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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.

Loma sp. salmonids from the Eastern United States: Associated lesions rainbow trout

A microsporidian of the genus Loma was noted in the gills of rainbow trout Oncorhynchus mykiss from a state hatchery (Buford Trout Hatchery) in Georgia. Mortalities of varying severity occur at this hatchery every fall, and the microsporidian was noted during an experiment from August 1991 to January 1992 to determine the effects of water source on disease. Infections first appeared to be systemic in the October sample; xenomas were observed in heart, spleen, and peripheral vessel walls. The presence of unidentified intracellular material preceded the appearance of xenomas in all tissues, but whether this material was associated with inflammation or represented immature stages of the parasite has yet to be determined. These structures were also noted in the intestine and liver, although xenomas were not noted in these organs. Mature xenomas did not elicit an inflammatory response but appeared to be short-lived. When the xenoma wall ruptured and released spores, an inflammatory response was again observed. The prevalence and severity of the infection were determined in fish maintained in troughs with well water, Chattahoochee River water, or hatchery (treated river) water. The infection tended to be more prevalent and more severe in fish maintained in the hatchery or river water than in those maintained in the well water. Stress induced by poor water quality may increase mortality from this parasite. This report extends the range of Loma sp. into the eastern United States.

Journal of Aquatic Animal Health

Host jump of an exotic fish rhabdovirus into a new class of animals poses a disease threat to amphibians

Spring viremia of carp virus (SVCV) is a rhabdovirus that primarily infects cyprinid finfishes and causes a disease notifiable to the World Organization for Animal Health. Amphibians, which are sympatric with cyprinids in freshwater ecosystems, are considered non-permissive hosts of rhabdoviruses. The potential host range expansion of SVCV in an atypical host species was evaluated by testing the susceptibility of amphibians native to the Pacific Northwest. Larval long-toed salamanders Ambystoma macrodactylum and Pacific tree frog Pseudacris regilla tadpoles were exposed to SVCV strains from genotypes Ia, Ib, Ic, or Id by either intraperitoneal injection, immersion, or cohabitation with virus-infected koi Cyprinus rubrofuscus . Cumulative mortality was 100% for salamanders injected with SVCV, 98–100% for tadpoles exposed to virus via immersion, and 0–100% for tadpoles cohabited with SVCV-infected koi. Many of the animals that died exhibited clinical signs of disease and SVCV RNA was found by in situ hybridization in tissue sections of immersion-exposed tadpoles, particularly in the cells of the gastrointestinal tract and liver. SVCV was also detected by plaque assay and RT-qPCR testing in both amphibian species regardless of the virus exposure method, and viable virus was detected up to 28 days after initial exposure. Recovery of infectious virus from naïve tadpoles cohabited with SVCV-infected koi further demonstrated that SVCV transmission can occur between classes of ectothermic vertebrates. Collectively, these results indicated that SVCV, a fish rhabdovirus, can be transmitted to and cause lethal disease in two amphibian species. Therefore, members of all five of the major vertebrate groups (mammals, birds, reptiles, fish, and amphibians) appear to be vulnerable to rhabdovirus infections. Future research studying potential spillover and spillback infections of aquatic rhabdoviruses between foreign and domestic amphibian and fish species will provide insights into the stressors driving novel interclass virus transmission events.

Viruses

Epistylis spp. infestation in two species of mud turtles (Kinosternon spp.) in the American Southwest

The protistan genus Epistylis contains freshwater colonial species that attach to aquatic organisms in an epibiotic or parasitic relationship. They are known to attach to the epidermis and shells of aquatic turtles, but have not been reported to cause heavy infestations or morbidity in turtles. We documented heavy infestations of Epistylis spp. in several populations of Sonoran mud turtles ( Kinosternon sonoriense ) inhabiting livestock ponds in Arizona, USA, and rough-footed mud turtles ( Kinosternon hirtipes ) from livestock ponds in Texas, USA, over the course of several years. Severe Epistylis spp. infestations on mud turtles appeared to alter diving and swimming behavior when compared to uninfested conspecifics. Infestations were cleared in captivity using tap water or a 10% salt solution, and the turtles had no permanent damage to their shell or epidermis upon clearing. While several of the mud turtles we observed had poor body condition, it is possible that the severe infestations we observed were caused by a comorbidity associated with a pathogen, parasite, or poor habitat quality that made the turtles more susceptible to the Epistylis spp. infestation. Further research on causes for these severe infestations are warranted because they contribute to changes in behavior of the heavily infested turtles and may contribute to morbidity in Kinosternon spp. when mud turtles inhabit extremely warm, shallow, eutrophic aquatic habitats, such as livestock ponds.

