Frontiers | Causes of Mortality in a Harbor Seal (Phoca vitulina) Population at Equilibrium

Frontiers | Causes of Mortality in a Harbor Seal (Phoca vitulina) Population at Equilibrium
ORIGINAL RESEARCH article
Front. Mar. Sci.
, 13 May 2020
Sec. Marine Megafauna
Volume 7 - 2020 |
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Frontiers in Marine Science
Marine Megafauna
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Alastair Martin Mitri Baylis
South Atlantic Environmental Research Institute, Falkland Islands
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Elizabeth McHuron
University of Washington, United States
Peter Douglas Shaughnessy
South Australian Museum, Australia
Mauricio Seguel
University of Georgia, United States
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ORIGINAL RESEARCH article
Front. Mar. Sci.
, 13 May 2020
Sec. Marine Megafauna
Volume 7 - 2020 |
Causes of Mortality in a Harbor Seal (
Phoca vitulina
) Population at Equilibrium
Elizabeth A. Ashley
Jennifer K. Olson
Tessa E. Adler
Stephen Raverty
Eric M. Anderson
5,3
Steven Jeffries
Joseph K. Gaydos
1.
The SeaDoc Society, UC Davis School of Veterinary Medicine, Karen C. Drayer Wildlife Health Center, Eastsound, WA, United States
2.
The Whale Museum, Friday Harbor, WA, United States
3.
Friday Harbor Laboratories, University of Washington, Friday Harbor, WA, United States
4.
Animal Health Centre, British Columbia Ministry of Agriculture, Abbotsford, BC, Canada
5.
Ecological Restoration Program, British Columbia Institute of Technology, Burnaby, BC, Canada
6.
Marine Mammal Investigations, Washington Department of Fish and Wildlife, Tacoma, WA, United States
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Abstract
The harbor seal (
Phoca vitulina richardii
) population in the Salish Sea has been at equilibrium since the mid-1990s. This stable population of marine mammals resides relatively close to shore near a large human population and offers a novel opportunity to evaluate whether disease acts in a density-dependent manner to limit population growth. We conducted a retrospective analysis of harbor seal stranding and necropsy findings in the San Juan Islands sub-population to assess age-related stranding trends and causes of mortality. Between January 01, 2002 and December 31, 2018, we detected 882 harbor seals that stranded and died in San Juan County and conducted necropsies on 244 of these animals to determine primary and contributing causes of death. Age-related seasonal patterns of stranded animals were evident, with pups found in the summer, weaned pups primarily recovered during fall, and adults and sub-adults recovered in summer and fall. Pups were the most vulnerable to mortality (64% of strandings). Pups predominantly died of nutritional causes (emaciation) (70%), whereas sub-adults and adults presented primarily with clinical signs and gross lesions of infectious disease (42%) and with non-anthropogenic trauma (27%). Primary causes of weaned pup mortality were distributed equally among nutritional, infectious, non-anthropogenic trauma, and anthropogenic trauma categories. Nutritional causes of mortality in pups were likely related to limitations in mid- and late-gestational maternal nutrition, post-partum mismothering, or maternal separation possibly related to human disturbance. Infectious causes were contributing factors in 33% of pups dying of nutritional causes (primarily emaciation–malnutrition syndrome), suggesting an interaction between poor nutritional condition and enhanced susceptibility to infectious diseases. Additional primary causes of harbor seal mortality were related to congenital disorders, predation, human interaction, and infections, including zoonotic and multidrug-resistant pathogens. Bottom-up nutritional limitations for pups, in part possibly related to human disturbance, as well as top-down predatory influences (likely under-represented through strandings) and infectious disease, are important regulators of population growth in this stable, recovered marine mammal population.
Introduction
Carrying capacity is a density-dependent phenomenon shaped by the interdependent relationships between consumers and the finite resources that control their population growth (
del Monte-Luna et al., 2004
). For abundant and stable populations, growth is limited by effects on reproduction and survivorship (
Fowler, 1981
). In birds and mammals, especially those with low reproductive rates and long lifespans, infection, starvation, and predation can act independently or synergistically in a density-dependent manner to limit growth in populations near carrying capacity (
Leader-Williams, 1982
Sinclair, 1985
Sullivan, 1989
Goss-Custard et al., 2002
Benskin et al., 2009
). Across vertebrate taxa, juveniles appear to be the age class most susceptible to density-dependent mortality for populations at carrying capacity (
Guinness et al., 1978
Sullivan, 1989
Linnell et al., 1995
). Although it is well accepted that disease is an important factor that can control wild population status and growth (e.g.,
May and Anderson, 1979
Deem et al., 2001
), few studies have assessed cause-specific mortality in wild animal populations at carrying capacity.
Harbor seals (
Phoca vitulina
) are small phocids distributed along the temperate coastal regions of Asia, Europe, and North America. While infectious diseases are well documented in harbor seals, few reports detail causes of mortality in populations at carrying capacity. Even a major epizootic caused by an influenza virus (A/Seal/Mass/1/80 H7N7) that killed hundreds of seals along the New England coast (United States) in 1979 had a conspicuous local geographic effect but no apparent population-level impact (
Geraci et al., 1982
). In contrast, the 1988 and 2002 phocine distemper virus epizootics in Europe killed 23,000 and 30,000 harbor seals, respectively, with estimated mortality as high as 57–66% in some populations (
Härkönen et al., 2006
). In some locations, predation may regulate harbor seal populations. For example, a major decline in harbor seals in the western Gulf of Alaska has been attributed to increased predation by killer whales (
Orcinus orca
) (
Springer et al., 2003
), though this claim has been debated (
DeMaster et al., 2006
). On Sable Island, Nova Scotia (Canada), shark predation was a significant cause of mortality in harbor seal pups and adults and contributed to a decline in the productivity of this small, localized population (
Lucas and Stobo, 2000
).
Within the Salish Sea, a 16,925 km
inland sea shared by Washington (United States) and British Columbia (Canada) (
Gaydos et al., 2008
), the harbor seal population (totaling around 50,000 individuals) has been at equilibrium for over two decades (
Jeffries et al., 2003
DFO, 2010
Majewski and Ellis, 2019
). Pre-exploitation harbor seal population size in the Salish Sea is unknown, but after the cessation of bounty programs in the early 1960s and the adoption of protective measures in the early 1970s, harbor seal numbers on both sides of the international border increased exponentially until reaching presumed carrying capacity in the mid-1990s. These populations have remained at equilibrium to date.
