Here we summarize the range of enteric bacterial pathogens infecting southern sea otters, including both classic fecal indicators (Salmonella
, C. perfringens
, C. difficile
and E. coli
O157:H7) and species that are more typically associated with water contact or consumption of food harvested from aquatic environments (Vibrio
spp. and P. shigelloides
). Our findings in sea otters were similar to reports of the prevalence of opportunistic enteric bacterial pathogens in marine invertebrates [1
] (). Miller et al. [29
] tested marine and estuarine invertebrates from central California for contamination by Salmonella
, C. perfringens
and P. shigelloides
, facilitating comparison of enteric bacterial prevalence between sea otters and their invertebrate prey. Over 80% of mussel (Mytilus californianus
) batches were positive for at least one enteric bacterial pathogen. The most common bacteria in marine invertebrates and sea otters were C. perfringens
spp., including V. parahaemolyticus
, non-O1 V. cholerae
and V. alginolyticus
. However, Salmonella
spp. detection was uncommon in both groups. Of the various bacteria above, only E. coli
O157:H7 was never identified from sea otters or marine invertebrates [29
], although this pathogen was recently traced to produce grown in coastal croplands draining into prime sea otter habitat [7
Environmental factors influencing detection of pathogenic bacteria or protozoa in sea otters and freshwater or marine invertebrates from coastal California.
Based on reports demonstrating that sea otters are excellent environmental sentinels [24
], we predicted that isolation of these opportunistic bacterial pathogens from sea otter feces would be more common in otters with greater exposure to freshwater runoff, sewage or more urbanized coastlines. Indeed, otters sampled near urbanized areas or regions with high freshwater runoff were more likely to test positive (). Other significant risk factors for bacterial isolation included male sex, sample season (wet or dry, depending on the bacteria of interest) and otters that died. The increased risk observed for males may be due to greater rangewide movement, leading to higher exposure to coastal point-sources of pathogen contamination, and stress due to competition for mates, food and territories.
Freshwater runoff has also been significantly associated with Toxoplasma gondii
infection in sea otters [24
]; the most likely source of exposure is water or prey contamination by feces from wild and domestic felids. Indeed, unique T. gondii
strains shared by terrestrial carnivores, shellfish and sea otters have been identified [25
]. Exposure to freshwater runoff and recent coastal precipitation were also risk factors for detection of Cryptosporidium
in California mussels [28
] (). The range of bacteria isolated from otter feces during the wet and dry seasons were similar to those isolated from sympatric marine invertebrates (). Invertebrates collected inside muddy embayments were more often positive for opportunistic enteric bacteria than those living in sandy areas, and freshwater clams collected close to the ocean were more likely to test positive than those collected further upstream [29
] (). Suspended mussels and benthic invertebrates from the same location were often culture-positive at the same time, suggesting that bacteria were passing through in the water column. Collectively, these findings suggest that bacterial contamination of invertebrates occurs commonly along interfaces between fresh and saltwater; these nearshore areas are favored habitat for sea otters.
The importance of surface runoff as a contributor of fecal pollution is emphasized by the fact that the largest river in central California discharges 432 times more untreated water to the ocean every year than the largest municipal sewage plant (Central Coast Water Quality Control Board, unpublished data). Land-based fecal deposition by pets, livestock and terrestrial wildlife inhabiting coastal watersheds may be substantial; in one coastal California community, fecal deposition by domestic cats alone was estimated at 107 metric tones/year, or 26 kg/ha [8
]. When nearshore marine environments are contaminated with feces for prolonged periods, opportunistic enteric bacteria may concentrate in sediments, invertebrate biota and resident vertebrates [9
]. Colonization of zooplankton and suspended marine particles by Vibrio
has been reported [20
], suggesting additional means for bacterial dissemination in marine habitats.
Associations between bacterial pathogen detection in sea otters and exposure to municipal sewage could not be determined in this study, because no otters were obtained from areas exposed to heavy discharges of municipal sewage. Additional nearshore fecal loading due to sewage spills, agricultural impoundments, septic tanks, lawns, pastures, hardscape and boats were not accounted for in this study.
In the current study, coastal urbanization proved to be an important risk factor for opportunistic enteric bacterial infection of sea otters. An increased density of paved surfaces in urbanized communities has been linked with negative impacts to local waterways: Young and Thackston [42
] found that streams in residential communities with increased hardscape had higher bacterial loads during storms than those from less developed communities. Paved surfaces such as parking lots, streets and sidewalks may facilitate land-sea transport of pet waste. Other factors that could promote bacterial contamination of water located adjacent to urbanized coastlines include fertilizer runoff (through nutrient enrichment), discharges of heated water, or algal blooms that can trigger explosive bacterial proliferation through enhanced bioavailability of dissolved organic material [20
Some interesting trends were noted for the various groups of enteric pathogens isolated from sea otters. C. perfringens
was more commonly isolated from otters during the cold, wet season, similar to prior reports for sympatric freshwater and marine invertebrates [29
] (). This finding could be due to greater downstream flushing during winter or more favorable conditions for C. perfringens
]. Postmortem proliferation likely contributed to higher detection of this bacterium in feces from necropsied otters. C. perfringens
appears to be part of the normal anaerobic microflora of otters and other marine species [3
], but it can also be an opportunistic pathogen [33
] and C. perfringens
-associated necrotizing enteritis was occasionally observed in our sample of necropsied otters.
