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A Review of Northern Fur Seal (Callorhinus ursinus) Literature to Direct Future Health Monitoring Initiatives

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  • Sea Change Health

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Northern fur seals (Callorhinus ursinus, NFS) are a vulnerable species broadly distributed throughout the north Pacific. Although commercial hunting stopped in 1984, the population has continued to decline for unknown reasons. The goal of this scoping review was to synthesize and review 50 years of literature relevant to the health of NFS to inform the development of health surveillance recommendations. Search criteria were developed and applied to three databases, followed by title and abstract screening and full text review. Articles published between 1 January 1972 and 31 December 2021 were included. Articles were categorized by health determinant, and further as relating to ten subcategories of disease. Data were summarized descriptively. A total of 148 publications met the criteria for inclusion. Infectious disease reports were common, primarily relating to metazoan parasite presence. The presence of zoonotic pathogens such as Coxiella burnetii and Brucella spp. is of public health interest, although a failure to link disease research to individual animal or population health outcomes was consistent across the literature. A shift away from the single agent focus of disease programs toward more holistic, health-oriented perspectives will require broader interdisciplinary collaboration. These findings can inform stakeholders and help them to prioritize and strategize on future NFS health research efforts.
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Oceans 2022, 3, 303–319. https://doi.org/10.3390/oceans3030021 www.mdpi.com/journal/oceans
Review
A Review of Northern Fur Seal (Callorhinus ursinus) Literature
to Direct Future Health Monitoring Initiatives
Valerie Cortés
1
, Kelly Patyk
2
, Claire Simeone
3
, Valerie Johnson
4
, Johanna Vega
5
, Kate Savage
6
and Colleen Duncan
1,
*
1
College of Veterinary Medicine and Biomedical Sciences, Colorado State University,
Fort Collins, CO 80526, USA; valerie.wright@colostate.edu
2
United States Department of Agriculture, Animal Plant and Health Inspection Service, Veterinary Services,
Strategy and Policy, Center for Epidemiology and Animal Health,
Fort Collins, CO 80526, USA; kelly.a.patyk@usda.gov
3
Sea Change Health, Sunnyvale, CA 94086, USA; claire@seachangehealth.org
4
College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA;
john7670@msu.edu
5
Animal Emergency and Specialty Center, Reno, NV 89511, USA; josephson44@yahoo.com
6
National Marine Fisheries Service (Affiliate), Juneau, AK 99801, USA; kate.savage@noaa.gov
* Correspondence: colleen.duncan@colostate.edu
Abstract: Northern fur seals (Callorhinus ursinus, NFS) are a vulnerable species broadly distributed
throughout the north Pacific. Although commercial hunting stopped in 1984, the population has
continued to decline for unknown reasons. The goal of this scoping review was to synthesize and
review 50 years of literature relevant to the health of NFS to inform the development of health sur-
veillance recommendations. Search criteria were developed and applied to three databases, fol-
lowed by title and abstract screening and full text review. Articles published between 1 January
1972 and 31 December 2021 were included. Articles were categorized by health determinant, and
further as relating to ten subcategories of disease. Data were summarized descriptively. A total of
148 publications met the criteria for inclusion. Infectious disease reports were common, primarily
relating to metazoan parasite presence. The presence of zoonotic pathogens such as Coxiella burnetii
and Brucella spp. is of public health interest, although a failure to link disease research to individual
animal or population health outcomes was consistent across the literature. A shift away from the
single agent focus of disease programs toward more holistic, health-oriented perspectives will re-
quire broader interdisciplinary collaboration. These findings can inform stakeholders and help
them to prioritize and strategize on future NFS health research efforts.
Keywords: Callorhinus ursinus; health; northern fur seal
1. Introduction
The northern fur seal (Callorhinus ursinus, further NFS) is an otariid (eared seal) that
is broadly distributed throughout the north Pacific Ocean. NFSs are the largest of the fur
seals who, similar to other members of the subfamily Arctocephalinae, exhibit significant
sexual dimorphism; adult males can weigh up to 270 kg while adult females are typically
~50 kg [1]. They have relatively long lifespans, up to 18 and 27 years for males and females,
respectively, and the generation length is estimated at ~14 years [2,3]. The species is highly
pelagic, with animals typically only on land during the breeding (and parturition) season.
There are six different breeding populations, i.e., three in the United States and three
in Russia: San Miguel Island, California; Bogoslof Island, eastern Bering Sea; Pribilof Is-
lands, Alaska; Commander Islands; Kuril Islands; and Robben Island. The largest breed-
ing population is on the Pribilof Islands, which supports about half the world’s NFS pop-
ulation [4]. After unregulated sealing ended in the 1950s, the population rose and was
Citation: Cortés, V.; Patyk, K.;
Simeone, C.; Johnson, V.; Vega, J.;
Savage, K.; Duncan, C. A Review of
Northern Fur Seal (Callorhinus
ursinus) Literature to Direct Future
Health Monitoring Initiatives.
Oceans 2022, 3, 303–319.
https://doi.org/10.3390/
oceans3030021
Academic Editor: Alexander Werth
Received: 5 May 2022
Accepted: 5 July 2022
Published: 7 July 2022
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional
claims in published maps and institu-
tional affiliations.
Copyright: © 2022 by the authors.
