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Ecotoxicology of Wild Mammals

An international group of 32 scientists has critically reviewed the scientific literature on exposure and effects of environmental contaminants in wild mammals. The underlying theme of this text is encompassed by the following four questions: What exactly do we know about environmental contaminants in mammals? What are the commonalities and differences between mammal orders/species in the effects that contaminants have? How and to what degree of accuracy can we predict the adverse effects of environmental contaminants on mammalian wildlife? How significant are contaminant insults compared with other density-independent and -dependent factors such as habitat loss, climatic factors and disease? The book is organized three topical sections including introductory chapters that provide a background on environmental contaminants and the mammalian orders, eight taxonomic chapters discussing all aspects of the exposure to and effects of contaminants in mammalian orders, and four thematic chapters that review and discuss generic issues including biomarkers, prediction and extrapolation of exposure and effects, hazard and risk assessment, and the relative significance of contaminants on mammals compared with other commonly encountered stressors. A final a summary chapter identifies phylogenetic trends, critical data gaps, and overarching research needs. Although the absolute number of toxicological studies in domesticated and wild mammals eclipses that wildlife species, a detailed examination of our knowledge base reveals that information for 'wild' birds is actually greater than that for 'wild' mammals. Of the various mammalian taxa, ecotoxicological data is most noticeably lacking for marsupials and monotremes. In contrast, rodents (comprising 43% of all mammal species) have been studied extensively, despite evidence of their tolerance to some organochlorine compounds, rodenticides, and even radionuclides. Mammalian species at greatest risk of exposure include those that consume a high percentage of their body weight on a daily basis. Aquatic mammals tend to bioaccumulate tremendous burdens of lipophilic contaminants, although storage in their fat depots may actually limit toxicity. Carnivores appear to be more sensitive to adverse effects of environmental contaminants than herbivores. Remarkably few of the thousands of compounds manufactured worldwide have been toxicologically evaluated in wild mammals, and concentrations of even fewer have been monitored in tissues.

Ecological & Environmental Toxicology Series.↗

White-nose syndrome in bats: U.S. Geological Survey updates

White-nose syndrome (WNS) is a devastating disease that has killed millions of hibernating bats since it first appeared in New York in 2007 and has spread at an alarming rate from the northeastern to the central United States and Canada. The disease is named for the white fungus Geomyces destructans that infects the skin of the muzzle, ears, and wings of hibernating bats. The U.S. Geological Survey (USGS) National Wildlife Health Center (NWHC), the USGS Fort Collins Science Center, the U.S. Fish and Wildlife Service, and other partners continue to play a primary role in WNS research. Studies conducted at the NWHC led to the discovery (Blehert and others, 2009), characterization, and naming (Gargas and others, 2009) of the cold-loving fungus G. destructans and to the development of standardized criteria for diagnosing the disease (Meteyer and others, 2009). Additionally, scientists at the NWHC have pioneered laboratory techniques for studying the effects of the fungus on hibernating bats (Lorch and others, 2011). To determine if bats are affected by white-nose syndrome, scientists look for a characteristic microscopic pattern of skin erosion caused by G. destructans (Meteyer and others, 2009). Field signs of WNS can include visible white fungal growth on the bat's muzzle, wings, or both, but these signs alone are not a reliable disease indicator - laboratory examination and testing are required for disease confirmation. Infected bats also arouse from hibernation more frequently than uninfected bats (Warnecke and others, 2012) and often display abnormal behaviors in their hibernation sites, such as congregating at or near cave openings and daytime flights during winter. These abnormal behaviors may contribute to the bat's accelerated consumption of stored fat reserves, causing emaciation, a characteristic documented in some of the bats that die with WNS. During hibernation, bats likely have lowered immunity (Bouma and others, 2010), which may facilitate the ability of G. destructans to colonize and damage large areas of wing membrane (fig. 2). A current hypothesis suggests that erosion or ulceration of wing membrane caused by the fungus has the potential to alter the physiology of hibernating bats, resulting in fatal disruption of hydration, electrolyte balance, circulation, and thermoregulation (Cryan and others, 2010). Current estimates of bat population declines in the northeastern United States since the emergence of WNS are over 80 percent (Turner and others, 2011). This sudden and widespread mortality associated with WNS is unprecedented in hibernating bats, among which large-scale disease outbreaks have not been previously documented. It is unlikely that species of bats affected by WNS will recover quickly because most are long-lived and have only a single pup per year. Consequently, repopulation after widespread mortality of breeding adults will be a slow process. Worldwide, bats play essential roles as pollinators, seed dispersers, and as primary consumers of insects. The true ecological consequences of the recent large-scale reductions in populations of hibernating bats are not yet known. However, farmers might feel the impact. A recent economic analysis indicated that insect control services (ecosystem services) provided by bats to U.S. agriculture is valued between 4 to 50 billion dollars nationwide per year (Boyles and others, 2011). The number of North American bats estimated to have died from WNS thus far had the capacity to consume up to 8,000 tons of insects per year (Boyles and others, 2011). The area of North America affected by WNS continues to expand. Within the last 2 years, the disease has been confirmed in several Central States, including Alabama, Indiana, Kentucky, Ohio, Tennessee, and Missouri. High mortality of bats has not yet been reported at these locations, and it remains to be seen if WNS will develop and manifest in other States with the same severity as that in the Northeast.

