| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Alaska Department of Fish and Game, 1300 College Road, Fairbanks, Alaska 99701-1599, USA
2 Oklahoma Animal Disease Diagnostic Laboratory, Oklahoma State University, Stillwater, Oklahoma 74078, USA
3 Statutory and Exotic Bacteria, Veterinary Laboratories Agency, New Haw, Addlestone, Surrey, KT15 3NB United Kingdom
4 Alaska Department of Fish and Game, 1255 W 8th Street, Juneau, Alaska 99802-5526, USA
6 Corresponding author (email: itrap2{at}acsalaska.net)
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Harbor seals are found primarily within 50–60 km of shore (Lowry et al., 2001; Small et al., 2005), where they feed, haul out to rest, give birth, care for their young, and molt. Females give birth to single pups once a year, usually in the first half of June in Alaska. Pups are weaned when they are 3–6 wk old. Adult females breed about 2 wk after their pups are weaned, and give birth about 11 mo later. Female harbor seals first become pregnant when they are 3–7 yr old (Hoover-Miller, 1994). Most information about the foods of harbor seals was collected in the mid-1970s (Pitcher and Calkins, 1979). The major prey in PWS and the Gulf of Alaska include pollock (Theragra chalcogramma), octopus/squid (class Cephalopoda), capelin (Mallotus villosus), Pacific cod (Gadus macrocephalus), and herring (Clupea pallasi).
Brucella was first isolated from the organs of four common seals (Phoca vitulina), two harbor porpoises (Phocoena phocoena), and one common dolphin (Delphis delphis) originating from the Scottish coasts (Ross et al., 1994). Brucella has been reported to cause abortion in bottlenose dolphins (Tursiops truncatus) in the USA (Ewalt et al., 1994; Miller et al., 1999). In addition, serologic evidence of Brucella infection exists in Atlantic walruses (Odobenus rosmarus rosmarus) and ringed seals (Phoca hispida) of Arctic Canada (Nielsen et al., 1996). Evidence of Brucella infection in Pacific harbor seals (Phoca vitulina richardsi), California sea lions (Zalophus californianus), and harbor porpoises in Puget Sound, Washington, USA has also been reported (Payeur et al., 1998). In the North Pacific, Brucella-associated testicular granulomas in common minke whales (Balaenoptera acutorostrata) have been reported. Molecular characterization of DNA isolated from testes that grossly had granular lesions showed that Brucella from North Pacific minke whales was different from terrestrial and North Atlantic marine mammal Brucella strains (Ohishi et al., 2004). In the Southern Hemisphere, detection of anti-Brucella antibodies in Weddell seals (Leptonychotes weddellii) from Cape Shirref, Antarctica (Blank et al., 2002) suggests the possibility of widespread infection. Brucella spp. have been isolated from numerous species of terrestrial animals, and they cause abortion in the majority of these species (Corbel and Morgan, 1975). It is therefore possible that Brucella spp. infections can also cause reproductive failure in marine mammals.
Phocid herpesvirus-1 (PhoHV-1; Varicellovirus, Alphaherpesvirinae) was first identified in 1984 when it caused the deaths of 11 captive harbor seal pups in a nursery in the Netherlands (Osterhaus et al., 1985). Mortality caused by PhoHV-1 infection has been observed only in captive animals, including neonates, seals acutely infected with phocine distemper virus (PDV), or seals that have been otherwise immunocompromised.
Clinical signs of PhoHV-1 disease included elevated body temperature, inflammation of the oral mucosa, nasal discharge, coughing, vomiting, diarrhea, anorexia, and lethargy (Visser et al., 1991). Duration of the illness ranged from 1 to 6 days (Borst et al., 1986). Interstitial pneumonia and necrosis of hepatic parenchyma were the primary histologic lesions. Less significant changes were also observed in kidneys, spleen, and lymph nodes (Borst et al., 1986).
Virus is shed in nasal and ocular discharges from naturally- and experimentally-infected animals (Horvat et al., 1989; Harder et al., 1997). Presumably, natural transmission occurs by means of aerosols or direct contact, as in other alpha herpesvirus infections.
Serum samples from 49 free-ranging harbor seals that were involved in the 1988 PDV epizootic in the North Atlantic yielded a PhoHV-1 antibody prevalence of approximately 50% (Frey et al., 1989). Despite this high antibody prevalence, PhoHV-1 was isolated from only four of 112 harbor seals that died during the 1988 PDV epizootic (Frey et al., 1989).
A second herpesvirus, phocid herpesvirus-2 (PhHV-2), has been isolated from a captive California sea lion (Kennedy-Stoskopf et al., 1986), free-ranging adult harbor seals from the North Sea (Lebich et al., 1994), and free-ranging harbor seals from the North Atlantic offshore of the United States (Harder et al., 1996). Based on nucleotide sequence data, PhHV-2 is a gamma-herpesvirus (Harder et al., 1996). There is no evidence that PhHV-2 causes clinical disease in pinnipeds.
