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Validation of laboratory tests for infectious diseases in wild mammals: Review and recommendations

Evaluation of the diagnostic sensitivity (DSe) and specificity (DSp) of tests for infectious diseases in wild animals is challenging, and some of the limitations may affect compliance with the OIE-recommended test validation pathway. We conducted a methodologic review of test validation studies for OIE-listed diseases in wild mammals published between 2008 and 2017 and focused on study design, statistical analysis, and reporting of results. Most published papers addressed Mycobacterium bovis infection in one or more wildlife species. Our review revealed limitations or missing information about sampled animals, identification criteria for positive and negative samples (case definition), representativeness of source and target populations, and species in the study, as well as information identifying animals sampled for calculations of DSe and DSp as naturally infected captive, free-ranging, or experimentally challenged animals. The deficiencies may have reflected omissions in reporting rather than design flaws, although lack of random sampling might have induced bias in estimates of DSe and DSp. We used case studies of validation of tests for hemorrhagic diseases in deer and white-nose syndrome in hibernating bats to demonstrate approaches for validation when new pathogen serotypes or genotypes are detected and diagnostic algorithms are changed, and how purposes of tests evolve together with the evolution of the pathogen after identification. We describe potential benefits of experimental challenge studies for obtaining DSe and DSp estimates, methods to maintain sample integrity, and Bayesian latent class models for statistical analysis. We make recommendations for improvements in future studies of detection test accuracy in wild mammals.

Journal of Veterinary Diagnostic Investigation

Dolphin swimming: A review

Research into dolphin swimming has historically been guided by false assumptions of ‘effortless’, ‘high-speed’ swimming. These assumptions have instigated the development of drag-reduction hypotheses but tests of these hypotheses have generally had little success. The autecological approach has dominated recent efforts and has been more successful. In this review we summarize results of decades of research efforts to study these creatures. (1) Drag is minimized primarily by the streamlined shape of the body and appendages, with no known contributions from compliant dampening, dermal ridges, secretions, boundary layer heating, or skin folds. All indications are that the boundary layer is turbulent. (2) Muscles for the upstroke and downstroke of swimming dolphins provide approximately equal power. (3) Output force is enhanced by insertions occurring on the long processes of the vertebrae and on the subdermal connective tissue sheath. (4) Measured swimming speeds are lower than previously believed, with maximum reported routine speeds being approximately 3 m/s. (5) Porpoising behaviour appears to be the most energetically conservative manner in which to breathe when swimming at high speed. (6) Riding surf and wind waves involves the balance between the wave slope and the weight of the animal whereas riding the bow wave involves the interaction of the pressure wave in front of a ship and the drag of the dolphin.

Mammal Review

Conservation issues and strategies for elephant-shrews

The recommendations and implementation of the IUCN conservation plan for African Insectivora and elephant-shrews (Nicoll & Rathbun, 1990) are reviewed. Of the 33 species and subspecies of elephant-shrews, only six forest-dwelling taxa are threatened. Until additional status data are gathered, assessed, and published no changes in the IUCN threatened categories should be made: Rhynchocyon chrysopygus is ‘vulnerable’; Rhynchocyon petersi petersi and Rhynchocyon petersi adersi are ‘rare’; and Rhynchocyon cirnei cirnei, Rhynchocyon cirnei hendersoni , and Petrodromus tetradactylus sangi are ‘insufficiently known’. Implementing status surveys that have not been completed, especially for the forms of R. petersi and P. t. sangi , are a high priority. Rhynchocyon petersi and R. chrysopygus densities are lower in altered and trapped forests compared with undisturbed forests. Because undisturbed forests in eastern Africa are highly fragmented, small, and disappearing due to human encroachment, it is important to determine the population dynamics of Rhynchocyon spp. that occupy degraded forest habitats, such as plantations, follow agricultural lands, and coastal scrub. In the face of the expanding human population, with its increasing need for land and natural resources, Rhynchocyon populations that occur in these degraded habitats may be all that remain in the future.

