Genomics-informed conservation units reveal spatial variation in climate vulnerability in a migratory bird.

Identifying genetic conservation units (CUs) in threatened species is critical for the preservation of adaptive capacity and evolutionary potential in the face of climate change. However, delineating CUs in highly mobile species remains a challenge due to high rates of gene flow and genetic signatures of isolation by distance. Even when CUs are delineated in highly mobile species, the CUs often lack key biological information about what populations have the most conservation need to guide management decisions. Here we implement a framework for CU identification in the Canada Warbler (Cardellina canadensis), a migratory bird species of conservation concern, and then integrate demographic modelling and genomic offset to guide conservation decisions. We find that patterns of whole genome genetic variation in this highly mobile species are primarily driven by putative adaptive variation. Identification of CUs across the breeding range revealed that Canada Warblers fall into two evolutionarily significant units (ESU), and three putative adaptive units (AUs) in the South, East, and Northwest. Quantification of genomic offset, a metric of genetic changes necessary to maintain current gene-environment relationships, revealed significant spatial variation in climate vulnerability, with the Northwestern AU being identified as the most vulnerable to future climate change. Alternatively, quantification of past population trends within each AU revealed the steepest population declines have occurred within the Eastern AU. Overall, we illustrate that genomics-informed CUs provide a strong foundation for identifying current and future regional threats that can be used to inform management strategies for a highly mobile species in a rapidly changing world.

Climate-informed forecasts reveal dramatic local habitat shifts and population uncertainty for northern boreal caribou.

Most research on boreal populations of woodland caribou (Rangifer tarandus caribou) has been conducted in areas of high anthropogenic disturbance. However, a large portion of the species' range overlaps relatively pristine areas primarily affected by natural disturbances, such as wildfire. Climate-driven habitat change is a key concern for the conservation of boreal-dependent species, where management decisions have yet to consider knowledge from multiple ecological domains integrated into a cohesive and spatially explicit forecast of species-specific habitat and demography. We used a novel ecological forecasting framework to provide climate-sensitive projections of habitat and demography for five boreal caribou monitoring areas within the Northwest Territories (NWT), Canada, over 90 years. Importantly, we quantify uncertainty around forecasted mean values. Our results suggest habitat suitability may increase in central and southwest regions of the NWT's Taiga Plains ecozone but decrease in southern and northwestern regions driven by conversion of coniferous to deciduous forests. We do not project that boreal caribou population growth rates will change despite forecasted changes to habitat suitability. Our results emphasize the importance of efforts to protect and restore northern boreal caribou habitat despite climate uncertainty while highlighting expected spatial variations that are important considerations for local people who rely on them. An ability to reproduce previous work, and critical thought when incorporating sources of uncertainty, will be important to refine forecasts, derive management decisions, and improve conservation efficacy for northern species at risk.

PERFICT: A Re-imagined foundation for predictive ecology.

Making predictions from ecological models-and comparing them to data-offers a coherent approach to evaluate model quality, regardless of model complexity or modelling paradigm. To date, our ability to use predictions for developing, validating, updating, integrating and applying models across scientific disciplines while influencing management decisions, policies, and the public has been hampered by disparate perspectives on prediction and inadequately integrated approaches. We present an updated foundation for Predictive Ecology based on seven principles applied to ecological modelling: make frequent Predictions, Evaluate models, make models Reusable, Freely accessible and Interoperable, built within Continuous workflows that are routinely Tested (PERFICT). We outline some benefits of working with these principles: accelerating science; linking with data science; and improving science-policy integration.

Knock-In Mouse Models to Investigate the Functions of Opioid Receptors in vivo.