Arizona

Effects of a low-lipid diet on the gut microbiome and head kidney transcriptome of juvenile Chinook Salmon

Objective Pacific salmon Oncorhynchus spp. reared in production hatcheries are typically fed high-lipid, energy-dense diets to achieve large size and high body condition prior to release. In contrast, juveniles in natural environments tend to consume low-lipid, high-protein diets, and fish reared for research or conservation purposes are sometimes fed diets that are formulated to mimic natural diets and promote wild-like phenotypes. Understanding how these alternative diets affect fish health beyond growth and body condition could ultimately contribute to improving hatchery fish fitness. Methods In this work, we evaluated changes in the fecal microbiome and gene expression of juvenile Chinook Salmon O. tshawytscha on a standard high-lipid hatchery diet versus a low-lipid diet formulated to mimic the nutrition profile of natural-origin fish. To evaluate the time scale at which diet alters the fecal microbiome, we collected longitudinal samples over a 12-week period and switched the diets of a subset of fish twice during the experiment. We used 16S ribosomal RNA gene amplicon sequencing to characterize fecal microbiome differences between fish on the two diets as well as hatchery-reared fish at a production hatchery, hatchery fish that had been captured after release into a stream, and natural-origin, stream-reared fish of similar ages. Additionally, we conducted RNA sequencing on head kidney samples from laboratory-reared fish to evaluate changes in gene expression in this important immune organ. Results We found that the low-lipid diet and the hatchery diet resulted in microbiomes that differed from the microbiome of natural-origin fish and from each other and that diet-driven changes to the microbiome could occur in under 14 d. The low-lipid diet did not result in a microbiome that resembled the microbiome of naturally produced fish. Instead, the low-lipid diet resulted in a microbiome community that was distinct from those of fish reared on the hatchery diet and fish sampled from the wild. The RNA sequencing results indicated differential enrichment of pathways related to immunity, metabolism, and hormone synthesis between fish that were fed the two experimental diets. Conclusions The results suggest that additional environmental factors influence the microbiome more strongly than diet formulation or that the low-lipid diet has a smaller effect on the microbiome than a natural, ­invertebrate-based diet. Given that the gut microbiome and systemic immune function contribute significantly to disease resistance, our findings highlight the importance of understanding how diets fed to fish in captivity may affect fish health beyond growth and body condition metrics.

Journal of Aquatic Animal Health

Infection by Nanophyetus salmincola and toxic contaminant exposure in out‐migrating steelhead from Puget Sound, Washington: Implications for early marine survival

Out‐migrating steelhead Oncorhynchus mykiss from four Puget Sound rivers and associated marine basins of Puget Sound in Washington State were examined for the parasite, Nanophyetus salmincola in 2014 to determine whether recent trends in reduced marine survival are associated with the presence of this pathogen. A subset of steelhead from three of these river–marine basin combinations was analyzed for the presence of persistent organic pollutants (POPs) to assess whether exposure to these contaminants is a contributing factor to their reduced marine survival. The prevalence and parasite load of N. salmincola were significantly higher in fish from central and southern Puget Sound than in fish from river systems in northern Puget Sound. The proportion of steelhead samples with concentrations of POPs higher than adverse effects thresholds (AETs) or concentrations known to cause adverse effects was also greater in fish from the central and southern regions of Puget Sound than in those from the northern region. Polybrominated diphenyl ether concentrations associated with increased disease susceptibility were observed in 10% and 40% of the steelhead sampled from central and southern Puget Sound regions, respectively, but in none of the fish sampled from the northern region. The AET for polychlorinated biphenyls was exceeded in steelhead collected from marine habitats: 25% of the samples from the marine basins in the central and southern regions of Puget Sound and 17% of samples from northern Puget Sound region. Both N. salmincola and POP levels suggest there are adverse health effects on out‐migrating steelhead from one southern and one central Puget Sound river that have lower early marine survival than those from a river system in northern Puget Sound.