Submitted for possible open access
publication under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (https://cre-
ativecommons.org/licenses/by/4.0/).
Oceans 2022, 3 304
estimated at two million, but hunting of female NFS for their pelts from 1956 to 1968 sig-
nificantly decreased the Pribilof Islands population [5]. Despite the cessation of commer-
cial hunting in 1984, the population has continued to decline for reasons that are un-
known, although a variety of contributory causes (e.g., entanglement in marine debris,
disease and parasites, nutrition, toxins and pollutants, and predation) have all been pro-
posed [1,2]. In 1988, the Pribilof Island population was listed as ‘depleted’ under The Ma-
rine Mammal Protection Act [6] and the species is currently ‘vulnerable’ according to the
IUCN red list [1].
In general, studying the health of wildlife populations is challenged by the charac-
teristics of the animals themselves as well as the environments in which they reside, there-
fore, making it difficult to access data or samples [7]. Such challenges are particularly ap-
parent in the study of marine mammals where the complexities of investigations have
great potential to introduce bias or limit the external validity of the study. For example, a
review of infectious disease research in polar bears (Ursus maritimus) found that the most
detailed health information was from captive animals housed in physical locations (e.g.,
zoos) and environments markedly different than their natural habitat, while information
from wild populations was overwhelmingly disassociated from any clinical, pathological,
or population health information [8]. Similarly, an extensive review of marine mammal
disease literature from North America highlighted substantial publication biases and pro-
tracted lag times between disease events and information sharing [9]. How these biases
have influenced NFS research, and how they may be addressed in the future, is less clear.
The definition and study of health in wildlife populations is a topic of increased at-
tention. Health was once thought of as ‘the absence of disease’ but more modern concepts
of health employ vulnerability, resilience, sustainability, and population stability [10]. In
an effort to understand and apply a more dynamic concept of wildlife health, a determi-
nants of health wildlife model has been proposed. These determinants of health include:
needs for daily living, biologic endowment, physical and social environment, direct mor-
tality pressures, and human expectations [11]. For a highly pelagic species such as the
NFS, meaningfully assessing health, at least in part, by characteristics of their environ-
ment would be helpful given the logistical hurdles of observing or sampling the animals
during all seasons and life stages.
Aggregation of historical and baseline health and disease information is an important
step in the development of any wildlife surveillance program [7]. Scoping reviews are a
particularly useful tool to assess the breadth and type of existing research on a topic, to
identify knowledge gaps, to clarify concepts/definitions in the literature, and to investi-
gate how research is conducted in a certain field [12]. The objective of this project was to
synthesize and review literature relevant to the health of the NFS to inform the develop-
ment of health surveillance recommendations.
2. Materials and Methods
An overview of search criteria, inclusions and exclusions in accordance with PRISMA
[13], is presented in Figure 1. We searched three electronic databases (PubMed, Web of
Science, and Zoological Record) using the search terms “northern fur seal” OR Callorhi-
nus ursinus” OR “northern fur seals”. Specific inclusion criteria included publications be-
tween 1 January 1972, (in accordance with [9]) and 31 December 2021, and printed in Eng-
lish. Records were limited to articles published in peer-reviewed journals, with ‘grey lit-
erature’ such as government reports, books, and conference proceedings excluded. We
read titles and abstracts and excluded publications that did not focus on NFS health [11]
or disease [9] and publications which concentrated on tools and techniques (e.g., tagging,
modeling, and methodologies).
Oceans 2022, 3 305
Figure 1. Schematic representation of the scoping literature process including original searches
through to classification of articles by determinants of health, as well as subcategories of disease.
Following the exclusion of duplicates and articles that failed to meet the inclusion
criteria, titles and abstracts of all remaining records were reviewed and categorized inde-
pendently by three authors (V.C., J.V., and C.D.) according to how they related to NFS
health or disease. Health categories were based on the determinants of wildlife health
model proposed by Wittrock et al., 2019: needs for daily living (e.g., nutrition and habitat
quality); abiotic environment (e.g., physical surroundings, weather, and water quality);
social environment (e.g., community dynamics, intra- and interspecies interactions); bio-
logic endowment (e.g., physiological or pathological aspects of wildlife health); direct
mortality pressures (e.g., factors that directly threaten survival); and human expectations
Oceans 2022, 3 306
(e.g., service-like entities involved in wildlife or ecosystem management) [11]. An article
was classified as relating to disease or not if it covered one of the infectious or non-infec-
tious disease conditions as described by Simeone et al., 2015 [9]. When classifications dif-
fered between authors, consensus was reached through discussion and complete article
review as necessary.
All disease publications were reviewed in full and further divided into 10 subcatego-
ries; 5 infectious (viruses, bacteria, fungi, metazoan parasites, and protozoa) and 5 non-
infectious (neoplasia, toxins and contaminants, anthropogenic trauma, non-anthropo-
genic/unknown source trauma and ‘other’), similar to classifications by Simeone et al.,
2015 [9]. Within each of the subcategories, articles were evaluated according to the type
of disease information available (i.e., indirect tests, direct tests, clinical disease/pathology,
or other detectable health impact), the management of the NFS under study (wild or cap-
tive) and the location where the work was done, similar to Fagre et al., 2015 [8]. When
articles included discussion of multiple disease categories that spanned multiple subcate-
gories, they were assessed within the broader disease review section in addition to
acknowledgement in relevant subcategories.