Due to their low expression levels, complex multi-pass transmembrane structure, and the current lack of highly specific antibodies, the assessment of endogenous G protein-coupled receptors (GPCRs) remains challenging. While most of the research regarding their functions was performed in heterologous systems overexpressing the receptor, recent advances in genetic engineering methods have allowed the generation of several unique mouse models. These animals proved to be useful to investigate numerous aspects underlying the physiological functions of GPCRs, including their endogenous expression, distribution, interactome, and trafficking processes. Given their significant pharmacological importance and central roles in the nervous system, opioid peptide receptors (OPr) are often referred to as prototypical receptors for the study of GPCR regulatory mechanisms. Although only a few GPCR knock-in mouse lines have thus far been generated, OPr are strikingly well represented with over 20 different knock-in models, more than half of which were developed within the last 5 years. In this review, we describe the arsenal of OPr (mu-, delta-, and kappa-opioid), as well as the opioid-related nociceptin/orphanin FQ (NOP) receptor knock-in mouse models that have been generated over the past years. We further highlight the invaluable contribution of such models to our understanding of the in vivo mechanisms underlying the regulation of OPr, which could be conceivably transposed to any other GPCR, as well as the limitations, future perspectives, and possibilities enabled by such tools.

A cost efficient spatially balanced hierarchical sampling design for monitoring boreal birds incorporating access costs and habitat stratification.

Predicting and mitigating impacts of climate change and development within the boreal biome requires a sound understanding of factors influencing the abundance, distribution, and population dynamics of species inhabiting this vast biome. Unfortunately, the limited accessibility of the boreal biome has resulted in sparse and spatially biased sampling, and thus our understanding of boreal bird population dynamics is limited. To implement effective conservation of boreal birds, a cost-effective approach to sampling the boreal biome will be needed. Our objective was to devise a sampling scheme for monitoring boreal birds that would improve our ability to model species-habitat relationships and monitor changes in population size and distribution. A statistically rigorous design to achieve these objectives would have to be spatially balanced and hierarchically structured with respect to ecozones, ecoregions and political jurisdictions. Therefore, we developed a multi-stage hierarchically structured sampling design known as the Boreal Optimal Sampling Strategy (BOSS) that included cost constraints, habitat stratification, and optimization to provide a cost-effective alternative to other common monitoring designs. Our design provided similar habitat and spatial representation to habitat stratification and equal-probability spatially balanced designs, respectively. Not only was our design able to achieve the desired habitat representation and spatial balance necessary to meet our objectives, it was also significantly less expensive (1.3-2.6 times less) than the alternative designs we considered. To further balance trade-offs between cost and representativeness prior to field implementation, we ran multiple iterations of the BOSS design and selected the one which minimized predicted costs while maximizing a multi-criteria evaluation of representativeness. Field implementation of the design in three vastly different regions over three field seasons showed that the approach can be implemented in a wide variety of logistical scenarios and ecological conditions. We provide worked examples and scripts to allow our approach to be implemented or adapted elsewhere. We also provide recommendations for possible future refinements to our approach, but recommend that our design now be implemented to provide unbiased information to assess the status of boreal birds and inform conservation and management actions.

Phylogeography of a migratory songbird across its Canadian breeding range: Implications for conservation units.

The objectives of this study were to describe and evaluate potential drivers of genetic structure in Canadian breeding populations of the Ovenbird, Seiurus aurocapilla. We performed genetic analyses on feather samples of individuals from six study sites using nuclear microsatellites. We also assessed species identity and population genetic structure of quill mites (Acariformes, Syringophilidae). For male Ovenbirds breeding in three study sites, we collected light-level geolocator data to document migratory paths and identify the wintering grounds. We also generated paleohindcast projections from bioclimatic models of Ovenbird distribution to identify potential refugia during the last glacial maximum (LGM, 21,000 years before present) as a factor explaining population genetic structure. Birds breeding in the Cypress Hills (Alberta/Saskatchewan) may be considered a distinct genetic unit, but there was no evidence for genetic differentiation among any other populations. We found relatively strong migratory connectivity in both western and eastern populations, but some evidence of mixing among populations on the wintering grounds. There was also little genetic variation among syringophilid mites from the different Ovenbird populations. These results are consistent with paleohindcast distribution predictions derived from two different global climate models indicating a continuous single LGM refugium, with the possibility of two refugia. Our results suggest that Ovenbird populations breeding in boreal and hemiboreal regions are panmictic, whereas the population breeding in Cypress Hills should be considered a distinct management unit.