Mammal Review

Multiple mortality events in bats: a global review

Despite conservation concerns for many species of bats, factors causing mortality in bats have not been reviewed since 1970. Here, we review and qualitatively describe trends in the occurrence and apparent causes of multiple mortality events (MMEs) in bats around the world. We compiled a database of MMEs, defined as cases in which ≥ 10 dead bats were counted or estimated at a specific location within a maximum timescale of a year, and more typically within a few days or a season. We tabulated 1180 MMEs within nine categories. Prior to 2000, intentional killing by humans caused the greatest proportion of MMEs in bats. In North America and Europe, people typically killed bats because they were perceived as nuisances. Intentional killing occurred in South America for vampire bat control, in Asia and Australia for fruit depredation control, and in Africa and Asia for human food. Biotic factors, accidents, and natural abiotic factors were also important historically. Chemical contaminants were confirmed causes of MMEs in North America, Europe, and in islands. Viral and bacterial diseases ranked low as causes of MMEs in bats. Two factors led to a major shift in causes of MMEs in bats at around 2000: the global increase of industrial wind-power facilities and the outbreak of white-nose syndrome in North America. Collisions with wind turbines and white-nose syndrome are now the leading causes of reported MMEs in bats. Collectively, over half of all reported MMEs were of anthropogenic origin. The documented occurrence of MMEs in bats due to abiotic factors such as intense storms, flooding, heat waves, and drought is likely to increase in the future with climate change. Coupled with the chronic threats of roosting and foraging habitat loss, increasing mortality through MMEs is unlikely to be compensated for, given the need for high survival in the dynamics of bat populations.

Mammal Review

Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals

Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and S. canis are related protozoans that can cause mortality in many species of domestic and wild animals. Recently, T. gondii and S. neurona were recognized to cause encephalitis in marine mammals. As yet, there is no report of natural exposure of N. caninum in marine mammals. In the present study, antibodies to T. gondii and N. caninum were assayed in sera of several species of marine mammals. For T. gondii, sera were diluted 1:25, 1:50, and 1:500 and assayed in the T. gondii modified agglutination test (MAT). Antibodies (MAT a?Y1:25) to T. gondii were found in 89 of 115 (77%) dead, and 18 of 30 (60%) apparently healthy sea otters (Enhydra lutris), 51 of 311 (16%) Pacific harbor seals (Phoca vitulina), 19 of 45 (42%) sea lions (Zalophus californianus), 5 of 32 (16%) ringed seals (Phoca hispida), 4 of 8 (50%) bearded seals (Erignathus barbatus), 1 of 9 (11.1%) spotted seals (Phoca largha), 138 of 141 (98%) Atlantic bottlenose dolphins (Tursiops truncatus), and 3 of 53 (6%) walruses (Odobenus rosmarus). For N. caninum, sera were diluted 1:40, 1:80, 1:160, and 1:320 and examined with the Neospora agglutination test (NAT) using mouse-derived tachyzoites. NAT antibodies were found in 3 of 53 (6%) walruses, 28 of 145 (19%) sea otters, 11 of 311 (3.5%) harbor seals, 1 of 27 (3.7%) sea lions, 4 of 32 (12.5%) ringed seals, 1 of 8 (12.5%) bearded seals, and 43 of 47 (91%) bottlenose dolphins. To our knowledge, this is the first report of N. caninum antibodies in any marine mammal, and the first report of T. gondii antibodies in walruses and in ringed, bearded, spotted, and ribbon seals. Current information on T. gondii-like and Sarcocystis-like infections in marine mammals is reviewed. New cases of clinical S. canis and T. gondii infections are also reported in sea lions, and T. gondii infection in an Antillean manatee (Trichechus manatus manatus).

Alaska, California, Washington

Unexplained patterns of grey wolf Canis lupus natal dispersal

Natal dispersal (movement from the site of birth to the site of reproduction) is a pervasive but highly varied characteristic of life forms. Thus, understanding it in any species informs many aspects of biology, but studying it in most species is difficult. In the grey wolf Canis lupus , natal dispersal has been well studied. Maturing members of both sexes generally leave their natal packs, pair with opposite‐sex dispersers from other packs, near or far, select a territory, and produce their own offspring. However, three movement patterns of some natal‐dispersing wolves remain unexplained: 1) long‐distance dispersal when potential mates seem nearby, 2) round‐trip travels from their natal packs for varying periods and distances, also called extraterritorial movements, and often not resulting in pairing, and 3) coincidental dispersal by individual wolves from a given area in the same basic directions and over the same long distances. This perspective article documents and discusses these unexplained dispersal patterns, suggests possible explanations, and calls for additional research to understand them more clearly.