3. Results
A total of 148 publications met the criteria for inclusion in this study (Figure 1), all of
which could be thematically classified according to the determinants of health. In contrast,
98 publications were classified as ‘disease’.
3.1. Disease Classification
The majority of the disease publications (n = 98) were focused on either a single agent,
or a group of related infectious or non-infectious agents that fit within the specific catego-
ries that follow. A smaller number (n = 5) spanned multiple disparate categories. Most
notable was an extensive case series of post-mortem findings from opportunistically col-
lected NFSs on St. Paul Island, Alaska, between 1986 and 2006, by Spraker and Lander
[14]. NFSs were also included in a large case series describing categories of disease in Cal-
ifornia stranded marine mammals from 1984 to 1990 [15]. The remaining multi-category
publications were largely infectious disease-oriented and are referenced in relevant sub-
sections below.
3.1.1. Infectious Disease
Viruses
Nine (9.2%) of the disease articles focused on viral diseases. Viral disease was also
described in the necropsy study and referenced in several other of the multi-pathogen
publications [14,16,17]. The majority of these articles, all published prior to 2000, were on
caliciviruses isolated from wild NFS, most commonly in California but also Alaska [17–
22]. Infection was typically devoid of pathology, although vesicular cutaneous lesions
have also been described [23]. Proliferative cutaneous lesions associated with pox virus
have been characterized by histopathology and electron microscopy, but were seen very
infrequently relative to the number of animals examined post mortem [14,24].
The remaining reports of viral pathogens were those detected in the reproductive
system. A novel polyomavirus was sequenced from a NFS placenta collected on St. Paul
Island after viral inclusions were seen histologically [25]. The single affected placenta had
been opportunistically collected from a rookery and no information was available regard-
ing fetal or maternal health. There was a single report of Otarine herpes virus 4 detected
by polymerase chain reaction (PCR) from vaginal swabs of free ranging NFSs in Alaska
devoid of any associated pathology or description of associated clinical disease [26].
Oceans 2022, 3 307
Bacteria
Thirteen (13%) of the disease articles focused on a single bacteria and several of the
multi-pathogen articles also included information on bacterial species. The most frequent
bacteria within this group was Coxiella burnetii. In 2010, 75% of the 146 opportunistically
collected NFS placentas from St. Paul Island, Alaska, were PCR positive for C. burnetii and
a subset (3%) of placentas had histologically identified intracytoplasmic bacteria con-
firmed as C. burnetii with immunohistochemistry (IHC) [27]. A similar molecular preva-
lence (77%) was reported in placentas collected from the same rookery the following year
[28]. Infected placentas had decreased apoptosis of placental trophoblasts suggesting a
functional change in the tissue, although no information on the associated NFS pup was
available to support this claim [29]. PCR conducted on multiple tissue types from 50
subadult male NFSs harvested during subsistence hunting were tested for C. burnetii bac-
terial DNA by real-time PCR; there were no positive samples [30]. Similarly, archived vag-
inal swabs from adult female NFSs were all negative [31]. A serosurvey using archived
samples collected from animals in the same location revealed high levels of exposure that
varied by age class but appeared to increase between 1994 and 2009/2011 (49–69%) [31].
Brucella spp. have also been identified in the NFS population on St. Paul Island. From
the same collection of placentas tested for C. burnetii above, a single case of necrotizing
placentitis with intracytoplasmic bacteria was seen and attributed to Brucella spp. by IHC
and PCR [32]. A total of 119 placentas collected during the 2011 pupping season were
screened by IS711 PCR with 6 (5%) testing positive; and serology using archived samples
suggested a similarly low level of exposure in the population (BMAT 2.5% positive, 30%
borderline) [32]. Another serosurvey of 107 archived samples collected in the same area,
but tested by enzyme-linked immunoassay (ELISA), were all negative [33]. Fifty subsist-
ence harvested subadult male NFSs were tested by PCR using eight tissue types, but only
a single spleen sample was positive and no disease was reportedly observed [30].
Pathogen-specific investigations have elucidated information on the presence, and in
some cases pathogenicity, of different bacteria. A variety of Salmonella spp. have been iso-
lated from the rectums of apparently healthy NFS pups in California and the authors con-
cluded that the organism could cause opportunistic infections but did not usually cause
disease in healthy animals [34]. That said, there was a single case report of a NFS pup with
meningoencephalitis and septicemia where S. enteriditis was cultured from the brain and
spinal cord [35]. Serologic screening and post-mortem examinations conducted on Pribilof
Island NFSs in the 1970s revealed a rare leptospiral infection characterized by interstital
nephritis in an adult and multisystem (renal, hepatic and placental) infection in neonates
[17,36]. Erysipelothrix rhusiopathiae was isolated from the oral cavity of 2/12 otherwise pre-
sumed healthy, free-ranging subadult male NFSs on St. Paul Island as part of a multi-
species investigation into the prevalence of the bacteria in the oral cavity of marine mam-
mals and bite wounds from marine mammals [37]. A cross-sectional survey of oral Pas-
teurellaceae isolates from captive NFSs and other species concluded that the bacteria are
part of normal marine mammal flora [38].
