Prevalence and characterization of Salmonella spp. among marine animals in the Channel Islands, California

Salmonella enterica is a zoonotic pathogen that has been isolated from free-ranging marine mammals throughout the world, with animals in the Channel Islands of California (USA) showing the highest prevalence. The goal of this study was to determine prevalence, antimicrobial sensitivity and genetic similarity using pulsed-field gel electrophoresis (PFGE) of Salmonella in several non-domestic animal species on San Miguel and San Nicolas Islands. Fecal samples were collected from 90 California sea lion Zalophus californianus pups, 30 northern elephant seal Mirounga angustirostris pups and 87 western gulls Larus occidentalis in the Channel Islands and 59 adult male sea lions in Puget Sound, WA (USA). Salmonella were isolated, identified and serotyped, followed by antimicrobial susceptibility testing and PFGE. Of the California sea lion pups that were sampled on the islands, 21% (n = 19) were positive for Salmonella, whereas no adults males in Puget Sound were positive. Of the northern elephant seal pups sampled, 87% (n = 26) were harboring Salmonella. Only 9% (n = 8) of western gulls were shedding Salmonella, with one of these gulls harboring the only antimicrobial resistant isolate. The serotypes found in these animals were Enteritidis, Montevideo, Newport, Reading, and Saint Paul. The only serotype that showed variation on PFGE was Newport. The pinnipeds of the Channel Islands harbor Salmonella at a higher prevalence than pinnipeds from other geographic areas observed in previous studies. Researchers and veterinarians should exercise increased caution when working with these animals due to the zoonotic potential of Salmonella.     

Salmonellae in feral pinnipeds off the Southern California coast

Rectal swabs were collected from 90 Northern fur seal (Callorhinus ursinus) and 50 California sea lion (Zalophus californianus) pups on San Miguel Island for Salmonella screening. Three serotypes (newport, heidelberg, and oranienburg) were recovered from 33% of the fur seals and 40% of the sea lions.     

Spatial and temporal variation in the seroprevalence of canine heartworm antigen in the island fox

Island foxes (Urocyon littoralis) are endemic to six of the eight California Channel Islands (USA). The island fox is classified as a threatened species by the State of California, and recently three of the six subspecies have experienced abrupt population declines. As part of a continuing effort to determine the cause of the declines, we tested island fox serum samples collected in 1988 (n = 176) and 1997-98 (n = 156) over the entire geographic range of the species for seroprevalence of canine heartworm (Dirofilaria immitis) antigen. Using a commercially available enzyme-linked immunosorbent assay (PetChek, Idexx Laboratories, Westbrook, Maine, USA) we detected heartworm antigen in four of the six populations of island foxes. On San Miguel and Santa Rosa Islands, seroprevalence in adult foxes was >85% (n = 62) in 1988 and increased to 100% (n = 24) in 1997-98. On Santa Cruz Island, seroprevalence in adult foxes decreased from 83% (n = 30) to 58% (n = 26), whereas on San Nicolas Island, seroprevalence increased from 25% (n = 32) to 77% (n = 30) during the same period. All of the pups assayed (n = 33) were seronegative. The seroprevalences of heartworm reported herein for the four populations of island foxes are the highest yet reported for a fox species. However, additional demographic data reported elsewhere suggests that heartworm has not been a major factor in the recent declines of island fox populations.     

Comparative biology of Uncinaria spp. in the California sea lion (Zalophus californianus) and the northern fur seal (Callorhinus ursinus) in California

Studies on several aspects of the life cycle of hookworms (Uncinaria spp.) in the California sea lion (Zalophus californianus) and northern fur seal (Callorhinus ursinus) were conducted on material collected on San Miguel Island (SMI), California and at The Marine Mammal Center, Sausalito, California in 1997, 1998, and 1999. Examination of Z. californianus intestines for adult hookworms and feces for eggs revealed that longevity of these parasites in pups is about 6-8 mo, and infections are probably not present in older sea lions. Parasitic third-stage larvae (L3) were recovered from the ventral abdominal tissue of Z. californianus, suggesting transmammary transmission. Callorhinus ursinus pups had no hookworm eggs in their feces or adult worms (except for 1 probable contaminant) in their intestines in the fall and early winter, revealing that adult Uncinaria spp. are spontaneously lost at <3 mo of age of the pups. Sand samples from rookeries, used by both Z. californianus and C. ursinus, on SMI were negative for free-living, L3 in summer months but positive in fall and winter months, indicating seasonality occurred.     