Alabama;Connecticut;Delaware;Illinois;Indiana;Iowa↗

The impact of disease in the American white pelican in North America

Records of reported die-offs of the American White Pelican (Pelicanus erythrorhynchos) held by the U.S. Geological Survey National Wildlife Health Center from 1978 through 2003 indicate that type C botulism (caused by Clostridium botulinum) was the major cause of mortality. In 1996, over 15,000 birds, including 8,500 American White Pelicans, were estimated to have died from type C botulism at the Salton Sea in California. This was the largest documented die-off of any pelican species and was estimated to represent 15-20% of the western metapopulation. This event was also notable in that it was the first time that fish, specifically Tilapia (Oreochromis mossambicus), were implicated as the source of type C botulinum toxin for birds. Type C botulism has recurred in both North American species of pelicans at the Salton Sea every year since, although the magnitude of mortality is much lower. West Nile virus caused mortality in both adult and immature American White Pelicans, but may have a more significant impact on nestlings. Emaciation and mortality is common in pelican nesting colonies. Further clarification of the cause of nestling mortality and the ability to differentiate background mortality from mortality due to infectious disease agents such as West Nile virus and Newcastle disease virus would be important in determining the impact of disease in pelicans. Although definitive conclusions cannot be drawn, the number of die-offs and the estimated losses of American White Pelicans appears to have increased along with declines in number in western U.S.

Waterbirds↗

Pathways for avian influenza virus spread: GPS reveals wild waterfowl in commercial livestock facilities and connectivity with the natural wetland landscape

Zoonotic diseases are of considerable concern to the human population and viruses such as avian influenza (AIV) threaten food security, wildlife conservation and human health. Wild waterfowl and the natural wetlands they use are known AIV reservoirs, with birds capable of virus transmission to domestic poultry populations. While infection risk models have linked migration routes and AIV outbreaks, there is a limited understanding of wild waterfowl presence on commercial livestock facilities, and movement patterns linked to natural wetlands. We documented 11 wild waterfowl (three Anatidae species) in or near eight commercial livestock facilities in Washington and California with GPS telemetry data. Wild ducks used dairy and beef cattle feed lots and facility retention ponds during both day and night suggesting use for roosting and foraging. Two individuals (single locations) were observed inside poultry facility boundaries while using nearby wetlands. Ducks demonstrated high site fidelity, returning to the same areas of habitats (at livestock facilities and nearby wetlands), across months or years, showed strong connectivity with surrounding wetlands, and arrived from wetlands up to 1251 km away in the week prior. Telemetry data provides substantial advantages over observational data, allowing assessment of individual movement behaviour and wetland connectivity that has significant implications for outbreak management. Telemetry improves our understanding of risk factors for waterfowl–livestock virus transmission and helps identify factors associated with coincident space use at the wild waterfowl–domestic livestock interface. Our research suggests that even relatively small or isolated natural and artificial water or food sources in/near facilities increases the likelihood of attracting waterfowl, which has important consequences for managers attempting to minimize or prevent AIV outbreaks. Use and interpretation of telemetry data, especially in near-real-time, could provide key information for reducing virus transmission risk between waterfowl and livestock, improving protective barriers between wild and domestic species, and abating outbreaks.

