals; however, predicting the direction and magnitude of those effects is speculative at 

best. A longer open water season is predicted to favor pelagic fish species over benthic species 

(e.g., Grebmeier et al. 2006a, 2006b). Stirling (2002) found reduced productivity of ringed seals 

in heavy ice years, and speculated this was due to a shorter open water season and reduced 

primary productivity. As such, ringed seal productivity might be increasing as the open water 

season increases. However, Kelly et al. (2010) speculate that these benefits, if they exist, will 

eventually be outweighed by increased costs of pup predation and thermoregulation. Hence, in 

the short-term, reduced sea ice may have positive effects. If sea ice habitat changes too much, 

seals may be negatively affected in the long-term, but it is unclear when this will happen. 

Given that there are no estimates of ringed seal abundance or trend, a critical question is 

whether or not this monitoring program could detect demographic changes that are the basis for 

listing ringed seals under the Endangered Species Act. Kelly et al. (2010) predict that climate 

warming will lead to less spring snow cover, reducing the availability of subnivean habitat 

ringed seals use for pupping lairs. Specifically, pups without lairs will be exposed to high 

mortality due to freezing and predation. Such changes will likely be detectable within the 

current monitoring program. If pups have non-lethal thermoregulation costs, we will likely see 

changes in the blubber thickness of pups and declining growth rates of seals. While we cannot 

directly document survival, we can identify changes in the proportion of pups in the harvest. For 

example, 1976 was clearly characterized by very few pups in the harvest and seals born in 1976 

grew less than expected. 

However the monitoring program does have limitations. While changes in pup survival 

will likely be detectable in age ratios and growth rates, we will not know how these changes 

directly relate to abundance. As such, efforts should continue to determine how to quantify the 

abundance of ringed seals. We also do not know how sensitive our indices are; subtle changes in 

survival or reproduction may be non-detectable, yet significantly affect population growth. As 

such, changes in growth, reproduction, and age distributions may not be detected until a number 

of years after changes occur. Because there are currently large numbers of ringed seals, this is 

probably not a serious limitation. 

Recommendations

The importance of this monitoring program is difficult to overstate, and it is especially 

important because agencies have yet to overcome the logistical constraints necessary to estimate 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

65 

seal abundance in remote, ice covered waters. As such, reliable estimates of ringed seal 

abundance or population trend are lacking. This monitoring program is capable of detecting 

changes in population parameters that affect abundance. While we cannot directly assess how 

abundance is changing, we should be able to detect changes predicted to occur with warming 

climate (e.g., thermoregulatory stress and mortality of pups). Until abundance can be quantified, 

this monitoring program will provide the best information available for assessing the status of 

ringed seals in Alaskan waters. If abundance is eventually quantified, the data collected by this 

monitoring program will also provide valuable insights of the mechanisms driving changes in 

abundance. As such, we recommend this harvest-based monitoring program be continued. 

ACKNOWLEDGMENTS

This study would not be possible without the willingness of the hunters to contribute 

samples from their harvest, the support of their communities, local governments, and Tribal 

Councils. Participating communities include Barrow, Wainwright, Point Hope, Kotzebue, 

Shishmaref, Diomede, Gambell, Savoonga, and Hooper Bay. We appreciate the support from 

the North Slope Borough and the Association of Village Council Presidents. John Burns, Kathy 

Frost, Lloyd Lowry, and others were instrumental in the development of this project and its great 

value comes from their early efforts to collect and process samples, as well as archive the data. 

We thank Gay Sheffield, Letty Hughes, Anna Bryan, and Mark Nelson for assistance in field 

collection and sample processing; Juan Leon Guerrero, Heidi Isernhagen, Louise Foster, and 

Andrew Brenner assisted with processing samples in the lab, entering and error checking historic 

and recent data. Funding for collections from Little Diomede Island during 2000–2005 was 

provided by the National Science Foundation (OPP Grant No. 9910319). The majority of 

funding for sample collection and analysis since 2002 was provided by the National Marine 

Fisheries Service with partial funding in 2005 from the North Pacific Research Board. Otoliths 

and cephalopod beaks were identified by William Walker at the National Marine Mammal 

Laboratory. Invertebrates were identified by Chris Stark at the Institute of Marine Science, 

University of Alaska, Fairbanks. Marine Mammal samples were collected under NMFS Permit 

Nos. 358-1585, 358-1787. Copies of original data from Project Chariot were provided by Gary 

Shugart of the Slater Museum of Natural History at the University of Puget Sound and we thank 

Juan Leon Guerrero for assistance with entering it. We thank Jill Seymour at the University of 

Alaska for testing for Trichinella, and Elizabeth Frame at Northwest Fisheries Science Center for 

testing for toxic algae. 

