Correction: Publication reform to safeguard wildlife from researcher harm.

[This corrects the article DOI: 10.1371/journal.pbio.3000193.].

Publication reform to safeguard wildlife from researcher harm.

Despite abundant focus on responsible care of laboratory animals, we argue that inattention to the maltreatment of wildlife constitutes an ethical blind spot in contemporary animal research. We begin by reviewing significant shortcomings in legal and institutional oversight, arguing for the relatively rapid and transformational potential of editorial oversight at journals in preventing harm to vertebrates studied in the field and outside the direct supervision of institutions. Straightforward changes to animal care policies in journals, which our analysis of 206 journals suggests are either absent (34%), weak, incoherent, or neglected by researchers, could provide a practical, effective, and rapidly imposed safeguard against unnecessary suffering. The Animals in Research: Reporting On Wildlife (ARROW) guidelines we propose here, coupled with strong enforcement, could result in significant changes to how animals involved in wildlife research are treated. The research process would also benefit. Sound science requires animal subjects to be physically, physiologically, and behaviorally unharmed. Accordingly, publication of methods that contravenes animal welfare principles risks perpetuating inhumane approaches and bad science.

Large carnivore hunting and the social license to hunt.

The social license to operate framework considers how society grants or withholds informal permission for resource extractors to exploit publicly owned resources. We developed a modified model, which we refer to as the social license to hunt (SLH). In it we similarly consider hunters as operators, given that wildlife are legally considered public resources in North America and Europe. We applied the SLH model to examine the controversial hunting of large carnivores, which are frequently killed for trophies. Killing for trophies is widespread, but undertaken by a minority of hunters, and can pose threats to the SLH for trophy-seeking carnivore hunters and potentially beyond. Societal opposition to large carnivore hunting relates not only to conservation concerns but also to misalignment between killing for trophies and dominant public values and attitudes concerning the treatment of animals. We summarized cases related to the killing of grizzly bears (Ursus arctos), wolves (Canis lupus), and other large carnivores in Canada, the United States, and Europe to illustrate how opposition to large carnivore hunting, now expressed primarily on social media, can exert rapid and significant pressure on policy makers and politicians. Evidence of the potential for transformative change to wildlife management and conservation includes proposed and realized changes to legislation, business practice, and wildlife policy, including the banning of some large carnivore hunts. Given that policy is ultimately shaped by societal values and attitudes, research gaps include developing increased insight into public support of various hunting policies beyond that derived from monitoring of social media and public polling. Informed by increased evidence, the SLH model can provide a conceptual foundation for predicting the likelihood of transient versus enduring changes to wildlife conservation policy and practice for a wide variety of taxa and contexts.

Cacería de Grandes Carnívoros y la Licencia Social para Cazar Resumen El marco de trabajo de la licencia social para operar considera cómo la sociedad otorga o restringe permisos informales para que los extractores de recursos puedan explotar los recursos públicos. Desarrollamos un modelo modificado, al cual nos referimos como la licencia social para cazar (LSC). En este modelo consideramos a los cazadores como símiles de los operadores puesto que en América del Norte y en Europa a la fauna se le considera legalmente como recurso público. Aplicamos el modelo de la LSC en un análisis de la cacería controversial de grandes carnívoros, a los cuales con frecuencia se les caza para convertirlos en trofeos. La cacería para trofeos es común pero sólo la realiza una minoría de los cazadores y puede presentar una amenaza para la LSC para los cazadores que cazan carnívoros para trofeos e incluso para otros tipos de cazadores. La oposición social a la cacería de grandes carnívoros se relaciona no sólo con el interés de conservación sino también con la discordancia entre la caza para trofeos y las actitudes y valores públicos dominantes con respecto al trato hacia los animales. Resumimos algunos casos relacionados con la muerte de osos pardos (Ursus arctos), lobos (Canis lupus) y otros grandes carnívoros en Canadá, los Estados Unidos y Europa para mostrar cómo la oposición a la cacería de grandes carnívoros, hoy en día expresada principalmente en las redes sociales, puede ejercer una presión rápida y significativa sobre los políticos y los formuladores de políticas. La evidencia de un potencial de cambio transformador en el manejo y conservación de fauna incluye los cambios propuestos y realizados a la legislación, la práctica comercial y las políticas para la fauna, incluyendo la prohibición de la caza de algunos grandes carnívoros. Ya que las políticas están finalmente moldeadas por las actitudes y los valores sociales, las lagunas en la investigación incluyen el desarrollo de un conocimiento mejorado del respaldo público para varias políticas de cacería más allá del conocimiento derivado del monitoreo de las redes sociales y las encuestas públicas. Si se informa con mucha más evidencia, el modelo de la LSC puede proporcionar una base conceptual para predecir la probabilidad de los cambios transitorios versus los duraderos en las políticas y las prácticas de conservación de fauna para una gama amplia de taxones y contextos.

