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Wildlife health surveillance: Gaps, needs and opportunities

Disease emergence represent a global threat for public health, economy, and biological conservation and most of the emerging diseases have zoonotic origin from wildlife. To prevent their spread and to support the implementation of control measures, disease surveillance and reporting systems are needed, and due to globalisation, these activities should be carried at world level. To define the main gaps affecting the performances of wildlife health surveillance and reporting systems at word level, we analysed the Wildlife Disease Surveillance Survey submitted to all Members of World Organisation for Animal Health which inquire on structure and limits of surveillance and reporting systems. The response from 103 Members, covering all world areas, showed that 54.4% of them have a wildlife disease surveillance programme and 66% implemented a strategy to manage their spread. The lack of dedicated budget affected the possibility of outbreak investigations, sampling collection and diagnostic testing. Although most Members maintain records relating to wildlife mortality or morbidity events in centralised databases, data analyses and disease risk assessment are reported as main needs. Our evaluation of surveillance capacity showed an overall low level associated to great variability between Members not restricted to specific geographical area. A better recognition of the value of wildlife disease surveillance resulting in allocation of adequate resources by governments would make wildlife disease surveillance systems more functional. Moreover, the future comprehension of the influence of socio-economic, cultural and biodiversity aspects will be essential to increase better disease surveillance under One Health approach.

Scientific and Technical Review

Fipronil baits as emerging tools for flea control and plague mitigation: Experiments with cricetid mice on prairie dog colonies

Plague is a zoonotic disease of mammalian hosts and flea vectors. Wildlife biologists most commonly mitigate plague by controlling flea populations. We evaluated the efficacy of edible baits for systemic flea control with two cricetid species on colonies of black-tailed prairie dogs ( Cynomys ludovicianus ): the western deer mouse ( Peromyscus sonoriensis ) and the northern grasshopper mouse ( Onychomys leucogaster ). We tested grain bait with 0.005% fipronil by weight and “FipBit” pellets with 0.46–1.52 mg of fipronil/pellet. Flea prevalence was assessed via combing of live-trapped mice. In one experiment with fipronil grain bait and FipBits ( n =564 combings), flea prevalence declined from 74% (grain) and 45% (FipBits) before treatments to 0% for both treatments from 30–44 d and from 324–413 d after treatments. During a second experiment with FipBits ( n =299 combings), flea prevalence declined from 13% to 32% before treatments to 0% from 11–15 d after treatments, but increased to 29–56% from 349–378 d after treatments. Results herein suggest annual fipronil bait treatments may be most effective for flea control.

Journal of Wildlife Diseases

Persistent organic pollutants in the blood of free-ranging sea otters (Enhydra lutris ssp.) in Alaska and California

As part of tagging and ecologic research efforts in 1997 and 1998, apparently healthy sea otters of four age-sex classes in six locations in Alaska and three in California were sampled for persistent organic pollutants (POPs) and other chemicals of ecologic or environmental concern (COECs). Published techniques for the detection of POPs (specifically Σpolychlorinated biphenyls [PCBs], ΣDDTs, Σhexachlorocyclohexanes [HCHs], Σpolycyclic aromatic hydrocarbons [PAHs], Σchlordanes [CHLs], hexachlorobenzene [HCB], dieldrin, and mirex) in the tissue of dead otters were modified for use with serum from live sea otters. Toxic equivalencies (TEQs) were calculated for POPs with proven bioactivity. Strong location effects were seen for most POPs and COECs; sea otters in California generally showed higher mean concentrations than those in Alaska. Differences in contaminant concentrations were detected among age and sex classes, with high levels frequently observed in subadults. Very high levels of ΣDDT were detected in male sea otters in Elkhorn Slough, California, where strong freshwater outflow from agricultural areas occurs seasonally. All contaminants except mirex differed among Alaskan locations; only ΣDDT, HCB, and chlorpyrifos differed within California. High levels of ΣPCB (particularly larger, more persistent congeners) were detected at two locations in Alaska where associations between elevated PCBs and military activity have been established, while higher PCB levels were found at all three locations in California where no point source of PCBs has been identified. Although POP and COEC concentrations in blood may be less likely to reflect total body burden, concentrations in blood of healthy animals may be more biologically relevant and less influenced by state of nutrition or perimortem factors than other tissues routinely sampled.