LITERATURE CITED

AMERICAN SOCIETY OF MAMMALOGISTS. 1967. Standard measurements of seals. Journal of 

Mammalogy 48:459–462. 

ARNOULD, J. P. Y. 1995. Indices of body condition and body composition in female Antarctic fur 

seals (Actocephalus gazelle). Marine Mammal Science 11:301–313. 

BARRETT, T., M. BILIXENKRONE-MØLLER, G. DI GUARDO, M. DOMINGO, P. DUIGNAN, A. HALL,

L. MAMAEV, A. D. M. E. OSTERHAUS. 1995. Morbilliviruses in aquatic mammals: report 

on round table discussion. Veterinary Microbiology 44:261–265. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

66 

BECKER, P. R., S. A. WISE, B. J. KOSTER, AND R. ZEISLER. 1991. Alaska Marine Mammal Tissue 

Archival Project: revised collection protocol. U.S. Dept. Commerce, National Institute of 

Standards and Technology Laboratory, Gaithersburg, MD. 33 pp. 

BENGTSON, B. J., L. M. HIRUKI-RARING, M. A. SIMPKINS, AND P. L. BOVENG. 2005. Ringed and 

bearded seal densities in the eastern Chukchi Sea, 1999–2000. Polar Biology 28:833–

845. 

BENSON, A. J., AND A. W. TRITES. 2002. Ecological effects of regime shifts in the Bering Sea 

and eastern North Pacific Ocean. Fish and Fisheries 3:95–113. 

BLUHM, B. A., AND R. GRADINGER. 2008. Regional variability in food availability for arctic 

marine mammals. Ecological Applications 18(2) Supplement, S77–S96. 

BOSSI, R., F. F. RIGET, AND R. DIETZ. 2005. Temporal and spatial trend of perfluorinated 

compounds in ringed seal (Phoca hispida) from Greenland. Environmental Science and 

Technology 39:7416–7422. 

BURNS, J.J. 1969. Marine Mammal Report. Alaska Department of Fish and Game, PittmanRobertson Project Report. Volume X, W-17-1. 25 pp. 

BURNS, J.J., L. H. SHAPIRO, AND F. H. FAY. 1981. Relationship of marine mammal distribution, 

densities, and activities to sea ice conditions. Outer Continental Shelf Environmental 

Assessment Program, Final Report 11:489–670.

BURNHAM, K. P., AND D. R. ANDERSON. 2002. Model selection and multimodel inference, 2nd

edition. Springer, New York, NY. 

COLEGROVE, K. M., D. J. GREIG, AND F. M. D. GULLAND. 2005. Causes of live strandings of 

northern elephant seals (Mirounga angustirostris) and Pacific harbor seals (Phoca 

vitulina) along the central California coast, 1992–2001. Aquatic Mammals 31:1–10. 

CONGDON, P. 2003. Applied Bayesian modeling. John Wiley and Sons, Ltd. West Sussex, UK. 

COMISO, J. C. 2006. Arctic warming signals from satellite observations. Weather 61(3):70–76. 

DAOUST, P-Y., D. M. HAINES, J. THORSEN, P.J. DUIGNAN, AND J. R. GERACI. 1993. Phocine 

distemper in a harp seal (Phoca groenlandica) from the Gulf of St. Lawrence, Canada. 

Journal of Wildlife Diseases 29:114–117. 

DARNERUD, P.O. 2003. Toxic effects of brominated flame retardants in man and in wildlife. 

Environment International 29: 841–853. 

DEHN, L-A., G. G. SHEFFIELD, E. H. FOLLMANN, L. K. DUFFY, D. L. THOMAS, G. R. BRATTON, R.

J. TAYLOR, AND T. M. O’HARA. 2005. Trace elements in tissues of phocid seals harvested 

in the Alaskan and Canadian Arctic: influence of age and feeding ecology. Canadian 

Journal of Zoology 83:726–746. 

DEHN, L-A., E. H. FOLLMANN, D. L. THOMAS, G. G. SHEFFIELD, C. ROSA, L. K. DUFFY, AND T. M. 

O’HARA. 2006. Trophic relationships in an Arctic food web and implications for trace 

metal transfer. Science of the Total Environment 362:103–123. 