Mammal Review

Bear diets and human-bear conflicts: Insights from isotopic ecology

Bears, Ursidae, are considered omnivores, except for giant pandas Ailuropoda melanoleuca and polar bears Ursus maritimus. However, omnivory includes a wide range of dietary variation and trophic positions, making bear dietary ecology unclear. We inferred bear trophic positions from δ 15 N (‰) values and examined their correlation with diets reported in the literature, including frequency of human–bear conflicts (livestock predation and crop damage incidents). Overall, 15N signatures were consistent with diet estimates. Bear species with higher 15 N signatures differed more from each other, including cases of large regional intraspecific variance, than bear species with lower 15 N signatures. Bear trophic position and frequency of reports of human–bear conflicts were uncorrelated, suggesting that livestock predation by bears is an opportunistic behaviour rather than a response to food availability dynamics.

Mammal Review

The American black bear (Ursus americanus) as an apex predator: Investigating the ecological role of the world’s most abundant large carnivore

Introduction American black bears ( Ursus americanus ) have been documented to have top-down effects, both consumptive (through predation) and nonconsumptive (through fear effects). However, their behavioural and dietary adaptability has led to uncertainty about the conditions under which these may occur. Objectives We aimed to (1) investigate when, where, and how often black bears influence lower trophic levels, and (2) critically assess the experimental design of such studies to determine trends and biases. Methods We conducted a systematic literature search and used linear mixed-effects models to assess the relationships among prey age class, the presence of other large carnivores, and the percentage of ungulate mortality due to black bears. We also summarised the measured effects of black bears on other carnivores and the results of any experimental studies. Results We found a strong negative relationship between puma presence and the percentage of ungulate mortality due to black bears, but only in areas with at least one other large carnivore (e.g., wolves). Among 16 studies of black bears' impacts on other carnivores, most documented negative behavioural effects. While only 5% of studies had strong experimental design, bear removal consistently increased juvenile ungulate survival. Discussion and Synthesis Our findings highlight black bears' strong top-down effects, resembling or exceeding those of other large carnivores. These effects were greatest when no other large carnivores were present, but as highly effective kleptoparasites, black bears can alter the feeding habits of other large carnivores. Thus, we argue that ‘apex’ is a conditional state, not a species-wide status.

Mammal Review

Assessment of photographs from wildlife monitoring cameras in Drakes Estero, Point Reyes National Seashore, California

Between 2007 and 2010, National Park Service (NPS) staff at the Point Reyes National Seashore, California, collected over 300,000 photographic images of Drakes Estero from remotely operated wildlife monitoring cameras. The purpose of the systems was to obtain photographic data to help understand possible relationships between anthropogenic activities and Pacific harbor seal ( Phoca vitulina richardsi ) behavior and distribution. The value of the NPS photographs for use in assessing the frequency and impacts of seal disturbance and displacement in Drakes Estero has been debated. In September 2011, the NPS determined that the photographs did not provide meaningful information for development of a Draft Environmental Impact Statement (DEIS) for the Drakes Bay Oyster Company Special Use Permit. Limitations of the photographs included lack of study design, poor photographic quality, inadequate field of view, incomplete estuary coverage, camera obstructions, and weather limitations. The Marine Mammal Commission (MMC) reviewed the scientific data underpinning the Drakes Bay Oyster Company DEIS in November 2011 and recommended further analysis of the NPS photographs for use in characterizing rates and consequences of seal disturbance (Marine Mammal Commission, 2011). In response to that recommendation, the NPS asked the U.S. Geological Survey (USGS) to conduct an independent review of the photographs and render an opinion on the utility of the remote camera data for informing the environmental impact analyses included in the DEIS. In consultation with the NPS, we selected the 2008 photographic dataset for detailed evaluation because it covers a full harbor seal breeding season (March 1 to June 30), provides two fields of view (two cameras were deployed), and represents a time period when cameras were most consistently deployed and maintained. The NPS requested that the photographs be evaluated in absence of other data or information pertaining to seal and human activity in the estuary and that we focus on the extent to which the photographs could be used in understanding the relationship between human activity (including commercial oyster production) and harbor seal disturbance and distribution in the estuary.

California

The current status of amphibian and reptile ecotoxicological research

The extent of research conducted on the effects of contaminants on reptiles and amphibians has been scant compared to that of other vertebrate classes including fishes, birds and mammals. In a review of literature from 1972 until 1998 we found that only about 2.7% of the papers published on ecotoxicology in vertebrates concerned amphibians and 1.4% for reptiles. Most studies on amphibian ecotoxicology were on metals, pesticides, and acid deposition. For reptiles the greatest frequency of papers included metals, organochlorines, and others. In proportion to the taxonomic importance, far more papers were written on turtles than on other reptile orders. Most of the papers dealt with residues and very few dealt with effects of contaminant exposure.

Book chapter

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.