Alaska, California

Evaluation of coproexamination as a diagnostic test for avian botulism

Fecal extracts and blood sera from 113 ducks showing clinical signs of botulism were examined for Clostridium botulinum type C toxin by means of the mouse toxicity test to evaluate coproexamination as a diagnostic procedure, as compared with demonstration of toxin in serum. When death of test mice unprotected with type specific antitoxin (while protected controls survived) was the criterion, 78.8% of the sera and 5.3% of the fecal extracts were positive. When characteristic signs of intoxication in the unprotected mice was included as evidence of toxin in the specimens, these percentages increased to 86.7 and 6.2, respectively. Fecal specimens were collected hourly for the first 6 h after peroral dosing of eight mallards ( Anas platyrhynchos ) with 1.0 LD 50 , of type C toxin and at 24, 48, and 72 h from birds surviving that long. From 2 to 4 toxin-positive specimens were passed by all eight ducks during the first 6 h, five specimens were positive at 24 h, and three were positive at 48 h. Only three specimens were collected at 72 h, all of which were negative. These findings suggest that attempts to detect toxin in the feces of wild ducks might have been more successful had the birds been captured earlier in the course of the disease.

Utah

A serosurvey of diseases of free-ranging gray wolves (Canis lupus) in Minnesota

We tested serum samples from 387 free-ranging wolves ( Canis lupus ) from 2007 to 2013 for exposure to eight canid pathogens to establish baseline data on disease prevalence and spatial distribution in Minnesota's wolf population. We found high exposure to canine adenoviruses 1 and 2 (88% adults, 45% pups), canine parvovirus (82% adults, 24% pups), and Lyme disease (76% adults, 39% pups). Sixty-six percent of adults and 36% of pups exhibited exposure to the protozoan parasite Neospora caninum . Exposure to arboviruses was confirmed, including West Nile virus (37% adults, 18% pups) and eastern equine encephalitis (3% adults). Exposure rates were lower for canine distemper (19% adults, 5% pups) and heartworm (7% adults, 3% pups). Significant spatial trends were observed in wolves exposed to canine parvovirus and Lyme disease. Serologic data do not confirm clinical disease, but better understanding of disease ecology of wolves can provide valuable insight into wildlife population dynamics and improve management of these species.

Minnesota

Estimating loss of Brucella abortus antibodies from age-specific serological data in elk

Serological data are one of the primary sources of information for disease monitoring in wildlife. However, the duration of the seropositive status of exposed individuals is almost always unknown for many free-ranging host species. Directly estimating rates of antibody loss typically requires difficult longitudinal sampling of individuals following seroconversion. Instead, we propose a Bayesian statistical approach linking age and serological data to a mechanistic epidemiological model to infer brucellosis infection, the probability of antibody loss, and recovery rates of elk ( Cervus canadensis ) in the Greater Yellowstone Ecosystem. We found that seroprevalence declined above the age of ten, with no evidence of disease-induced mortality. The probability of antibody loss was estimated to be 0.70 per year after a five-year period of seropositivity and the basic reproduction number for brucellosis to 2.13. Our results suggest that individuals are unlikely to become re-infected because models with this mechanism were unable to reproduce a significant decline in seroprevalence in older individuals. This study highlights the possible implications of antibody loss, which could bias our estimation of critical epidemiological parameters for wildlife disease management based on serological data.

EcoHealth

Has the time come for big science in wildlife health?

The consequences of wildlife emerging diseases are global and profound with increased burden on the public health system, negative impacts on the global economy, declines and extinctions of wildlife species, and subsequent loss of ecological integrity. Examples of health threats to wildlife include Batrachochytrium dendrobatidis , which causes a cutaneous fungal infection of amphibians and is linked to declines of amphibians globally; and the recently discovered Pseudogymnoascus (Geomyces) destructans , the etiologic agent of white nose syndrome which has caused precipitous declines of North American bat species. Of particular concern are the novel pathogens that have emerged as they are particularly devastating and challenging to manage. A big science approach to wildlife health research is needed if we are to make significant and enduring progress in managing these diseases. The advent of new analytical models and bench assays will provide us with the mathematical and molecular tools to identify and anticipate threats to wildlife, and understand the ecology and epidemiology of these diseases. Specifically, new molecular diagnostic techniques have opened up avenues for pathogen discovery, and the application of spatially referenced databases allows for risk assessments that can assist in targeting surveillance. Long-term, systematic collection of data for wildlife health and integration with other datasets is also essential. Multidisciplinary research programs should be expanded to increase our understanding of the drivers of emerging diseases and allow for the development of better disease prevention and management tools, such as vaccines. Finally, we need to create a National Fish and Wildlife Health Network that provides the operational framework (governance, policies, procedures, etc.) by which entities with a stake in wildlife health cooperate and collaborate to achieve optimal outcomes for human, animal, and ecosystem health.