This stable population of marine mammals that resides relatively close to shore and near large human populations offers a novel opportunity to evaluate mortality in a population at carrying capacity to better understand how disease could limit population growth. We conducted a retrospective analysis of harbor seal stranding data and necropsy findings in the San Juan Islands sub-population to assess age-related stranding trends and causes of mortality. San Juan County, Washington is located in the center of the Salish Sea, is comprised entirely of islands, has nearly 150 haul-out sites used by harbor seals (
Jeffries et al., 2000
), and has one of the highest harbor seal densities within this inland sea (
Jeffries et al., 2003
).
Materials and Methods
Study Site and Sub-Population
San Juan County (SJC), Washington is comprised of more than 400 rocks and islands with elevations above mean high tide. The county’s land and ocean occupy 450 km
and 1,160 km
, respectively
. Harbor seals found in SJC are part of Washington’s Inland Stock, specifically the Northern Inland Waters sub-stock (
Huber et al., 2012
). Aerial surveys were used to count harbor seals in SJC as previously described in
Jeffries et al. (2003)
. Aerial surveys were flown 2 h before to 2 h after low tide during the pupping season when the maximum numbers of animals were hauled out. All known haul-out sites were surveyed, and potential new sites were examined on each survey. A standardized correction factor was applied to correct for the proportion of the population not ashore during the survey.
Carcass Collection and Necropsy
The SJC Marine Mammal Stranding Network is authorized by the United States National Oceanic and Atmospheric Administration, National Marine Fisheries Service to respond to stranded marine mammals in SJC (Permit #18786). Members of the public and field biologists typically report strandings, and network personnel recover carcasses. We analyzed harbor seal stranding and necropsy data from January 01, 2002 to December 31, 2018. Stranding response, necropsy effort, and necropsy procedures were consistent over the study period. Cases used in this study included dead stranded animals or animals that stranded live, were admitted to rehabilitation, and then died or were euthanized (
= 882). Data collected for all recovered carcasses included the date, time, and coordinates of the stranding, age class, sex, weight, axillary girth, straight body length, body condition, postmortem condition, and evidence of human interaction (
Geraci and Lounsbury, 2005
). Complete necropsies were performed for all seals found in suitable postmortem condition (carcass code 2 or 3;
Geraci and Lounsbury, 2005
) to determine cause of death and to document health and natural history findings. Briefly, external examinations were performed on fresh, chilled or frozen and thawed carcasses. While sample collection varied based on lesions noted grossly, a standard set of tissues were systematically collected and preserved in 10% neutral buffered formalin for microscopic examination. If present, these included, but were not limited to: adrenal gland, bladder, brain (cerebellum, cerebrum, and brain stem), diaphragm, eye, heart, large and small intestine, kidney, liver, lung, lymph nodes, skeletal muscle, skin, spleen, testicle, thymus, thyroid, tongue, trachea, umbilicus, and uterus. Samples also were placed fresh in sterile packs and frozen for ancillary testing. Aerobic bacteriology was routinely performed and virology if histopathology warranted. As previously described (
Ashley et al., 2020
), liver was collected from a subset of animals and tested for trace elements. Feces were collected for biotoxins screening as previously described (
Lefebvre et al., 2016
), macroscopic metazoan parasites were identified to genus or species, and age for some sub-adult and adult seals was determined by cementum analysis of canine teeth. Histopathology and laboratory testing were conducted at the British Columbia Ministry of Agriculture, Animal Health Center (Abbotsford, BC, Canada). Because all harbor seals were dead prior to inclusion in this study, an Institutional Animal Care and Use Committee protocol was not required by the UC Davis Office of Research for this work.
Age and Cause of Death Classifications
As previously described (
Lambourn et al., 2013
), harbor seals were classified as pups (<2 months), weaned pups (2–12 months), sub-adults (12–48 months), or adults (>48 months). Pups were considered weaned if they (1) had a standard length >90 cm; and/or (2) stranded after October 1 of their first year (
Geraci and Lounsbury, 2005
). Non-pups were considered adults if they (1) had a standard length >150 cm, (2) were greater than 4 years old based on cementum analysis of a canine tooth, or (3) were females that were pregnant or showed evidence of past reproduction.
Two authors (JG and SR) collaboratively assigned cause of death for each animal using initial stranding reports, gross photographs of lesions, necropsy notes, histopathology, and ancillary diagnostic results. For each animal, we determined the most likely proximate (inciting) cause of death, defined as the disease, disorder, or injury that initiated the animal’s decline and subsequent death. Classifications for proximate cause of death included: congenital; infectious (e.g., bacteria, fungi, and viruses); metabolic; neoplastic; nutritional; parasitic (e.g., metazoan and protozoan); reproductive; non-anthropogenic trauma; anthropogenic trauma; or unknown (
Table 1
). These categories were adapted from the DAMNIT-V classification system used in veterinary medicine (
Lorenz, 2009
Huggins et al., 2015
). The same classification scheme was used to identify most likely contributing (secondary and tertiary) causes of death when observed. If an animal was humanely euthanized or died incidentally during rehabilitation, cause of death was assigned based on the pre-existing condition that necessitated euthanasia or rehabilitation. Where possible, we provided additional details on the specific etiology or cause of disease (or death) for each case.
TABLE 1
Mortalities by age class
Cause of death
Diagnoses (in order of prevalence within cause of death category)
Pups
Weaned pups
Sub-adults
Adults
Congenital
Palatoschisis; facial deformity; stillbirth
Infectious
Pneumonia; encephalitis; peritonitis; septicemia; etc.
12
18
Metabolic
Ammonium urate urolithiasis; hydronephrosis
Neoplastic
Spindle cell tumor
Nutritional
Malnutrition
110
Parasitic
Verminous pneumonia
Reproductive
Dystocia; perinatal asphyxiation
Trauma (anthropogenic)
Propeller strikes; gunshot
Trauma (non-anthropogenic)
Predation; intraspecific aggression; esophageal impaction
21
10
10
Undetermined
Totals
157
35
12
40
Causes of death for harbor seals necropsied between 2002 and 2018 in San Juan County, Washington.
Statistical Analyses
Analyses were performed with R v3.3.3 (R Core Team 2017) using an α-level of 0.05. To analyze seasonal variation in frequency of mortality by age class for all stranded harbor seals, we summarized data by season: winter (December–February); spring (March–May); summer (June–August); and fall (September–November). We performed the chi-square goodness-of-fit test to assess sex bias within each age class for all stranded harbor seals (
= 388 stranded animals with known age and sex). Assuming the harbor seal population has an even (1:1) sex ratio, we used 100 as the expected frequency of males per 100 females in each age class of stranded animals.
We also performed the chi-square goodness-of-fit test to assess whether the sex ratio of necropsied seals (
= 243) differed from those of non-necropsied, stranded seals (
= 145) with known age and sex. We used the proportion of males to females in each age class of stranded harbor seals (excluding necropsied animals) as the expected values. The observed values were the number of males and females in each age class of necropsied seals.