Correction: Within-Site Variation in Feather Stable Hydrogen Isotope (δ2Hf) Values of Boreal Songbirds: Implications for Assignment to Molt Origin.

[This corrects the article DOI: 10.1371/journal.pone.0163957.].

Within-Site Variation in Feather Stable Hydrogen Isotope (δ2Hf) Values of Boreal Songbirds: Implications for Assignment to Molt Origin.

Understanding bird migration and dispersal is important to inform full life-cycle conservation planning. Stable hydrogen isotope ratios from feathers (δ2Hf) can be linked to amount-weighted long-term, growing season precipitation δ2H (δ2Hp) surfaces to create δ2Hf isoscapes for assignment to molt origin. However, transfer functions linking δ2Hp with δ2Hf are influenced by physiological and environmental processes. A better understanding of the causes and consequences of variation in δ2Hf values among individuals and species will improve the predictive ability of geographic assignment tests. We tested for effects of species, land cover, forage substrate, nest substrate, diet composition, body mass, sex, and phylogenetic relatedness on δ2Hf from individuals at least two years old of 21 songbird species captured during the same breeding season at a site in northeastern Alberta, Canada. For four species, we also tested for a year × species interaction effect on δ2Hf. A model including species as single predictor received the most support (AIC weight = 0.74) in explaining variation in δ2Hf. A species-specific variance parameter was part of all best-ranked models, suggesting variation in δ2Hf was not consistent among species. The second best-ranked model included a forage substrate × diet interaction term (AIC weight = 0.16). There was a significant year × species interaction effect on δ2Hf suggesting that interspecific differences in δ2Hf can differ among years. Our results suggest that within- and among-year interspecific variation in δ2Hf is the most important source of variance typically not being explicitly quantified in geographic assignment tests using non-specific transfer functions to convert δ2Hp into δ2Hf. However, this source of variation is consistent with the range of variation from the transfer functions most commonly being propagated in assignment tests of geographic origins for passerines breeding in North America.

ENSO, nest predation risk, food abundance, and male status fail to explain annual variations in the apparent survival rate of a migratory songbird.

Adult mortality can be a major driver of population decline in species whose productivity is relatively low. Yet, little is known about the factors influencing adult survival rates in migratory bird species, nor do we know much about the longer-term effects of habitat disturbance on the fitness of individuals. The Ovenbird (Seiurus aurocapilla) is one of the vertebrate species most sensitive to forest management, yet it is still common and widespread. We monitored the fate of 330 colour-banded Ovenbird males in four pairs of 25-ha plots during 9 successive breeding seasons. One plot of each pair was treated through selection harvesting (30-40% basal area removed) during the first winter. We tested the following hypotheses: (1) higher physiological costs in harvested plots as a result of lower food abundance will reduce apparent survival rate (ASR) relative to controls; (2) lower ASR following years with low nest survival and higher probability of renesting; (3) fluctuations in ASR reflecting El Niño Southern Oscillation (ENSO); and (4) higher ASR in returning males than in recruits (unbanded immigrants) owing to greater site familiarity in the former. We tested the relative importance of these hypotheses, or combinations thereof, by generating 23 models explaining variation in ASR. The year-dependent model received the most support, showing a 41% decrease in ASR from 2007 to 2014. The important year-to-year variation we observed in ASR (Σw(i) = 0.99) was not explained by variation in nest predation risk nor by ENSO. There was also little evidence for an effect of selection harvesting on ASR of Ovenbird males, despite a slight reduction in lifespan relative to males from control plots (2.7 vs 2.9 years). An avenue worth exploring to explain this intriguing pattern would be to determine whether conditions at migratory stopover sites or in the wintering area of our focal population have gradually worsened over the past decade.