Transboundary and Emerging Diseases↗

Sylvatic plague vaccine: combating plague in prairie dogs and black-footed ferrets

After achieving promising results in laboratory trials, researchers at the USGS National Wildlife Health Center (NWHC) and University of Wisconsin at Madison will soon begin field testing a new oral vaccine for sylvatic plague, a devastating disease affecting prairie dogs and other mammals, particularly the endangered black-footed ferret. Our team has developed and is currently registering a sylvatic plague vaccine (SPV) that uses raccoon poxvirus (RCN) to express two key antigens of the Yersinia pestis bacterium, the causative agent of plague.

The Wildlife Professional↗

Baylisascaris Larva Migrans

Summary Baylisascaris procyonis , the common raccoon roundworm, is the most commonly recognized cause of clinical larva migrans (LM) in animals, a condition in which an immature parasitic worm or larva migrates in a host animal’s tissues, causing obvious disease. Infection with B. procyonis is best known as a cause of fatal or severe neurologic disease that results when the larvae invade the brain, the spinal cord, or both; this condition is known as neural larva migrans (NLM). Baylisascariasis is a zoonotic disease, that is, one that is transmissible from animals to humans. In humans, B. procyonis can cause damaging visceral (VLM), ocular (OLM), and neural larva migrans. Due to the ubiquity of infected raccoons around humans, there is considerable human exposure and risk of infection with this parasite. The remarkable disease-producing capability of B. procyonis in animals and humans is one of the most significant aspects of the biology of ascarids (large roundworms) to come to light in recent years. Infection with B. procyonis has important health implications for a wide variety of free-ranging and captive wildlife, zoo animals, domestic animals, as well as human beings, on both an individual and population level. This report, eighth in the series of U.S. Geological Survey Circulars on zoonotic diseases, will help us to better understand the routes of Baylisascaris procyonis infections and how best to adequately monitor this zoonotic disease.

Circular↗

Environmental influences on major waterfowl diseases

The decline of North American waterfowl resources since the 1960s is well-known to this audience and need not be detailed to establish that population numbers for several key waterfowl species are at or near their lowest levels since records have been kept. Loss of habitat is an accepted major cause for the decline of waterfowl numbers and the wildlife conservation community is responding with initiatives to prevent further loss of existing wetland acreage, restoration for degraded wetlands and creation of new wetlands. Numerous joint ventures focusing on key waterfowl habitat requirements are being developed under the North American Waterfowl Plan. The importance of habitat loss also is reflected in many of the presentations at this conference on wetland conservation, including one special session devoted solely to that topic. A basic premise of the focus on wetlands is that restoration of waterfowl populations is habitat dependent. This is a tenable thesis if other factors suppressing waterfowl numbers are dealt with and the habitat base being enhanced sustains waterfowl rather than contributes to their death. My presentation addresses disease as a factor suppressing waterfowl numbers and the relation of habitat quantity and quality with waterfowl disease.