Natural re-colonization and admixture of wolves (Canis lupus) in the US Pacific Northwest: challenges for the protection and management of rare and endangered taxa.

Admixture resulting from natural dispersal processes can potentially generate novel phenotypic variation that may facilitate persistence in changing environments or result in the loss of population-specific adaptations. Yet, under the US Endangered Species Act, policy is limited for management of individuals whose ancestry includes a protected taxon; therefore, they are generally not protected under the Act. This issue is exemplified by the recently re-established grey wolves of the Pacific Northwest states of Washington and Oregon, USA. This population was likely founded by two phenotypically and genetically distinct wolf ecotypes: Northern Rocky Mountain (NRM) forest and coastal rainforest. The latter is considered potentially threatened in southeast Alaska and thus the source of migrants may affect plans for their protection. To assess the genetic source of the re-established population, we sequenced a ~ 300 bp portion of the mitochondrial control region and ~ 5 Mbp of the nuclear genome. Genetic analysis revealed that the Washington wolves share ancestry with both wolf ecotypes, whereas the Oregon population shares ancestry with NRM forest wolves only. Using ecological niche modelling, we found that the Pacific Northwest states contain environments suitable for each ecotype, with wolf packs established in both environmental types. Continued migration from coastal rainforest and NRM forest source populations may increase the genetic diversity of the Pacific Northwest population. However, this admixed population challenges traditional management regimes given that admixture occurs between an adaptively distinct ecotype and a more abundant reintroduced interior form. Our results emphasize the need for a more precise US policy to address the general problem of admixture in the management of endangered species, subspecies, and distinct population segments.

Salmonid species diversity predicts salmon consumption by terrestrial wildlife.

Resource waves-spatial variation in resource phenology that extends feeding opportunities for mobile consumers-can affect the behaviour and productivity of recipient populations. Interspecific diversity among Pacific salmon species (Oncorhynchus spp.) creates staggered spawning events across space and time, thereby prolonging availability to terrestrial wildlife. We sought to understand how such variation might influence consumption by terrestrial predators compared with resource abundance and intra- and interspecific competition. Using stable isotope analysis, we investigated how the proportion of salmon in the annual diet of male black bears (Ursus americanus; n = 405) varies with species diversity and density of spawning salmon biomass, while also accounting for competition with sympatric black and grizzly bears (U. arctos horribilis), in coastal British Columbia, Canada. We found that the proportion of salmon in the annual diet of black bears was ≈40% higher in the absence of grizzly bears, but detected little effect of relative black bear density and salmon biomass density. Rather, salmon diversity had the largest positive effect on consumption. On average, increasing diversity from one salmon species to ~four (with equal biomass contributions) approximately triples the proportion of salmon in diet. Given the importance of salmon to bear life histories, this work provides early empirical support for how resource waves may increase the productivity of consumers at population and landscape scales. Accordingly, terrestrial wildlife management might consider maintaining not only salmon abundance but also diversity.

Population genetic structure of gray wolves (Canis lupus) in a marine archipelago suggests island-mainland differentiation consistent with dietary niche.

