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Wendte J.M.,U.S. National Institutes of Health | Wendte J.M.,Oklahoma State University | Wendte J.M.,Howard Hughes Medical Institute | Miller M.A.,Marine Wildlife Veterinary Care and Research Center | And 4 more authors.
PLoS Genetics | Year: 2010

Tissue-encysting coccidia, including Toxoplasma gondii and Sarcocystis neurona, are heterogamous parasites with sexual and asexual life stages in definitive and intermediate hosts, respectively. During its sexual life stage, T. gondii reproduces either by genetic out-crossing or via clonal amplification of a single strain through self-mating. Out-crossing has been experimentally verified as a potent mechanism capable of producing offspring possessing a range of adaptive and virulence potentials. In contrast, selfing and other life history traits, such as asexual expansion of tissue-cysts by oral transmission among intermediate hosts, have been proposed to explain the genetic basis for the clonal population structure of T. gondii. In this study, we investigated the contributing roles self-mating and sexual recombination play in nature to maintain clonal population structures and produce or expand parasite clones capable of causing disease epidemics for two tissue encysting parasites. We applied high-resolution genotyping against strains isolated from a T. gondii waterborne outbreak that caused symptomatic disease in 155 immune-competent people in Brazil and a S. neurona outbreak that resulted in a mass mortality event in Southern sea otters. In both cases, a single, genetically distinct clone was found infecting outbreak-exposed individuals. Furthermore, the T. gondii outbreak clone was one of several apparently recombinant progeny recovered from the local environment. Since oocysts or sporocysts were the infectious form implicated in each outbreak, the expansion of the epidemic clone can be explained by self-mating. The results also show that out-crossing preceded selfing to produce the virulent T. gondii clone. For the tissue encysting coccidia, self-mating exists as a key adaptation potentiating the epidemic expansion and transmission of newly emerged parasite clones that can profoundly shape parasite population genetic structures or cause devastating disease outbreaks.


Miller M.A.,Marine Wildlife Veterinary Care and Research Center | Byrne B.A.,University of California at Davis | Jang S.S.,University of California at Davis | Dodd E.M.,Marine Wildlife Veterinary Care and Research Center | And 7 more authors.
Veterinary Research | Year: 2010

Although protected for nearly a century, California's sea otters have been slow to recover, in part due to exposure to fecally-associated protozoal pathogens like Toxoplasma gondii and Sarcocystis neurona. However, potential impacts from exposure to fecal bacteria have not been systematically explored. Using selective media, we examined feces from live and dead sea otters from California for specific enteric bacterial pathogens (Campylobacter, Salmonella, Clostridium perfringens, C. difficile and Escherichia coli O157:H7), and pathogens endemic to the marine environment (Vibrio cholerae, V. parahaemolyticus and Plesiomonas shigelloides). We evaluated statistical associations between detection of these pathogens in otter feces and demographic or environmental risk factors for otter exposure, and found that dead otters were more likely to test positive for C. perfringens, Campylobacter and V. parahaemolyticus than were live otters. Otters from more urbanized coastlines and areas with high freshwater runoff (near outflows of rivers or streams) were more likely to test positive for one or more of these bacterial pathogens. Other risk factors for bacterial detection in otters included male gender and fecal samples collected during the rainy season when surface runoff is maximal. Similar risk factors were reported in prior studies of pathogen exposure for California otters and their invertebrate prey, suggesting that land-sea transfer and/or facilitation of pathogen survival in degraded coastal marine habitat may be impacting sea otter recovery. Because otters and humans share many of the same foods, our findings may also have implications for human health. © 2009 INRA EDP Sciences.