Herpesviruses have been implicated in recent fatal and nonfatal infections of harbor seals in the North Pacific. Twenty-six harbor seals were collected during the investigation of the 1989 Exxon Valdez oil spill in PWS, Alaska, USA. One male had lesions on the penis and prepuce. Intra-nuclear inclusion bodies typical of herpesvirus were observed during histologic examination of the lesions (Spraker et al., 1994). The death of a single harbor seal off the coast of Washington, USA, in 1990 was attributed to a herpesvirus. This diagnosis was based upon gross lesions, light microscopy, and electron microscopy. Hepatic and adrenal necrosis were found in 12 harbor seal pups that died at a rehabilitation center in Sausalito, California, USA, in 1990. Herpesvirus virions were detected in these necrotic areas by use of electron microscopy (Lowenstine et al., 1992).
Herpesviruses have also been detected in other Northern Hemisphere marine mammal species, including harbor porpoise (Kennedy et al., 1992), California sea lion (Kennedy-Stoskopf et al., 1986), sea otter (Enhydra lutris) (Harris et al., 1990), and beluga (Delphinapterus leucas) (Barr et al., 1989).
A previous serologic survey of several marine mammal species (including harbor seals) from Alaskan waters revealed exposure to both PhoHV-1 and PhHV-2 (Zarnke et al., 1997). Serum antibody prevalence for PhoHV-1 was 100% in 25 apparently healthy Weddell seals and three apparently healthy crabeater seals (Lobodon carcinophagus) from the eastern Weddell Sea (Harder et al., 1991). Neutralizing antibodies against PhHV-2 have been detected in a small cohort of harbor seals of the North Sea but not in Weddell seals of Antarctica (Lebich et al., 1994).
Phocine distemper virus (Morbillivirus, Paramyxoviridae) was first isolated from harbor seals following the 1988 epizootic off northwestern Europe (Osterhaus et al., 1990). Clinical signs included respiratory distress and oculonasal discharge (Kennedy et al., 1989). The primary postmortem finding was severe pneumonia (Kennedy et al., 1989).
An estimated 18,000 seals died during the 1988 PDV epizootic (Osterhaus et al., 1990). Harp seals (Phoca groenlandica) have been implicated as a reservoir species and a possible source of PDV for this major die-off (Duignan et al., 1994). Subsequent investigations indicate continued transmission of PDV in the waters of northwestern Europe (Visser et al., 1993). In 2002, approximately 22,000 seals died in a second PDV epidemic in northwestern Europe (Müller et al., 2004).
Several thousand Lake Baikal seals (Phoca sibirica) died in Russia in 1987. Retrospective investigation implicated canine distemper virus as the cause of this mortality (Grachev et al., 1989).
Recent research revealed morbillivirus exposure in additional European species, including gray seal (Halichoerus grypus) (Harder et al., 1991), harbor porpoise (Kennedy, 1990), and Mediterranean striped dolphin (Stenella coeruleoalba) (van Bressem et al., 1991).
Identical or closely-related morbilliviruses have been identified in recent years from several species on the Atlantic coast of North America, including harbor seal (Duignan et al., 1993), harp seal (Daoust et al., 1993), walrus (Duignan et al., 1994), and ringed seal (Duignan et al., 1997).
The primary objective of this study was to determine the serum antibody prevalence of Brucella spp., PhoHV-1, PhHV-2, and PDV in harbor seals from four regions of coastal Alaska. The secondary objective was to determine the relationship between antibody prevalence and host sex, age, year of capture, and geographic region.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Standard descriptive data (sex, location, and date of capture) were recorded for each animal. Animals were assigned to one of four age categories: pup, yearling, subadult, and adult. Age determination was based on body length and weight (Lowry et al., 2001). For the purpose of data analysis, samples were grouped by year of collection, which does not necessarily reflect year of exposure.
|
Sera were tested for evidence of exposure to Brucella spp. by means of both competitive (MacMillan et al., 1990) and indirect enzyme-linked immunosorbent assay (ELISA) (Alton et al., 1988). The competitive ELISA (cELISA) described by MacMillan et al. (1990) was used at a single dilution. Briefly, microtiter plates coated with lipopolysaccharide (LPS) extracted from B. melitensis (strain 16M) were prepared and 20 µl of the test serum was added, followed immediately by 100 µl of a dilution of an anti-Brucella LPS monoclonal-peroxidase conjugate. After incubation at room temperature, while shaking at 160 rpm, the plates were washed and the chromogen, o-phenylenediamine dihydrochloride, and the substrate, 3% hydrogren peroxide, were added. The color development was measured at 405 nm using a microtiter plate spectrophotometer. The optical density (OD) of the test samples was expressed as a percentage of the mean OD of the wells to which a negative control serum had been added. The negative control serum was obtained from a sheep that was clear of any clinical signs of disease and that was negative to all the standard serologic tests for brucellosis. Samples with an OD of less than 30% were classified as positive, and samples with an OD of more than 30% were classified as negative.
