Katherine C. Prager

Climate Change Influences on Marine Infectious Diseases: Implications for Management and Society

Infectious diseases are common in marine environments, but the effects of a changing climate on marine pathogens are not well understood. Here we review current knowledge about how the climate drives host-pathogen interactions and infectious disease outbreaks. Climate-related impacts on marine diseases are being documented in corals, shellfish, finfish, and humans; these impacts are less clearly linked for other organisms. Oceans and people are inextricably linked, and marine diseases can both directly and indirectly affect human health, livelihoods, and well-being. We recommend an adaptive management approach to better increase the resilience of ocean systems vulnerable to marine diseases in a changing climate. Land-based management methods of quarantining, culling, and vaccinating are not successful in the ocean; therefore, forecasting conditions that lead to outbreaks and designing tools/approaches to influence these conditions may be the best way to manage marine disease.

Contact with domestic dogs increases pathogen exposure in endangered African wild dogs (Lycaon pictus).

Background Infectious diseases have contributed to the decline and local extinction of several wildlife species, including African wild dogs (Lycaon pictus). Mitigating such disease threats is challenging, partly because uncertainty about disease dynamics makes it difficult to identify the best management approaches. Serious impacts on susceptible populations most frequently occur when generalist pathogens are maintained within populations of abundant (often domestic) “reservoir” hosts, and spill over into less abundant host species. If this is the case, disease control directed at the reservoir host might be most appropriate. However, pathogen transmission within threatened host populations may also be important, and may not be controllable by managing another host species. Methodology/Principal Findings We investigated interspecific and intraspecific transmission routes, by comparing African wild dogs exposure to six canine pathogens with behavioural measures of their opportunities for contact with domestic dogs and with other wild dogs. Domestic dog contact was associated with exposure to canine parvovirus, Ehrlichia canis, Neospora caninum and perhaps rabies virus, but not with exposure to canine distemper virus or canine coronavirus. Contact with other wild dogs appeared not to increase the risk of exposure to any of the pathogens. Conclusions/Significance These findings, combined with other data, suggest that management directed at domestic dogs might help to protect wild dog populations from rabies virus, but not from canine distemper virus. However, further analyses are needed to determine the management approaches – including no intervention – which are most appropriate for each pathogen.

Rabies Virus and Canine Distemper Virus in Wild and Domestic Carnivores in Northern Kenya: Are Domestic Dogs the Reservoir?

Rabies virus (RV) and canine distemper virus (CDV) can cause significant mortality in wild carnivore populations, and RV threatens human lives. We investigated serological patterns of exposure to CDV and RV in domestic dogs (Canis familiaris), African wild dogs (Lycaon pictus), black-backed jackals (Canis mesomelas), spotted hyenas (Crocuta crocuta), striped hyenas (Hyaena hyaena) and African lions (Panthera leo), over a 10-year period, in a Kenyan rangeland to assess the role domestic dogs may play in the transmission dynamics of these two important canid pathogens. Observed patterns of RV exposure suggested that repeated introduction, rather than maintenance, occurred in the wild carnivore species studied. However, RV appeared to have been maintained in domestic dogs: exposure was more likely in domestic dogs than in the wild carnivores; was detected consistently over time without variation among years; and was detected in juveniles (≤1-year-old) as well as adults (>1-year-old). We conclude that this domestic dog population could be a RV reservoir. By contrast, the absence of evidence of CDV exposure for each carnivore species examined in the study area, for specific years, suggested repeated introduction, rather than maintenance, and that CDV may require a larger reservoir population than RV. This reservoir could be a larger domestic dog population; another wildlife species; or a “metareservoir” consisting of multiple interconnected carnivore populations. Our findings suggest that RV risks to people and wild carnivores might be controlled by domestic dog vaccination, but that CDV control, if required, would need to target the species of concern.

A Serosurvey of Viral Infections in Lions (Panthera leo), from Queen Elizabeth National Park, Uganda

Serum samples from 14 lions (Panthera leo) from Queen Elizabeth National Park, Uganda, were collected during 1998 and 1999 to determine infectious disease exposure in this threatened population. Sera were analyzed for antibodies against feline immunodeficiency virus (FIV), feline calicivirus (FCV), feline herpesvirus 1 (feline rhinotracheitis: FHV1), feline/canine parvovirus (FPV/CPV), feline infectious peritonitis virus (feline coronavirus: FIPV), and canine distemper virus (CDV) or for the presence of feline leukemia virus (FeLV) antigens. Ten lions (71%) had antibodies against FIV, 11 (79%) had antibodies against CDV, 11 (79%) had antibodies against FCV, nine (64%) had antibodies against FHV1, and five (36%) had antibodies against FPV. Two of the 11 CDV-seropositive lions were subadults, indicating recent exposure of this population to CDV or a CDV-like virus. No lions had evidence of exposure to FeLV or FIPV. These results indicate that this endangered population has extensive exposure to common feline and canine viruses.