Transactions of the North American Wildlife and Na↗

Serotypes and DNA fingerprint profiles of Pasteurella multocida isolated from raptors

Pasteurella multocida isolates from 21 raptors were examined by DNA fingerprint profile and serotyping methods. Isolates were obtained from noncaptive birds of prey found in 11 states from November 28, 1979, through February 10, 1993. Nine isolates were from bald eagles, and the remaining isolates were from hawks, falcons, and owls. Seven isolates were members of capsule group A, and 14 were nonencapsulated. One isolate was identified as somatic type 3, and another was type 3,4,7; both had unique HhaI DNA fingerprint profiles. Nineteen isolates expressed somatic type 1 antigen; HhaI profiles of all type 1 isolates were identical to each other and to the HhaI profile of the reference somatic type 1, strain X-73. The 19 type 1 isolates were differentiated by sequential digestion of DNA with HpaII; four HpaII fingerprint profiles were obtained. The HpaII profile of one isolate was identical to the HpaII profile of strain X-73. Incidence of P. multocida somatic type 1 in raptors suggests that this type may be prevalent in other wildlife or wildlife environments.

Avian Diseases↗

Morbidity in California giant salamander (Dicamptodon ensatus Eschscholtz, 1833) caused by Euryhelmis sp. Poche, 1926 (Trematoda: Heterophyiidae)

In the fall of 2021, California Department of Fish and Wildlife reported larval and adult California giant salamanders ( Dicamptodon ensatus Eschscholtz, 1833) with skin lesions at multiple creeks in Santa Clara and Santa Cruz Counties, California, USA. Field signs in both stages included rough, lumpy textured skin, and larvae with tails that were disproportionately long, flat, wavy, and flaccid. Presence of large-bodied larvae suggested delayed metamorphosis, with some larvae having cloudy eyes and suspected blindness. To determine the cause of the disease, three first-of-the-year salamanders from one location were collected, euthanized with 20% benzocaine, and submitted for necropsy to the U.S. Geological Survey, National Wildlife Health Center. Upon gross examination, all salamanders were emaciated with no internal fat stores, and had multiple pinpoint to 1.5-mm diameter raised nodules in the skin over the body, including the head, gills, dorsum, ventrum, all four limbs, and the tail; one also had nodules in the oral cavity and tongue. Histologically all salamanders had multiple encysted metacercariae in the dermis, subcutis, and skeletal muscles of the head, body, and tail that were often associated with granulomatous and granulocytic inflammation and edema. A small number of encysted meta cercariae or empty cysts were present in the gills with minimal inflammation, and rarely in the kidney with no associated inflammation. Morphology of live metacercariae (Trematoda: Heterophyiidae), and sequencing of the 28S rRNA gene identified a species of Euryhelmis (Poche, 1926). Artificial digestion of a 1.65 g, decapitated, eviscerated carcass yielded 773 metacercariae, all of similar size and morphology as the live specimens. Based on these findings, the poor body condition of these salamanders was concluded to be due to heavy parasite burden. Environmental factors such as drought, increased temperature, and overcrowded conditions may be exacerbating parasite infections in these populations of salamander.

California↗

Environmental conditions associated with lesions in introduced free-ranging sheep in Hawai‘i

Wildlife species which have been translocated between temperate and tropical regions of the world provide unique opportunities to understand how disease processes may be affected by environmental conditions. European mouflon sheep (Ovis gmelini musimon) from the Mediterranean Islands were introduced to the Hawaiian Islands for sport hunting beginning in 1954 and were subsequently hybridized with feral domestic sheep (O. aries), which had been introduced in 1793. Three isolated mouflon populations have become established in the Hawaiian Islands but diseases in these populations have been little studied. The objective of this study was to evaluate and compare gross and histologic lesions in respiratory, renal, and hepatic systems of free-ranging sheep in two isolated volcanic environments on Hawai‘i Island. Tissue and fecal samples were collected in conjunction with population reductions during February 2011. We found gross or histologic evidence of lungworm infection in 44/49 sheep from Mauna Loa which were exposed to gaseous emissions from Kīlauea Volcano. In contrast, only 7/50 sheep from Mauna Kea had lesions consistent with lungworm, but Mauna Kea sheep had significantly more upper respiratory tract inflammation and hyperplasia consistent with chronic antigenic stimulation, possibly associated with exposure to fine airborne particulates during extended drought conditions. We hypothesize that gasses from Kīlauea Volcano contributed to severity of respiratory disease principally associated with chronic lungworm infections at Mauna Loa; however, there were numerous other potentially confounding environmental factors and interactions that merit further investigation.