Multiple tissues have been cultured from subsistance-harvested subadult male NFSs
in Alaska and a variety of mixed bacteria were identified; however, there was no associa-
tion with disease and the high apparent prevalence in some normally sterile locations,
suggested a high likelihood of contamination [39]. The remaining publications describing
bacterial disease were typically case reports or case series investigations. While routine
bacterial cultures were not conducted as part of the Alaska NFS necropsy program, beta-
hemolytic Escherichia coli was isolated from 11 pups with pneumona [14]. Similarly, a cap-
tive subadult male NFS died following a period of anorexia and vomiting and a hemolytic
E. coli isolated from the intestine was determined to be the causative agent [40].
Oceans 2022, 3 308
Fungi
Only a single article was identified on fungal disease where Candida albicans was iso-
lated from asymptomatic NFS in an aquarium setting where phocid seals exhibited clini-
cal signs associated with infection [41].
Metazoan Parasites
The subcategory with the largest number of infectious disease articles (27%) was met-
azoan parasites. This body of research was well summarized in 2021 as an extensive liter-
ature review in addition to describing the intestinal helminth communities from hundreds
of additional NFSs [42]. While this work explored both spatial and temporal patterns of
infection as well as prevalence and abundance, samples were collected from presumably
healthy animals and, as with the overwhelming majority of the literature on the topic,
there was little association with pathology or population health impacts. Hookworm (Un-
cinaria lucasi) is an exception. The topic of hookworms made up more than half of the
metazoan parasite publications and has been well reviewed by Lyons et al. (2011).The
pattern of disease is variable by region, with hookworms recognized as a major cause of
death in NFS pups in California but uncommon in other sites [43]. Gastric lesions associ-
ated with anisakid nematodes were identified in 21% of the stomachs from subadult males
harvested on St. Paul Island, Alaska, 2011–2013; down from 92% as reported from the
1960s [44].
Protozoan Parasites
Two reports of protozoal infection were reviewed. Significant pathology was at-
tributed to disseminated Toxoplasma gondii (diagnosed by IHC) infection in an adult fe-
male NFS that was stranded in California [45]. A brief description of histologically diag-
nosed sarcocystis in the muscle of a wild seal found on St. Paul Island was reported in the
1970s, but no additional information on the animal, or impact on the population, was in-
cluded [46].
3.1.2. Non-Infectious Disease
Neoplasia
Two case reports focused on neoplastic disease; both reports were on neonates found
dead on the Pribilof Islands, one of which had a renal fibrosarcoma [47] and the other
diagnosed with multicentric lymphoma in which viral particles were suspected, but not
confirmed, by electron microscopy [48]. A variety of neoplastic processes have been de-
scribed by Spraker and Lander including a fetal ganglioneuroblastoma, an adrenal cortical
carcinoma, ovarian dysgerminoma, fibromas, and a squamous papilloma [14].
Toxins and Contaminants
Twenty-eight percent of the disease publications focused on toxins or contaminants.
Overwhelmingly, these publications report contaminant levels in a variety of tissue or
secretory products, but are devoid of any association with individual or population health
or disease information (Table 1). There were two reports on algal toxins, most notably a
case series of stranded, multiple age class NFSs in California that characterized the clinical
and post-mortem disease in NFS with domoic acid poisoning, including central nervous
system signs and pathology of the nervous and cardiac systems consistent with disease in
other species [49]. Lower domoic acid and saxitoxin exposures in NFSs relative to other
marine mammals were attributed to differences in foraging behavior [50].
Oceans 2022, 3 309
Table 1. A summary of the identified literature on contaminants in NFS.
Contaminant
US
Japan
Heavy metals (e.g., mercury, cadmium,
arsenic, silver, vanadium) [51–57] [52,57–60]
Microplastics [61]
Persistent organic pollutants (
e.g., PCB,
DDT, PBDEs) [62–70] [71–74]
Radiocesium [75]
Trauma
: A
nthropogenic
Of the six articles focused on trauma, all reported traumas attributable to anthropo-
genic causes. The majority described the frequency and severity of NFS enganglement in
different parts of their geographic range collectively highlighting the hazards of fishing
materials and marine debris [76–79]. The energetics of entanglement were estimated in a
study on captive animals which highlighted the difficulty that entangled animals can have
both swimming and resting [80]. Enganglement as both a cause of death and cause of
observed chronic pathology was also described in the Alaskan necropsy case series
[14].
A single article described the pathology associated with acute head trauma sustained dur-
ing NFS harvest activities [81].
Trauma Non-Anthropogenic/Unknown Source
As noted above, all of the disease articles that focused on trauma were classified as
anthropogenic; however, non-anthropogenic or unknown trauma was a very common
finding in the necropsy study in Alaska [14]. Trauma in adults was largely the result of
fighting, while, in pups, crushing injuries and bite wounds were both commonly ob-
served.
Other
Seven of the disease papers were classified as ‘other’ by default as they failed to align
with the above criteria, but were broader than the congenital/metabolic category used by
[9]. Two of these presumably uncommon disease conditions in captive animals were writ-
ten up as case reports. These included an animal with gastric dilatation with volvulus and
a gastric intramural hematoma with hemoperitoneum, both of unknown origin [82,83].
