Landscape-scale conservation mitigates the biodiversity loss of grassland birds.

The decline of biodiversity from anthropogenic landscape modification is among the most pressing conservation problems worldwide. In North America, long-term population declines have elevated the recovery of the grassland avifauna to among the highest conservationpriorities. Because the vast majority of grasslands of the Great Plains are privately owned, the recovery of these ecosystems and bird populations within them depend on landscape-scale conservation strategies that integrate social, economic, and biodiversity objectives. The Conservation Reserve Program (CRP) is a voluntary program for private agricultural producers administered by the United States Department of Agriculture that provides financial incentives to take cropland out of production and restore perennial grassland. We investigated spatial patterns of grassland availability and restoration to inform landscape-scale conservation for a comprehensive community of grassland birds in the Great Plains. The research objectives were to (1) determine how apparent habitat loss has affected spatial patterns of grassland bird biodiversity, (2) evaluate the effectiveness of CRP for offsetting the biodiversity declines of grassland birds, and (3) develop spatially explicit predictions to estimate the biodiversity benefit of adding CRP to landscapes impacted by habitat loss. We used the Integrated Monitoring in Bird Conservation Regions program to evaluate hypotheses for the effects of habitat loss and restoration on both the occupancy and species richness of grassland specialists within a continuum-modeling framework. We found the odds of community occupancy declined by 37% for every 1 SD decrease in grassland availability [loge (km2 )] and increased by 20% for every 1 SD increase in CRP land cover [loge (km2 )]. There was 17% turnover in species composition between intact grasslands and CRP landscapes, suggesting that grasslands restored by CRP retained considerable, but incomplete, representation of biodiversity in agricultural landscapes. Spatially explicit predictions indicated that absolute conservation outcomes were greatest at high latitudes in regions with high biodiversity, whereas the relative outcomes were greater at low latitudes in highly modified landscapes. By evaluating community-wide responses to landscape modification and CRP restoration at bioregional scales, our study fills key information gaps for developing collaborative strategies, and for balancing conservation of avian biodiversity and social well-being in the agricultural production landscapes of the Great Plains.

Variable tropical moisture and food availability underlie mixed winter space-use strategies in a migratory songbird.

Identifying environmental correlates driving space-use strategies can be critical for predicting population dynamics; however, such information can be difficult to attain for small mobile species such as migratory songbirds. We combined radio-telemetry and high-resolution GPS tracking to examine space-use strategies under different moisture gradients for wood thrush (Hylocichla mustelina). We explored the role moisture plays in driving food abundance and, in turn, space-use strategies at a wintering site in Belize across 3 years. Individuals occupying drier habitats experienced lower food abundance and poorer body condition. Using data from our radio-tracked study population and GPS tracking from across five breeding populations, we detected low rates of overwinter site persistence across the wood thrush wintering range. Contrary to expectations, individuals in wetter habitats were more likely to engage in permanent mid-winter relocations, up to 148 km. We suggest facultative movements are instead a condition-dependent strategy that enables wintering wood thrush to locate alternative habitat as food availability declines throughout the dry season. Increased aridity is predicted across the wintering range of wood thrush, and future research should delve deeper into understanding how moisture impacts within and between season space-use dynamics and its ultimate impact on the population dynamics of this declining species.

Gene expression in the social behavior network of the wire-tailed manakin (Pipra filicauda) brain.

The vertebrate basal forebrain and midbrain contain a set of interconnected nuclei that control social behavior. Conserved anatomical structures and functions of these nuclei have now been documented among fish, amphibians, reptiles, birds and mammals, and these brain regions have come to be known as the vertebrate social behavior network (SBN). While it is known that nuclei (nodes) of the SBN are rich in steroid and neuropeptide activity linked to behavior, simultaneous variation in the expression of neuroendocrine genes among several SBN nuclei has not yet been described in detail. In this study, we use RNA-seq to profile gene expression across seven brain regions representing five nodes of the vertebrate SBN in a passerine bird, the wire-tailed manakin Pipra filicauda. Using weighted gene co-expression network analysis, we reconstructed sets of coregulated genes, showing striking patterns of variation in neuroendocrine gene expression across the SBN. We describe regional variation in gene networks comprising a broad set of hormone receptors, neuropeptides, steroidogenic enzymes, catecholamines and other neuroendocrine signaling molecules. Our findings show heterogeneous patterns of brain gene expression across nodes of the avian SBN and provide a foundation for future analyses of how the regulation of gene networks may mediate social behavior. These results highlight the importance of region-specific sampling in studies of the mechanisms of behavior.