BACKGROUND: Emerging evidence suggests that ecological heterogeneity across space can influence the genetic structure of populations, including that of long-distance dispersers such as large carnivores. On the central coast of British Columbia, Canada, wolf (Canis lupus L., 1758) dietary niche and parasite prevalence data indicate strong ecological divergence between marine-oriented wolves inhabiting islands and individuals on the coastal mainland that interact primarily with terrestrial prey. Local holders of traditional ecological knowledge, who distinguish between mainland and island wolf forms, also informed our hypothesis that genetic differentiation might occur between wolves from these adjacent environments. RESULTS: We used microsatellite genetic markers to examine data obtained from wolf faecal samples. Our results from 116 individuals suggest the presence of a genetic cline between mainland and island wolves. This pattern occurs despite field observations that individuals easily traverse the 30 km wide study area and swim up to 13 km among landmasses in the region. CONCLUSIONS: Natal habitat-biased dispersal (i.e., the preference for dispersal into familiar ecological environments) might contribute to genetic differentiation. Accordingly, this working hypothesis presents an exciting avenue for future research where marine resources or other components of ecological heterogeneity are present.

Humanity's diverse predatory niche and its ecological consequences.

Although humans have long been predators with enduring nutritive and cultural relationships with their prey, seldom have conservation ecologists considered the divergent predatory behavior of contemporary, industrialized humans. Recognizing that the number, strength and diversity of predator-prey relationships can profoundly influence biodiversity, here we analyze humanity's modern day predatory interactions with vertebrates and estimate their ecological consequences. Analysing IUCN 'use and trade' data for ~47,000 species, we show that fishers, hunters and other animal collectors prey on more than a third (~15,000 species) of Earth's vertebrates. Assessed over equivalent ranges, humans exploit up to 300 times more species than comparable non-human predators. Exploitation for the pet trade, medicine, and other uses now affects almost as many species as those targeted for food consumption, and almost 40% of exploited species are threatened by human use. Trait space analyses show that birds and mammals threatened by exploitation occupy a disproportionally large and unique region of ecological trait space, now at risk of loss. These patterns suggest far more species are subject to human-imposed ecological (e.g., landscapes of fear) and evolutionary (e.g., harvest selection) processes than previously considered. Moreover, continued overexploitation will likely bear profound consequences for biodiversity and ecosystem function.

Influence of landscape and social interactions on transmission of disease in a social cervid.

The mechanisms of pathogen transmission are often social behaviours. These occur at local scales and are affected by landscape-scale population structure. Host populations frequently exist in patchy and isolated environments that create a continuum of genetic and social familiarity. Such variability has an important multispatial effect on pathogen spread. We assessed elk dispersal (i.e. likelihood of interdeme pathogen transmission) through spatially explicit genetic analyses. At a landscape scale, the elk population was composed of one cluster within a southeast-to-northwest cline spanning three spatially discrete subpopulations of elk across two protected areas in Manitoba (Canada). Genetic data are consistent with spatial variability in apparent prevalence of bovine tuberculosis (TB) in elk. Given the existing population structure, between-subpopulation spread of disease because of elk dispersal is unlikely. Furthermore, to better understand the risk of spread and distribution of the TB, we used a combination of close-contact logging biotelemetry and genetic data, which highlights how social intercourse may affect pathogen transmission. Our results indicate that close-contact interaction rate and duration did not covary with genetic relatedness. Thus, direct elk-to-elk transmission of disease is unlikely to be constrained to related individuals. That social intercourse in elk is not limited to familial groups provides some evidence pathogen transmission may be density-dependent. We show that the combination of landscape-scale genetics, relatedness and local-scale social behaviours is a promising approach to understand and predict landscape-level pathogen transmission within our system and within all social ungulate systems affected by transmissible diseases.

Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago.

Parasites are increasingly recognized for their profound influences on individual, population and ecosystem health. We provide the first report of gastrointestinal parasites in gray wolves from the central and north coasts of British Columbia, Canada. Across 60 000 km(2), wolf feces were collected from 34 packs in 2005-2008. At a smaller spatial scale (3300 km(2)), 8 packs were sampled in spring and autumn. Parasite eggs, larvae, and cysts were identified using standard flotation techniques and morphology. A subset of samples was analysed by PCR and sequencing to identify tapeworm eggs (n=9) and Giardia cysts (n=14). We detected ≥14 parasite taxa in 1558 fecal samples. Sarcocystis sporocysts occurred most frequently in feces (43·7%), followed by taeniid eggs (23·9%), Diphyllobothrium eggs (9·1%), Giardia cysts (6·8%), Toxocara canis eggs (2·1%), and Cryptosporidium oocysts (1·7%). Other parasites occurred in ≤1% of feces. Genetic analyses revealed Echinococcus canadensis strains G8 and G10, Taenia ovis krabbei, Diphyllobothrium nehonkaiense, and Giardia duodenalis assemblages A and B. Parasite prevalence differed between seasons and island/mainland sites. Patterns in parasite prevalence reflect seasonal and spatial resource use by wolves and wolf-salmon associations. These data provide a unique, extensive and solid baseline for monitoring parasite community structure in relation to environmental change.