Washington

Effect of climate change on disease spread in wildlife

A growing body of evidence indicates that climate change alone, or acting synergistically with current anthropogenic threats, is affecting the health of wild populations of aquatic and terrestrial wildlife. Measurable by-products of climate change include elevated atmospheric concentrations of greenhouse gases, higher average global temperatures; variations in global precipitation patterns, rising and warming oceans, altered hydrographs of rivers, and increased mid-continental drying during summer. These consequences affect the terrestrial environment through shifts in phenology, vegetation cover, and fire regimes. Warmer ocean temperatures, increased acidification, rise in sea levels, and reduction in sea ice cover are also leading to widespread ecological changes in marine systems. Wildlife populations face a variety of climate-related pressures, such as changes in animal distribution or density, limitation of food resources, and alteration to critical habitats. The increased potential for emergence and resurgence of diseases that are responsive to environmental conditions also has implications for wildlife populations. Shifts in temperature or other climatic factors may directly affect the incidence of disease in wildlife by altering host-pathogen interactions, promoting vector populations or allowing new ranges for vectors, or reducing development times for parasites. A number of examples from both field and laboratory studies have demonstrated a clear link between warming environments and disease spread. Many climate-related environmental changes also influence wildlife health indirectly. For example, increasing temperatures, in combination with shifts in rainfall and humidity, may aggravate current trends for water resource limitation and habitat degradation or destruction and lead to increased crowding of animal populations, thereby promoting transmission opportunities of pathogens within populations or across species. Although it may be difficult to disentangle the influences of other anthropogenic changes from the direct effects of warming, some ecosystems provide especially useful models for studying climate-related disease spread in wildlife. For example, the effects of climate change on parasite dynamics may be easily observed in the Arctic, where environmental changes are occurring rapidly, anthropogenic influences are relatively limited, and biodiversity is generally low. Marine ecosystems are also undergoing rapid rates of change and may be vulnerable to a variety of natural and anthropogenic perturbations. Although many factors affect the health of organisms in ocean environments, temperature has been clearly linked to an increase in disease prevalence among sessile organisms such as corals. In this chapter, we discuss observed and predicted changes to wildlife health resulting from climate change. Our review will not include all aspects of wildlife health, but will instead focus on established or suspected links between climate drivers and disease spread and discuss examples from the current literature. Here, we define disease spread to include: 1) change in geographical or altitudinal distribution of pathogens, parasites, and vectors and the diseases they cause; 2) change in prevalence or severity of disease; and 3) emergence of novel diseases. Additionally, because wildlife species serve as reservoirs for zoonotic diseases that affect both animals and humans, we include select examples of the effect of climate change on the capacity of wildlife to harbor and spread these disease agents.

Book chapter

Evidence that coded-wire-tagging procedures can enhance transmission of Renibacterium salmoninarum in chinook salmon

Binary coded wire tags (CWTs) are used extensively for identification and management of anadromous salmonid populations. A study of bacterial kidney disease (BKD) in two brood year groups of hatchery-reared spring chinook salmon Oncorhynchus tshawytscha provided strong evidence that horizontal transmission of Renibacterium salmoninarum, the causative agent of BKD, might be enhanced by CWT-marking procedures. About 4 months after CWTs were implanted in the snouts of juvenile fish, 14-16 different tissues were sampled from each of 60 fish per brood year group for histological analysis. Of the fish that were positive for R. salmoninarum by histological examination, 41% (7 of 17) of the 1988 brood year fish and 24% (10 of 42) of the 1989 brood year fish had BKD lesions confined to the head near the site of tag implantation. These lesions often resulted in the destruction of tissues of one or both olfactory organs. No focal snout infections were observed in fish that had not been marked with CWTs. Further data obtained from tissue analyses by use of an enzyme-linked immunosorbent assay and a fluorescent antibody test for detection of R. salmoninarum supported the hypothesis that infections of R. salmoninarum can be initiated in the snout tissues of CWT-marked fish and then spread to other organs. The tagging procedures might promote transmission of the pathogen among fish via contaminated tagging needles, by facilitating the entry of pathogens through the injection wound, or both. Limited evidence from this study suggested that implantation of passive integrated transponder tags in the peritoneal cavities of fish might also promote the transmission of R. salmoninarum or exacerbate existing infections. The results indicated a need for strict sanitary procedures during the tagging of fish in populations positive for R. salmoninarum to reduce the probability of enhanced horizontal transmission of the pathogen.