Spatial and temporal drivers of avian population dynamics across the annual cycle.

Untangling the spatial and temporal processes that influence population dynamics of migratory species is challenging, because changes in abundance are shaped by variation in vital rates across heterogeneous habitats and throughout the annual cycle. We developed a full-annual-cycle, integrated, population model and used demographic data collected between 2011 and 2014 in southern Indiana and Belize to estimate stage-specific vital rates of a declining migratory songbird, the Wood Thrush (Hylocichla mustelina). Our primary objective was to understand how spatial and temporal variation in demography contributes to local and regional population growth. Our full-annual-cycle model allowed us to estimate (1) age-specific, seasonal survival probabilities, including latent survival during both spring and autumn migration, and (2) how the relative contribution of vital rates to population growth differed among habitats. Wood Thrushes in our study populations experienced the lowest apparent survival rates during migration and apparent survival was lower during spring migration than during fall migration. Both mortality and high dispersal likely contributed to low apparent survival during spring migration. Population growth in high-quality habitat was most sensitive to variation in fecundity and apparent survival of juveniles during spring migration, whereas population growth in low-quality sites was most sensitive to adult apparent breeding-season survival. These results elucidate how full-annual-cycle vital rates, particularly apparent survival during migration, interact with spatial variation in habitat quality to influence population dynamics in migratory species.

Quantifying drivers of population dynamics for a migratory bird throughout the annual cycle.

Worldwide, migratory species are undergoing rapid declines but understanding the factors driving these declines is hindered by missing information about migratory connectivity and the lack of data to quantify environmental processes across the annual cycle. Here, we combined range-wide information about migratory connectivity with global remote-sensing data to quantify the relative importance of breeding and non-breeding environmental processes to persistent long-term population declines of a migratory songbird, the wood thrush (Hylocichla mustelina). Consistent with theoretical predictions about population limitation of migratory birds, our results suggest that habitat loss and climate have contributed to the observed declines in wood thrush breeding abundance, yet the relative importance of breeding versus non-breeding factors is population-specific. For example, high-abundance core breeding populations appear to be more limited by habitat loss, whereas low-abundance, peripheral populations appear to be limited by climate-driven seasonal interactions. Further, our analysis indicates that the relative impact of breeding habitat loss is at least three to six times greater than the impact of equivalent non-breeding habitat loss and therefore the steepest regional declines have likely been driven by the loss of breeding habitat. These results underscore the need for population-specific conservation strategies implemented throughout the annual cycle to reverse long-term declines.

Climate, demography and lek stability in an Amazonian bird.

Lekking is a rare, but iconic mating system where polygynous males aggregate and perform group displays to attract females. Existing theory postulates that demographic and environmental stability are required for lekking to be an evolutionarily viable reproductive strategy. However, we lack empirical tests for the hypotheses that lek stability is facilitated by age-specific variation in demographic rates, and by predictable, abundant resources. To address this knowledge gap, we use multistate models to examine how two demographic elements of lek stability-male survival and recruitment-vary with age, social status and phase of the El Niño Southern Oscillation (ENSO) in a Neotropical frugivorous bird, the wire-tailed manakin (Pipra filicauda). Our results show that demographic and environmental conditions were related to lek stability in the Ecuadorean Amazon. Apparent annual survival probability of territorial males was higher than that of non-territorial floaters, and recruitment probability increased as males progressed in an age-graded queue. Moreover, annual survival of territorial males and body condition of both floaters and territory holders were higher following years with El Niño conditions, associated with reduced rainfall and probably higher fruit production in the northern Neotropics, and lower after years with wet, La Niña conditions that predominated our study. Recruitment probabilities varied annually, independent of ENSO phase, and increased over our study period, but the annual mean number of territorial males per lek declined. Our results provide empirical support for hypothesized demographic and environmental drivers of lek dynamics. This study also suggests that climate-mediated changes in resource availability can affect demography and subsequent lek stability in a relatively buffered, lowland rainforest.

Experimental resource pulses influence social-network dynamics and the potential for information flow in tool-using crows.