The remaining articles focused on the ocular or oral cavity. Cross-sectional surveys of op-
portunistically collected eyes from both wild and captive NFSs, contributed general infor-
mation on gross and histologic changes in NFS eyes, but lacked associated information on
individual or population health impacts [84–86]. Similarly, two articles described dental
disease and temporomandibular joint pathology in museum collection NFS skulls, but
nothing was reported about the relationship between observed lesions and other causes
of morbidity or mortality [86,87].
An important condition of NFSs that was highlighted in the necropsy case series from
Alaska and California, was emaciation [14,15]. Emaciation was not only the most common
cause of death in NFS pups on St. Paul Island, but it has reportedly increased over time
[14]. A variety of additional conditions such as congenital anomalies
, predominantly mus-
culoskeletal, were described in the longtudinal necropsy study in Alaska
[14].
3.2. Health Classification
All of the 148 health and disease publications fit within one of the six determinants
of health categories, although interestingly only 15 (10%) contained the words ‘health’ or
‘healthy’ in the title or abstract. The overwhelming majority (50%) of the articles were
classified as biologic endowment. These were predominantly (89%) the infectious and
non-infectious disease articles described above, with the remaining nine studies focused
on fetal and pup growth and birth weight as related to survival or mortality, as well as
Oceans 2022, 3 310
several articles on reproductive indices. Thirty percent of the articles were classified as
abiotic environment. These were largely about exposure to toxins or contaminants in the
environment (n = 27, as included above) or anthropogenic trauma such as entanglements
described above (n = 5). The remaining papers classified as abiotic environment were not
included in any of the disease categories but described important topics such as the way
adverse weather conditions and extreme water temperatures impact seal survival and dis-
persal.
All the remaining determinants of health categories were represented, but consider-
ably less frequently. Needs for daily living (10%) included articles on how foraging be-
havior, food web dynamics, prey composition, and selection all affect NFS energetics and
overall success. For example, an article by Short et al. (2021) tied prey availability to NFS
pup survival by showing that commercial pollock fishing in close proximity to the Pribilof
Islands thinned out schools of fish that were normally readily available to lactating female
NFSs, which may have perpetuated low pup survival rates [88]. None of these articles was
represented in the disease classification system.
Social environment (4%) also had no overlap with the disease classification system.
These articles were largely investigations into inter- and intraspecific competition for
prey, natal sites, and territoriality. None of these articles were represented in the disease
category. Of particular interest were articles that linked this competition to population
trends, such as a study by Kuhn et al. (2014) that showed increased densities of NFS may
have negative effects on population growth, due to the increased energy output required
to obtain prey [89]. Articles classified as direct mortality pressures largely addressed im-
pacts from hunting and harvesting of NFSs with emphasis on how the sex of harvested
seals could impact population growth. A single study in this category describing pathol-
ogy associated with blunt head trauma in harvested seals [54], was also classified as trau-
matic, non-infectious disease. Only a single article that discussed the relationship between
NFS management and population carrying capacity [90] was included in human expecta-
tions. Three articles spanned more than one category and were subsequently classified as
‘multiple’.
4. Discussion
“Absence of evidence is not evidence of absence.”
- Carl Sagan
The presence and absence of information from these 50 years of peer-reviewed NFS
literature can both help to inform research and management programs specific to the spe-
cies. Traditionally, such programs are disease focused and based on conditions that have
been observed in the past, and there is a good foundation of NFS disease literature avail-
able to build upon. A particularly noteworthy contribution is the 20-year case series con-
ducted on St. Paul Island, Alaska, by Spraker and Lander [14]. This work involved post-
mortem examination of more than 3000 NFSs, creating a dataset that could be explored
for trends, and could facilitate the collection of biologic samples, generate several hypoth-
esis, and generally serve as a foundation for several other projects included in this review
(e.g., [25,28,29,43,44]). Post-mortem examination has been cited as ‘the single most critical
step in diagnosis for general wild animal disease surveillance’ [91]. There are several rea-
sons for this including circumvention of hazards related to capture and handling of live
animals, necropsy as a source of information on variations in ‘normal’ within a species,
identification of several concurrent disease or physiologic changes, and as a sample source
for more targeted disease investigations [92–94]. The long-term necropsy program on St.
Paul Island is a unique opportunity that could serve as a foundation to which other NFS
health and disease studies should be linked.
If necropsy data is to be used for these purposes however, it is important to under-
stand both strengths and limitations of the work. The study of pinniped pathology is well
known to be biased by issues of access; overrepresenting animals housed in captive
Oceans 2022, 3 311
facilities, species and age groups that strand more commonly, or populations that are eas-
ier to observe and sample [95]. Unique access to NFSs highlights this pathology bias. Nec-
ropsy work that has been conducted on St. Paul Island has been made possible by way of
a ‘catwalk system’, i.e., raised walkways above some NFS rookeries from which research-
ers can safely observe a subset of NFS (those on the rookery) and collect deceased animals
using hooked poles. Limitations to sample collection include size of the deceased animal
(light enough to be picked up) and proximity to the catwalks. Animals included in the
Spraker and Lander paper were overwhelmingly (90%) pups [14] which were largely rep-
resentative of the number of pups in that location at that time and the lower survival
probability of young animals, however, causes of death and disease are variable by life
stage which limits the external validity of pup necropsy findings. Strategically aligning
(e.g., examination, record keeping, sample collection, testing, and archiving) the necropsy
program with other collection opportunities, such as young adult males harvested for
consumption, could partially help to address this problem. Additionally, as the catwalk
system serves as a sampling transect for the necropsy program, it will be important to
ensure it is appropriately located relative to the rookery. Aerial photos clearly demon-
strate changes in the distribution of NFSs on rookeries as the population declines, result-
ing in fewer animals adjacent to the catwalks [96,97]. Analysis of necropsy findings in
conjunction with appropriate population (‘denominator’) information will help to keep
findings in context.