EcoHealth

Using transcriptomics to predict and visualize disease status in bighorn sheep (Ovis canadensis)

Increasing risk of pathogen spillover coupled with overall declines in wildlife population abundance in the Anthropocene make infectious disease a relevant concern for species conservation worldwide. While emerging molecular tools could improve our diagnostic capabilities and give insight into mechanisms underlying wildlife disease risk, they have rarely been applied in practice. Here, employing a previously reported gene transcription panel of common immune markers to track physiological changes, we present a detailed analysis over the course of both acute and chronic infection in one wildlife species where disease plays a critical role in conservation, bighorn sheep ( Ovis canadensis ). Differential gene transcription patterns distinguished between infection statuses over the course of acute infection and differential correlation (DC) analyses identified clear changes in gene co-transcription patterns over the early stages of infection, with transcription of four genes—TGFb, AHR, IL1b and MX1—continuing to increase even as transcription of other immune-associated genes waned. In a separate analysis, we considered the capacity of the same gene transcription panel to aid in differentiating between chronically infected animals and animals in other disease states outside of acute disease events (an immediate priority for wildlife management in this system). We found that this transcription panel was capable of accurately identifying chronically infected animals in the test dataset, though additional data will be required to determine how far this ability extends. Taken together, our results showcase the successful proof of concept and breadth of potential utilities that gene transcription might provide to wildlife disease management, from direct insight into mechanisms associated with differential disease response to improved diagnostic capacity in the field.

Conservation Physiology

Introduction

This is the third iteration of the National Wildlife Health Center's (NWHC) field guide developed primarily to assist field managers and biologists address diseases they encounter. By itself, the first iteration, “Field Guide of Wildlife Diseases: General Field Procedures and Diseases of Migratory Birds,” was simply another addition to an increasing array of North American field guides and other publications focusing on disease in free-ranging wildlife populations. Collectively, those publications were reflecting the ongoing transition in the convergence of wildlife management and wildlife disease as foundational components within the structure of wildlife conservation as a social enterprise serving the stewardship of our wildlife resources. For context, it is useful to consider those publications relative to a timeline of milestones involving the evolution of wildlife conservation in North America.

Techniques and Methods

Avian influenza shedding patterns in waterfowl: implications for surveillance, environmental transmission, and disease spread

Despite the recognized importance of fecal/oral transmission of low pathogenic avian influenza (LPAI) via contaminated wetlands, little is known about the length, quantity, or route of AI virus shed by wild waterfowl. We used published laboratory challenge studies to evaluate the length and quantity of low pathogenic (LP) and highly pathogenic (HP) virus shed via oral and cloacal routes by AI-infected ducks and geese, and how these factors might influence AI epidemiology and virus detection. We used survival analysis to estimate the duration of infection (from virus inoculation to the last day virus was shed) and nonlinear models to evaluate temporal patterns in virus shedding. We found higher mean virus titer and longer median infectious period for LPAI-infected ducks (10–11.5 days in oral and cloacal swabs) than HPAI-infected ducks (5 days) and geese (7.5 days). Based on the median bird infectious dose, we found that environmental contamination is two times higher for LPAI- than HPAI-infectious ducks, which implies that susceptible birds may have a higher probability of infection during LPAI than HPAI outbreaks. Less environmental contamination during the course of infection and previously documented shorter environmental persistence for HPAI than LPAI suggest that the environment is a less favorable reservoir for HPAI. The longer infectious period, higher virus titers, and subclinical infections with LPAI viruses favor the spread of these viruses by migratory birds in comparison to HPAI. Given the lack of detection of HPAI viruses through worldwide surveillance, we suggest monitoring for AI should aim at improving our understanding of AI dynamics (in particular, the role of the environment and immunity) using long-term comprehensive live bird, serologic, and environmental sampling at targeted areas. Our findings on LPAI and HPAI shedding patterns over time provide essential information to parameterize environmental transmission and virus spread in predictive epizootiologic models of disease risks.

Journal of Wildlife Diseases

Climate change and wildlife health: direct and indirect effects

Climate change will have significant effects on the health of wildlife, domestic animals, and humans, according to scientists. The Intergovernmental Panel on Climate Change projects that unprecedented rates of climate change will result in increasing average global temperatures; rising sea levels; changing global precipitation patterns, including increasing amounts and variability; and increasing midcontinental summer drought (Intergovernmental Panel on Climate Change, 2007). Increasing temperatures, combined with changes in rainfall and humidity, may have significant impacts on wildlife, domestic animal, and human health and diseases. When combined with expanding human populations, these changes could increase demand on limited water resources, lead to more habitat destruction, and provide yet more opportunities for infectious diseases to cross from one species to another. Awareness has been growing in recent years about zoonotic diseases— that is, diseases that are transmissible between animals and humans, such as Lyme disease and West Nile virus. The rise of such diseases results from closer relationships among wildlife, domestic animals, and people, allowing more contact with diseased animals, organisms that carry and transmit a disease from one animal to another (vectors), and people. Disease vectors include insects, such as mosquitoes, and arachnids, such as ticks. Thus, it is impossible to separate the effects of global warming on wildlife from its effects on the health of domestic animals or people. Climate change, habitat destruction and urbanization, the introduction of exotic and invasive species, and pollution—all affect ecosystem and human health. Climate change can also be viewed within the context of other physical and climate cycles, such as the El Niño Southern Oscillation (El Niño), the North Atlantic Oscillation, and cycles in solar radiation that have profound effects on the Earth’s climate. The effects of climate change on wildlife disease are summarized in several areas of scientific study discussed briefly below: geographic range and distribution of wildlife diseases, plant and animal phenology (Walther and others, 2002), and patterns of wildlife disease, community and ecosystem composition, and habitat degradation.