Antibodies to marine caliciviruses in the Steller sea lion (Eumetopias jubatus Schreber)

Sera from 145 Steller sea lions (76 adults, three subadults, 37 pups, and 29 fetuses) were tested for neutralizing antibodies to nine marine calicivirus serotypes. Antibodies were found to San Miguel sea lion virus (SMSV) types 1, 5, 6, 7, 8, 10 and 13, and to Tillamook (bovine) calicivirus, but no antibodies were found to the walrus calicivirus. Titers (microtiter neutralization assay) ranged from 1:20 to 1:320, with many positive reactions at the higher dilutions (greater than or equal to 1:80). Antibodies to SMSV's 5 and 10 were most common among animals sampled in Alaskan waters, while antibodies to SMSV-6 were most common among pups from the southern Oregon coast. These data provide evidence that Steller sea lions, like their California sea lion (Zalophus c. californianus Lesson) counterparts, have experienced widespread exposure to multiple serotypes of marine caliciviruses.     

Age‐ and sex‐specific survival of California sea lions (Zalophus californianus) at San Miguel Island,California

We conducted a mark‐recapture study of California sea lions (Zalophus californianus) using pups branded on San Miguel Island, California, from 1987 to 2014, and annual resightings from 1990 to 2015. We used the Burnham model (Burnham 1993), an extension of the Cormack‐Jolly‐Seber mark‐recapture model, which includes recoveries of dead animals, to analyze age, sex, and annual patterns in survival. Generally, females had higher survival than males. For female pups, the average annual survival was 0.600 and for male pups it was 0.574. Yearling survival was 0.758 and 0.757 for females and males, respectively. Peak annual survival was at age 5 and was 0.952 for females and 0.931 for males. Pups with larger mass at branding had higher survival as pups and yearlings, but the effect was relative within each cohort because of large between‐cohort variability in survival. Annual variability in sea surface temperature (SST) affected survival. For each 1°C increase in SST, the odds of survival decreased by nearly 50% for pups and yearlings; negative SST anomalies yielded higher survival. Annual variation in male survival was partly explained by leptospirosis outbreaks. Our study provides a unique view of one demographic parameter that contributed to the successful recovery of the California sea lion population.     

Genetic structure of black abalone (Haliotis cracherodii) populations in the California islands and central California coast: Impacts of larval dispersal and decimation from withering syndrome

The genetic structure of black abalone populations in the southern California Islands and central California coast was investigated by protein electrophoresis. Detailed sampling of San Nicolas Island (SN) permitted investigation of microgeographic genetic differentiation among local geomorphological features. In addition, temporal genetic differentiation was assessed by comparing juveniles and adults at three islands, San Miguel (SM), Santa Cruz (SC) and San Nicolas (SN). Mainland and island locations were genetically differentiated based on allele frequency differences and the presence of private alleles in some island populations. Although microgeographic genetic structure among sites on SN was weak and not statistically significant, heterozygosity varied among sites, with diversity decreasing from west to east. In addition, investigation among cohorts showed that adults were genetically differentiated among island locations, whereas no differences among juveniles were detected. Genetic differentiation between adult and juvenile abalones was detected at SC but not SM or SN. These data are generally consistent with local recruitment augmented by relatively more gene flow among island populations than among island and mainland populations, and possible selection acting on immigrant recruits.     