Hawai'i↗

Development and application of a risk assessment tool for aquatic invasive species in the international Rainy-Lake of the Woods Basin, United States and Canada

The Rainy-Lake of the Woods Basin covers 70,000 square kilometers in mid-central North America and is contained within the Provinces of Ontario and Manitoba in Canada and the State of Minnesota in the United States. This basin contains natural wilderness areas, national parks, and thousands of lakes that bring outdoor enthusiasts from around the world for hunting, fishing, backpacking, boating, and other forms of recreation. However, trade, commerce, visitors, and wildlife can inadvertently transport hitchhiking exotic invasive species that affect the functioning of natural systems by displacing native organisms, introducing diseases, and modifying predator/prey relations. In cooperation with the International Joint Commission, the U.S. Geological Survey evaluated the aquatic invasive species that pose a possible threat to North America. The outcome of this project is a set of lists of invasive species that have traits amenable or proximity to the Rainy-Lake of the Woods Basin. These lists can be referenced to further evaluate known and potential nonindigenous invasive species. The lists were derived by evaluating more than 1,500 species from several online sources including Non-Indigenous Aquatic Species, Great Lakes Aquatic Nonindigenous Species Information System, Biodiversity Information Serving Our Nation, and other State, Provincial, and Federal lists in the United States and Canada. The purpose of these lists is to be a coarse filter to determine which species pose the greatest risk to the Rainy-Lake of the Woods Basin. Using this filter, seven categories of risk assessment priorities were developed: Very High-Approaching, Very High-Present, High-Approaching, High-Present, Moderate, Low, and Native. These categories can be used by the International Rainy-Lake of the Woods Multi-Agency Arrangement Aquatic Invasive Species Subcommittee to prioritize which species will be evaluated further focusing on five risk factors: arrival risk, vulnerability assessment, ecological impact, socioeconomic impact, and beneficial impact. Based on proximity, ease of transport or introduction, and known impact to Rainy-Lake of the Woods or other impacted ecosystems, this project identified the following 10 species that could be prioritized first for risk evaluations: Bythotrephes longimanus (spiny waterflea), Faxonius rusticus (rusty crayfish), Neogobius melanostomus (round goby), Dreissena polymorpha (zebra mussel), Bithynia tentaculata (mud Bithynia or faucet snail), Potamopyrgus antipodarum (New Zealand mud snail), Butomus umbellatus (flowering rush), Nitellopsis obtusa (starry stonewort), Myriophyllum spicatum (Eurasian watermilfoil), and Phragmites australis australis (common reed).

Open-File Report↗

Partly cloudy with a chance of mosquitoes: Developing a flexible approach to forecasting mosquito populations

Climate-induced shifts in mosquito phenology and population structure have important implications for the health of humans and wildlife. The timing and intensity of mosquito interactions with infected and susceptible hosts are a primary determinant of vector-borne disease dynamics. Like most ectotherms, rates of mosquito development and corresponding phenological patterns are expected to change under shifting climates. However, developing accurate forecast of mosquito phenology under climate change that can be used to inform management programs remains challenging despite an abundance of available data. As climate change will have variable effects on mosquito demography and phenology across species it is vital that we identify associated traits which may explain the observed variation. Here, we review a suite of modeling approaches that could be applied to generate forecasts of mosquito activity under climate change and evaluate the strengths and weaknesses of the different approaches. We describe four primary life-history and physiological traits that can be used to constrain models and demonstrate how this prior information can be harnessed to develop a more general understanding of how mosquito activity will shift under changing climates. Combining a trait-based approach with appropriate modeling techniques can allow for the development of actionable, flexible, and multi-scale forecasts of mosquito population dynamics and phenology for diverse stakeholders.