BLACK-BACKED JACKAL EXPOSURE TO RABIES VIRUS, CANINE DISTEMPER VIRUS, AND BACILLUS ANTHRACIS IN ETOSHA NATIONAL PARK, NAMIBIA

Canine distemper virus (CDV) and rabies virus (RABV) occur worldwide in wild carnivore and domestic dog populations and pose threats to wildlife conservation and public health. In Etosha National Park (ENP), Namibia, anthrax is endemic and generates carcasses frequently fed on by an unusually dense population of black-backed jackals (Canis mesomelas). Using serology, phylogenetic analyses (on samples obtained from February 2009–July 2010), and historical mortality records (1975–2011), we assessed jackal exposure to Bacillus anthracis (BA; the causal bacterial agent of anthrax), CDV, and RABV. Prevalence of antibodies against BA (95%, n=86) and CDV (71%, n=80) was relatively high, while that of antibodies against RABV was low (9%, n=81). Exposure to BA increased significantly with age, and all animals >6 mo old were antibody-positive. As with BA, prevalence of antibodies against CDV increased significantly with age, with similar age-specific trends during both years of the study. No significant effect of age was found on the prevalence of antibodies against RABV. Three of the seven animals with antibodies against RABV were monitored for more than 1 yr after sampling and showed no signs of active infection. Mortality records revealed that rabid animals are destroyed nearly every year inside the ENP tourist camps. Phylogenetic analyses demonstrated that jackal RABV in ENP is part of the same transmission cycle as other dog-jackal RABV cycles in Namibia.

Complementary approaches to diagnosing marine diseases: a union of the modern and the classic.

Linking marine epizootics to a specific aetiology is notoriously difficult. Recent diagnostic successes show that marine disease diagnosis requires both modern, cutting-edge technology (e.g. metagenomics, quantitative real-time PCR) and more classic methods (e.g. transect surveys, histopathology and cell culture). Here, we discuss how this combination of traditional and modern approaches is necessary for rapid and accurate identification of marine diseases, and emphasize how sole reliance on any one technology or technique may lead disease investigations astray. We present diagnostic approaches at different scales, from the macro (environment, community, population and organismal scales) to the micro (tissue, organ, cell and genomic scales). We use disease case studies from a broad range of taxa to illustrate diagnostic successes from combining traditional and modern diagnostic methods. Finally, we recognize the need for increased capacity of centralized databases, networks, data repositories and contingency plans for diagnosis and management of marine disease.

Asymptomatic and chronic carriage of Leptospira interrogans serovar Pomona in California sea lions (Zalophus californianus)

Since 1970, periodic outbreaks of leptospirosis, caused by pathogenic spirochetes in the genus Leptospira, have caused morbidity and mortality of California sea lions (Zalophus californianus) along the Pacific coast of North America. Yearly seasonal epizootics of varying magnitude occur between the months of July and December, with major epizootics occurring every 3-5 years. Genetic and serological data suggest that Leptospira interrogans serovar Pomona is the infecting serovar and is enzootic in the California sea lion population, although the mechanism of persistence is unknown. We report asymptomatic carriage of Leptospira in 39% (33/85) of wild, free-ranging sea lions sampled during the epizootic season, and asymptomatic seroconversion with chronic asymptomatic carriage in a rehabilitated sea lion. This is the first report of asymptomatic carriage in wild, free-ranging California sea lions and the first example of seroconversion and asymptomatic chronic carriage in a sea lion. Detection of asymptomatic chronic carriage of Leptospira in California sea lions, a species known to suffer significant disease and mortality from the same Leptospira strain, goes against widely-held notions regarding leptospirosis in accidental versus maintenance host species. Further, chronic carriage could provide a mechanism for persistent circulation of Leptospira in the California sea lion population, particularly if these animals shed infectious leptospires for months to years.