DEMASTER, D. P. 1978. Calculation of the average age of sexual maturity in marine mammals. 

Journal of the Fisheries Research Board of Canada. 35:912–915. 

DUIGNAN, P. J., O. NIELSEN, C. HOUSE, K. M. KOVACS, N. DUFFY, G. EARLY, S. SADOVE, D. J. ST.

AUBIN, B. K. RIMA, AND J. R. GERACI. 1997. Epizootiology of morbillivirus infection in 

harp, hooded, and ringed seals from the Canadian arctic and western Atlantic. Journal of 

Wildlife Diseases 33:7–19. 

EBBESMEYER, C. C., D. R. CAYAN, D. R. MCLAIN, F. H. NICHOLS, D.H. PETERSON, AND K. T.

REDMOND. 1991. 1976 step in the Pacific climate: Forty environmental changes between 

1968–1975 and 1977–1984. Pages 129–141 in J. L. Bentancourt and A. V. Tyler, eds. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

67 

Proceedings of the Seventh Annual Pacific Climate Workshop, April 1990, California 

Department of Water Resources Interagency Ecological Studies Program Technical 

Report No. 26. 

FEDOSEEV, G. A. 1965. Age and sex composition of the kill of the ringed seal (Phoca hispida 

ochotensis Pall.) as an index of the age structure of the population. Fisheries Research 

Board of Canada Translation Series No. 799 (1966). 

FEDOSEEV, G. A. 2000. Population biology of ice-associated forms of seals and their role in the 

northern Pacific ecosystems. Center for Russian Environmental Policy, Russian Marine 

Mammal Council, Moscow. 271 pp. 

FERGUSON, S. H., I. STIRLING, AND P MCLOUGHLIN. 2005. Climate change and ringed seal 

(Phoca hispida) recruitment in western Hudson Bay. Marine Mammal Science 21:121–

135. 

FINLEY, K. J., G. W. MILLER, R. A. DAVIS, AND W. R. KOSKI. 1983. A distinctive population of 

ringed seals (Phoca hispida) inhabiting the Baffin Bay pack ice. Arctic 36:162–173. 

FOSTER, G., A. P. MACMILLAN, J. GODFROID, F. HOWIE, H. M. ROSS, A. CLOECKAERT, R. J. REID,

S. BREW, I. A. P. PATTERSON. 2002. A review of Brucella sp. infection of sea mammals 

with particular emphasis on isolates from Scotland. Veterinary Microbiology 90: 563–

580. 

FOLLMANN, E. H., G. W. GARNER, J. F. EVERMANN, AND A. J. MCKEIRNAN. 1996. Serological 

evidence of morbillivirus infection in polar bears (Ursus maritimus) form Alaska and 

Russia. Veterinary Record 138:615–618. 

FROST, K. J., AND L. F. LOWRY. 1981. Ringed, Baikal and Caspian seals—Phoca hispida, Phoca 

sibirica, and Phoca caspica. Pages 29–53 in: S. H. Ridgway and R. J. Harrison, eds. 

Handbook of Marine Mammals. Vol. 2 Seals. Academic Press, New York. 

FROST, K. J., L. F. LOWRY, J. R. GILBERT, AND J.J. BURNS. 1988. Ringed seal monitoring: 

relationships of distribution and abundance to habitat attributes and industrial activities. 

Final Report Contract No. 84-ABC-00210 to USDI, Minerals Management Service, 

Anchorage, AK. 66 p + Appendices. 

GALES, R., AND D. RENOUF. 1994. Assessment of body condition of harp seals. Polar Biology 

14:381–387. 

GARLICH-MILLER, J. L., L. T. QUAKENBUSH, AND J. F. BROMAGHIN. 2006. Trends in age structure 

and productivity of Pacific walruses harvested in the Bering Strait region of Alaska, 

1952–2002. Marine Mammal Science 22: 880–896. 

GARNER, G. W,J. F. EVERMANN, J. T. SALIKI, E. H. FOLLMANN, A. J. MCKEIRNAN. 2000. 

Morbillivirus ecology in polar bears (Ursus maritimus). Polar Biology 23:474–478. 

GELMAN, A., J. B. CARLIN, H. S. STERN, AND D. B. RUBIN. 2004. Bayesian data Analysis, 2nd ed. 

Chapman and Hall/CRC, Boca Raton, FL. 