Multiple correspondence analysis (MCA) is a form of multivariate exploratory data analysis used to reveal underlying patterns in datasets encompassing several categorical variables (
Greenacre and Blasius, 2006
). For MCA, we used only stranding cases categorized into one of the four most common causes of death (infectious, nutritional, anthropogenic trauma, and non-anthropogenic trauma), representing 89% of necropsied harbor seals (144 of 157 pups, 30 of 35 weaned pups, 12 of 12 sub-adults, and 32 of 40 adults). Once categorical variables were transformed into continuous principal components through MCA, hierarchical clustering was performed using the Ward’s criterion to group individuals with shared characteristics. A minimum of three clusters was selected based on partitioning of a hierarchical tree. Statistical analyses and graphics were computed using three R packages: (1) FactoMineR (
Lê et al., 2008
), (2) factoextra (
Kassambara and Mundt, 2017
), and (3) ggplot2 (
Wickham, 2016
).
Results
The SJC harbor seal sub-population grew exponentially between 1970 and the mid-1990s (
Figure 1
) (
Jeffries et al., 2003
). Aerial surveys were not conducted again until 2019, when 5,202 harbor seals were reported in SJC (
Figure 1
) (S. Jeffries, unpublished data).
FIGURE 1
Between January 01, 2002 and December 31, 2018, we found 847 dead-stranded harbor seals in SJC. An additional 35 stranded and died or were humanely euthanized in rehabilitation. Annually, dead strandings (“strandings” or “stranded” hereafter) ranged from 27 to 93 cases per year with an average of 51.8 (
SD
= 16.8), and complete necropsies were performed on an average of 28.8% (
SD
= 6.9%) of stranded seals (
Figure 2
). Cases of stranded seals and those that were necropsied were well distributed throughout the county (
Figure 3
).
FIGURE 2
FIGURE 3
Seasonal patterns were evident for stranded seals by age class: pups were found in the summer, weaned pups were mainly found during fall, and adults and sub-adults were mainly found in summer and fall (
Figure 4
).
FIGURE 4
For all stranded harbor seals (necropsied animals included), the sex ratio (males per 100 females) for stranded harbor seals where sex and age class were known (
= 388) was 88:100 for pups, 74:100 for weaned pups, 36:100 for sub-adults, and 78:100 for adults. Compared to a hypothetical even sex ratio for stranded animals, only sub-adults diverged [
(1,
= 38) = 8.52,
= 0.004]; however, sex was unknown for 36% (21 of 59) of stranded sub-adults.
For necropsied seals with known age class and sex (
= 243), sex ratios diverged from the expected values (proportion of males to females per age class of stranded seals, excluding necropsied seals) only for adults, with the male:female ratio for necropsied seals being 43:100 and expected ratio 188:100 [X
(1,
= 40) = 20.1,
< 0.001].
The most frequently observed causes of mortality were infectious, nutritional, anthropogenic trauma, and non-anthropogenic trauma, which differed by age class and accounted for 89% of necropsies (
Table 1
and
Figure 5
). Pups primarily died of nutritional causes (70%), whereas sub-adults and adults mainly died of infectious causes (42%) and non-anthropogenic trauma (27%). Weaned pup mortality was distributed equally among the four predominant causes of death. Cause of death could not be determined for thirteen cases (6 pups, 4 weaned pups, and 3 adults).
FIGURE 5
The two-dimension MCA solution expressed 33.8% of the total variation contained in the dataset, which was significantly greater than the variation obtained by the 0.95 quantile of random distributions (24.5%). The first and second dimensions used were eigenvalue, 0.54 and 0.39, and inertia, 19.6 and 14.2%. The variables correlated most strongly with each dimension are shown in
Supplementary Table 1
. Hierarchical clustering analysis on principal components of the MCA revealed that most harbor seal mortalities could be grouped into three clusters based on shared age class, season of stranding, and cause of death. Stranded seals belonging to cluster 1 were pups (
< 0.001,
= 14.6) that died in summer (
< 0.001,
= 10.8) of nutritional causes (
< 0.001,
= 9.69). Cluster 2 was characterized by weaned pups (
< 0.001,
= 10.8) that died of anthropogenic trauma (
< 0.001,
= 6.6) in the fall (
< 0.001,
= 6.69). In cluster 3, adults (
< 0.001,
= 10.7) and sub-adults (
< 0.001,
= 3.76) that died of infectious causes (
< 0.001,
= 6.83) and non-anthropogenic trauma (
= 0.04,
= 2.04) in spring (
< 0.001,
= 6.03) and fall (
= 0.004,
= 2.86) were most strongly represented.
Most pups (70%) exhibited nutritional causes of death with 97% of these diagnosed with emaciation-malnutrition syndrome. Our case definition for this diagnosis was suboptimal body weight compared to known average birth weight and expected daily weight gain based on a random sample published by
Cottrell et al. (2002)
, or as evidenced by lack of subcutaneous adipose layer and prominent boney protuberances, where insufficient nutrition was the driver of body condition loss. A contributing cause of death was identified in 46 cases where the primary cause of death was nutritional, including infection (
= 37) and non-anthropogenic trauma (
= 9). Important contributing infectious diagnoses included omphalitis or omphalophlebitis (
= 25) and phocine herpesvirus-1 associated adrenal adenitis (
= 4) (
Himworth et al., 2010
). Non-anthropogenic trauma was an important primary cause of death for pups (
= 21). Often the cause of trauma could not be determined, but incomplete predation by mammal-eating killer whales (
Orcinus orca
) was documented in four cases in addition to the two pups and three weaned pups previously described in
Gaydos et al. (2005)
. As expected, all four cases where congenital disease was the primary cause of death occurred in pups.
The weaned pup age class had the highest number of deaths from anthropogenic trauma (
= 7); all were suspected propeller strikes. Weaned pups also died from non-anthropogenic trauma including suspected predation events. Of the five weaned pups that died of infectious causes, all were in the fall, three were cases of bronchopneumonia, one of pleuropneumonia, and one of encephalitis.
Infectious primary causes of death in adults and sub-adults (affecting 44% of seals in these age classes) were dominated by bacterial bronchopneumonia (17 of 23 cases). With the exception of suspected killer whale predation and one case of esophageal perforation by a spotted ratfish spine (
Akmajian et al., 2012
), the underlying cause of most non-anthropogenic trauma in adults and sub-adults (
= 14) could not be determined. The only case of neoplasia was an emaciated adult (29-year-old) female that had a perigastric spindle cell tumor in the muscularis at the junction of the esophagus and cardia, which likely impinged upon and interfered with normal gastrointestinal transit.
Of the 12 cases for which the primary cause of death was anthropogenic trauma, nine were propeller strikes (1 pup, 7 weaned pups, and 1 adult) and three were gunshot cases (2 sub-adults, one adult).