The complete post-mortem examination process is typically overseen by
pathologist(s) and informed by patient history, signalment, clinical disease, and gross nec-
ropsy findings. The nature and severity of changes seen within an organ system then drive
the selection of additional diagnostic tests to confirm or exclude etiologic agents with the
potential to cause the observed disease. However, because some etiologic agents of con-
cern may not cause grossly identifiable pathology in any or all animals, routine screening
of tissues for pathogens, toxins, or contaminants may be warranted. Despite numerous
publications on the topic, as highlighted in this review, infectious disease was rarely (3%)
implicated as a cause of pup mortality in the St. Paul Island necropsy study [14]. Unfor-
tunately, systematic screening of tissues for pathogens, toxins, or contaminants, does not
appear to have been conducted. Standardized protocols used to screen for infectious and
non-infectious agents can ensure that the post-mortem examination is sensitive enough to
identify any etiologic agents of concern.
As with biases associated with accessing animals for necropsy, our review high-
lighted biases associated with different sample types. The majority of the infectious dis-
ease articles reviewed in this study focused on intestinal parasites, however, with the ex-
ception of well described pathological and epidemiological investigations into hookworm
infections [43], this work is largely devoid of associated health or disease information,
making it challenging to tie much of the historical parasitological research into future
monitoring programs. As noted in other reviews of Alaskan wildlife, the overrepresenta-
tion of parasites in disease research is likely, at least in part, to be a function of collection
bias as fecal samples are relatively easy to collect [8].
Similarly, there were many publications on diseases of the NFS placenta (e.g.,
[25,27,29,32]). Publications on C. burnetii are undoubtably overrepresented in the litera-
ture because of the novelty of this pathogen in the species and geographic location, as well
as its potential risk to humans. However, as with the collection of pups and material for
parasitological investigations, sample availability undoubtably adds additional bias as the
opportunity to systematically collect wild animal placentas is extremely uncommon, and
therefore novel. While several of the pathogens within the NFS placentas have been
demonstrated to cause disease in other species, including humans, use of this sample
without any information on the associated maternal and pup outcomes makes it impossi-
ble to link these findings to the overall health of the population. Awareness of sample
biases will be important to consider in future research efforts.
Oceans 2022, 3 312
Failure to link disease research to individual or population outcomes was consistent
across the NFS literature overall. This gap supports arguments for a paradigm shift away
from the siloed, single agent focus of wildlife disease programs to the more holistic,
health-oriented perspective that encompasses the broader social and environmental fac-
tors that are needed in resilient animal populations [10,98]. Doing this requires strong
collaboration between those with broader (e.g., population, ecosystem) perspectives and
experience, and also recognition that disciplines not classically thought of as ‘health’ do-
mains are, in fact, most central to this work. Such disciplines may include, but are not
limited to, wildlife (including fisheries) biologists and ecologists, oceanographers, climate
scientists, immunologists, and toxicologists. Through these collaborations, we would be
better positioned to transition the narrative away from looking at sick animals and screen-
ing for what is wrong (disease focus) to looking at healthy populations and identifying
characteristics that help them be well (health focus).
As part of this review we included, and then subclassified, articles based on relevance
to the six determinants of wildlife health proposed by Wittrock et al., 2019 [11]. The rank
order of frequency of these in the NFS literature review (biologic endowment, abiotic en-
vironment, and needs for daily living being the top three) were similar to those of barren
ground caribou (Rangifer tarandus groenlandicus) and Pacific salmon (Oncorhyncus spp.)
[11]. It should be noted that our search methods (only including the common and scientific
names for NFSs) differed from those of Wittrock et al. and the resulting list of publications
is unlikely to fully represent the scope of research into factors influencing NFS health. For
example, there is undoubtably a vast body of literature on abundance and distribution of
NFS prey species that is relevant to NFS nutrition (‘needs for daily living’), but these pub-
lications are unlikely to have NFSs as a key word, and therefore, would not have been
identified in our literature search. By restricting full-text review to articles with the com-
mon and/or scientific names for the NFS in the title or abstract we undoubtably excluded
some relevant disease articles as well. That said, it is notable that our review included
peer-reviewed publications spanning all six of the health determinants, suggesting that
this framework may be appropriate for use in a NFS health program in the future. Inter-
estingly, only 15 (all ‘biologic endowment’ or ‘abiotic environment’) of the 148 reports in
the final review contained the words ‘health’ or ‘healthy’ in the title or abstract, the ma-
jority (n = 12) of which were also classified as disease publications. This highlights the fact
that although the work is relevant to factors influencing the health of NFSs, numerous
researchers and authors may not communicate it that way. Similarly, of the 148 reports
included in our review, 50 publications were determined to be important to NFS health
but were not classified as ‘disease’ articles and half of the health determinant categories
such as (‘needs for daily living’, ‘social environment’, and ‘human expectations‘) con-
tained no articles that were also captured in the ‘disease’ category. Collectively, this indi-
cates how much important information could be missed using only a disease centric ap-
proach. Work is needed to engage with individuals and groups working in these more
diverse branches of science that contribute to NFS population ‘health’, covering topics that
include, but are not limited to, ecosystem dynamics, food availability, nutrition, genetic
diversity, and stress.