GOLDSTEIN, T., J. A. K. MAZET, V. GILL, A. M. DOROFF, K. A. BUREK, AND J. A. HAMMOND.

2009. Phocine distemper virus in northern sea otters in the Pacific Ocean, Alaska, USA. 

Emerging Infectious Diseases 15(6):925–927. 

GOYER, R. A. 1991. Toxic effects of metals. Pages 634–638 in M. O. Amdur, J. Doull, and C. 

D. Klassen, eds. The Basic Science of Poisons. Pergammon Press, NY.

GRACHEV, M. A., V. P. KUMAREV, L. V. MAMAEV, V. L. ZORIN, L. V. BARANOVA, N. N.

DENIKINA, S. I. BELIKOV, E. A. PETROV, V. S. KOLESNIK, R. S. KOLESNIK, V. M.

DOROFEEV, A. M. BEIM, V. N. KUDELIN, F. G. NAGIEVA, AND V. N. SIDOROV. 1998. 

Distemper virus in Baikal seals. Nature 338:209. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

68 

GREBMEIER, J. M.,J. E. OVERLAND, S. E. MOORE, E. B. FARLEY, E. C. CARMACK, L. W. COOPER,

K. E. FREY, J. H. HELLE, F. A. MC LAUGHLIN, AND S. L. MCNUTT. 2006a. A major 

ecosystem shift in the northern Bering Sea. Science 311:1461–1463. 

GREBMEIER, J. M., L. W. COOPER, H. M. FEDER, AND B. I SIRENKO. 2006b. Ecosystem dynamics 

of the Pacific-influenced northern Bering and Chukchi seas in the Amerasian Arctic. 

Progress in Oceanography 71:331–361. 

GROTEN, J. P., E.J. SINKELDAM, J. B. LUTEN, AND P.J. VAN BLADEREN. 1990. Comparison of the 

toxicity of inorganic and liver-incorporated cadmium: A 4-wk feeding study in rats. 

Chemical Toxicology 28(6):435–441. 

HAMMILL, M. O., T. G. SMITH. 1991. The role of predation in the ecology of the ringed seal in 

Barrow Strait, Northwest Territories, Canada. Marine Mammal Science 7:123–135. 

HAMMOND, J. A., P. P. POMEROY, A. J. HALL, AND V. J. SMITH. 2005. Identification and realtime PCR quantification of phocine distempervirus from two colonies of Scottish grey 

seals in 2002. Journal of General Virology 86:2563–2567. 

HARDER, T. C., M. HARDER, H. W. VOS, K. KULONEN, S. KENNEDY-STOSKOPF, B. LIESS, M. J. G.

APPEL AND A. D. M. E. OSTERHAUS. 1996. Characterization of phocid herpesviruses 

type-1 and type-2 as putative α- and γ-herpesviruses of North American and European 

pinnipeds. Journal of General Virology 77:27–35. 

HARDY, M. H., E. ROFF, T. G. SMITH, AND M. RYG. 1991. Facial skin glands of ringed and grey 

seals, and their possible function as odoriferous organs. Canadian Journal of Zoology 

69:189–200. 

HÄRKÖNEN, T., R. DIETZ, P. REIJNDERS, J. TEILMANN, K. HARDING, A. HALL, S. BRASSEUR, U.

SIEBERT, S. J. GOODMAN, P. D.JEPSON, T. DAU RASMUSSEN, P. THOMPSON. 2006. The 

1988 and 2002 phocine distemper virus epidemics in European harbour seals. Diseases 

of Aquatic Organisms 68:115–130. 

HARRISON, R. J., AND G. L. KOOYMAN. 1968. General physiology of the pinnipedia. Pages 211–

296 in: R. J. Harrison et al., eds. The Behavior and Physiology of Pinnipeds. AppletonCentury-Crofts, New York, NY. 

HARWOOD, L. A., T. G. SMITH, AND H. MELLING. 2000. Variation in reproduction and body 

condition of the ringed seal (Phoca hispida) in Western Prince Albert Sound, NT, 

Canada, as assessed through a harvest-based sampling program. Arctic 53(4):422–431. 

HEIDE-JØRGENSEN M.-P., T. HÄRKÖNEN, R. DIETZ, AND P. M. THOMPSON. 1992. Retrospective 

of the 1988 European seal epizootic. Diseases of Aquatic Organisms 13:37–62. 

HEWER, H. R. 1960. Age determination of seals. Nature 187:959–960. 