Toxins were not identified as a primary cause of death for any harbor seal necropsied in this study. However, one adult female had a liver cadmium (Cd) concentration of 22.6 μg/g wet weight, which exceeds the putative lower limit for renal dysfunction in marine mammals (20 μg/g wet weight;
Law, 1996
) and is over four times greater than the mean liver Cd concentration observed in adult harbor seals in SJC (
Ashley et al., 2020
). This seal died of septicemia caused by
Streptococcus phocae
. Because possible immunosuppression from elevated liver Cd concentrations cannot be discounted, toxins were identified as a contributing cause of death.
Zoonotic pathogens were detected at a low frequency in all age classes and may reflect potential environmental and public health concerns. As previously described,
Brucella pinnipedialis
was isolated or detected by PCR in two sub-adults and one weaned pup (
Lambourn et al., 2013
).
Salmonella enterica
subsp. Arizonae and subsp. Litchfield were isolated from the small intestine of two pups, as was
Salmonella typhimurium
from the small intestine of a weaned pup. One adult and three pups were infected with parapoxviruses, and it is likely that two of the pups were exposed to the viruses while in rehabilitation. One of these pups was simultaneously infected with methicillin-resistant
Staphylococcus aureus
(MRSA) that we suspect was acquired during rehabilitation as well. Genotyping of the isolate revealed spa type 1 that could be either CMRSA-5 or CMRSA 7/10, which is equivalent to USA300, the most common community-associated clone in people in some areas, including British Columbia. Multidrug-resistant enterococci, which have emerged as a formidable pathogen associated with serious human infections in hospital settings (
Grassotti et al., 2018
), were isolated from an adult male seal. Parasitic nematodes in the family Anisakidae were identified in 12 adults, seven sub-adults, and two weaned pups. While not directly transmitted to humans by harbor seals, unembryonated nematode eggs shed by seals can infect crustaceans, squid, and fish when they ingest free-living second-stage larvae. Fish and squid infected with third-stage nematode larvae can then infect humans (
Dailey, 2005
).
Mucormycosis, an emerging fungal disease in marine mammals of the Pacific Northwest (
Huggins et al., 2018
), was identified in one sub-adult harbor seal in 2009 and one adult in 2019 (the latter was not included in the dataset for this study). During a 2007
Cryptococcus gattii
epizootic in Dall’s porpoises (
Phocoenoides dalli
) and harbor porpoises (
Phocoena phocoena
), a sub-adult harbor seal was diagnosed with multisystemic
C. gattii
infection. The clinical presentation and pathologic findings of this animal were consistent with those described by
Rosenberg et al. (2016)
Discussion
Rapid population growth in the SJC harbor seal population plateaued in the mid-1990s (
Jeffries et al., 2003
). Surveys conducted in 2019 found the harbor seal population to be approximately the same size almost two decades later (
Figure 1
). While population density could have oscillated during the time when no surveys were conducted (2000–2018), the relatively stable annual stranding patterns we documented (
Figure 2
) suggest that any changes in harbor seal density were neither as pronounced nor as lasting as the dramatic asymptotic growth documented between 1970 and the mid-1990s, suggesting a population at equilibrium. Strandings represent an unknown percentage and bias of the population that dies. That said, our consistent stranding response and the lack of major variation seen in annual stranding rate (
Figure 2
) support that periodic steep population declines, such as those expected after an epizootic (
Eguchi, 2002
Osinga et al., 2012
), followed by years of population rebound were not responsible for maintaining this harbor seal population at equilibrium. Instead, the high level of mortality in pups observed every summer suggests that stability is maintained by a small annual population recruitment just large enough to compensate for some low level of mortality occurring in older seals.
Marine mammal strandings are an excellent opportunity to gather mortality data from a population that can be otherwise challenging to study. However, stranded animals represent a potential sample bias, as not all stranded seals are reported or are in suitable condition for postmortem examination once found (
Eguchi, 2002
). As has been done in other studies (e.g.,
Osinga et al., 2012
), bias was minimized by responding to all reported strandings in all seasons, collecting all animals in suitable condition, and performing consistent complete postmortem examinations on animals.
The observed high percentage of pups dying of malnutrition during summer (
Table 1
and
Figures 4
) suggests that a large fraction of pups born annually are unable to survive. While we were unable to identify the precipitating factors for each emaciation-malnutrition case, possibilities include
in utero
malnutrition, placental insufficiency, primiparous dams, insufficient alimentation and subsequent milk production by dams during the 32 ± 1.5 days of lactation prior to weaning (
Cottrell et al., 2002
), and post-partum maternal neglect or separation, which may or may not have been related to human interaction.
FIGURE 6
While malnutrition mainly drives pup mortality in SJC, infectious diseases also contribute to pup loss. Of the 110 pups that died of nutritional causes, 34% (
= 37) had contributing secondary infectious causes, suggesting an interaction between poor nutritional condition and enhanced susceptibility to infectious diseases, likely mediated through immunosuppression, generalized debilitation, or agonal metabolic derangements. The nutrition- and infection-mediated mortality we identify in pups operates in a density-dependent manner in juveniles in other vertebrate populations at or near carrying capacity, such as reindeer (
Rangifer tarandus
) introduced to the sub-Antarctic island of South Georgia, (
Leader-Williams, 1982
), some African plains species that compete for forage (
Sinclair, 1985
), and yellow-eyed juncos (
Junco phaeonotus
Sullivan, 1989
). Likewise, juveniles often appear to be the age class most susceptible to density-dependent mortality for populations at carrying capacity, as has been shown with red deer (
Cervus elaphus scoticus
) in Scotland (
Guinness et al., 1978
), multiple species of mule deer (
Odocoileus hemionus
spp.;
Robinette et al., 1957
), and yellow-eyed juncos (
Sullivan, 1989
). For some mammalian populations at carrying capacity, juvenile mortality is higher among males than females (e.g.,
Clutton-Brock et al., 1985
); however, this was not apparent in our data.
While nutritional factors are considered bottom-up constraints on population growth, in many of the above-cited examples, it is difficult to separate the density-dependent force of nutritional limitation from the top-down influence of predation. In our 17-year retrospective analysis, we only detected cases of predation-related trauma from mammal-eating killer whales in two adults and nine pups or weaned pups. We suspect a far higher level of killer whale-associated predation on harbor seals occurs in SJC (
Shields et al., 2018
), but this influence is not demonstrable via stranding data as most carcasses are likely consumed rather than beach cast. Even with limited available stranding data on predation, we hypothesize that the factors keeping the harbor seal population in SJC at equilibrium are probably a combination of bottom-up nutritional limitations and top-down predatory influences.