The indirect ELISA (iELISA) was based on that described by Alton et al. (1988) but differed in a number of respects. The iELISA requires anti-immunoglobulin conjugate with specificity for the immunoglobulin isotypes of the species under test. Such reagents were not available, but protein A has been shown to bind to the IgG of a range of marine mammals (Eliasson et al., 1988; Sikkema, 1989). The antigen was as described for the cELISA. The conjugate was a protein A-peroxidase conjugate. In this case the OD of the test samples was expressed as a percentage of the mean OD of the wells to which a positive control serum had been added. The positive control serum was obtained from a pig infected with Brucella suis. This sample was chosen as the control because it is detected using protein A. Samples with an OD of more than 30% were classified as positive, and samples with an OD of less than 30% were classified as negative.
Sera meeting the cELISA and iELISA criteria will be referred to as positive. In the absence of sera either from animals known to be free of Brucella spp. infection, or from animals from which Brucella spp. had been isolated, it is impossible to set the diagnostic thresholds for the tests with certainty. Therefore, thresholds were selected on the basis of experience gained in testing a wide range of terrestrial mammals for brucellosis from Great Britain.
Antibodies to PhoHV-1, PhHV-2, and PDV were detected using the serum neutralization test (SNT). The test was performed using the PDV1-2-6A strain of PDV, the A92-10/4 isolate of PhoHV-1, and the A92-10/5 isolate of PhHV-2. The viruses were grown in either Vero cells (PDV and PhHV-2) or Crandell feline kidney (CRFK) cells (PhoHV-1). The SNT was performed following a modification of a microtiter method (Rossiter et al., 1985) as previously described for morbilliviruses (Saliki et al., 1993). Briefly, for PDV, serial twofold dilutions of heat-inactivated sera were made in duplicate columns of 96-well plates using the alpha modification of Eagle’s minimum essential medium, starting at a 1:4 dilution. For PhoHV-1 and PhHV-2, a single 1:4 dilution was made in duplicate wells. An equal volume (25 µl) of each virus, containing about 100 median tissue culture infective doses (TCID50) of the appropriate virus, was added to corresponding appropriate plates. This yielded a starting dilution of 1:8 for PDV and a single dilution of 1:8 for PhoHV-1 and PhHV-2. The virus-serum mixtures were incubated at 37 C for 1 hr in 5% CO2, and a Vero or CRFK cell suspension (150 µl containing 104 cells/well) was added to PDV/PhHV-2 and PhoHV-1 plates, respectively. The plates were incubated at 37 C in 5% CO2 for 4 days. The test was read by examining cell monolayers under an inverted microscope for virus-specific cytopathic effects (CPE). Antibody titers for PDV were expressed as the reciprocal of the highest dilution of serum that completely neutralized CPE in duplicate wells. Results for PhoHV-1 and PhHV-2 were scored as positive (absence of CPE in both wells) or negative (presence of CPE in one or both wells) at 1:8 dilution.
A generalized linear model (McCullagh and Nelder, 1989) with repeated measures was used to determine whether there was significant dependence of antibody prevalence on host characteristics: age, sex, year, or geographic region. The model used a logit link with a binomial distribution. Serologic test result is a binary response variable. Year was treated as a continuous variable. Age was treated as a categoric variable with four classes: pup, yearling, subadult, and adult. Geographic area was treated as a categoric variable with four classes: Kodiak, central Gulf of Alaska, PWS, and southeast Alaska. Sex was also treated as a categoric variable. All main and interaction effects of these variables were examined. During the modeling process, all higher-order terms were removed from the model if they did not substantially (P > 0.05) increase the fit of the model based on the deviance function compared to a chi-squared distribution (McCullagh and Nelder, 1989). The GENMOD procedure of the SAS statistical software package, version 8.02 (SAS Institute, Cary, North Carolina, USA), was used to fit the model with maximum likelihood parameter estimates.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Overall antibody prevalences for all four agents are presented in Table 1. The most striking feature was the difference in prevalence for PhoHV-1 (225/243, 93%) as compared to PhHV-2 (0/286, 0%).
|
). These differences were not statistically significant. However, prevalences for all three cohorts were significantly different from the prevalence for pups. Hence, we collapsed age into two classes: pups and nonpups. A difference in prevalence between nonpups (44/82, 54%), and pups (2/18, 11%) was detected (P = 0.0044).
|
). Hence, we collapsed geographic region into two classes, PWS and the other three regions. A significant difference (P = 0.0188) was detected between prevalence rates for the three regions (106/120, 88%) and PWS (119/123, 97%).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The interactive behavior of pinniped species, especially during haulout periods, should be considered as an opportunity for transmission. The isolation of Brucella from reproductive organs in marine mammals (Miller et al., 1999) suggests venereal transmission as a possible route of infection. Maternal transfer may occur congenitally or while pups are suckled, as observed in terrestrial mammals. Young, sick, and malnourished seal pups may be predisposed to a variety of diseases, including Brucella, and exposure to pollutants may also reduce resistance. Another potential means of transfer is through parasites. The reported case of Brucella infection in Parafilaroides lungworm species from a Pacific harbor seal and Pseudalius inflexus lungworms from a juvenile male harbor porpoise from which Brucella was also recovered demonstrated this to be a potential route (Garner et al., 1997; Perrett et al., 2004).