Ants as first intermediate hosts of Mesocestoides on San Miguel Island, USA

This study tested the hypotheses that ants (Formicidae) function as a first intermediate host of Mesocestoides (Cestoda: Mesocestoididae) and that deer mice (Peromyscus maniculatus) develop metacestode infections after ingesting cysticercoid or procercoid-infected ants. Field studies were conducted at an island fox (Urocyon littoralis littoralis) breeding facility located on San Miguel Island, California Channel Islands National Park, USA, where > 40% of captive foxes were infected with adult Mesocestoides. Eight percent (8%) of deer mice at the fox pen site were infected with Mesocestoides metacestodes while none were infected at a distant site where foxes were absent (campground), thereby indicating the potential localized presence of a first intermediate host. To test whether ants from San Miguel Island contained Mesocestoides DNA, a polymerase chain reaction (PCR)-based diagnostic assay was developed using nested primers that could detect a single hexacanth larva within pooled samples of ten ants. Ants (Lasius niger and Tapinoma sessile) collected near the fox breeding facility were tested using the nested-PCR assay. Seven of 223 pooled samples of L. niger (3.1%) and 2 of 84 pooled samples of T. sessile (2.4%) tested positive for Mesocestoides DNA, while none of the ants were positive at the campground site. Positive samples were sequenced and found to match DNA sequences from Mesocestoides obtained from island fox and deer mice. Finally, to determine whether ants function as a first intermediate host for Mesocestoides, colony-raised deer mice (n = 47) were fed L. niger (n = 3860) or T. sessile (n = 339) collected from the San Miguel Island fox breeding facility. No mouse became infected with Mesocestoides metacestodes after ingesting ants. While both L. niger and T. sessile from SMI were positive for Mesocestoides DNA, they were not infective to deer mice in the laboratory.     

DNA damage and biliary PAH metabolites in flatfish from Southern California bays and harbors, and the Channel Islands

Southern California bays and harbors have been shown to contain high concentrations of a variety of contaminants, including polycyclic aromatic hydrocarbons (PAHs), metals, and pesticides. Conventional monitoring tools do not assess exposure to PAHs in fish, or sublethal effects, which can be more sensitive indicators of stress than traditional methods. This study was conducted to evaluate DNA damage (a sublethal effect) and PAH exposure in flatfish from southern California bays and harbors, and the Channel Islands. California halibut (Paralichthys californicus) were collected from eight bays and harbors (Ventura Harbor, Channel Islands Harbor, Marina del Rey, King Harbor, Alamitos Bay, Long Beach Harbor, Newport Bay, San Diego Bay), and a reference site off Camp Pendleton. Pacific sanddab (Citharichthys sordidus) were collected near four of the Channel Islands (San Miguel Island, Santa Cruz Island, Anacapa Island, Santa Barbara Island). Metabolites of high molecular weight PAHs in fish bile were characterized using a semi-quantitative technique that measures fluorescent aromatic compounds (FACs) in fish bile. DNA damage in fish blood cells was assessed by measuring the amount of single-strand breaks in stained DNA using the Comet assay. The concentration of FACs in fish from all bays and harbors was elevated, with average concentrations ranging from three to ten times greater than FACs in reference fish. FAC levels were elevated in Pacific sanddabs from a Channel Islands station located between Santa Cruz Island and Anacapa Island. DNA damage varied by a factor of five among California halibut from bays and harbors, with significant damage occurring in fish from Alamitos Bay. There was a significant association between FAC concentrations and DNA damage in California halibut at Marina del Rey and Ventura Harbor, but not at other locations, presumably due to contaminants other than PAHs.     

Weak polygyny in California sea lions and the potential for alternative mating tactics

Female aggregation and male territoriality are considered to be hallmarks of polygynous mating systems. The development of genetic parentage assignment has called into question the accuracy of behavioral traits in predicting true mating systems. In this study we use 14 microsatellite markers to explore the mating system of one of the most behaviorally polygynous species, the California sea lion (Zalophus californianus). We sampled a total of 158 female-pup pairs and 99 territorial males across two breeding rookeries (San Jorge and Los Islotes) in the Gulf of California, Mexico. Fathers could be identified for 30% of pups sampled at San Jorge across three breeding seasons and 15% of sampled pups at Los Islotes across two breeding seasons. Analysis of paternal relatedness between the pups for which no fathers were identified (sampled over four breeding seasons at San Jorge and two at Los Islotes) revealed that few pups were likely to share a father. Thirty-one percent of the sampled males on San Jorge and 15% of the sampled males on Los Islotes were assigned at least one paternity. With one exception, no male was identified as the father of more than two pups. Furthermore, at Los Islotes rookery there were significantly fewer pups assigned paternity than expected given the pool of sampled males (p<0.0001). Overall, we found considerably lower variation in male reproductive success than expected in a species that exhibits behavior associated with strongly polygynous mating. Low variation in male reproductive success may result from heightened mobility among receptive females in the Gulf of California, which reduces the ability of males to monopolize groups of females. Our results raise important questions regarding the adaptive role of territoriality and the potential for alternative mating tactics in this species.     