Tracking natal dispersal in a coastal population of a migratory songbird using feather stable isotope (δ2H, δ34S) tracers.

Adult birds tend to show high fidelity to their breeding territory or disperse over relatively short distances. Gene flow among avian populations is thus expected to occur primarily through natal dispersal. Although natal dispersal is a critical demographic process reflecting the area over which population dynamics take place, low recapture rates of birds breeding for the first time have limited our ability to reliably estimate dispersal rates and distances. Stable isotope approaches can elucidate origins of unmarked birds and so we generated year- and age-specific δ2H and δ34S feather isoscapes (ca. 180 000 km2) of coastal-breeding Ovenbirds (Seiurus aurocapilla) and used bivariate probability density functions to assign the likely natal areas of 35 males recruited as first-year breeders into a population located in northwestern New Brunswick, Canada. Most individuals (80-94% depending on the magnitude of an age correction factor used; i.e. 28-33 out of 35) were classified as residents (i.e. fledged within our study area) and estimated minimum dispersal distances of immigrants were between 40 and 240 km. Even when considering maximum dispersal distances, the likely origin of most first-year breeders was<200 km from our study area. Our method identified recruitment into our population from large geographic areas with relatively few samples whereas previous mark-recapture based methods have required orders of magnitude more individuals to describe dispersal at such geographic scales. Natal dispersal movements revealed here suggest the spatial scale over which many population processes are taking place and we suggest that conservation plans aiming to maintain populations of Ovenbirds and ecologically-similar species should consider management units within 100 or at most 200 km of target breeding populations.

Age-specific response of a migratory bird to an experimental alteration of its habitat.

1. Recruitment, i.e. the influx of new breeding individuals into a population, is an important demographic parameter, especially in species with a short life span. Few studies have measured this parameter in solitary-breeding animal populations even though it may yield critical information on habitat suitability and functional connectivity. 2. Using a before-after, control-impact pairs (BACIP) experimental design, we measured: (i) the return rate and apparent survival rate of individually marked territorial males of a neotropical migrant bird species, the Ovenbird Seiurus aurocapilla Linnaeus and (ii) the age-specific recruitment rate. Study plots (n = 10) were paired: one was treated through single-tree selection harvesting (30-40% basal area removal) and the other acted as a control. We hypothesized that experienced males would out-compete inexperienced ones and tend to avoid settling in lower-quality, treated stands. 3. In the first year post-harvest, the mean density of territorial males was significantly lower in treated plots (-41%) than in controls and the difference remained relatively stable thereafter. This lower density mainly reflected a lower recruitment rate compared to controls (17.9 vs. 49.0% of males present), itself driven by a lower recruitment rate of experienced males (2.8 vs. 22.8%). Return rate was similar between controls and treated plots in the first year post-harvest (59 vs. 55%, respectively) but it decreased in treated plots during the second (-15.8% relative to controls) and third (-12.7%) year post-harvest. The trend was even stronger when considering only experienced males. The treatment was followed by a major expansion in mean territory size in treated plots (+49% relative to controls, 3rd year post-treatment). 4. Neither apparent survival rate nor recruitment rate varied as predicted. There was a strong year effect but no treatment effect on apparent survival rate, whereas male recruitment patterns were both year- and age-specific. Three years post-harvest, recruitment rate was sufficient to fill most territory vacancies in treated plots, due mainly to first-time breeders. 5. To our knowledge, this is the first study documenting the effects of experimental habitat alteration on recruitment rate in a songbird species using a BACI design. The response of this male subpopulation highlights the influence of recruitment on the density of open populations of solitary-nesting birds and age-specific patterns in the response of individuals to habitat alterations.