HOLST, M. and I. STIRLING. 2002. A comparison of ringed seal (Phoca hispida) biology on the 

east and west sides of the North Water Polynya, Baffin Bay. Aquatic Mammals 28: 221–

230. 

HOLST, M., I. STIRLING and W. CALVERT. 1999. Age structure and reproductive rates of ringed 

seals (Phoca hispida) on the northwestern coast of Hudson Bay in 1991 and 1992. 

Marine Mammal Science 15:1357–1364. 

JOHNSON, M. L., C. H. FISCUS, B. T. OSTENSON, AND M. L. BARBOUR. 1966. Marine mammals. 

Pages 877–924 in: N.J. Wilimovsky and J. N. Wolfe, eds. Environment of the Cape 

Thompson region, Alaska. U.S. Atomic Energy Commission, Oak Ridge, TN. 

KELLY, B. P., J. L. BENGTSON, P. L. BOVENG, M. F. CAMERON, S. P. DAHLE, J. K.JANSEN, E. A.

LOGERWELL, J. E. OVERLAND, C. L. SABINE, G. T. WARING, AND J. M. WILDER. 2010. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

69 

Status review of the ringed seal (Phoca hispida). U.S. Department of Commerce, NOAA 

Technical Memorandum NMFS-AFSC-212. 250 pp. 

KENNEDY, S. 1998. Morbillivirus infections in aquatic mammals. Journal of Comparative 

Physiology 119:201–225. 

KENNEDY, S., T. KUIKEN, P. D.JEPSON, R. DEAVILLE, M. FORSYTH, T. BARRETT, M. W. G. VAN 

DE BILDT, A. D. M. E., OSTERHAUS, T. EYBATOV, C. DUCK, A. KYDYRMANOV, I.

MITROFANOV, AND S. WILSON. 2000. Mass die-off of Caspian seals caused by canine 

distemper virus. Emerging Infectious Diseases 6:637–645. 

KOEMAN, J. H., W. S. M. VAN DE VEN, J. J. M. DE GOEIJ, P.S. TJIOE, AND J.L. VAN HAAFTEN. 

1975. Mercury and selenium in marine mammals and birds. Science of the Total 

Environment 3:279–287. 

LEBICH, M., T. C. HARDER, H. R. FREY, I. K. G. VISSER, A. D. M. E. OSTERHAUS, AND B. LIESS. 

1994. Comparative immunological characterization of type-specific and conserved B cell 

epitopes of pinniped, felid and canid herpesviruses. Archives of Virology 136:335–347. 

LYDERSEN, C., AND I. GJERTZ. 1987. Population parameters of ringed seals (Phoca hispida 

Schreber, 1775) in the Svalbard area. Canadian Journal of Zoology 65:1021–1027. 

MACMILLAN, A. 1992. Conventional serological tests. Pages 153–197 in: K. Nielsen and J. R. 

Duncan (eds.), Animal brucellosis. CRC Press, Boca Raton, FL.

MARTIN, J.W., SMITHWICK, M.M., BRAUNE, B.M., HOEKSTRA, P.F., MUIR, D.C.G., AND MABURY,

S., 2004. Identification of long-chain perfluorinated acids in biota from the Canadian 

Arctic. Environmental Science and Technology 38:373–380. 

MAMAEV, L. V., N. N. DENIKINA, S. I. BELIKOV, V. E. VOLCHKOV, I. K. G. VISSER, M. FLEMING,

C. KAI, T. C. HARDER, B. LIESS, A. D. M. E. OSTERHAUS, T. BARRETT. 1995. 

Characterization of morbilliviruses isolated from Lake Baikal seals (Phoca sibirica). 

Veterinary Microbiology 44:251–259. 

MANSFIELD, A. W., AND H. F. FISHER. 1960. Age determination in the harbour seal, Phoca 

vitulina L. Nature 186: 92. 

MCLAREN, I. A. 1958. The biology of the ringed seal (Phoca hispida Schreber) in the eastern 

Canadian Arctic. Fisheries Research Board of Canada Bulletin No. 118. 97 pp. 

MCLAREN, I. A. 1993. Growth in pinnipeds. Biological Review 68:1–79. 

METHOD 1630. EPA-821-R-01-020. 2001. Methyl mercury in water by distillation, aqueous 

ethlyation, purge and trap, and CVAFS. U.S. Environmental Protection Agency, Office 

of Water, Office of Science and Technology, Washington, D.C. 