Vanwormer E.,University of California at Davis | Conrad P.A.,University of California at Davis | Miller M.A.,University of California at Davis | Miller M.A.,Marine Wildlife Veterinary Care and Research Center | And 3 more authors.
EcoHealth | Year: 2013

Environmental transmission of Toxoplasma gondii, a global zoonotic parasite, adversely impacts human and animal health. Toxoplasma is a significant cause of mortality in threatened Southern sea otters, which serve as sentinels for disease threats to people and animals in coastal environments. As wild and domestic felids are the only recognized hosts capable of shedding Toxoplasma oocysts into the environment, otter infection suggests land-to-sea pathogen transmission. To assess relative contributions to terrestrial parasite loading, we evaluated infection and shedding among managed and unmanaged feral domestic cats, mountain lions, and bobcats in coastal California, USA. Infection prevalence differed among sympatric felids, with a significantly lower prevalence for managed feral cats (17%) than mountain lions, bobcats, or unmanaged feral cats subsisting on wild prey (73-81%). A geographic hotspot of infection in felids was identified near Monterey Bay, bordering a high-risk site for otter infection. Increased odds of oocyst shedding were detected in bobcats and unmanaged feral cats. Due to their large populations, pet and feral domestic cats likely contribute more oocysts to lands bordering the sea otter range than native wild felids. Continued coastal development may influence felid numbers and distribution, increase terrestrial pathogens in freshwater runoff, and alter disease dynamics at the human-animal-environment interface. © 2013 International Association for Ecology and Health.


Rosevelt C.,California State University, Monterey Bay | Los Huertos M.,California State University, Monterey Bay | Garza C.,California State University, Monterey Bay | Nevins H.M.,Marine Wildlife Veterinary Care and Research Center | Nevins H.M.,University of California at Davis
Marine Pollution Bulletin | Year: 2013

Monitoring beach litter is essential for reducing ecological threats towards humans and wildlife. In Monterey Bay, CA information on seasonal and spatial patterns is understudied. Central California's coastal managers require reliable information on debris abundance, distribution, and type, to support policy aimed at reducing litter. We developed a survey method that allowed for trained citizen scientists to quantify the types and abundance of beach litter. Sampling occurred from July 2009-June 2010. Litter abundance ranged from 0.03 to 17.1itemsm-2 . Using a mixed model approach, we found season and location have the greatest effect on litter abundance. Styrofoam, the most numerically abundant item, made up 41% of the total amount of litter. Unexpected items included fertilizer pellets. The results of this study provide a baseline on the types and abundance of litter on the central coast and have directly supported policy banning Styrofoam take out containers from local municipalities. © 2013 Elsevier Ltd.


Backer L.C.,Centers for Disease Control and Prevention | Landsberg J.H.,Florida Fish And Wildlife Conservation Commission | Miller M.,Marine Wildlife Veterinary Care and Research Center | Miller M.,University of California at Davis | And 2 more authors.
Toxins | Year: 2013

Cyanobacteria (also called blue-green algae) are ubiquitous in aquatic environments. Some species produce potent toxins that can sicken or kill people, domestic animals, and wildlife. Dogs are particularly vulnerable to cyanotoxin poisoning because of their tendency to swim in and drink contaminated water during algal blooms or to ingestalgal mats. Here, we summarize reports of suspected or confirmed canine cyanotoxin poisonings in the U.S. from three sources: (1) The Harmful Algal Bloom-related Illness Surveillance System (HABISS) of the National Center for Environmental Health (NCEH), Centers for Disease Control and Prevention (CDC); (2) Retrospective case files from a large, regional veterinary hospital in California; and (3) Publicly available scientific and medical manuscripts; written media; and web-based reports from pet owners, veterinarians, and other individuals. We identified 231 discreet cyanobacteria harmful algal bloom (cyanoHAB) events and 368 cases of cyanotoxin poisoning associated with dogs throughout the U.S. between the late 1920s and 2012. The canine cyanotoxin poisoning events reviewed here likely represent a small fraction of cases that occur throughout the U.S. each year. © 2013 by the authors; licensee MDPI, Basel, Switzerland.