Social-network dynamics have profound consequences for biological processes such as information flow, but are notoriously difficult to measure in the wild. We used novel transceiver technology to chart association patterns across 19 days in a wild population of the New Caledonian crow--a tool-using species that may socially learn, and culturally accumulate, tool-related information. To examine the causes and consequences of changing network topology, we manipulated the environmental availability of the crows' preferred tool-extracted prey, and simulated, in silico, the diffusion of information across field-recorded time-ordered networks. Here we show that network structure responds quickly to environmental change and that novel information can potentially spread rapidly within multi-family communities, especially when tool-use opportunities are plentiful. At the same time, we report surprisingly limited social contact between neighbouring crow communities. Such scale dependence in information-flow dynamics is likely to influence the evolution and maintenance of material cultures.

Assessing migratory connectivity for a long-distance migratory bird using multiple intrinsic markers.

Patterns of migratory connectivity are a vital yet poorly understood component of the ecology and evolution of migratory birds. Our ability to accurately characterize patterns of migratory connectivity is often limited by the spatial resolution of the data, but recent advances in probabilistic assignment approaches have begun pairing stable isotopes with other sources of data (e.g., genetic and mark-recapture) to improve the accuracy and precision of inferences based on a single marker. Here, we combine stable isotopes and geographic variation in morphology (wing length) to probabilistically assign Wood Thrush (Hylocichla mustilena) captured on the wintering grounds to breeding locations. In addition, we use known-origin samples to validate our model and assess potentially important impacts of isotopic and morphological covariates (age, sex, and breeding location). Our results show that despite relatively high levels of mixing across their breeding and nonbreeding ranges, moderate levels of migratory connectivity exist along an east-west gradient. In addition, combining stable isotopes with geographic variation in wing length improved the precision of breeding assignments by 10% and 37% compared to assignments based on isotopes alone or wing length alone, respectively. These results demonstrate that geographical variation in morphological traits can greatly improve estimates of migratory connectivity when combined with other intrinsic markers (e.g., stable isotopes or genetic data). The wealth of morphological data available from museum specimens across the world represents a tremendously valuable, but largely untapped, resource that is widely applicable for quantifying patterns of migratory connectivity.

Decay of interspecific avian flock networks along a disturbance gradient in Amazonia.

Our understanding of how anthropogenic habitat change shapes species interactions is in its infancy. This is in large part because analytical approaches such as network theory have only recently been applied to characterize complex community dynamics. Network models are a powerful tool for quantifying how ecological interactions are affected by habitat modification because they provide metrics that quantify community structure and function. Here, we examine how large-scale habitat alteration has affected ecological interactions among mixed-species flocking birds in Amazonian rainforest. These flocks provide a model system for investigating how habitat heterogeneity influences non-trophic interactions and the subsequent social structure of forest-dependent mixed-species bird flocks. We analyse 21 flock interaction networks throughout a mosaic of primary forest, fragments of varying sizes and secondary forest (SF) at the Biological Dynamics of Forest Fragments Project in central Amazonian Brazil. Habitat type had a strong effect on network structure at the levels of both species and flock. Frequency of associations among species, as summarized by weighted degree, declined with increasing levels of forest fragmentation and SF. At the flock level, clustering coefficients and overall attendance positively correlated with mean vegetation height, indicating a strong effect of habitat structure on flock cohesion and stability. Prior research has shown that trophic interactions are often resilient to large-scale changes in habitat structure because species are ecologically redundant. By contrast, our results suggest that behavioural interactions and the structure of non-trophic networks are highly sensitive to environmental change. Thus, a more nuanced, system-by-system approach may be needed when thinking about the resiliency of ecological networks.

Transient exposure to low levels of insecticide affects metabolic networks of honeybee larvae.