The reproductive conditions associated with Brucella sp. infection in terrestrial mammals have been well documented. Effects of Brucella sp. infection in marine mammals are not fully understood. Brucella sp. has been isolated from the reproductive tissues of marine mammals (Foster et al., 2002). Bottlenose dolphins have aborted in captivity (Ewalt et al., 1994; Miller et al., 1999). In addition, high serum antibody prevalences for Brucella sp. have been reported for a variety of species. Thus, Brucella sp. may indeed have a significant effect on the population dynamics of some marine mammal species.
The 54% antibody prevalence reported for Brucella sp. in the adult cohort in the current study is comparable to the 49% reported for common seals inhabiting Scottish waters (Foster et al., 2002). However, the age profile of that study was not reported. Thus, the two values are not directly comparable.
Brucella has also been isolated from the lymph nodes of four ringed seals off Baffin Island and one harp seal from the Gulf of St Lawrence, Canada. This was the first confirmed report of Brucella in marine mammals from Canada and the first report of the organism in ringed and harp seals. Ages of the animals were not stated (Forbes et al., 2000).
Antibody prevalences of 4% (10 of 248) for ringed seals and 12% (7 of 59) for walrus were reported in a study at eight locations in the Canadian arctic (Nielsen et al., 1996). Samples from seals ranging in age from 0 to 18 yr were collected at three widely distant sites. The random distribution of positive animals may have indicated sporadic exposure from another enzootically-infected phocid, or from a predator such as an arctic fox (Alopex lagopus). Limited epizootics may have occurred in the areas where these positive seals were found. A comparable situation may also have existed regarding the single population of walrus in Fox Basin.
Prevalence of 35% was reported for a sample of 16 Antarctic fur seals (Arctocephalus gazelle) and one Weddell seal from the Southern Hemisphere. Unfortunately, once again no age data were available for these animals (Retamoil et al., 2000). Few serologic surveys reported low antibody prevalence. A prevalence of 0% was found for 45 Lake Baikal seals (Ross et al., 1996), assessed as a landlocked species. Introduction of Brucella sp. could have a major impact on the health of this population.
Low antibody prevalence in the pup cohort may have been related to age. All pups included in the survey were between 2 and 5 wk of age. Pups in this age range were probably still suckling, though some may have been recently weaned. If their mothers had been previously exposed to Brucella sp., the pups may have acquired passive immunity via antibodies in the colostrum. Potential exposure of pups to natural infection (aborting adult females, venereal transmission, etc.) would be unlikely.
Test results demonstrate that serum antibody prevalence of PhoHV-1 is high in harbor seals throughout the range of this study. These results concur with previous studies from both the Atlantic and Pacific coasts of the United States (Zarnke et al., 1997; Goldstein et al., 2003).
Antibody prevalence for PhoHV-1 was higher in seals from PWS than from other areas studied. Reasons for this difference are unclear. The harbor seal population in PWS has declined > 60% since the late 1980s (Frost et al., 1999; Ver Hoef and Frost, 2003). Many seals were exposed to oil, as well as increased human activity, following the Exxon Valdez oil spill in 1989 (Frost et al., 1994; Lowry et al., 1994). Spill activities and the oil itself may have caused reactivation of latent PhoHV-1 infections. Sea otters held in captivity after the spill experienced herpes outbreaks that were attributed to stress (Harris et al., 1990; Spraker et al., 1994).
Food limitation associated with an oceanic regime shift has been suggested as a possible cause of harbor seal population decline in both PWS and the Gulf of Alaska during the 1970s and 1980s (Frost et al., 2001). If food-related stress resulted in activation of latent PhoHV-1 infection, we would have expected antibody prevalences to be higher both near Kodiak and in PWS, because both populations experienced severe population declines. However, antibody prevalence was only elevated in the PWS population. The seal population near Kodiak is now increasing, whereas the PWS population continues to decline (Small et al., 2003; Ver Hoef and Frost, 2003). However, there is no indication that the PWS decline is caused by food limitation (Hastings et al., 2004; Small et al., 2005; Frost, pers. comm.). Young seals captured in PWS during 1997–2000 were larger and had more body fat than seals captured elsewhere in their range (Burns et al., 2005; Frost and Iverson, pers. comm.). Other possible causes of the population decline, such as hunting or predation, have no obvious relationship to antibody prevalence.
Conversely, the 0% antibody prevalence for PhHV-2 in the current study is in marked contrast to the 42% (52/124) prevalence reported previously for the same geographic area (Zarnke et al., 1997). Serologic tests for these two studies were performed in different laboratories utilizing different reagents and procedures.
Serologic evidence of exposure to PDV is widely distributed among harbor seal populations in North America marine waters (Duignan et al., 1993). However, antibody prevalence varies widely. The two samples reported as positive for PDV in this study are believed to be "false positives"; antibody titers barely exceeded the minimum threshold. Additional tests could not be conducted because samples were exhausted during the original test. Morbilliviruses typically spread widely through immunologically-näive populations, and the current results suggest that the harbor seal populations in Alaskan waters had not been recently exposed to PDV prior to this study.