Within the Salish Sea, adult harbor seals display moderate to high site fidelity (
Hardee, 2008
), usually remaining within 30 km of their primary haul-out sites (
DFO, 2010
Peterson et al., 2012
). Thus, it is unclear whether our observed age-related causes of mortality are specific to SJC or more widespread in the Salish Sea. It is possible that specific causes of mortality vary regionally with factors such as harbor seal density (
Jeffries et al., 2003
), human disturbance (
Acevedo-Gutierrez and Cendejas-Zarelli, 2011
), pathogen and contaminant exposure (
Ross et al., 2013
Ashley et al., 2020
), and mammal-eating killer whale presence (
London et al., 2012
Shields et al., 2018
). Regardless of regional variation in the contribution of these factors, malnutrition-related mortality likely contributes to harbor seal population regulation elsewhere in the Salish Sea, as harbor seals are at carrying capacity throughout the ecosystem (
DFO, 2010
Jeffries et al., 2003
). Over a 7-year period at a site south of SJC, the primary causes of harbor seal mortality were infections followed by malnutrition (
Huggins et al., 2013
). They also documented up to 25% perinatal mortality in some years. We therefore hypothesize that patterns noted in SJC are likely applicable to populations throughout the Salish Sea.
When looking at harbor seal populations outside of the Salish Sea, a somewhat similar pattern was noted in a study that looked at disease in European harbor seals at two different time points on their population growth curve (
Siebert et al., 2007
). They found no difference in the pathological changes noted in stranded seals when the population was recovering or recovered from a past epizootic (1996–2002) compared to those examined after a 2002 phocine distemper virus epizootic (2003–2005) when the population was at a much lower density. The major cause of death in all seals over both time periods was bronchopneumonia (
Siebert et al., 2007
). Interestingly, for the time period when the population was highest (1996–2002), the second most common causes of death were perinatal mortality and cachexia. When the population density was low (2003–2005), the second most common cause of death was infectious (septicemia), and fewer newborns were found to be weak.
It is important to note that while we identified and evaluated mortality factors in a population at equilibrium, we were not able to test for density-dependent effects. Mortality factors might be regulating population density in this population but be present in other harbor seal populations without regulating density. For example, one multi-decadal study looking at mortality in a population of harbor seals that was mostly increasing (with the exception of two phocine distemper virus outbreaks) (
Osinga et al., 2012
) found multiple categories of disease similar to our findings. These included a wide suite of infectious diseases, trauma cases, and nutrition-related mortality (pup starvation) (
Osinga et al., 2012
).
Identifying and tracking zoonotic pathogens in harbor seals is important to assess disease risk in other wildlife species, domestic animals, and humans (
Greig et al., 2014
). For example, while we do not believe that
Brucella pinnipedialis
affects harbor seals at the population level in the Salish Sea, humans may be at increased risk of contracting brucellosis when they handle weaned harbor seal pups, are exposed to their feces through rehabilitation facilities, or consume raw marine fish or invertebrates (
Waltzek et al., 2012
Lambourn et al., 2013
). Furthermore, exposure to
B. pinnipedialis
could pose a risk to mammal-eating or endangered southern resident (fish-eating) killer whales by reducing their fecundity (
Gaydos et al., 2004
).
S. enterica
(subsp. Arizonae and Litchfield) and
Salmonella typhimurium
are common bacteria in pinnipeds that are not typically associated with illness (
Greig et al., 2014
), but their isolation in harbor seals suggests land-based fecal pollution may also expose humans that swim or fish in SJC. Similarly, while gastrointestinal roundworms of the family Anisakidae are common and usually innocuous in healthy marine mammals, they are a potential concern for human health; humans that consume raw or undercooked seafood infected with the third stage larvae could develop anisakiasis (
Dailey, 2005
). Pinniped parapoxviruses are widespread globally and can be transmitted to humans via contact, causing painful cutaneous lesions, fever, and myalgia (
Hicks and Worthy, 1987
Clark et al., 2005
). The presence of poxviruses in SJC harbor seals emphasizes the importance of using personal protective equipment during stranding response and rehabilitation, as well as continued public education to prevent human-seal pup contact.
We did not identify pathogens known to cause large-scale epizootics in harbor seals from other regions, such as morbilliviruses (
Härkönen et al., 2006
). While bottom-up nutrition-related mortality and top-down predation are likely the major constraints to Salish Sea harbor seal population growth, exposure to a pathogen capable of causing a large epizootic could dramatically shift the SJC harbor seal population away from equilibrium. For example, during the 1988 and 2002 phocine distemper virus (PDV) outbreaks in the North Sea, the harbor seal population plummeted 60 and 50%, respectively, driving population size far below carrying capacity (
Reijnders et al., 1997
). Remaining harbor seal populations required 5–10 years of rapid exponential growth to recover (
Reijnders et al., 1997
Brasseur et al., 2018
).
Harbor seals are important components of the Salish Sea ecosystem, occupying a variety of habitats and serving as high trophic level predators. The decades-long stability of the SJC harbor seal population suggests that growth is limited by some combination of prey availability and mammal-eating killer whale predation. However, the corollary that the harbor seal population limits growth of one or more of the sixty or so species of fish and invertebrates they consume has not been demonstrated (
Lance et al., 2012
). The current factors keeping the harbor seal population at equilibrium could change rapidly and dramatically with the introduction of a pathogen capable of causing a large-scale epizootic.
Statements
Data availability statement
The datasets generated for this study are available on request to the corresponding author.
Ethics statement
IACUC approval was not required by the UC Davis Office of Research for this work, as all carcasses used in this study were found dead prior to inclusion in the study.
Author contributions
JG, JO, EMA, and TA conceived the central ideas guiding the project. EAA assisted with 2 years of carcass collection and necropsies, scrubbed, collated, and analyzed data, and co-wrote the manuscript with JG. JO oversaw the stranding network and helped conduct gross necropsies for 6 years. TA collated and scrubbed data, conducted preliminary analyses, and wrote the initial framework for the manuscript. For all 17 years of data collection, SR analyzed histology samples and oversaw ancillary testing. SR also assigned causes of death with JG. EMA helped conceive the project and supervised TA’s work on the direction of the manuscript. SJ provided harbor seal population data and expertise. For all 17 years, JG co-authored all grants supporting the work, conducted necropsies and prepared final necropsy reports, assigned final causes of death with SR, and co-wrote the manuscript with EAA. All authors contributed to manuscript revision and approved the submitted version.
Funding
All samples were collected under permit from the National Marine Fisheries Service Marine Mammal Health and Stranding Response Program (#18786). This study was started while TA was an intern through the Friday Harbor Laboratories Adopt-a-Student Program. Harbor seal stranding response and necropsies were performed using funding from numerous John H. Prescott Marine Mammal Rescue Assistance Grants with in-kind support from The Whale Museum and the SeaDoc Society, a program of the Karen C. Drayer Wildlife Health Center, University of California, Davis School of Veterinary Medicine.