The effect of protected areas on pathogen exposure in endangered African wild dog (Lycaon pictus) populations

n Abstractn n Infectious diseases impact African wild dogs (Lycaon pictus), but the nature and magnitude of this threat likely varies among populations according to different factors, such as the presence and prevalence of pathogens and land-use characteristics. We systematically evaluated these factors to assist development of locally appropriate strategies to mitigate disease risk. Wild dogs from 16 sites representing five unconnected populations were examined for rabies virus, canine distemper virus (CDV), canine parvovirus, canine coronavirus, and Babesia spp. exposure. Analyses revealed widespread exposure to viral pathogens, but Babesia was never detected. Exposure to CDV was associated with unprotected and protected-unfenced areas where wild dogs likely have a high probability of domestic dog contact and, in the case of protected-unfenced areas, likely reside amongst high wildlife densities. Our findings also suggest that domestic dog contact may increase rabies and coronavirus exposure risk. Therefore, domestic dogs may be a source of CDV, rabies and coronavirus, while wildlife may also play an important role in CDV transmission dynamics. Relatively high parvovirus seroprevalence across land-use types suggests that it might persist in the absence of spillover from domestic dogs. Should intervention be needed to control pathogens in wild dogs, efforts to prevent rabies and coronavirus exposure might be directed at reducing infection in the presumed domestic dog reservoir through vaccination. If prevention of CDV and parvovirus infections were deemed a management necessity, control of disease in domestic dogs may be insufficient to reduce transmission risks, and vaccination of wild dogs themselves may be the optimal strategy.n n

Detecting signals of chronic shedding to explain pathogen persistence: Leptospira interrogans in California sea lions

Summary Identifying mechanisms driving pathogen persistence is a vital component of wildlife disease ecology and control. Asymptomatic, chronically infected individuals are an oft‐cited potential reservoir of infection, but demonstrations of the importance of chronic shedding to pathogen persistence at the population‐level remain scarce. Studying chronic shedding using commonly collected disease data is hampered by numerous challenges, including short‐term surveillance that focuses on single epidemics and acutely ill individuals, the subtle dynamical influence of chronic shedding relative to more obvious epidemic drivers, and poor ability to differentiate between the effects of population prevalence of chronic shedding vs. intensity and duration of chronic shedding in individuals. We use chronic shedding of Leptospira interrogans serovar Pomona in California sea lions (Zalophus californianus) as a case study to illustrate how these challenges can be addressed. Using leptospirosis‐induced strands as a measure of disease incidence, we fit models with and without chronic shedding, and with different seasonal drivers, to determine the time‐scale over which chronic shedding is detectable and the interactions between chronic shedding and seasonal drivers needed to explain persistence and outbreak patterns. Chronic shedding can enable persistence of L. interrogans within the sea lion population. However, the importance of chronic shedding was only apparent when surveillance data included at least two outbreaks and the intervening inter‐epidemic trough during which fadeout of transmission was most likely. Seasonal transmission, as opposed to seasonal recruitment of susceptibles, was the dominant driver of seasonality in this system, and both seasonal factors had limited impact on long‐term pathogen persistence. We show that the temporal extent of surveillance data can have a dramatic impact on inferences about population processes, where the failure to identify both short‐ and long‐term ecological drivers can have cascading impacts on understanding higher order ecological phenomena, such as pathogen persistence.

Antibiotic Efficacy in Eliminating Leptospiruria in California Sea Lions (Zalophus californianus) Stranding with Leptospirosis

Stranded California sea lions (Zalophus californianus) along the California coast have been diagnosed with leptospirosis every year since at least the 1980s. Between September 2010 and November 2011, we followed 14 stranded California sea lions that survived to release and evaluated antibiotic efficacy in eliminating leptospiruria (urinary shedding of leptospires). Leptospiruria was assessed by real-time PCR of urine and urine culture, with persistence assessed using longitudinally collected samples. Serum chemistry was used to assess recovery of normal renal function. Microscopic agglutination testing (MAT) was performed to assess serum anti-Leptospira antibody titers, and the MAT reactivity patterns were consistent with L. interrogans serovar Pomona infection frequently observed in this population. Animals were initially treated for 6 to 16 d (median = 10.5; mean = 10.8) with antibiotics from the penicillin family, with some receiving additional antibiotics to treat other medical conditions. All urine cultures were negative; therefore, the presence of leptospiruria was assessed using PCR. Leptospiruria continued beyond the initial course of penicillin family antibiotics in 13 of the 14 sea lions, beyond the last antibiotic dose in 11 of the 14 sea lions, beyond recovery of renal function in 13 of the 14 sea lions, and persisted for at least 8 to 86 d (median = 45; mean = 46.8). Five animals were released with no negative urine PCR results detected; thus, their total shedding duration may have been longer. Cessation of leptospiruria was more likely in animals that received antibiotics for a greater duration, especially if coverage was uninterrupted. Real-time PCR results indicate that an antibiotic protocol commonly used to treat leptospirosis in rehabilitating California sea lions does not eliminate leptospiruria. It is possible that antibiotic protocols given for a longer duration and/or including other antibiotics may be effective in eliminating leptospiruria. These results may have important human and animal health implications, especially in rehabilitation facilities, as Leptospira transmission may occur through contact with animals with persistent leptospiruria.