Journal of Aquatic Animal Health

Diagnostic criteria for selenium toxicosis in aquatic birds: dietary exposure, tissue concentrations, and macroscopic effects

A feeding study with mallard ducks ( Anas platyrhynchos ) was conducted during March to July 1988 in Laurel, Maryland (USA), to identify diagnostic criteria for selenium toxicosis in birds. One-year-old male mallards in groups of 21 were fed diets containing 0, 10, 20, 40, or 80 parts per million (ppm) selenium, as seleno-DL-methionine, for 16 weeks. All ducks receiving 80 ppm died. Ducks receiving 40 or 80 ppm selenium consumed less feed than ducks in the other treatment groups. Body weights of ducks receiving 40 or 80 ppm selenium declined during the study. The post-breeding molt was delayed in ducks receiving 40 ppm; most ducks receiving 80 ppm selenium died prior to the onset of molt. At necropsy, numerous abnormalities were observed in ducks that died but only a small number of abnormalities were observed in ducks surviving to the end of the study in the 40 ppm group. Weights of the heart, spleen, and pancreas were mostly lower and weights of the kidney were higher for ducks dying during the study than for euthanized ducks. Liver weights were unaffected. Selenium accumulated in soft tissues approximately in proportion to dietary concentrations. Selenium concentrations in tissues of all ducks that died were different from those of surviving ducks in the 0, 10, and 20 ppm groups, but were not different from those of surviving ducks in the 40 ppm group. Proposed diagnostic criteria for fatal chronic selenosis were derived from body weight, macroscopic abnormalities, organ weights, and concentrations of selenium in the liver. Proposed diagnostic criteria for non-fatal chronic selenosis were derived from body weight, plumage condition, macroscopic abnormalities, concentrations of selenium in the liver, reproductive failure, and alterations of blood and tissue chemistries. Lead or dioxin poisoning have diagnostic criteria most similar to selenium toxicosis.

Journal of Wildlife Diseases

Monitoring amphibians in Great Smoky Mountains National Park

Amphibian species have inexplicably declined or disappeared in many regions of the world, and in some instances, serious malformations have been observed. In the United States, amphibian declines frequently have occurred even in protected areas. Causes for the declines and malformations probably are varied and may not even be related. The seemingly sudden declines in widely separated areas, however, suggests a need to monitor amphibian populations as well as identify the causes when declines or malformations are discovered. In 2000, the President of the United States and Congress directed Department of the Interior (DOI) agencies to develop a plan to monitor the trends in amphibian populations on DOI lands and to conduct causes of declines. The DOI has stewardship responsibilities over vast land holdings in the United States, much of it occupied by, or potential habitat for, amphibians. The U.S. Geological Survey (USGS) was given lead responsibility for planning and organizing this program, named the Amphibian Research and Monitoring Initiative (ARMI). Authorization carried the mandate to set up a national amphibian monitoring program on Federal lands, to develop the sampling techniques and biometrical analyses necessary to determine status and trends, and to identify possible causes of amphibian declines and malformations. The biological importance of Great Smoky Mountains National Park has been recognized by its designation as an International Biosphere Reserve. As such, it is clearly the leading region of significance for amphibian research. Although no other region shares the wealth of amphibians as found in the Great Smokies (31 species of salamanders, and 13 of frogs), the entire southern and mid-section of the Appalachian Mountain chain is characterized by a high diversity of amphibians, and inventories and monitoring protocols developed in the Smokies likely will be applicable to other Appalachian National Park Service properties. From 1998 to 2001, USGS biologists carried out a pilot inventory and monitoring research project in Great Smoky Mountains National Park. A variety of inventory, sampling, and monitoring techniques were employed and tested. These included wide-scale visual encounter surveys of amphibians at terrestrial and aquatic sites, intensive monitoring of selected plots, randomly placed small-grid plot sampling, litterbag sampling in streams, monitoring nesting females of selected species, call surveys, and monitoring specialized habitats, such as caves. Coupled with information derived from amphibian surveys on Federal lands using various other techniques (automated frog call data loggers, PVC pipes, drift fences, terrestrial and aquatic traps), an amphibian monitoring program was designed to best meet the needs of biologists and natural resource managers after taking into consideration the logistics, terrain, and life histories of the species found within Great Smoky Mountains National Park. This report provides an overview of the Park’s amphibians, the factors affecting their distribution, a review of important areas of biodiversity, and a summary of amphibian life history in the Southern Appalachians. In addition, survey techniques are described as well as examples of how the techniques are set up, a critique of what the results tell the observer, and a discussion of the limitations of the techniques and the data. The report reviews considerations for site selection, outlines steps for biosecurity and for processing diseased or dying animals, and provides resource managers with a decision tree on how to monitor the Park’s amphibians based on different levels of available resources. It concludes with an extensive list of references for inventorying and monitoring amphibians. USGS and Great Smoky Mountains National Park biologists need to establish cooperative efforts and training to ensure that congressionally mandated amphibian surveys are performed in a statistically rigorous and biologically meaningful manner, and that amphibian populations on Federal lands are monitored to ensure their long-term survival. The research detailed in this report will aid these cooperative efforts.