To address concerns regarding bias and limitations of the historical work, and ways
to better focus on health outcomes, it would be prudent to convene a group of NFS-in-
vested individuals to develop a strategy for assessing health and disease of NFSs in the
future. As resources (e.g., samples, time, and funding) are finite, it will be necessary to
prioritize indices and conditions upon which to focus. Prioritization models developed
and used successfully in public health livestock and wildlife domains (e.g., [99–103]) could
help to inform similar efforts for the NFS. The general process involves compiling a list of
conditions for prioritization, selecting appropriate measurement criteria, defining the
range and weighting of levels for each criterion, aggregating scores for each condition,
and ranking conditions by their total score for the final ordering [104]. While specific cri-
teria may vary by species and location, those used in animal health typically include:
Oceans 2022, 3 313
1. General characteristics of the condition in question (e.g., susceptible hosts, reservoirs,
speed of spread, virulence, pathogenicity, and immune response);
2. Animal health impacts (e.g., morbidity, mortality, reproductive consequences, and
welfare considerations);
3. Public health impacts (e.g., transmissibility to humans, severity of human disease,
opportunities for human protection, food safety and security, bio/agroterrorism po-
tential, spread amongst humans, and economic consequences);
4. Regulatory impacts (e.g., local, federal, or international trade consequences);
5. Mitigation (e.g., diagnosis, prevention, and treatment).
Our review has highlighted a body of literature that could aid in the prioritization
process, particularly for diseases of the NFS. For example, several pathogens identified in
this scoping review are zoonotic and some can have significant public health impacts. In-
dividuals handling marine mammals, including researchers, have unique exposure op-
portunities to a variety of organisms they may not normally encounter [105,106]. Some of
the zoonotic pathogens reported in NFSs, such as calicivirus or parapoxvirus, typically
elicit only mild skin lesions, while others such as C. burnetii and Brucella spp., have the
potential to cause more severe systemic disease [105,107]. Emphasis should be placed on
conditions that are overrepresented in cohorts with increased opportunities for, or evi-
dence of, exposure such as C. burnetii where the seroprevalence of Alaskan Native resi-
dents of the Pribilof Islands was almost four times the U.S. average [108]. Efforts should
also be made to systematically survey for pathogens that may not have not been a topic
of significant NFS research in the past, but are zoonotic, common in sympatric species,
and have demonstrated ability to infect NFSs, such as Toxoplasma or Leptospira [45,95,109].
Engagement with public health personnel as part of the prioritization effort is scientifi-
cally justified and socially relevant, but may also be logistically and financially strategic
as human and public health agencies can often access resources (e.g., laboratory expertise
and funding sources) not typically utilized by wildlife professionals.
Similar to the benefits of collaborating with public health professionals, involving
those who study conditions in sympatric species aids in the development of the initial
disease list for use in the prioritization process. This is particularly important for novel
animal health threats where little species-specific information is available; therfore, learn-
ing from others can help inform the development of a surveillance or testing program as
necessary. Spatially clustered health risks (e.g., elevated mercury in Steller sea lions from
the western part of their range [110]) could inform targeted data or sample collection. This
collaborative effort may benefit multiple species. For example, infectious diseases such as
leptospirosis or toxoplasmosis occur infrequently in NFSs [36,45], but can cause devastat-
ing disease in other marine species such as California sea lions and monk seals [111,112].
As the ecology of these pathogens is complex, synthesis of information from different spe-
cies, geographic regions, and different environmental conditions may elucidate new in-
formation.
Finally, this prioritization process needs to be inclusive of all stakeholders and per-
spectives. Wild animals are a public resource. In addition to engaging scientists who may
not already consider themselves a health professional as previously described, the NFS
health prioritization should include members of the public. Involving the public, even
those with little background on the topic, in zoonotic disease prioritization has been
shown to yield meaningful results [113]. Northern fur seals are an important subsistence
resource for indigenous people throughout their range, most notably Aleuts [114]. The
benefit of incorporating local and traditional knowledge (LTK) is well recognized [115–
117] and NFS population declines are a sign of changes within the Bering Sea ecosystem
that is well recognized by the local community [118]. Frameworks to aid in the systematic
and transparent approach to include LTK in wildlife assessments already exist [119]. In-
clusivity of local hunters, fisherman, and indigenous populations with their unique LTK
would make for a more holistic NFS health program.