Human predators outpace other agents of trait change in the wild.

The observable traits of wild populations are continually shaped and reshaped by the environment and numerous agents of natural selection, including predators. In stark contrast with most predators, humans now typically exploit high proportions of prey populations and target large, reproductive-aged adults. Consequently, organisms subject to consistent and strong 'harvest selection' by fishers, hunters, and plant harvesters may be expected to show particularly rapid and dramatic changes in phenotype. However, a comparison of the rate at which phenotypic changes in exploited taxa occurs relative to other systems has never been undertaken. Here, we show that average phenotypic changes in 40 human-harvested systems are much more rapid than changes reported in studies examining not only natural (n = 20 systems) but also other human-driven (n = 25 systems) perturbations in the wild, outpacing them by >300% and 50%, respectively. Accordingly, harvested organisms show some of the most abrupt trait changes ever observed in wild populations, providing a new appreciation for how fast phenotypes are capable of changing. These changes, which include average declines of almost 20% in size-related traits and shifts in life history traits of nearly 25%, are most rapid in commercially exploited systems and, thus, have profound conservation and economic implications. Specifically, the widespread potential for transitively rapid and large effects on size- or life history-mediated ecological dynamics might imperil populations, industries, and ecosystems.

Landscape resistance to dispersal: simulating long-term effects of human disturbance on a small and isolated wolf population in southwestern Manitoba, Canada.

Landscape fragmentation affects wildlife population viability, in part, through the effects it has on individual dispersal. In addition, some forms of human disturbance impinge on dispersal without physically fragmenting habitats. Here, we use the term "landscape resistance" to capture constraints to dispersal that cannot be linked directly to fragmentation. The extent to which landscape resistance can influence population persistence is not well understood. Agricultural development over the past 60 years has resulted in considerable habitat fragmentation in the Riding Mountain National Park (RMNP) region in southwestern Manitoba, Canada. We examined how park boundaries, roads outside park boundaries and negative human attitudes have altered dispersal success and population persistence. We examined whether stochastic disturbance, representing infectious disease epidemics, further reduced long-term population persistence for various scenarios. Finally, we assessed whether the simultaneous occurrence of the three features had additive effects. We simulated dispersal using HexSim, a spatially explicit individual-based population model, parameterised with data on wolves (Canis lupus) in the RMNP region. Simulations that separately accounted for negative human attitudes and roads outside the park boundaries exhibited lower mean population size than those that ignored these details. Increasing deflection from park boundaries did not appear to have significant impacts. Our results did not indicate the presence of additive effects, and scenarios incorporating all three features had similar results as that of roads. Stochastic disturbance further reduced mean population size. Our results do illustrate how less-visible human disturbances (i.e. those that do not clearly alter landscape characteristics) can significantly limit dispersal and population persistence.

The relevance of genetic structure in ecotype designation and conservation management.

The concept of ecotypes is complex, partly because of its interdisciplinary nature, but the idea is intrinsically valuable for evolutionary biology and applied conservation. The complex nature of ecotypes has spurred some confusion and inconsistencies in the literature, thereby limiting broader theoretical development and practical application. We provide suggestions for how incorporating genetic analyses can ease confusion and help define ecotypes. We approach this by systematically reviewing 112 publications across taxa that simultaneously mention the terms ecotype, conservation and management, to examine the current use of the term in the context of conservation and management. We found that most ecotype studies involve fish, mammals and plants with a focus on habitat use, which at 60% was the most common criterion used for categorization of ecotypes. Only 53% of the studies incorporated genetic analyses, and major discrepancies in available genomic resources among taxa could have contributed to confusion about the role of genetic structure in delineating ecotypes. Our results show that the rapid advances in genetic methods, also for nonmodel organisms, can help clarify the spatiotemporal distribution of adaptive and neutral genetic variation and their relevance to ecotype designations. Genetic analyses can offer empirical support for the ecotype concept and provide a timely measure of evolutionary potential, especially in changing environmental conditions. Genetic variation that is often difficult to detect, including polygenic traits influenced by small contributions from several genes, can be vital for adaptation to rapidly changing environments. Emerging ecotypes may signal speciation in progress, and findings from genome-enabled organisms can help clarify important selective factors driving ecotype development and persistence, and thereby improve preservation of interspecific genetic diversity. Incorporation of genetic analyses in ecotype studies will help connect evolutionary biology and applied conservation, including that of problematic groups such as natural hybrid organisms and urban or anthropogenic ecotypes.