Porotic hyperostosis in a marine-dependent California Indian population

A maize-based iron- and protein-deficient diet is commonly cited as the most important cause of porotic hyperostosis among American Indian agriculturalists. An alternative to this maize dependence hypothesis is suggested by the analysis of 432 crania from the nonagricultural, fish-dependent population of the Channel Island area of southern California. Cribra orbitalia, a form of porotic hyperostosis associated with iron deficiency anemia, is just as common among these fisherpeople, whose diet was rich in iron and essential amino acids, as it is among maize-dependent agriculturalists. Northern Channel Island crania have much more cribra orbitalia than those from the California mainland. The highest incidence is on San Miguel, a small geographically isolated island with a shortage of fresh water and terrestrial resources. The Indians who lived on Santa Cruz, the largest of the northern Channel Islands with the greatest diversity of terrestrial plants and animals, have less cribra orbitalia than those who lived on Santa Rosa or San Miguel Island. This geographical distribution appears to be explained by island-mainland and interisland differences in water contamination, exposure to fish-borne parasites, and nutritional adequacy of the diet. The prevalence of porotic hyperostosis in a population with a heavy dietary dependence on marine resources shows that among prehistoric American Indians, this condition is not always associated with an iron- and protein-deficient diet of cultigens. It seems likely that high nutrient losses associated with diarrheal disease are often more significant in the etiology of porotic hyperostosis than a low dietary intake of essential nutrients.     

Photoperiod and delayed implantation in the northern fur seal (Callorhinus ursinus)

An equation for determination of the photoperiod at any given latitude for any given date is presented and used in an analysis of reproductive timing in the northern fur seal in which there is an obligatory delay of implantation. Fur seals breeding on San Miguel Island, California (33 degrees N) displayed a mean date of parturition that was 14 days earlier (P less than 0.001) than that of the parent stock on the Pribilof Islands, Alaska (57 degrees N). Previous studies have shown that changes occur in the corpus luteum, in follicles in the ovary containing the corpus luteum, in concentrations of plasma progesterone and oestradiol-17 beta, and in the uterine lining when there is a mean photoperiod of 12.5 h/day. This photoperiod occurs at both locations at 62 days after the mean dates of parturition, and may act as a cue for the initiation of implantation in these seals.     

First isolation of a calicivirus from the Steller sea lion (Eumetopias jubatus)

A calicivirus was isolated from the rectum of a Steller sea lion (Eumetopias jubatus) pup on Rogue Reef, off the southern Oregon coast. Based on the results of neutralization tests with specific typing antisera, the isolate was identified as San Miguel sea lion virus serotype 6 (SMSV-6). Blood obtained from nine of 37 pups (24%) during virus sample collection procedures had specific neutralizing antibodies to SMSV-6. The isolation of SMSV-6 from a Steller sea lion represents, to our knowledge, the first isolation of any virus from this widely distributed marine mammal species, and serves to reconfirm the host-nonspecificity of yet another calicivirus of marine origin.     

Blood parasites in some birds from eastern plains of Colombia.

A total of 315 birds representing 75 species (23 families) from Villavicencio and San Miguel (Meta, Colombia) were examined for haematozoa. Fifty birds (15.9%) harbored blood parasites. Microfilariae were the most common haematozoans encountered, followed by species of the genera Haemoproteus, Plasmodium and Trypanosoma. This survey included 15 new host-parasite records and 8 species of birds that were examined for haematozoa for the first time. The prevalence registered in this research was similar to others recorded in the Neotropical region, but in sharp contrast with the prevalence of blood parasites in other major land masses.     