Field personnel have rarely reported signs of clinical disease in harbor seals during the period of this study (Spraker et al., 1994). Population levels of harbor seals declined in some regions of the Gulf of Alaska during the 1970s and 1980s. However, no massive die-offs were reported. Over the last decade the seal population near Kodiak has increased steadily (yet abundance remains low), whereas the PWS population continues to decline, but a slower rate. The current survey has provided no link (either geographically or chronologically) between antibody prevalence of the four disease agents and changes in the dynamics of harbor seal populations. For these reasons, we do not believe that any of the four agents included in this survey represent significant sources of mortality for harbor seals in the coastal waters of Alaska.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
BARR, B., J. L. DUNN, M. D. DANIEL, AND A. BAMFORD. 1989. Herpes-like viral dermatitis in a beluga whale (Delphinapterus leucas). Journal of Wildlife Diseases 25: 608–611.[Abstract]
BLANK, O., P. RETAMAL, P. ABALOS, AND D. TORRES. 2002. Detection of anti-Brucella antibodies in Weddell seals (Leptonychotes weddellii) from Cape Shirref, Antarctica. Archivos de Medicina Veterinaria 34 (1): 117–122.
BORST, G. H. A., H. C. WALVOORT, P. J. H. REIJNDERS, J. S. VAN DER KAMP, AND A. D. M. E. OSTERHAUS. 1986. An outbreak of herpesvirus infection in harbor seals (Phoca vitulina). Journal of Wildlife Diseases 2: 1–6.[Medline]
BURNS, J. M., D. P. COSTA, K. J. FROST, AND J. T. HARVEY. 2005. Development of body oxygen stores in harbor seals: effects of age, mass, and body composition. Physiological and Biochemical Zoology 78: 1057–1058.[Medline]
CORBEL, M. J., AND W. J. MORGAN. 1975. Proposal for minimal standards for descriptions of new species and biotypes of the genus Brucella. International Journal of Systemic Bacteriology 25: 83–89.
———, F. A. STUART, AND R. A. BREWER. 1984. Observations on serological cross-reactions between smooth Brucella species and organisms of other genera. Developments in Biological Standardisation 56: 341–348.
DAOUST, P-Y., D. M. HAINES, J. THORSEN, P. J. DUIGNAN, AND J. R. GERACI. 1993. Phocine distemper in a harp seal (Phoca groenlandica) from the gulf of St. Lawrence, Canada. Journal of Wildlife Diseases 29: 114–117.[Abstract]
DUIGNAN, P. J., S. SADOVE, J. T. SALIKI, AND J. R. GERACI. 1993. Phocine distemper in harbor seals (Phoca vitulina) from Long Island, New York. Journal of Wildlife Diseases 29: 465–469.[Abstract]
———, J. T. SALIKI, D. J. ST. AUBIN, J. A. HOUSE, AND J. R. GERACI. 1994. Neutralizing antibodies to phocine distemper virus in Atlantic walruses (Odobenus rosmarus) from arctic Canada. Journal of Wildlife Diseases 30: 90–94.[Abstract]
———, O. NIELSEN, C. HOUSE, K. M. KOVACS, N. DUFFY, G. EARLY, S. SADOVE, D. J. ST AUBIN, B. K. RIMA, AND J. R. GERACI. 1997. Epizootiology of morbillivirus infection in harp, hooded, and ringed seals from the Canadian Arctic and western Atlantic. Journal of Wildlife Diseases 33: 7–19.[Abstract]
ELIASSON, M., A. OLSSON, E. PALMCRANTZ, K. WIBERG, M. INGANAS, B. GUSS, M. LINDERBERG, AND M. UHLEN. 1988. Chimeric IgG-binding receptors engineered from staphylococcal protein A and streptococcal protein G. Journal of Biological Chemistry 263: 4323–4327.
EWALT, D. R., J. B. PAYEUR, B. M. MARTIN, D. R. CUMMINS, AND W. G. MILLER. 1994. Characteristics of a Brucella species from a bottlenose dolphin (Tursiops truncatus). Journal of Veterinary Diagnostic Investigation 6: 448–452.
FORBES, L. B., O. NIELSEN, L. MEASURES, AND D. R. EWALT. 2000. Brucellosis in ringed seals and harp seals from Canada. Journal of Wildlife Diseases 36: 595–598.[Abstract]
FOSTER, G., A. P. MACMILLAN, J. GODFROID, F. HOWIE, H. M. ROSS, A. CLOECKAERT, R. J. REID, S. BREW, AND I. A. P. PATTERSON. 2002. A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland. Veterinary Microbiology 90: 563–580.[Medline]
FREY, H. R., B. LIESS, L. HAAS, H. LEHMANN, AND H. J. MARSCHALL. 1989. Herpesvirus in harbour seals (Phoca vitulina): Isolation, partial characterization and distribution. Journal of Veterinary Medicine Series B 36: 699–708.
FROST, K. J., L. F. LOWRY, E. SINCLAIR, J. VER HOEF, AND D. C. MCALLISTER. 1994. Impacts on distribution, abundance, and productivity of harbor seals. In Marine mammals and the Exxon Valdez, T. R. Loughlin (ed.). Academic Press, Inc., San Diego, California, pp. 97–118.