Oceans 2022, 3 314
Working as a team of NFS health and disease experts to prioritize and strategize on
future research efforts would help to address several limitations present in this study. Our
review included only English literature which undoubtably restricted the number of arti-
cles included. NFSs range throughout the North Pacific and research is conducted in many
countries other than the United States. By convening an international team of NFS re-
searchers and managers, publications identified in this review can be expanded to include
results and perspectives from others that may not be captured here. Similarly, the smallest
of our NFS health determinant categories was human expectations which was also likely
a bias because of our exclusion of ‘grey literature’ in this review. According to [11], this
category should include factors such as management policy, education programs, habitat
funding and economics, and traditional knowledge. NFSs are federally managed, and
therefore, inclusion of reports from governing bodies would markedly expand the avail-
able information on this topic. Similarly, the peer-reviewed scientific literature is not a
channel though which LTK is typically shared, re-emphasizing the need to integrate this
information using other established methods [119]. Collaboration would also facilitate the
synthesis of ‘negative’ results which could be extremely important information for the
prioritization process. The peer-reviewed literature is biased to focus on novel diseases
and less likely to publish ‘negative’ findings [9]. Local people and managing agencies play
a role in approving sample collection and animal handling; their records undoubtably
contain considerably more information than is represented in the peer-reviewed litera-
ture.
5. Conclusions
This review of 50 years of scientific literature highlights the fact that NFS health is
more than the presence or absence of innumerable disease-causing agents. Addressing the
complexity of what makes an individual or population healthy requires a system ap-
proach to look at the many interacting factors (e.g., determinants of health and cumulative
effects) from many different perspectives. Results of this work will be helpful in the next
phase of an inclusive prioritization process that includes strategic planning and establish-
ing mid- and long-range goals for consistent and targeted assessment and monitoring of
NFS health.
Author Contributions: Conceptualization, C.D., K.P., C.S., K.S. and V.J.; methodology, C.D., K.P.,
J.V. and V.C.; formal analysis, J.V. and V.C.; investigation, V.C., K.P., C.S., J.V., V.J., K.S. and C.D.;
data curation, V.C. and J.V.; writing—original draft preparation, C.D., J.V., V.C. and K.P.; writing—
review and editing, V.C., K.P., C.S., J.V., V.J., K.S. and C.D.; visualization, V.C., K.P., J.V. and C.D.;
supervision, C.D.; project administration, C.D.; funding acquisition, C.D., C.S., K.P. and V.J. All au-
thors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the NOAA Fisheries AK Region under award
NA16NMF4390028 to Colorado State University.
Institutional Review Board Statement: Not applicable; retrospective literature review that did not
involve live animals.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable
Acknowledgments: This work was inspired by thoughtful discussions with our marine mammal
colleagues, particularly Mike Williams, Tom Gelatt, and Rolf Ream. Special thanks also to Maddi
Funk and Ah Young Kim for their assistance preparing our graphical abstract.
Conflicts of Interest: The sponsors had no role in the design, execution, interpretation, or writing
of the study.
Oceans 2022, 3 315
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Background: Q fever is a febrile illness caused by infection with the bacterium Coxiella burnetii. It is most often transmitted by inhalation of the bacteria after it is shed by infected livestock. Recent studies have found very high C. burnetii infection rates among marine mammals, but it is not known if shedding by marine mammals creates a risk of Q fever among humans. To better understand infection of humans with exposure to marine mammals, the prevalence of antibodies against C. burnetii in serum samples taken from Alaskan Native persons residing on the Pribilof Islands was evaluated. The Pribilof Islands support large populations of northern fur seals infected with C. burnetii that may increase the risk of exposure for island residents. Methods: Serum testing for IgG antibodies against C. burnetii (phase I and phase II) was performed, and demographic data were analysed utilizing banked serum specimens drawn from island residents from 1980 to 2000. Results: The overall seroprevalence rate was 11.6% (95% CI = 9.3%-14.4%; 72/621). This is higher than the previously reported 3.1% (95% CI = 2.1%-4.3%) seroprevalence for the U.S. Population: Conclusions: These results suggest that Alaskan Native persons may be at higher risk for exposure to C. burnetii than the general US. population, possibly due to proximity to large populations of infected marine mammals.
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The systematic annual observations of the northern fur seal rookery on Tyuleniy (= Robben) Island, Sea of Okhotsk, were started in 1958. Since 1975, all seals entangled in marine debris have been registered. Some of the data on this issue, collected on the island in the late 20th century, were published earlier. This report provides data for the period of completion of the commercial sealing (from 1998 to 2013). During this period, a total of 867 fur seals were observed entangled in marine debris, including 212 bulls, 97 half-bulls, 223 bachelors, and 335 females. The estimated mean annual number of entangled fur seals in 1998-2013 is 1113 individuals. Marine debris was found mainly on the neck and, less frequently, on the head and front flippers of the animals. This included pieces of fishing nets, packaging bands, ropes, fishing lines, and other items of anthropogenic origin.
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Environmental microplastics are widely documented in marine life and bioaccumulation may present risks to marine predators. Investigations of microplastics in marine mammals are increasing, though none have examined animals routinely consumed by humans. Here, we investigate microplastic exposure in the northern fur seal (Callorhinus ursinus), a species consumed by humans, using fecal material. We examined 44 feces (scat) at sites encompassing the seals' eastern Pacific range. Multiple contamination control measures were implemented, including field and laboratory controls. Fragments were the most common microplastic recovered, in 55% (24/44) of scat and no controls (range 1 to 86 fragments/scat, mean 16.6, sd 19.1). Microplastic fibers were recovered from 41% of scats (18/44), though some controls contained fibers confounding fiber results. Fecal analysis documented northern fur seal exposure to microplastics throughout their eastern Pacific range.