Michigan, Wisconsin↗

Intra-annual patterns in adult band-tailed pigeon survival estimates

Context: The band-tailed pigeon ( Patagioenas fasciata ) is a migratory species occurring in western North America with low recruitment potential and populations that have declined an average of 2.4% per year since the 1960s. Investigations into band-tailed pigeon demographic rates date back to the early 1900s, and existing annual survival rate estimates were derived in the 1970s using band return data. Aims: The primary purpose of the paper was to demonstrate that the apparent paradox between band-tailed pigeon population dynamics (long-term steady decline) and breeding season survival rates (very high) can be explained by changes in survival probability during the remainder of the year. Methods: We trapped Pacific coast band-tailed pigeons during two separate periods: we equipped pigeons with very high frequency (VHF) radio-transmitters in 1999–2000 (1999 = 20; 2000 = 34); and outfitted pigeons with solar powered platform transmitting terminal (PTT) transmitters in 2006–08 (n = 20). We used known fate models to estimate annual survival rates and seasonal survival variation among four periods based on an annual behavioural cycle based on phenological events (nesting, autumn migration, winter and spring migrations). We used model averaged parameter estimates to account for model selection uncertainty. Key results: Neither body condition nor sex were associated with variation in band-tailed pigeon survival rates. Weekly survival during the nesting season did not differ significantly between VHF-marked (0.996; CI = 0.984–0.999) and PTT-marked pigeons (0.998; CI = 0.990–1.00). Model averaged annual survival of PTT-marked pigeons was 0.682 (95% CI = 0.426–0.861) and was similar to annual survival estimated in previous studies using band return data. Survival probability was lowest during both migration periods and highest during the nesting period. Conclusions: Our survival estimates are consistent with those of prior studies and suggest that mortality risk is greatest during migration. Weekly survival probability during winter was nearly the same as during the nesting season; however, winter was the longest period and survival throughout winter was lower than other seasons. Implications: We present the first inter-seasonal analysis of survival probability of the Pacific coast race of band-tailed pigeons and illustrate important temporal patterns that may influence future species management including harvest strategies and disease monitoring.

Wildlife Research↗

Avian cholera in the central and Mississippi flyways 1979-80

Waterfowl mortality from avian cholera during July 1979-May 1980 was widespread in the Central and Mississippi flyways, occurring in a wide variety of species and locations from nesting grounds of snow geese ( Chen caerulescens ) on Hudson Bay south to waterfowl wintering areas on the Texas coast and playa lakes region. Mortality estimates at the various sites ranged from several birds to over 72,000. The chronological and geographic occurrence of outbreaks corresponded closely to waterfowl migrations from infected sites, suggesting that waterfowl served to distribute avian cholera along migration routes. Recurrent outbreaks at several locations suggest that these sites have become enzootic for this disease. The magnitude of avian cholera mortality and its geographic spread during 1979-80 underscores the need to address management of this disease on an intra- and inter-flyway basis.

Central & Mississippi flyways↗

Tumors in sea turtles: The insidious menace of fibropapillomatosis

Early in July 2013, a colleague in New Caledonia reported the stranding of a green sea turtle on the far northwest of the island. The animal had washed up dead on a rocky beach with multiple large tumors on its neck and hind flippers. To all appearances, the turtle had fibropapillomatosis (FP), a tumor disease affecting marine turtles globally. This was the first known case of FP on the island—an alarming find, and another example of the creeping expansion of this disease in green turtles around the world.

The Wildlife Professional↗