Fact Sheet

Habitat, wildlife and one health: Arcanobacterium pyogenes in Maryland and Upper Eastern Shore white-tailed deer populations

Background : Understanding the distribution of disease in wildlife is key to predicting the impact of emerging zoonotic one health concerns, especially for wildlife species with extensive human and livestock interfaces. The widespread distribution and complex interactions of white - tailed deer ( Odocoileus virginianus ) with humans suggest deer population health and management may have implications beyond stewardship of the animals. The intracranial abscessation suppurative meningitis (IASM) disease complex in deer has been linked to Arcanobacterium pyogenes , an under - diagnosed and often misdiagnosed organism considered commensal in domestic livestock but associated with serious disease in numerous species, including humans. Methods : Our study used standard bacterial culture techniques to assess A. pyogenes prevalence among male deer sampled across six physiogeographic regions in Maryland and male and female deer in the Upper Eastern Shore under Traditional Deer Management (TDM) and Quality Deer Management (QDM), a management protocol that alters population demographics in favor of older male deer. Samples were collected from antler pedicles for males, the top of the head where pedicles would be if present for females, or the whole dorsal frontal area of the head for neonates. We collected nasal samples from all animals by swabbing the nasopharyngeal membranes. A gram stain and catalase test were conducted, and aerobic bacteria were identified to genus and species when possible. We evaluated the effect of region on whether deer carried A. pyogenes using Pearson's chi-square test with Yates’ continuity correction. For the white-tailed deer management study, we tested whether site, age class and sex predisposed animals to carrying A. pyogenes using binary logistic regression. Results : A. pyogenes was detected on deer in three of the six regions studied, and was common in only one region, the Upper Eastern Shore. In the Upper Eastern Shore, 45% and 66% of antler and nasal swabs from deer were positive for A. pyogenes , respectively. On the Upper Eastern Shore, prevalence of A. pyogenes cultured from deer did not differ between management areas, and was abundant among both sexes and across all age classes. No A. pyogenes was cultured from a small sample of neonates. Conclusion : Our study indicates A. pyogenes may be carried widely among white-tailed deer regardless of sex or age class, but we found no evidence the pathogen is acquired in utero. The distribution of A. pyogenes across regions and concentration in a region with low livestock levels suggests the potential for localized endemicity of the organism and the possibility that deer may serve as a maintenance reservoir for an emerging one health concern.

Infection Ecology and Epidemiology

Fungal disease and the developing story of bat white-nose syndrome

Two recently emerged cutaneous fungal diseases of wildlife, bat white-nose syndrome (WNS) and amphibian chytridiomycosis, have devastated affected populations. Fungal diseases are gaining recognition as significant causes of morbidity and mortality to plants, animals, and humans, yet fewer than 10% of fungal species are known. Furthermore, limited antifungal therapeutic drugs are available, antifungal therapeutics often have associated toxicity, and there are no approved antifungal vaccines. The unexpected emergence of WNS, the rapidity with which it has spread, and its unprecedented severity demonstrate both the impacts of novel fungal disease upon naïve host populations and challenges to effective management of such diseases.

PLoS Pathogens

Studies on the control of whirling disease (Myxosoma cerebralis)

Based on presumptive evidence of death (extrusion of polar filaments and disintegration of sporoplasm) 1.0%, 0.5%, and 0.25% calcium oxide or potassium hydroxide killed the spores of Myxosoma cerebrallis in vitro . Chlorine at 400 ppm destroyed 36% to 90% of the spores but 13% to 37% of those in the controls perished. Calcium hydroxide, ammonium chloride, sodium borate, potassium permanganate, Roccal (alkyl dimethylbenzylammonium chloride), and copper sulfate allowed survival of 38–96% of the spores, usually not much less than the rate of survival of the controls. In simulated pond testing, quicklime at 380 grams or more per square meter (3360 lbs/acre) of pond bottom prevented whirling disease in rainbow trout ( Salmo gairdneri ).

Journal of Wildlife Diseases