———, ———, AND J. M. VER HOEF. 1999. Monitoring the trend of harbor seals in Prince William Sound, Alaska, after the Exxon Valdez oil spill. Marine Mammal Science 15: 494–506.
———, M. A. SIMPKINS, AND L. F. LOWRY. 2001. Diving behavior of harbor seals in Prince William Sound, Alaska. Marine Mammal Science 17: 813–834.
———, ———, R. J. SMALL, AND L. F. LOWRY. Development of diving by harbor seal pups in two regions of Alaska: use of the water column. Marine Mammal Science 42: In press.
GARNER, M. M., D. M. LAMBOURNE, S. J. JEFFRIES, P. HALL BRIGGS, J. C. RHYAN, D. R. EWALT, L. M. POLZIN, AND N. F. CHEVILLE. 1997. Evidence of Brucella infection in Parafilaroides lungworms in a Pacific harbour seal (Phoca vitulina richardsi). Journal of Veterinary Diagnostic Investigation 9: 298–303.
GOLDSTEIN, T., F. M. D. GULLAND, B. M. ALDRIDGE, J. T. HARVEY, T. ROWLES, D. M. LAMBOURNE, S. J. JEFFRIES, L. MEASURES, P. K. YOCHEM, B. S. STEWART, R. J. SMALL, D. P. KING, J. L. STOTT, AND J. A. K. MAZET. 2003. Antibodies to phocine herpesvirus-1 are common in North American harbor seals (Phoca vitulina). Journal of Wildlife Diseases 39: 487–494.[Abstract]
GRACHEV, M. A., V. P. KUMAREV, L. V. MAMAEV, V. L. ZORIN, L. V. BARANOVA, N. N. DENIKINA, S. I. BELIKOV, E. A. PETROV, V. S. KOLESNIK, R. S. KOLESNIK, V. M. DOROFEEV, A. M. BEIM, V. N. KUDELIN, F. G. NAGIEVA, AND V. N. SIDOROV. 1989. Distemper virus in Baikal seals. Nature 338: 209–210.[Medline]
HARDER, T. C., J. PLOTZ, AND B. LIESS. 1991. Antibodies against European phocine herpesvirus isolates detected in sera of Antarctic seals. Polar Biology 11: 509–512.
———, M. HARDER, H. W. VOS, K. KULONEN, S. KENNEDY-STOSKOPF, B. LIESS, M. J. G. APPEL, AND A. D. M. E. OSTERHAUS. 1996. Characterization of phocid herpesviruses type-1 and type-2 as putative 
- and 
-herpesviruses of North American and European pinnipeds. Journal of General Virology 77: 27–35.
———, H. VOS, R. L. DE SWART, AND A. D. OSTERHAUS. 1997. Age-related disease in recurrent outbreak of phocid herpesvirus type-1 infections in a seal rehabilitation centre: evaluation of diagnostic methods. The Veterinary Record 140: 500–503.
HARRIS, R. K., R. B. MOELLER, T. P. LIPSCOMB, J. M. PLETCHER, R. J. HAEBLER, P. A. TUOMI, C. R. MCCORMICK, A. R. DEGANGE, D. MULCAHY, AND T. D. WILLIAMS. 1990. Identification of a herpes-like virus in sea otters during rehabilitation after the T/V Exxon Valdez oil spill. In Sea otter symposium: Proceedings of a symposium to evaluate the response effort on behalf of sea otters after the T/V Exxon Valdez oil spill into Prince William Sound, Anchorage, Alaska, K. Bayha and J. Kennedy (eds.). Biological Report 90(12). US Fish and Wildlife Service, Anchorage, Alaska, pp. 366–368.
HASTINGS, K. K., K. J. FROST, M. A. SIMPKINS, G. W. PENDLETON, U. G. SWAIN, AND R. J. SMALL. 2004. Regional differences in diving behavior of harbor seals in the Gulf of Alaska. Canadian Journal of Zoology 82: 1755–1773.
HOOVER-MILLER, A. A. 1994. Harbor seal (Phoca vitulina) biology and management in Alaska. Final Report. Contract No. T75134749 to US Marine Mammal Commission, Washington, D.C., 45 pp. Available from: MMC, 4340 East–West Hwy Suite 905, Bethesda, Maryland 20814.
HORVAT, B., T. WILHAUS, H. R. FREY, AND B. LIESS. 1989. Herpesvirus in harbour seals (Phoca vitulina): Transmission in homologous host. Journal of Veterinary Medicine Series B 36: 715–718.
KENNEDY, S. 1990. A review of the 1988 European seal morbillivirus epizootic. The Veterinary Record 127: 563–567.[Abstract]
———, J. A. SMYTH, P. F. CUSH, P. DUIGNAN, M. PLATTEN, S. J. MCCULLOUGH, AND G. M. ALLAN. 1989. Histopathologic and immunohistochemical studies of distemper in seals. Veterinary Pathology 26: 97–103.[Abstract]
———, I. J. LINDSTEDT, M. M. MCALISKEY, S. A. MCCONNELL, AND S. J. MCCULLOUGH. 1992. Herpesviral encephalitis in a harbor porpoise (Phocoena phocoena). Journal of Zoo and Wildlife Medicine 23: 374–379.