Cross-continental comparison of parasite communities in a wide-ranging carnivore suggests associations with prey diversity and host density.

Parasites are integral to ecosystem functioning yet often overlooked. Improved understanding of host-parasite associations is important, particularly for wide-ranging species for which host range shifts and climate change could alter host-parasite interactions and their effects on ecosystem function.Among the most widely distributed mammals with diverse diets, gray wolves (Canis lupus) host parasites that are transmitted among canids and via prey species. Wolf-parasite associations may therefore influence the population dynamics and ecological functions of both wolves and their prey. Our goal was to identify large-scale processes that shape host-parasite interactions across populations, with the wolf as a model organism.By compiling data from various studies, we examined the fecal prevalence of gastrointestinal parasites in six wolf populations from two continents in relation to wolf density, diet diversity, and other ecological conditions.As expected, we found that the fecal prevalence of parasites transmitted directly to wolves via contact with other canids or their excreta was positively associated with wolf density. Contrary to our expectations, the fecal prevalence of parasites transmitted via prey was negatively associated with prey diversity. We also found that parasite communities reflected landscape characteristics and specific prey items available to wolves.Several parasite taxa identified in this study, including hookworms and coccidian protozoans, can cause morbidity and mortality in canids, especially in pups, or in combination with other stressors. The density-prevalence relationship for parasites with simple life cycles may reflect a regulatory role of gastrointestinal parasites on wolf populations. Our result that fecal prevalence of parasites was lower in wolves with more diverse diets could provide insight into the mechanisms by which biodiversity may regulate disease. A diverse suite of predator-prey interactions could regulate the effects of parasitism on prey populations and mitigate the transmission of infectious agents, including zoonoses, spread via trophic interactions.

Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate.

1. Inquiries into niche variation within populations typically focus on proximate ecological causes such as competition. Here we examine how landscape heterogeneity and allochthonous (marine) subsidy might ultimately generate intrapopulation niche diversity. 2. Using stable isotope analysis, we detected extensive terrestrial-marine isotopic niche variation among subpopulations, social groups, and individual grey wolves (Canis lupus) that occupy a spatially heterogeneous landscape in coastal British Columbia comprising a mainland area and adjacent archipelago. 3. The inner island subpopulation exhibited the widest isotopic niche in the population, consuming extensive terrestrial and marine resources. Mainland and outer island subpopulations occupied comparatively narrow and primarily terrestrial, and primarily marine, niches respectively. Within these biogeographical subpopulations, social groups also diverged in niche. 4. To support examination at the individual level, we used an isotopic approach to test Van Valen's (1965) niche variation hypothesis. Consistent with the hypothesis, we observed that among-individual variation increased with subpopulation niche width. 5. Patterns at all levels related to how a spatially heterogeneous coastal landscape structured the competitive environment, which in turn mediated the availability and use of terrestrial and marine resources. Broadly, our results suggest that spatial heterogeneity and allochthonous subsidy--both widespread but commonly subject to contemporary anthropogenic change--might provide novel opportunities for examination and conservation of ecological variation within populations.

Functional response of wolves to human development across boreal North America.