MILLER, A. J., D. R. CAYAN, T. P. BARNETT, N. E. GRAHAM and J. M. OBERHUBER. 1994. The 

1976–77 climate shift of the Pacific Ocean. Oceanography 7:21–26. 

MILLER, W. G., L. G. ADAMS, T. A. FICHT, N. F. CHEVILLE, J. B. PAYEUR, D. R. HARLEY, C.

HOUSE, AND S. H. RIDGWAY. 1999. Brucella-induced abortions and infections in 

bottlenose dolphins (Tursiops truncatus). Journal of Zoo and Wildlife Medicine 30:100–

110. 

MOORE, S. E.,J. M. GREBMEIER, AND J. R. DAVIES. 2003. Gray whale distribution relative to 

forage habitat in the northern Bering Sea: current conditions and retrospective summary. 

Canadian Journal of Zoology 81:734–742. 

MOULTON, F. D., W. J. RICHARDSON, T. L. MCDONALD, R. E. ELLIOTT, AND M. T. WILLIAMS. 

2002. Factors influencing local abundance and haulout behavior of ringed seals (Phoca 

hispida) on landfast ice of the Alaskan Beaufort Sea. Canadian Journal of Zoology

80:1900–1917. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

70 

MUETER, F. J. and M. A. LITZOW. 2008. Sea ice retreat alters the biogeography of the Bering Sea 

Continental Shelf. Ecological Applications 18:309–320. 

NAKATA, H., S. TANABE, R. TATSUKAWA, Y. KOYAMA, N. MIYAZAKI, S. BELIKOV, AND A.

BOLTUNOV. 1998. Persistent organochlorine contaminants in ringed seals (Phoca hispida) 

from the Kara Sea, Russian Arctic. Environmental Toxicology and Chemistry, Vol. 

17(9):1745–1755. 

NIEBAUER, H. J. 1980. Sea ice and temperature fluctuations in the eastern Bering Sea and the 

relationship to meteorological fluctuations. Journal of Geophysical Research 85:7505–

7515. 

NIEBAUER, H. J. 1983. Multiyear sea ice variability in the eastern Bering Sea: An update. Journal 

of Geophysical Research 88:2733–2742. 

NIEBAUER, H. J. 1988. Effects of El Niño-Southern Oscillation and North Pacific weather 

patterns on interannual variability in the subarctic Bering Sea. Journal of Geophysical 

Research 93:5051–5068. 

NEILSEN, O., K. NIELSEN, AND R. E. A. STEWART. 1996. Serologic evidence of Brucella spp. 

exposure in Atlantic walruses (Odobenus rosmarus rosmarus) and ringed seals (Phoca 

hispida) of Arctic Canada. Arctic (49)4:383–386. 

NORTHERN CONTAMINANTS PROGRAM. 2003. Canadian Arctic contaminants assessment report II: 

Contaminant levels, trends, and effects in the biological environment. Minister of Public 

Works and Government Service Canada, Ottawa, Canada.

OSTERHAUS, A. D. M. E., H. YANG, H. E. M. SPIJKERS, J. GROEN,J. S. TEPPEMA, AND G. VAN 

STEENIS. 1985. The isolation and partial characterization of a highly pathogenic 

herpesvirus from the harbor seal (Phoca vitulina). Archives of Virology 86:239–251. 

PARSONS, J. L. 1977. Metabolic studies on ringed seals (Phoca hispida). MS thesis, University of 

Guelph, Guelph, Canada. 

QUAKENBUSH, L. T. 2007. Polybrominated diphenyl ether compounds in ringed, bearded, 

spotted, and ribbon seals from the Alaskan Bering Sea. Baseline/Marine Pollution 

Bulletin 54:226–246. 

QUAKENBUSH, L. T., AND J.J. CITTA. 2008a. Biology of the ribbon seal in Alaska. Unpublished 

report to NMFS. 45 pp. 

QUAKENBUSH, L. T., AND J.J. CITTA. 2008b. Perfluorinated contaminants in ringed, bearded, 

spotted, and ribbon seals from the Alaskan Bering and Chukchi seas. Marine Pollution 

Bulletin 56:1802–1814. 

QUAKENBUSH, L. T., J. J. CITTA, AND J. A. CRAWFORD. 2009. Biology of the spotted seal. 

Unpublished report to NMFS. 66 pp. 

RAFTERY, A. E., AND S. M. LEWIS. 1995. The number of iterations, convergence diagnostics and 

generic Metropolis algorithms. In Practical Markov Chain Monte Carlo (W.R. Gilks, 

D.J. Spiegelhalter and S. Richardson, eds.). London, U.K.: Chapman and Hall. 