Acknowledgments
We thank the numerous SJC Marine Mammal Stranding Network volunteers and student interns who collected carcasses and assisted with necropsies.
Conflict of interest
SR has served as consulting pathologist for the San Juan County Marine Mammal Stranding Network since its inception and is a guest editor for the special edition of “Pathologic Findings in Stranded Marine Mammals: A Global Perspective” for
Frontiers in Marine Science
. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary material
The Supplementary Material for this article can be found online at:
Footnotes
1.
www.census.gov
References
Acevedo-Gutierrez
A.
Cendejas-Zarelli
S.
2011
).
Nocturnal haul-out patterns of harbor seals (
Phoca vitulina
) related to airborne noise levels in Bellingham, Washington, USA.
Aquat. Mamm.
37
167
174
10.1578/AM.37.2.2011.167
CrossRef
Google Scholar
Akmajian
A. M.
Lambourn
D. M.
Lance
M. M.
Raverty
S. S.
Gaydos
J. K.
2012
).
Mortality related to spotted ratfish (
Hydrolagus colliei
) in Pacific harbor seals (
Phoca vitulina
) in Washington State.
J. Wild. Dis.
48
1057
1062
10.7589/2011-12-348
Pubmed Abstract
CrossRef
Google Scholar
Ashley
E. A.
Olson
J. K.
Raverty
S.
Wilkinson
K.
Gaydos
J. K.
2020
).
Trace element concentrations in livers of Pacific harbor seals (
Phoca vitulina richardii
) from San Juan County, Washington, USA.
J. Wildl. Dis.
56
429
436
10.7589/2019-04-087
Pubmed Abstract
CrossRef
Google Scholar
Benskin
C. M. H.
Wilson
K.
Kones
K.
Hartley
I. H.
2009
).
Bacterial pathogens in wild birds: a review of the frequency and effects of infection.
Biol. Rev.
84
349
373
10.1111/j.1469-185X.2008.00076.x
Pubmed Abstract
CrossRef
Google Scholar
Brasseur
S. M. J. M.
Reijnders
P. J. H.
Cremer
J.
Meesters
E.
Kirkwood
R.
Jensen
L. F.
et al
2018
).
Echoes from the past: regional variations in recovery within a harbor seal population.
PLoS One
13
e0189674
10.1371/journal.pone.0189674
Pubmed Abstract
CrossRef
Google Scholar
Clark
C.
McIntyre
P. G.
Evans
A.
McInnes
C. J.
Lewis-Jones
S.
2005
).
Human sealpox resulting from a seal bite: confirmation that sealpox virus is zoonotic.
Br. J. Dermatol.
152
791
793
10.1111/j.1365-2133.2005.06451.x
Pubmed Abstract
CrossRef
Google Scholar
Clutton-Brock
T. H.
Albon
S. D.
Guinness
F. E.
1985
).
Parental investment and sex differences in juvenile mortality in birds and mammals.
Nature
313
131
Google Scholar
Cottrell
P.
Jeffries
S.
Beck
B.
Ross
P. S.
2002
).
Growth and development in free-ranging harbor seal (
Phoca vitulina
) pups from southern British Columbia, Canada.
Mar. Mamm. Sci.
18
721
733
10.1111/j.1748-7692.2002.tb01069.x
CrossRef
Google Scholar
Dailey
M. D.
2005
). “
Parasites of marine mammals
,” in
Marine Parasitology
ed.
Rohde
K.
Clayton, VIC
Csiro Publishing
),
408
414
Google Scholar
10
Deem
S. L.
Karesh
W. B.
Weisman
W.
2001
).
Putting theory into practice: wildlife health in conservation.
Conserv. Biol.
15
1224
1233
Google Scholar
11
del Monte-Luna
P.
Brook
B. W.
Zetina-Rejón
M. J.
Cruz-Escalona
V. H.
2004
).
The carrying capacity of ecosystems.
Glob. Ecol. Biogeogr.
13
485
495
Google Scholar
12
DeMaster
D. P.
Trites
A. W.
Clapham
P.
Mizroch
S.
Wade
P.
Small
R. J.
et al
2006
).
The sequential megafaunal collapse hypothesis: testing with existing data.
Prog. Oceanogr.
68
329
342
Google Scholar
13
DFO
2010
).
Population Assessment Pacific Harbour Seal (Phoca vitulina richardsi
): Canadian Science Advisory Secretariat Science Advisory Report 2009/011.
Vancouver, BC
Fisheries and Oceans Canada
Google Scholar
14
Eguchi
T.
2002
).
A method for calculating the effect of a die off from stranding data.
Mar. Mamm. Sci.
18
698
e709
10.1111/j.1748-7692.2002.tb01067.x
CrossRef
Google Scholar
15
Fowler
C. W.
1981
).
Density dependence as related to life history strategy.
Ecology
62
602
610
Google Scholar
16
Gaydos
J. K.
Balcomb
K. C.
III
Osborne
R. W.
Dierauf
L.
2004
).
Evaluating potential infectious disease threats for southern resident killer whales,
Orcinus orca
: a model for endangered species.
Biol. Conserv.
117
253
262
Google Scholar
17
Gaydos
J. K.
Dierauf
L.
Kirby
G.
Brosnan
D.
Gilardi
K.
Davis
G. E.
2008
).
Top 10 principles for designing healthy coastal ecosystems like the Salish Sea.
EcoHealth
460
471
10.1007/s10393-009-0209-1
Pubmed Abstract
CrossRef
Google Scholar
18
Gaydos
J. K.
Raverty
S.
Baird
R. W.
Osborne
R. W.
2005
).
Suspected surplus killing of harbor seal pups (
Phoca vitulina
) by killer whales (
Orcinus orca
).
Northwest Nat.
86
150
154
Google Scholar
19
Geraci
J. R.
Lounsbury
V. J.
2005
).
Marine Mammals Ashore: A Field Guide for Strandings.
Baltimore, MD
National Aquarium in Baltimore, Inc
Google Scholar
20
Geraci
J. R.
St Aubin
D. J.
Barker
I. K.
Webster
R. G.
Hinshaw
V. S.
Bean
W. J.
et al
1982
).
Mass mortality of harbor seals: pneumonia associated with influenza-a virus.
Science
215
1129
1131
10.1126/science.7063847
Pubmed Abstract
CrossRef
Google Scholar
21
Goss-Custard
J. D.
Stillman
R. A.
West
A. D.
Caldow
R. W. G.
McGrorty
S.
2002
).
Carrying capacity in overwintering migratory birds.
Biol. Conserv.