KENNEDY-STOSKOPF, S., M. K. STOSKOPF, M. A. ECKHAUS, AND J. D. STRANDBERG. 1986. Isolation of a retrovirus and a herpesvirus from a captive sea lion. Journal of Wildlife Diseases 22: 156–164.[Abstract]
LEBICH, M., T. C. HARDER, H. R. FREY, I. K. G. VISSER, A. D. M. E. OSTERHAUS, AND B. LIESS. 1994. Comparative immunological characterization of type-specific and conserved B cell epitopes of pinniped, felid and canid herpesviruses. Archives of Virology 136: 335–347.[Medline]
LOWENSTINE, L. J., L. J. GAGE, D. M. SMITH, AND C. FITZGERALD. 1992. Mortality in neonatal Pacific harbor seals (Phoca vitulina richardsi) from the California coast: Possible role of a herpes-like virus infection. In World Association of Veterinary Microbiologists, Immunologists and Specialists in Infectious Diseases 12th international symposium proceedings: New and emerging infectious diseases. B. Osburn, G. Castrucci and C. Shore (eds.). University of California–Davis, Davis, California, 8–12 September, pp. 243–247.
LOWRY, L. F., K. J. FROST, AND K. W. PITCHER. 1994. Observations of oiling of harbor seals in Prince William Sound. In Marine mammals and the Exxon Valdez, T. R. Loughlin (ed.). Academic Press, San Diego, California, pp. 209–225.
———, ———, J. M. VER HOEF, AND R. A. DELONG. 2001. Movements of satellite-tagged subadult and adult harbor seals in Prince William Sound, Alaska. Marine Mammal Science 17: 835–861.
MACMILLAN, A. P., I. GREISER-WILKE, V. MOENNIG, AND L. A. MATHIAS. 1990. A competition enzyme immunoassay for brucellosis diagnosis. Deutsche Tierarzliche Wochenschrift 97 (2): 83–85.
MCCULLAGH, P., AND J. A. NELDER. 1989. Generalized linear models. 2nd Edition. Chapman and Hall, London, United Kingdom, 511 pp.
MILLER, W. G., L. G. ADAMS, T. A. FICHT, N. F. CHEVILLE, J. B. PAYEUR, D. R. HARLEY, C. HOUSE, AND S. H. RIDGWAY. 1999. Brucella-induced abortions and infections in bottlenose dolphins (Tursiops truncatus). Journal of Zoo and Wildlife Medicine 30: 100–110.[Medline]
MULLER, G., P. WOHLSEIN, A. BEINEKE, L. HAAS, I. GREISER-WILKE, U. SIEBERT, S. FONFARA, T. HARDER, M. STEDE, A. D. GRUBER, AND W. BAUMGARTNER. 2004. Phocine distemper in German seals, 2002. Emerging Infectious Diseases 10: 723–725.[Medline]
NIELSEN, K. H., L. KELLY, D. GALL, P. NICOLETTI, AND W. KELLY. 1985. Improved competitive enzyme immunoassay for the diagnosis of bovine brucellosis. Veterinary Immunology and Immumopathology 46: 285–291.
NIELSEN, O., K. NIELSEN, AND R. E. A. STEWART. 1996. Serological evidence of Brucella spp. exposure in Atlantic walruses (Odobenus rosmarus rosmarus) and ringed seals (Phoca hispida) of Arctic Canada. Arctic 49: 383–386.
OHISHI, K., K. TAKISHITA, M. KAWATO, R. ZENITANI, T. BANDO, Y. FUJISE, Y. GOTO, S. YAMAMOTO, AND T. MARUYAMA. 2004. Molecular evidence of new variant Brucella in North Pacific common minke whales. Microbes and Infection 6: 1199–1204.
OSTERHAUS, A. D. M. E., H. YANG, H. E. M. SPIJKERS, J. GROEN, J. S. TEPPEMA, AND G. VAN STEENIS. 1985. The isolation and partial characterization of a highly pathogenic herpesvirus from the harbour seal (Phoca vitulina). Archives of Virology 86: 239–251.[Medline]
———, J. GROEN, H. E. M. SPIJKERS, H. W. J. BOERDERS, F. C. G. M. UYTDEHAAG, P. DE VRIES, J. S. TEPPEMA, I. K. G. VISSER, M. W. G. VAN dE BILDT, AND E. J. VEDDER. 1990. Mass mortality in seals caused by a newly discovered morbillivirus. Veterinary Microbiology 23: 343–350.[Medline]
PAYEUR, J. B., L. CARPENTER, D. R. EWALT, M. M. GARNER, S. J. JEFFRIES, D. M. LAMBOURNE, B. NORBERG, L. POLZIN, AND J. C. RHYAN. 1998. Evidence of Brucella species infection in Pacific harbour seals (Phoca vitulina richardsi), Californian sea lions (Zalophus californianus), and harbour porpoises (Phocoena phocoena) in Puget Sound, Washington. Proceedings of the ARC-Onderstepoort, OIE international congress with WHO cosponsorship on anthrax, brucellosis, CBPP, clostridial and mycobacterial diseases, Bergen-Dal, Kruger National Park, South Africa, 9–15 August, pp. 173–177.