VanWormer E.,University of California at Davis | Miller M.A.,University of California at Davis | Miller M.A.,Marine Wildlife Veterinary Care and Research Center | Conrad P.A.,University of California at Davis | And 4 more authors.
PLoS Neglected Tropical Diseases | Year: 2014

Background:Environmental transmission of the zoonotic parasite Toxoplasma gondii, which is shed only by felids, poses risks to human and animal health in temperate and tropical ecosystems. Atypical T. gondii genotypes have been linked to severe disease in people and the threatened population of California sea otters. To investigate land-to-sea parasite transmission, we screened 373 carnivores (feral domestic cats, mountain lions, bobcats, foxes, and coyotes) for T. gondii infection and examined the distribution of genotypes in 85 infected animals sampled near the sea otter range.Methodology/Principal Findings:Nested PCR-RFLP analyses and direct DNA sequencing at six independent polymorphic genetic loci (B1, SAG1, SAG3, GRA6, L358, and Apico) were used to characterize T. gondii strains in infected animals. Strains consistent with Type X, a novel genotype previously identified in over 70% of infected sea otters and four terrestrial wild carnivores along the California coast, were detected in all sampled species, including domestic cats. However, odds of Type X infection were 14 times higher (95% CI: 1.3-148.6) for wild felids than feral domestic cats. Type X infection was also linked to undeveloped lands (OR = 22, 95% CI: 2.3-250.7). A spatial cluster of terrestrial Type II infection (P = 0.04) was identified in developed lands bordering an area of increased risk for sea otter Type II infection. Two spatial clusters of animals infected with strains consistent with Type X (P≤0.01) were detected in less developed landscapes.Conclusions:Differences in T. gondii genotype prevalence among domestic and wild felids, as well as the spatial distribution of genotypes, suggest co-existing domestic and wild T. gondii transmission cycles that likely overlap at the interface of developed and undeveloped lands. Anthropogenic development driving contact between these cycles may increase atypical T. gondii genotypes in domestic cats and facilitate transmission of potentially more pathogenic genotypes to humans, domestic animals, and wildlife.


Rankin K.A.,Flathead Animal Clinic | Alroy K.A.,Friendship Hospital for Animals | Kudela R.M.,University of California at Santa Cruz | Oates S.C.,Marine Wildlife Veterinary Care and Research Center | And 2 more authors.
Toxins | Year: 2013

A two and a half year old spayed female Miniature Australian Shepherd presented to a Montana veterinary clinic with acute onset of anorexia, vomiting and depression. Two days prior, the dog was exposed to an algal bloom in a community lake. Within h, the animal became lethargic and anorexic, and progressed to severe depression and vomiting. A complete blood count and serum chemistry panel suggested acute hepatitis, and a severe coagulopathy was noted clinically. Feces from the affected dog were positive for the cyanobacterial biotoxin, microcystin-LA (217 ppb). The dog was hospitalized for eight days. Supportive therapy consisted of fluids, mucosal protectants, vitamins, antibiotics, and nutritional supplements. On day five of hospitalization, a bile acid sequestrant, cholestyramine, was administered orally. Rapid clinical improvement was noted within 48 h of initiating oral cholestyramine therapy. At 17 days post-exposure the dog was clinically normal, and remained clinically normal at re-check, one year post-exposure. To our knowledge, this is the first report of successful treatment of canine cyanobacterial (microcystin) toxicosis. Untreated microcystin intoxication is commonly fatal, and can result in significant liver damage in surviving animals. The clinical success of this case suggests that oral administration of cholestyramine, in combination with supportive therapy, could significantly reduce hospitalization time, cost-of-care and mortality for microcystin-poisoned animals. © 2013 by the authors; licensee MDPI, Basel, Switzerland.