RAMSEY, F. L., AND D. W. SCHAFER. 2002. The statistical sleuth: A course in methods of data 

analysis. Second edition. Duxbury, Pacific Grove, CA, USA. 

RIGET, F., D. MUIR, M. KWAN, T. SAVINOVA, M. NYMAN, V. WOSHNER, AND T. O’HARA. 2005. 

Circumpolar pattern of mercury and cadmium in ringed seals. Science of the Total 

Environment 351–352:312–322. 

RIGOR, I. G., AND J. M. WALLACE. 2004. Variations in the age of Arctic sea-ice and summer seaice extent. Geophysical Research Letters, Vol. 31, L09401, doi:10.1029/2004GL019492. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

71 

ROBERTSON, J. L., R. M. RUSSELL, H. K. PREISLER, AND N. E. SAVIN. 2007. Bioassays with 

arthropods, 2nd Edition. CRC Press. 224 pp. 

RYG, M., C. LYDERSEN, N. H. MAKUSSEN, T. G. SMITH, AND N. A. ORISLAND. 1990a. Estimating 

the blubber content of phocid seals. Canadian Journal of Fisheries and Aquatic Sciences 

47:1223–1227. 

RYG, M., T. G. SMITH, AND N. A. ORISLAND. 1990b. Seasonal changes in body mass and body 

composition of ringed seals (Phoca hispida) on Svalbard. Canadian Journal of Zoology 

68:470–475. 

RYG, M., Y. SOLBERG, C. LYDERSEN, AND T. G. SMITH. 1992. The scent of rutting male ringed 

seals (Phoca hispida). Journal of Zoology, London 226:681–689. 

SALIKI, J. T., AND T. W. LEHENBAUER. 2001. Monoclonal antibody-based competitive enzymelinked immunosorbent assay for detection of morbillivirus antibody in marine mammal 

sera. Journal of Clinical Microbiology 39:1877–1881. 

SAS Institute Inc. 2004. SAS/STAT 9.1 User’s Guide. Cary, NC, USA. 

SCHNUTE, J. 1981. A versatile growth model with statistically stable parameters. Canadian 

Journal of Fisheries and Aquatic Sciences 38:1128–1140. 

SERREZE, M. C., M. M. HOLLAND, AND J. STROEVE. 2007. Perspectives on the Arctic’s shrinking 

sea-ice cover. Science 315:1533–1536. 

SIMPSON, E. H. 1949. Measurement of diversity. Nature (London) 163:688.

SINCLAIR, E. H., L. S. VLIETSTRA, D. S. JOHNSON, T. K. ZEPPELIN, G. V. BYRD, A. M. SPRINGER,

R. R. REAM, AND G. L. HUNT JR. 2008. Patterns in prey use among fur seals and seabirds 

in the Pribilof Islands. Deep-Sea Research II 55:1897–1918. 

SKALSKI, J. R., K. E. RYDING, AND J.J. MILLSPAUGH. 2005. Wildlife demography: Analysis of 

sex, age, and count data. Elsevier Academic Press. San Diego, California, USA. 656 pp. 

SMITH, T. G. 1973. Population dynamics of the ringed seal in the Canadian eastern Arctic. 

Fisheries Research Board of Canada Bulletin No. 181. 55 pp. 

SMITH, T. G. 1987. The ringed seal, Phoca hispida, of the Canadian Western Arctic. Canadian 

Bulletin of Fisheries and Aquatic Sciences 216: 81pp. 

SPIEGELHALTER, D. J., N. G. BEST, B. P. CARLIN , AND A. VAN DER LINDE. 2002. Bayesian 

measures of model complexity and fit (with discussion). Journal of the Royal Statistical 

Society, Series B. 64:583–640. 

SPIEGELHALTER, D., A. THOMAS, N. BEST, AND D. LUNN. 2003. WinBUGS user manual, version 

1.4. Available online at: http://www.mrc-bsu.cam.ac.uk/bugs/ winbugs/manual14.pdf. 

STEWART, R. E. A., B. E. STEWART, I. STIRLING, E. STREET. 1996. Counts of growth layer groups 

in cementum and dentine in ringed seals (Phoca hispida). Marine Mammal Science 

12:383–401. 