This is the first report of isolation of both C. difficile
spp. from sea otters. The prevalence of C. difficile
infection was significantly higher in dead otters, suggesting possible disease implications and/or postmortem overgrowth. Common terrestrial hosts for C. difficile
include dogs, horses, humans and wildlife, and asymptomatic fecal shedding is common [13
]. The majority of Campylobacter
isolates were C. lari
-like and C. coli
, along with some less well characterized strains. Environmental sources for Campylobacter
include sewage, urban or farm runoff and birds [1
]. Contamination of shellfish beds by C. jejuni
has been reported from California, Washington and Oregon [1
]. The pathogenicity of Campylobacter
spp for some terrestrial mustellids is well established [4
]; in the current study, a few necropsied sea otters with enteric Campylobacter
infections exhibited mild intestinal mural thickening. A higher prevalence of fecal shedding of C. jejuni
(48.5%) was reported for sick, stranded elephant seals (Mirounga angustirostris
) in California, compared to healthy seals (13.3%) [37
infection was uncommon in sea otters (< 1.0%) compared to the frequency of detection in sympatric terrestrial and marine vertebrates [11
]. A high prevalence of Salmonella
infection (13.6%) was reported in California sea lions [37
] and sick, stranded elephant seals were 41 times more likely to test positive for Salmonella
than natal-site seals [39
contamination has been demonstrated in mussels (Mytilus
spp.), oysters (Ostrea edulis
), clams (Corbicula
spp.) and cockles (Cerastoderma
spp.), even at fecal coliform concentrations below regulatory levels for human consumption. In a survey of marine invertebrates from coastal California, S.
Typhimurium and S.
Heidelberg were isolated from Pismo clams (Tivela stultorum
) and fat innkeeper worms (Eurechis caupo
In the current study, nearly all Salmonella
-infected otters were recovered near pinniped rookeries, where densely packed, immunologically naive pinnipeds may experience enhanced fecal shedding of facultative pathogens. Salmonella enterica
serovars reported from Pacific coastal marine mammals and birds include S.
Saint Paul, S.
Montevideo and S.
]. Infection by Salmonella
Newport appears to be especially prevalent among California wildlife. Salmonella
. Enteriditis, S
. Saint Paul and nontypeable Salmonella
spp. have all been isolated from sea otters [35
], including a few animals in the present study with lesions of enteritis, intestinal volvulus and/or septicemia. However, some clinically normal sea otters also tested positive. Salmonella
infections in other marine species have been associated with enteritis, cholecystitis, abscesses, pneumonia and septicemia [11
Sea otters sampled during the dry season were more likely to test positive for V. cholerae
, V. parahaemolyticus
and V. alginolyticus
, similar to findings for sympatric freshwater and marine invertebrates (). Many Vibrio
spp. reach peak numbers in water, sediment and invertebrates during the summer [15
] and high isolation rates from otters may reflect high environmental exposure. In California, non-01 V. cholerae
numbers may increase 5 to 56-fold during summer, with the highest concentrations in waterways with the greatest fecal pollution, as indicated by total coliform counts [16
]. Isolated from 19% of otters, V. parahaemolyticus
is the single most common cause of seafood-associated human illness in the USA [38
]. This bacterium is cosmopolitan in saline and brackish water; human disease is commonly associated with consumption of raw or undercooked shellfish harvested from waters > 15 °C [23
]. Vibrio parahaemolyticus
has been isolated from a wide range of invertebrates and can proliferate in shellfish, increasing 790-fold within 24 h at 26 °C [29
]. In the current study, systemic V. parahaemolyticus
or related Vibrio
spp. infections were detected in some otters with lesions of enteritis and septicemia.
and the related bacterium V. fluvialis
were obtained primarily from feces of live otters captured during periods of decreased precipitation, and from otters inhabiting regions that were less impacted by surface runoff or coastal urbanization, such as the Big Sur coast. Thus, fecal isolation of V. alginolyticus
and V. fluvialis
appeared to be representative of live, ostensibly healthy otters from more pristine habitats that were likely to be actively feeding when sampled. For other marine wildlife, isolation of V. alginolyticus
is relatively common and pathogenicity appears to be relatively low [5
]. However, a few sea otters in the current study exhibited lesions of septicemia in association with isolation of V. alginolyticus
from multiple tissues. Isolation of V. alginolyticus
from marine invertebrates was positively correlated with salinity and inversely correlated with precipitation [29
], suggesting that this bacterium prefers saline habitat with minimal freshwater influence.
was isolated from 15 otters. Like the Vibrio
s, P. shigelloides
is endemic to estuarine and marine habitats and can be an opportunistic pathogen [14
]. The degree of pathogenicity of P. shigelloides
for marine mammals is debated, although P. shigelloides
has been isolated from feces, lungs, livers and brains of Pacific coastal pinnipeds [39
]. It was occasionally isolated from the blood and viscera of necropsied sea otters in this study and was considered to be a weak opportunistic pathogen.
Our study findings offer insights for guiding public policy and management decisions regarding southern sea otter population recovery and coastal water quality. Our epidemiological data suggest that California otters are at highest risk of enteric infection by opportunistic bacterial pathogens when living near more urbanized coastlines, such as those along Monterey Bay, and regions with moderate to high freshwater runoff. Although our investigation was focused on sea otters, the potential impacts of this research extend well beyond otter health and conservation, because both sea otters and humans rely on the health of coastal ecosystems and the safety of marine foods for their survival.