DYNAMIC RESPONSE ANALYSIS. III. A CONSISTENCY FILTER AND APPLICATION TO FOUR NORTHERN ELEPHANT SEAL COLONIES

Dynamic response analysis, a technique for determining stock size relative to the maximum net productivity level (MNPL), was applied to northern elephant seal populations from the South Farallon Islands, Año Nuevo Island, San Nicolas Island and San Miguel Island. Pup counts were used as indices of population size. The application of dynamic response analysis presented here involved some methodological innovations. We present a moving interval method which involves calculating separate dynamic response analyses for intervals of various lengths ranging from four counts to the total number available for the colony. The sign of the second order polynomial regression coefficient computed from a particular interval was used to indicate the colony's apparent status (relative to its MNPL, += above MNPL, - = below MNPL) on that interval. Consistency in the sign of the second order coefficient, as the interval was moved along the trajectory, was used to determine the minimum reliable interval size. Each colony exhibited growth similar to that of a population below its MNPL. These results are consistent with recent natural history observations at San Nicolas, San Miguel and the South Farallon islands. Natural history observations at Año Nuevo Island suggest that the colony there is now at equilibrium. Thus, if our results from dynamic response analysis of the Ano Nuevo colony are correct, it appears that the MNPL may be close to the carrying capacity for these animals.     

110 years of Avipoxvirus in the Galapagos Islands

The role of disease in regulating populations is controversial, partly owing to the absence of good disease records in historic wildlife populations. We examined birds collected in the Galapagos Islands between 1891 and 1906 that are currently held at the California Academy of Sciences and the Zoologisches Staatssammlung Muenchen, including 3973 specimens representing species from two well-studied families of endemic passerine birds: finches and mockingbirds. Beginning with samples collected in 1899, we observed cutaneous lesions consistent with Avipoxvirus on 226 (6.3%) specimens. Histopathology and viral genotyping of 59 candidate tissue samples from six islands showed that 21 (35.6%) were positive for Avipoxvirus, while alternative diagnoses for some of those testing negative by both methods were feather follicle cysts, non-specific dermatitis, or post mortem fungal colonization. Positive specimens were significantly nonrandomly distributed among islands both for mockingbirds (San Cristobal vs. Espanola, Santa Fe and Santa Cruz) and for finches (San Cristobal and Isabela vs. Santa Cruz and Floreana), and overall highly significantly distributed toward islands that were inhabited by humans (San Cristobal, Isabela, Floreana) vs. uninhabited at the time of collection (Santa Cruz, Santa Fe, Espanola), with only one positive individual on an uninhabited island. Eleven of the positive specimens sequenced successfully were identical at four diagnostic sites to the two canarypox variants previously described in contemporary Galapagos passerines. We conclude that this virus was introduced late in 1890's and was dispersed among islands by a variety of mechanisms, including regular human movements among colonized islands. At present, this disease represents an ongoing threat to the birds on the Galapagos Islands.     

Helminths of the wild rabbit (Oryctolagus cuniculus) in Macaronesia

Two hundred and four rabbits from 8 Macaronesian islands (Pico, San Jorge, San Miguel, Terceira, and Flores from Azores Archipelago; Tenerife and Alegranza from Canary Islands; and Madeira from Madeira Archipelago) were examined for helminth parasites between 1995 and 2000. Three species of cestodes, Taenia pisiformis (larvae), Andrya cuniculi, and Mosgovoyia ctenoides, and 5 species of nematodes, Trichuris leporis, Graphidium strigosum, Trichostrongylus retortaeformis, Passalurus ambiguus, and Dermatoxys hispaniensis, were identified. Only 3 species (M. ctenoides, T. retortaeformis, and P. ambiguus) were regularly distributed over the 3 archipelagos. Taenia pisiformis was not collected in Madeira, nor was A. cuniculi in the Azores and G. strigosum in the Canary Islands. Trichuris leporis and D. hispaniensis were only found in Madeira. Significant differences in the general prevalence of the nematodes G. strigosum and T. retortaeformis were detected between Azores and Madeira. The prevalence of T. retortaeformis differs significantly between the Azores and the Canaries and that of P. ambiguus was higher in Madeira than in Azores and Canaries. The helminth richness found in the wild rabbit in these Macaronesian archipelagos was very low compared with the Palearctic helminth fauna of this host. The wild rabbit was introduced from the Iberian Peninsula into different Macaronesian islands. Helminths introduced with Oryctolagus cuniculus into these islands also are commonly found in Iberian wild rabbits, which are excellent colonizers, as demonstrated in this study.     