105
27
41
Google Scholar
22
Grassotti
T. T.
Zvoboda
D. D.
Costa
L. D. X.
de Araujo
A. J. G.
Pereira
R. I.
Soares
R. O.
et al
2018
).
Antimicrobial resistance profiles in
Enterococcus spp
. isolates from fecal samples of wild and captive black capuchin monkeys (
Sapajus nigritus
) in south Brazil.
Front. Microbiol.
2366
10.3389/fmicb.2018.02366
Pubmed Abstract
CrossRef
Google Scholar
23
Greenacre
M.
Blasius
J. eds
2006
).
Multiple Correspondence Analysis and Related Methods.
Boca Raton, FL
Chapman & Hall
Google Scholar
24
Greig
D. J.
Gulland
F. M. D.
Smith
W. A.
Conrad
P. A.
Field
C. L.
Fleetwood
M.
et al
2014
).
Surveillance for zoonotic and selected pathogens in harbor seals
Phoca vitulina
from central California.
Dis. Aquat. Org.
111
93
106
10.3354/dao02762
Pubmed Abstract
CrossRef
Google Scholar
25
Guinness
F. E.
Clutton-Brock
T. H.
Albon
S. D.
1978
).
Factors affecting calf mortality in red deer (
Cervus elaphus
).
J. Anim. Ecol.
47
817
832
Google Scholar
26
Hardee
S. E.
2008
).
Movements and Home Ranges of Harbor Seals (Phoca vitulina
) in the inland waters of the Pacific Northwest.
Ph.D. thesis
Western Washington University
Bellingham, WA
148
Google Scholar
27
Härkönen
T.
Dietz
R.
Reijnders
P.
Teilmann
J.
Harding
K.
Hall
A.
et al
2006
).
A review of the 1988 of 2002 phocine distemper virus epidemics in European harbor seals.
Dis. Aquat. Org.
68
115
130
Pubmed Abstract
Google Scholar
28
Hicks
B. D.
Worthy
G. A. J.
1987
).
Sealpox in captive grey seals (
Halichoerus grypus
) and their handlers.
J. Wildl. Dis.
23
10.7589/0090-3558-23.1.1
Pubmed Abstract
CrossRef
Google Scholar
29
Himworth
C.
Haulena
M.
Lambourn
D.
Gaydos
J. K.
Huggins
J.
Calambokidis
J.
et al
2010
).
Pathology and epidemiology of phocid herpesvirus-1 in wild and rehabilitating harbor seals (
Phoca vitulina richardsi
) in the northeastern Pacific.
J. Wildl. Dis.
46
1046
1051
10.7589/0090-3558-46.3.1046
Pubmed Abstract
CrossRef
Google Scholar
30
Huber
H. S.
Jeffries
S.
Lambourn
D.
Dickerson
B.
2012
).
Population substructure of harbor seals (
Phoca vitulina richardsi
) in Washington State using mtDNA.
Can. J. Zool.
88
280
288
Google Scholar
31
Huggins
J. L.
Lambourn
D. M.
Raverty
S. J.
Hanson
M. B.
Rhodes
L. D.
Norman
S. A.
et al
2018
). “
Mucormycosis: an emerging disease in marine mammals of the Pacific Northwest
,” in
Proceedings of the 49th Annual International Association for Aquatic Animal Medicine
Long Beach, CA
Google Scholar
32
Huggins
J. L.
Leahy
J.
Calambokidis
J.
Lambourn
D.
Jeffries
S. J.
Norman
S. A.
et al
2013
).
Causes and patterns of harbor seal (
Phoca vitulina
) pup mortality at Smith Island, Washington, 2004–2010.
Northwest Nat.
94
198
208
Google Scholar
33
Huggins
J. L.
Raverty
S.
Norman
S. A.
Calambokidis
J.
Gaydos
J. K.
Duffield
D. A.
et al
2015
).
Increased harbor porpoise mortality in the Pacific Northwest, USA: understanding when higher levels may be normal.
Dis. Aquat. Org.
115
93
102
10.3354/dao02887
Pubmed Abstract
CrossRef
Google Scholar
34
Jeffries
S.
Gearin
P. J.
Huber
H. R.
Saul
D. L.
Pruett
D. A.
2000
).
Atlas of Seal and Sea Lion Haulout Sites in Washington.
Olympia WA
Washington Department of Fish and Wildlife
, 150.
Google Scholar
35
Jeffries
S.
Huber
H.
Calambokidis
J.
Laake
J.
2003
).
Trends and status of harbor seals in Washington State: 1978-1999.
J. Wildl. Manage.
67
207
218
Google Scholar
36
Kassambara
A.
Mundt
F.
2017
).
Package “factoextra”.
Available online at:
(accessed November 1, 2019)
Google Scholar
37
Lambourn
D. M.
Garner
D.
Ewalt
J.
Rhyan
S.
Raverty
S.
Jeffries
S.
et al
2013
).
Brucella pinnipedialis
infections in Pacific harbor seals (
Phoca vitulina richardsi
) from Washington State.
J. Wildl. Dis.
49
802
815
10.7589/2012-05-137
Pubmed Abstract
CrossRef
Google Scholar
38
Lance
M. M.
Chang
W. Y.
Jeffries
S.
Pearson
S.
2012
).
Harbor seal diet in northern Puget sound: implications for the recovery of depressed fish stocks.
Mar. Ecol. Prog. Ser.
464
257
271
10.3354/meps09880
CrossRef
Google Scholar
39
Law
R. J.
1996
). “
Metals in marine mammals
,” in
Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations
eds
Beyer
W. N.
Heinz
G.
Redmon-Norwood
A.
Boca Raton, FL
Lewis Publishers
),
357
376
Google Scholar
40
Lê
S.
Josse
J.
Husson
F.
2008
).
Package factoMineR: a package for multivariate analysis.
J. Stat. Softw.
25
18
10.18637/jss.v025.i01
CrossRef
Google Scholar
41
Leader-Williams
N.
1982
).
Relationship between a disease, host density and mortality in a free-living deer population.
J. Anim. Ecol.
51
235
240
Google Scholar
42
Lefebvre
K. A.
Quakenbush
L.
Frame
E.
Burek-Huntington
K.
Sheffield
G.
Stimmelmayr
R.
et al
2016
).
Prevalence of algal toxins in Alaskan marine mammals foraging in a changing arctic and subarctic environment.
Harmful Algae
55
13
24
10.1016/j.hal.2016.01.007
Pubmed Abstract
CrossRef
Google Scholar
43
Linnell
J. D.
Aanes
R.
Anderson
R.
1995
).
Who killed Bambi? The role of predation in the neonatal mortality of temperate ungulates.
Wildl. Biol.
209
223
Google Scholar
44
London
J. M.
Ver Hoef
J. M.
Jeffries
S. J.
Lance
M. M.
Boveng
P. L.
2012
).