AIM: The influence of humans on large carnivores, including wolves, is a worldwide conservation concern. In addition, human-caused changes in carnivore density and distribution might have impacts on prey and, indirectly, on vegetation. We therefore tested wolf responses to infrastructure related to natural resource development (i.e., human footprint). LOCATION: Our study provides one of the most extensive assessments of how predators like wolves select habitat in response to various degrees of footprint across boreal ecosystems encompassing over a million square kilometers of Canada. METHODS: We deployed GPS-collars on 172 wolves, monitored movements and used a generalized functional response (GFR) model of resource selection. A functional response in habitat selection occurs when selection varies as a function of the availability of that habitat. GFRs can clarify how human-induced habitat changes are influencing wildlife across large, diverse landscapes. RESULTS: Wolves displayed a functional response to footprint. Wolves were more likely to select forest harvest cutblocks in regions with higher cutblock density (i.e., a positive functional response to high-quality habitats for ungulate prey) and to select for higher road density in regions where road density was high (i.e., a positive functional response to human-created travel routes). Wolves were more likely to use cutblocks in habitats with low road densities, and more likely to use roads in habitats with low cutblock densities, except in winter when wolves were more likely to use roads regardless of cutblock density. MAIN CONCLUSIONS: These interactions suggest that wolves trade-off among human-impacted habitats, and adaptively switch from using roads to facilitate movement (while also risking encounters with humans), to using cutblocks that may have higher ungulate densities. We recommend that conservation managers consider the contextual and interacting effects of footprints when assessing impacts on carnivores. These effects likely have indirect impacts on ecosystems too, including on prey species.

Spawning salmon disrupt trophic coupling between wolves and ungulate prey in coastal British Columbia.

BACKGROUND: As a cross-boundary resource subsidy, spawning salmon can strongly affect consumer and ecosystem ecology. Here we examine whether this marine resource can influence a terrestrial wolf-deer (Canis lupus-Odocoileus hemionus) predator-prey system in coastal British Columbia, Canada. Data on resource availability and resource use among eight wolf groups for three seasons over four years allow us to evaluate competing hypotheses that describe salmon as either an alternate resource, consumed in areas where deer are scarce, or as a targeted resource, consumed as a positive function of its availability. Faecal (n=2203 wolf scats) and isotopic analyses (n=60 wolf hair samples) provide independent data sets, also allowing us to examine how consistent these common techniques are in estimating foraging behaviour. RESULTS: At the population level during spring and summer, deer remains occurred in roughly 90 and 95% of faeces respectively. When salmon become available in autumn, however, the population showed a pronounced dietary shift in which deer consumption among groups was negatively correlated (r=-0.77, P<0.001) with consumption of salmon, which occurred in 40% of all faeces and up to 70% of faeces for some groups. This dietary shift as detected by faecal analysis was correlated with seasonal shifts in delta13C isotopic signatures (r=0.78; P=0.008), which were calculated by intra-hair comparisons between segments grown during summer and fall. The magnitude of this seasonal isotopic shift, our proxy for salmon use, was related primarily to estimates of salmon availability, not deer availability, among wolf groups. CONCLUSION: Concordance of faecal and isotopic data suggests our intra-hair isotopic methodology provides an accurate proxy for salmon consumption, and might reliably track seasonal dietary shifts in other consumer-resource systems. Use of salmon by wolves as a function of its abundance and the adaptive explanations we provide suggest a long-term and widespread association between wolves and salmon. Seasonally, this system departs from the common wolf-ungulate model. Broad ecological implications include the potential transmission of marine-based disease into terrestrial systems, the effects of marine subsidy on wolf-deer population dynamics, and the distribution of salmon nutrients by wolves into coastal ecosystems.

Working constructively toward an improved North American approach to wildlife management.

Mawdsley et al. (2018) respond disapprovingly to our 2018 review of 667 wildlife management systems across Canada and the United States, which found that many of these systems lacked the scientific hallmarks of clear objectives, evidence, transparency, and independent review. Although we strongly agree with several of Mawdsley et al.'s points about the role of science in management, their response suggests confusion about three elements of our approach that we clarify herein: (i) the selection of hallmarks, (ii) the role of science in wildlife management, and (iii) our engagement with wildlife agencies. We contend that both critics and defenders of the current approach to wildlife management in Canada and the United States similarly desire rigorous management that achieves social and ecological benefits. Our original study-which used a clear approach to define hallmarks of science-based management, employed a reasonable set of indicator criteria to test for them, and was based on data available to the general public on whose behalf management is conducted-found evidence that the current approach falls short. However, it also provided a framework for addressing shortcomings moving forward. We suggest that advancing discussion on the operational role of science in management, including clarifying what "science-based management" actually means, could curtail practitioners and critics of the status quo talking over each other's heads and encourage all parties to work constructively to improve the governance of wildlife at a continental scale.