North Carolina, Tennessee

From headwaters to coast: Influence of human activities on water quality of the Potomac River Estuary

The natural aging process of Chesapeake Bay and its tributary estuaries has been accelerated by human activities around the shoreline and within the watershed, increasing sediment and nutrient loads delivered to the bay. Riverine nutrients cause algal growth in the bay leading to reductions in light penetration with consequent declines in sea grass growth, smothering of bottom-dwelling organisms, and decreases in bottom-water dissolved oxygen as algal blooms decay. Historically, bay waters were filtered by oysters, but declines in oyster populations from overfishing and disease have led to higher concentrations of fine-sediment particles and phytoplankton in the water column. Assessments of water and biological resource quality in Chesapeake Bay and tributaries, such as the Potomac River, show a continual degraded state. In this paper, we pay tribute to Owen Bricker’s comprehensive, holistic scientific perspective using an approach that examines the connection between watershed and estuary. We evaluated nitrogen inputs from Potomac River headwaters, nutrient-related conditions within the estuary, and considered the use of shellfish aquaculture as an in-the-water nutrient management measure. Data from headwaters, nontidal, and estuarine portions of the Potomac River watershed and estuary were analyzed to examine the contribution from different parts of the watershed to total nitrogen loads to the estuary. An eutrophication model was applied to these data to evaluate eutrophication status and changes since the early 1990s and for comparison to regional and national conditions. A farm-scale aquaculture model was applied and results scaled to the estuary to determine the potential for shellfish (oyster) aquaculture to mediate eutrophication impacts. Results showed that (1) the contribution to nitrogen loads from headwater streams is small (about 2 %) of total inputs to the Potomac River Estuary; (2) eutrophic conditions in the Potomac River Estuary have improved in the upper estuary since the early 1990s, but have worsened in the lower estuary. The overall system-wide eutrophication impact is high, despite a decrease in nitrogen loads from the upper basin and declining surface water nitrate nitrogen concentrations over that period; (3) eutrophic conditions in the Potomac River Estuary are representative of Chesapeake Bay region and other US estuaries; moderate to high levels of nutrient-related degradation occur in about 65 % of US estuaries, particularly river-dominated low-flow systems such as the Potomac River Estuary; and (4) shellfish (oyster) aquaculture could remove eutrophication impacts directly from the estuary through harvest but should be considered a complement—not a substitute—for land-based measures. The total nitrogen load could be removed if 40 % of the Potomac River Estuary bottom was in shellfish cultivation; a combination of aquaculture and restoration of oyster reefs may provide larger benefits.

Maryland, Pennsylvania, Virginia, West Virginia