The survival of a species depends on its capacity to adjust to changing environmental conditions, and new stressors. Such new, anthropogenic stressors include the neonicotinoid class of crop-protecting agents, which have been implicated in the population declines of pollinating insects, including honeybees (Apis mellifera). The low-dose effects of these compounds on larval development and physiological responses have remained largely unknown. Over a period of 15 days, we provided syrup tainted with low levels (2 µg/L(-1)) of the neonicotinoid insecticide imidacloprid to beehives located in the field. We measured transcript levels by RNA sequencing and established lipid profiles using liquid chromatography coupled with mass spectrometry from worker-bee larvae of imidacloprid-exposed (IE) and unexposed, control (C) hives. Within a catalogue of 300 differentially expressed transcripts in larvae from IE hives, we detect significant enrichment of genes functioning in lipid-carbohydrate-mitochondrial metabolic networks. Myc-involved transcriptional response to exposure of this neonicotinoid is indicated by overrepresentation of E-box elements in the promoter regions of genes with altered expression. RNA levels for a cluster of genes encoding detoxifying P450 enzymes are elevated, with coordinated downregulation of genes in glycolytic and sugar-metabolising pathways. Expression of the environmentally responsive Hsp90 gene is also reduced, suggesting diminished buffering and stability of the developmental program. The multifaceted, physiological response described here may be of importance to our general understanding of pollinator health. Muscles, for instance, work at high glycolytic rates and flight performance could be impacted should low levels of this evolutionarily novel stressor likewise induce downregulation of energy metabolising genes in adult pollinators.

Estimates of dietary overlap for six species of Amazonian manakin birds using stable isotopes.

We used stable isotope ratios to determine the metabolic routing fraction of carbon and nitrogen in feathers in addition to faecal analysis to estimate diet overlap of six sympatric species of manakins in the eastern lowland forest of Ecuador. Collectively, all species varied from-23.7 to-32.7 ‰ for δ(13)C, and from 6.0 to 9.9‰ for δ(15)N, with Machaeropterus regulus showing isotopic differences from the other species. We developed a mixing model that explicitly addresses the routing of carbon and nitrogen to feathers. Interestingly, these results suggest a higher proportion of nitrogen and carbon derived from insects than anticipated based on feeding observations and faecal analysis. A concentration-dependent mixing isotopic model was also used to look at dietary proportions. While larvae and arachnids had higher δ(15)N values, these two groups may also be preferred prey of manakins and may be more assimilated into tissues, leading to a potential overestimation of the contribution to diet. This study supports the finding that manakin species, previously thought be primarily frugivorous, contain a significant amount of arthropods in their diet.

Proximity data-loggers increase the quantity and quality of social network data.

Social network analysis is an ideal quantitative tool for advancing our understanding of complex social behaviour. However, this approach is often limited by the challenges of accurately characterizing social structure and measuring network heterogeneity. Technological advances have facilitated the study of social networks, but to date, all such work has focused on large vertebrates. Here, we provide proof of concept for using proximity data-logging to quantify the frequency of social interactions, construct weighted networks and characterize variation in the social behaviour of a lek-breeding bird, the wire-tailed manakin, Pipra filicauda. Our results highlight how this approach can ameliorate the challenges of social network data collection and analysis by concurrently improving data quality and quantity.

The ecological-evolutionary interplay: density-dependent sexual selection in a migratory songbird.

Little is understood about how environmental heterogeneity influences the spatial dynamics of sexual selection. Within human-dominated systems, habitat modification creates environmental heterogeneity that could influence the adaptive value of individual phenotypes. Here, we used the gray catbird to examine if the ecological conditions experienced in the suburban matrix (SM) and embedded suburban parks (SP) influence reproductive strategies and the strength of sexual selection. Our results show that these habitats varied in a key ecological factor, breeding density. Moreover, this ecological factor was closely tied to reproductive strategies such that local breeding density predicted the probability that a nest would contain extra-pair offspring. Partitioning reproductive variance showed that while within-pair success was more important in both habitats, extra-pair success increased the opportunity for sexual selection by 39% at higher breeding densities. Body size was a strong predictor of relative reproductive success and was under directional selection in both habitats. Importantly, our results show that the strength of sexual selection did not differ among habitats at the landscape scale but rather that fine-scale variation in an ecological factor, breeding density, influenced sexual selection on male phenotypes. Here, we document density-dependent sexual selection in a migratory bird and hypothesize that coarse-scale environmental heterogeneity, in this case generated by anthropogenic habitat modification, changed the fine-scale ecological conditions that drove the spatial dynamics of sexual selection.

Understanding testosterone variation in a tropical lek-breeding bird.