Factors Affecting Glucocorticoid and Thyroid Hormone Production of Island Foxes

The island fox (Urocyon littoralis) is native to 6 of the 8 Channel Islands of California, USA. The species experienced a population decline in the 1990s but recovered after predatory golden eagles (Aquila chrysaetos) were relocated and feral pigs (Sus scrofa), a main food source for the eagles, were removed. As part of an ongoing conservation program, the National Park Service conducts yearly health surveys on foxes residing on Santa Rosa and San Miguel islands. In this study, we document non-invasive measures of stress and nutritional status from fecal samples collected during surveys from 2009 to 2015. We collected samples defecated in traps overnight or during handling and measured concentrations of glucocorticoid (GC) and triiodothyronine (T3) metabolites using validated assays. We used generalized linear mixed models to assess the relationships between hormones, season, island, age class, sex, body condition, reproductive status, and ectoparasite presence. Overall, males had marginally lower fecal T3 concentrations than females. Concentrations of both hormones positively correlated with body condition. Fecal GC production varied seasonally; concentrations were highest from December to February and declined through the summer and fall. During summer, younger females and those with signs of recent reproduction had higher fecal GC concentrations than older females or those without evidence of reproduction. Fecal T3 concentrations did not vary in relation to season, age, or reproductive status, but on San Miguel Island were positively correlated with ectoparasite presence. There were no other significant differences between islands. Our results provide hormone data for island foxes and demonstrate that production varies in relation to seasonal and biological factors. These reference data will serve as a comparison for future health surveys and allow managers to identify factors associated with increased stress or reduced nutritional state. © 2019 The Wildlife Society.     

Ontogenetic dietary information of the California sea lion (Zalophus californianus) assessed using stable isotope analysis

We used stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopes to examine ontogenetic dietary changes in 289 California sea lions (Zalophus californianus) at San Miguel Island, California during 2004–2007. Tissues analyzed included fur, red blood cells, plasma, and serum. For all tissues, pups had higher δ¹⁵N values and lower δ¹³C values compared to adults, which indicated that pups were feeding higher trophically than older conspecifics and on a lipid‐rich milk diet prior to weaning. Yearling δ¹⁵N values were slightly lower than pup or nearly indistinguishable from adult values depending on the tissue analyzed, indicating a dietary shift from maternal dependency to independent foraging. Juveniles (2–4 yr) and adults (>4 yr) had similar δ¹⁵N values indicating they fed at a similar trophic level. There did not appear to be a pronounced dietary shift in δ¹³C values. However, δ¹³C values integrated with telemetry data indicated that postweaned individuals fed in similar foraging areas. Dietary changes during early life stages may be due to differences in physiology, morphology, experience, or energetic requirements; however, young animals are able to attain the skills needed to consume adult prey types near the end of their second year of life.     

Epizootic vesicular disease in captive California sea lions

An epizootic of vesicular disease occurred in a group of semi-domesticated California sea lions (Zalophus californianus) during the months of April and May 1997. Ten castrated mature male sea lions, ages 12 to 19 yr, were housed in three adjacent open-ocean net enclosures in San Diego Bay (California, USA). Four animals (40%) developed oral and extremity vesicles, anorexia, and were reluctant to perform learned behaviors. One animal developed vesicles but maintained a normal appetite and behavior. The remaining animals showed no clinical signs of infection. Virus (designated FADDL 7005) was isolated from four of the five animals that developed vesicles. Serum antibody titers to FADDL 7005, a previously untyped calicivirus, were demonstrated in animals that showed any combination of clinical signs and in two animals that did not show any clinical signs. No virus was isolated from five fecal samples collected from four of the group animals. Clinical signs lasted 4 to 20 days in affected animals. All affected animals recovered from infection. An experimental swine was inoculated with FADDL 7005 and developed vesicular disease, which was transmitted to another experimental swine upon contact. It is proposed that FADDL 7005 is a new San Miguel sea lion virus.