PERRETT, L. L., C. E. DAWSON, N. DAVISON, AND S. QUINNEY. 2004. Brucella infection of lungworms from a harbor porpoise. The Veterinary Record 154: 800.[Medline]
PITCHER, K. W. 1989. Harbor seal trend count surveys in southern Alaska, 1988. Final Report. Contract MM4465852-1 to US Marine Mammal Commission, Washington, D.C., 15 pp.
———. 1990. Major decline in number of harbor seals, Phoca vitulina richardsi, on Tugidak Island, Gulf of Alaska. Marine Mammal Science 6: 121–134.
———, AND D. G. CALKINS. 1979. Biology of the harbor seal, Phoca vitulina richardsi, in the Gulf of Alaska. US Department of Commerce, NOAA, Outer Continental Environmental Assessment Program Final Report 19: 231–310.
RETAMOIL, P., O. BLANK, P. ABALOS, AND D. TORRES. 2000. Detection of anti-Brucella antibodies in pinnipeds from Antarctic territory. The Veterinary Record 146: 166–167.
ROSS, H. M., G. FOSTER, R. J. REID, K. L. JAHANS, AND A. P. MACMILLAN. 1994. Brucella species infection in sea-mammals. The Veterinary Record 134: 359.[Medline]
———, K. L. JAHANS, A. P. MACMILLAN, R. J. REID, P. M. THOMPSON, AND G. FOSTER. 1996. Brucella species infection in North Sea seal and cetacean populations. The Veterinary Record 138: 647–648.
ROSSITER, P. B., D. M. JESSETT, AND W. P. TAYOR. 1985. Microneutralisation systems for use with different strains of peste des petits ruminants virus and rinderpest virus. Tropical Animal Health and Production 17: 75–81.[Medline]
SALIKI, J. T., G. LIBEAU, J. A. HOUSE, C. A. MEBUS, AND E. J. DUBOVI. 1993. Monoclonal antibody-based enzyme-linked immunosorbent assay for specific detection and titration of peste-des-petits-ruminants virus antibody in caprine and ovine sera. Journal of Clinical Microbiology 31: 1075–1082.
SEASE, J. L. 1992. Status review of harbor seals (Phoca vitulina) in Alaska. National Marine Mammal Laboratory, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington. 74 pp.
SIKKEMA, W. D. 1989. An Fc-binding protein. American Biotechnology Laboratory 7: 42.
SMALL, R. J., G. W. PENDLETON, AND K. W. PITCHER. 2003. Trends in abundance of Alaska harbor seals, 1983–2001. Marine Mammal Science 19: 344–362.
———, L. F. LOWRY, J. M. VER HOEF, K. J. FROST, R. A. DELONG, AND M. J. REHBERG. 2005. Differential movements by harbor seal pups in contrasting Alaska environments. Marine Mammal Science 21: 671–694.
SPRAKER, T. R., L. F. LOWRY, AND K. J. FROST. 1994. Gross necropsy and histopathological lesions found in harbor seals. In Marine mammals and the Exxon Valdez, T. R. Loughlin (ed.). Academic Press, San Diego, California, pp. 281–311.
VAN BRESSEM, M-F., I. K. G. VISSER, M. W. G. VAN DE BILDT, J. S. TEPPEMA, J. A. RAGA, AND A. D. M. E. OSTERHAUS. 1991. Morbillivirus infection in Mediterranean striped dolphins (Stenella coeruleoalba). The Veterinary Record 129: 471–472.[Medline]
VER HOEF, J. M., AND K. J. FROST. 2003. A Bayesian hierarchical model for monitoring harbor seal changes in Prince William Sound, Alaska. Environmental and Ecological Statistics 10: 201–209.
VISSER, I. K. G., J. S. TEPPEMA, AND A. D. M. E. OSTERHAUS. 1991. Virus infections of seals and other pinnipeds. Reviews in Medical Microbiology 2: 105–114.
———, E. J. VEDDER, H. W. VOS, M. W. G. VAN DE BILDT, AND A. D. M. E. OSTERHAUS. 1993. Continued presence of phocine distemper virus in the Dutch Wadden Sea seal population. The Veterinary Record 133: 320–322.[Medline]
ZARNKE, R. L., T. C. HARDER, H. W. VOS, J. M. VER HOEF, AND A. D. M. E. OSTERHAUS. 1997. Serologic survey for phocid herpesvirus-1 and -2 in marine mammals from Alaska and Russia. Journal of Wildlife Diseases 33: 459–465.[Abstract]
Received for publication 16 November 2004.
This article has been cited by other articles:
|
|
 |
|
  R. L. Zarnke, J. M. Ver Hoef, and R. A. DeLong Geographic pattern of serum antibody prevalence for Brucella spp. In caribou, grizzly bears, and wolves from alaska, 1975-1998. J. Wildl. Dis., July 1, 2006; 42(3): 570 - 577. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