STIRLING, I. 2002. Polar bears and seals in the eastern Beaufort Sea and Amundsen Gulf: a 

synthesis of population trends and ecological relationships over three decades. Arctic 

55(Supplement): 59–76. 

STIRLING, I. 2005. Reproductive rates of ringed seals and survival of pups in northwestern 

Hudson Bay, Canada, 1991–2000. Polar Biology 28:381–387. 

STRANDBERG, B., N. G. DODDER, I. BASU, AND R.A. HITES. 2001. Concentrations and spatial 

variations of polybrominated diphenyl ethers and other organohalogen compounds in 

Great Lakes air. Environmental Science and Technology 46:745–755. 
Quakenbush, Citta, and Crawford. 2011. The biology of the ringed seal, 1960–2010 

72 

STROEVE, J., M. SERREZE, S. DROBOT, S. GEARHEARD, M. M. HOLLAND, J. MASLANIK, W. MEIER,

AND T. SCAMBOS. 2008. Arctic sea ice extent plummets in 2007. Eos Transactions, 

American Geophysical Union 89:13–14. 

TIKHOMIROV, E. A. 1966. On the reproduction of the seals belonging to the family Phocinae in 

the North Pacific. Zoological Journal 45:275–281. FRBC Translation No. 1889. 

TRENBERTH, K. E. 1990. Recent observed interdecadal climate changes in the Northern 

Hemisphere. American Meteorological Society 71(1):988–993. 

TRIPPEL, E. A. AND H. H. HARVEY. Comparison of methods used to estimate age and length of 

fishes at sexual maturity using populations of white sucker (Catostomus commersoni). 

Canadian Journal of Fisheries and Aquatic Sciences 48:1446–1459. 

TRYLAND, M., A. E. DEROCHER, Ø. WIIG, AND J. GODFROID. 2001. Brucella sp. antibodies in 

polar bears from Svalbard and the Barents Sea. Journal of Wildlife Diseases 37:523–531. 

VIBERG, H., FREDRIKSSON, A., AND ERIKSSON, P. 2004. Investigations of strain and/or gender 

differences in developmental neurotoxic effects of polybrominated diphenyl ethers in 

mice. Toxicological Sciences 81:344–353. 

VISSER, I. K. G., J. S. TEPPEMA, AND A. D. M. E. OSTERHAUS. 1991. Virus infections of seals 

and other pinnipeds. Reviews in Medical Microbiology 2:105–114. 

WEIS, I. M., AND D.C. G. MUIR. 1997. Geographical variation of persistent organochlorine 

concentrations in blubber of ringed seal (Phoca hispida) from the Canadian Arctic: 

univariate and multivariate approaches. Environmental Pollution 96(3):321–333. 

Wheeler, M. W., R. M. PARK, AND J. A. BAILER. 2006. Comparing median lethal concentration 

values using confidence interval overlap or ratio tests. Environmental Toxicology and 

Chemistry 25:1441–1444. 

WILIMOVSKY, N. J., AND J. N. WOLFE, EDITORS. 1966. Environment of the Cape Thompson 

region, Alaska. United States Atomic Energy Commission. Washington, D.C., USA. 

1250 pp. 

WOSHNER, V.M., O’HARA, T.M., BRATTON, G.R., SUYDAM, R.S. AND BEASLEY, V.R. 2001a. 

Concentrations and interactions of selected essential and non-essential elements in 

bowhead and beluga whales of Arctic Alaska. Journal of Wildlife Diseases 37:693–710. 

WOSHNER, V.M., O’HARA, T.M., BRATTON, G.R. AND BEASLEY, V.R. 2001b. Concentrations and 

interactions of selected essential and non-essential elements in ringed seals and polar 

bears of Arctic Alaska. Journal of Wildlife Diseases 37:711–721. 

ZARNKE, R. L., T. C. HARDER, H. W. VOS,J. M. VER HOEF, AND A.D.M.E. OSTERHAUS. 1997. 

Serologic survey for phocid herpesvirus-1 and -2 in marine mammals from Alaska and 

Russia. Journal of Wildlife Diseases 33:459–465. 

ZARNKE, R. L., J. T. SALIKI, A. P. MACMILLAN, S. D. BREW, C. E. DAWSON, J. M. VER HOEF, K. J.

FROST, AND R. J. SMALL. 2006. Serologic survey for Brucella spp., phocid herpesvirus1, phocid herpesvirus-2, and phocine distemper virus in harbor seals from Alaska, 1976–

1999. Journal of Wildlife Diseases 42:290–300.