Tinker M.T.,U.S. Geological Survey | Hatfield B.B.,U.S. Geological Survey | Harris M.D.,Marine Wildlife Veterinary Care and Research Center | Ames J.A.,Marine Wildlife Veterinary Care and Research Center
Marine Mammal Science | Year: 2016

Although southern sea otters (Enhydra lutris nereis) are not considered prey for white sharks (Carcharodon carcharias), sharks do nonetheless bite sea otters. We analyzed spatial and temporal trends in shark bites on sea otters in California, assessing the frequency of shark bite wounds in 1,870 carcasses collected since 1985. The proportion of stranded sea otters having shark bites has increased sharply since 2003, and white shark bites now account for >50% of recovered carcasses. The trend was most pronounced in the southern part of the range, from Estero Bay to Point Conception, where shark bite frequency has increased eightfold. Seasonal trends were also evident: most shark-bitten carcasses are recovered in late summer and fall; however, the period of elevated shark bite frequency has lengthened. The causes of these trends are unclear, but possible contributing factors include increased white shark abundance and/or changes in white shark behavior and distribution. In particular, the spatiotemporal patterns of shark-bitten sea otters match increases in pinniped populations, and the increased availability of marine mammal prey for white sharks may have led to more sharks spending more time in nearshore waters utilized by both sea otters and pinnipeds. © 2016 Society for Marine Mammalogy.


Donnelly-Greenan E.L.,Moss Landing Marine Laboratories | Donnelly-Greenan E.L.,Marine Wildlife Veterinary Care and Research Center | Harvey J.T.,Moss Landing Marine Laboratories | Nevins H.M.,Marine Wildlife Veterinary Care and Research Center | And 2 more authors.
Marine Pollution Bulletin | Year: 2014

Marine plastic pollution affects seabirds, including Pacific Northern Fulmars (Fulmarus glacialis rodgersii), that feed at the surface and mistake plastic for prey or incidentally ingest it. Direct and indirect health issues can result, including satiety and possibly leading to inefficient foraging. Our objective was to examine fulmar body condition, identify cephalopod diet to species, enumerate and weigh ingested plastic, and determine if prey number and size were correlated with ingested plastics in beach-cast fulmars wintering in Monterey Bay California (2003, n= 178: 2007, n= 185). Fulmars consumed mostly Gonatus pyros, G. onyx, and G. californiensis of similar size for both years. We found a significant negative correlation between pectoral muscle index and average size of cephalopod beaks per stomach; a significant increase in plastic categories between 2003 and 2007; and no significant correlation between number and mass of plastic compared with number and size of prey for either year. © 2014 Elsevier Ltd.


Law C.J.,University of California at Santa Cruz | Young C.,Marine Wildlife Veterinary Care and Research Center | Mehta R.S.,University of California at Santa Cruz
Physiological and Biochemical Zoology | Year: 2016

Sexual dimorphism attributed to niche divergence is often linked to differentiation between the sexes in both dietary resources and characters related to feeding and resource procurement. Although recent studies have indicated that southern sea otters (Enhydra lutris nereis) exhibit differences in dietary preferences as well as sexual dimorphism in skull size and shape, whether these intersexual differences translate to differentiation in feeding performances between the sexes remains to be investigated. To test the hypothesis that scaling patterns of bite force, a metric of feeding performance, differ between the sexes, we calculated theoretical bite forces for 55 naturally deceased male and female southern sea otters spanning the size ranges encountered over ontogeny. We then used standardized major axis regressions to simultaneously determine the scaling patterns of theoretical bite forces and skull components across ontogeny and assess whether these scaling patterns differed between the sexes. We found that positive allometric increases in theoretical bite force resulted from positive allometric increases in physiological cross-sectional area for the major jaw adductor muscle and mechanical advantage. Closer examination revealed that allometric increases in temporalis muscle mass and relative allometric decreases in out-lever lengths are driving these patterns. In our analysis of sexual dimorphism, we found that scaling patterns of theoretical bite force and morphological traits do not differ between the sexes. However, adult sea otters differed in their absolute bite forces, revealing that adult males exhibited greater bite forces as a result of their larger sizes.We found intersexual differences in biting ability that provide some support for the niche divergence hypothesis. Continued work in this field may link intersexual differences in feeding functional morphology with foraging ecology to show how niche divergence has the potential to reinforce sexual dimorphism in southern sea otters. © 2016 by The University of Chicago. All rights reserved.

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