Haul-Out behavior of harbor seals (
Phoca vitulina
) in Hood Canal, Washington.
PLoS One
e38180
10.1371/journal.pone.0038180
Pubmed Abstract
CrossRef
Google Scholar
45
Lorenz
M. D.
2009
). “
The problem-oriented approach
,” in
Small Animal Medical Diagnosis
eds
Lorenz
M. D.
Neer
T. M.
DeMars
P.
Ames, IA
Wiley-Blackwell
),
12
Google Scholar
46
Lucas
Z.
Stobo
W.
2000
).
Shark-inflicted mortality on a population of harbour seals (
Phoca vitulina
) at Sable Island, Nova Scotia.
J. Zool.
252
405
414
Google Scholar
47
Majewski
S. P.
Ellis
G. M.
2019
).
Abundance and Distribution of Harbour Seals (Phoca vitulina
British Columbia, VIC
Prep Publishing
Google Scholar
48
May
R. M.
Anderson
R. M.
1979
).
Population biology of infectious diseases: part II.
Nature
280
455
461
10.1038/280455a0
Pubmed Abstract
CrossRef
Google Scholar
49
Osinga
N.
Shahi Ferdous
M. M.
Morick
D.
Garcia Hartmann
M.
Ulloa
J. A.
Vedder
L.
et al
2012
).
Patterns of stranding and mortality in common seals (
Phoca vitulina
) and grey seals (
Halichoerus grypus
) in the Netherlands between 1979 and 2008.
J. Comp. Path.
147
550
565
10.1016/j.jcpa.2012.04.001
Pubmed Abstract
CrossRef
Google Scholar
50
Peterson
S. H.
Lance
M. M.
Jeffries
S. J.
Acevedo-Gutierrez
A.
2012
).
Long distance movements and disjunct spatial use of harbor seals (
Phoca vitulina
) in the inland waters of the Pacific Northwest.
PLoS One
e39046
10.1371/journal.pone.0039046
Pubmed Abstract
CrossRef
Google Scholar
51
R Core Team
2017
).
R: A Language and Environment for Statistical Computing.
Vienna
R Foundation for Statistical Computing
Google Scholar
52
Reijnders
P. J. H.
Ries
E. H.
Tougaard
S.
Norgaard
N.
Heidemann
G.
Schwarz
J.
et al
1997
).
Population development of harbor seals
Phoca vitulina
in the Wadden Sea after the 1988 virus epizootic.
J. Sea Res.
38
161
168
Google Scholar
53
Robinette
W. L.
Gashwiler
J. S.
Low
J. B.
Jones
A.
1957
).
Differential mortality by sex and age among mule deer.
J. Wildl. Manage.
21
16
Google Scholar
54
Rosenberg
J.
Haulena
M.
Hoang
L. M. N.
Morshed
M.
Zabek
E.
Raverty
S.
2016
).
Cryptococcus gattii
type VGIIa infection in harbor seals (
Phoca vitulina
) in British Columbia, Canada.
J. Wildl. Dis.
52
677
681
10.7589/2015-11-299
Pubmed Abstract
CrossRef
Google Scholar
55
Ross
P. S.
Noel
M.
Lambourn
D.
Dangerfield
N.
Calambokidis
J.
Jeffries
S.
2013
).
Declining concentrations of persistent PCBs, PBDEs, PCDEs, and PCNs in harbor seals (
Phoca vitulina
) from the Salish Sea.
Prog. Oceanogr.
115
160
170
10.1016/j.pocean.2013.05.027
CrossRef
Google Scholar
56
Shields
M. W.
Hysong-Shimazu
S.
Shields
J. C.
Woodruff
J.
2018
).
Increased presence of mammal-eating killer whales in the Salish Sea with implications for predator-prey dynamics.
PeerJ
c6062
10.7717/peerj.6062
Pubmed Abstract
CrossRef
Google Scholar
57
Siebert
U.
Wohlseiny
P.
Lehnert
K.
Baumgartnery
W.
2007
).
Pathological findings in harbour seals (
Phoca vitulina
): 1996 – 2005.
J. Comp. Path
137
47
58
10.1016/j.jcpa.2007.04.018
Pubmed Abstract
CrossRef
Google Scholar
58
Sinclair
A. R. E.
1985
).
Does interspecific competition or predation shape the African Ungulate community?
J. Anim. Ecol.
54
899
918
Google Scholar
59
Springer
A. M.
Estes
J. A.
Van Vliet
G. B.
Williams
T. M.
Doak
D. F.
Danner
E. M.
et al
2003
).
Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling?
PNAS
100
12223
12228
10.1073/pnas.1635156100
Pubmed Abstract
CrossRef
Google Scholar
60
Sullivan
K. A.
1989
).
Predation and starvation: age-specific mortality in juvenile juncos (
Junco phaenotus
).
J. Anim. Ecol
58
275
286
Google Scholar
61
Waltzek
T. B.
Cortes-Hinojosa
G.
Wellehan
J. F. X.
Jr.
Gray
G. C.
2012
).
Marine mammal zoonoses: a review of disease manifestations.
Zoonoses Public Health
59
521
535
10.1111/j.1863-2378.2012.01492.x
Pubmed Abstract
CrossRef
Google Scholar
62
Wickham
H.
2016
).
Ggplot2: Elegant Graphics for Data Analysis.
New York
Springer-Verlag
Google Scholar
Summary
Keywords
carrying capacity
equilibrium population
harbor seal
marine mammals
pathology
Salish Sea
San Juan Islands
stranding network
Citation
Ashley EA, Olson JK, Adler TE, Raverty S, Anderson EM, Jeffries S and Gaydos JK (2020)
Causes of Mortality in a Harbor Seal (
Phoca vitulina
) Population at Equilibrium
Front. Mar. Sci.
7:319. doi:
10.3389/fmars.2020.00319
Received
15 February 2020
Accepted
20 April 2020
Published
13 May 2020
Volume
7 - 2020
Edited by
Alastair Martin Mitri Baylis, South Atlantic Environmental Research Institute, Falkland Islands
Reviewed by
Mauricio Seguel, University of Georgia, United States; Elizabeth McHuron, University of California, Santa Cruz, United States; Peter Douglas Shaughnessy, South Australian Museum, Australia
Updates
© 2020 Ashley, Olson, Adler, Raverty, Anderson, Jeffries and Gaydos.
This is an open-access article distributed under the terms of the
Creative Commons Attribution License (CC BY)
. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Joseph K. Gaydos,
jkgaydos@ucdavis.edu
This article was submitted to Marine Megafauna, a section of the journal Frontiers in Marine Science
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High-impact AI
AI playbook for researchers
Your step by step support for responsible and impactful AI use
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