Male reproductive coalitions, in which males cooperate to attract females, are a rare strategy among vertebrates. While some studies have investigated ultimate aspects of these relationships, little is known about the mechanistic role that hormones play in modulating cooperative behaviours. Here, we examined male testosterone variation in a tropical lekking bird, the wire-tailed manakin (Pipra filicauda), which exhibits cooperative male-male display coalitions. We found that testosterone levels in territorial males were comparable to those of temperate breeding birds, a surprising result given their environmental, social and reproductive dynamics. In addition, social status rather than plumage was a strong predictor of testosterone variation. Territorial males had significantly higher testosterone levels than did two other plumage classes of floater males, who do not hold territories. We hypothesize that testosterone variation plays an important role in the establishment of male dominance hierarchies (competition), while concurrently facilitating stable display partnerships (cooperation).

Quantifying avian nest survival along an urbanization gradient using citizen- and scientist-generated data.

Despite the increasing pace of urbanization little is known about the factors that limit bird populations (i.e., population-level processes) within the urban/suburban land-use matrix. Here, we report rates of nest survival within the matrix of an urban land-use gradient in the greater Washington, D.C., USA, area for five common songbirds using data collected by scientists and citizens as part of a project called Neighborhood Nestwatch. Using program MARK, we modeled the effects of species, urbanization at multiple spatial scales (canopy cover and impervious surface), and observer (citizen vs. scientist) on nest survival of four open-cup and one cavity-nesting species. In addition, artificial nests were used to determine the relative impacts of specific predators along the land-use gradient. Our results suggest that predation on nests within the land-use matrix declines with urbanization but that there are species-specific differences. Moreover, variation in nest survival among species was best explained by urbanization metrics measured at larger "neighborhood" spatial scales (e.g., 1000 m). Trends were supported by data from artificial nests and suggest that variable predator communities (avian vs. mammalian) are one possible mechanism to explain differential nest survival. In addition, we assessed the quality of citizen science data and show that citizens had no negative effect on nest survival and provided estimates of nest survival comparable to Smithsonian biologists. Although birds nesting within the urban matrix experienced higher nest survival, individuals also faced a multitude of other challenges such as contaminants and invasive species, all of which could reduce adult survival.

It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird.

Variance in reproductive success among individuals is a defining characteristic of many social vertebrates. Yet, our understanding of which male attributes contribute to reproductive success is still fragmentary in most cases. Male-male reproductive coalitions, where males jointly display to attract females, are of particular interest to evolutionary biologists because one male appears to forego reproduction to assist the social partner. By examining the relationship between social behaviour and reproductive success, we can elucidate the proximate function of coalitions in the context of mate choice. Here, we use data from a 4-year study of wire-tailed manakins (Pipra filicauda) to provide molecular estimates of reproductive skew and to test the hypothesis that male-male social interactions, in the context of coordinated displays, positively influence a male's reproductive success. More specifically, we quantify male-male social interactions using network metrics and predict that greater connectivity will result in higher relative reproductive success. Our data show that four out of six leks studied had significant reproductive skew, with success apportioned to very few individuals in each lek. Metrics of male social affiliations derived from our network analysis, especially male connectivity, measured as the number of males with whom the focal male has extended interactions, were strong predictors of the number of offspring sired. Thus, network connectivity is associated with male fitness in wire-tailed manakins. This pattern may be the result of shared cues used by both sexes to assess male quality, or the result of strict female choice for coordinated display behaviour.

Social networks in the lek-mating wire-tailed manakin (Pipra filicauda).

How social structure interacts with individual behaviour and fitness remains understudied despite its potential importance to the evolution of cooperation. Recent applications of network theory to social behaviour advance our understanding of the role of social interactions in various contexts. Here we applied network theory to the social system of lek-mating wire-tailed manakins (Pipra filicauda, Pipridae, Aves). We analysed the network of interactions among males in order to begin building a comparative framework to understand where coordinated display behaviour lies along the continuum from solitary to obligately cooperative dual-male displays in the family Pipridae. Network degree (the number of links from a male to others) ranged from 1 to 10, with low mean and high variance, consistent with the theory for the evolution of cooperation within social networks. We also assessed factors that could predict social and reproductive success of males. Four network metrics, degree, eigenvector centrality, information centrality and reach, some of which assess circuitous as well as the shortest (geodesic) paths of male connectivity, predicted male social rise. The duration of a male's territorial tenure during the 4 years of the study predicted his probability of siring offspring.

The External RNA Controls Consortium: a progress report.

Standard controls and best practice guidelines advance acceptance of data from research, preclinical and clinical laboratories by providing a means for evaluating data quality. The External RNA Controls Consortium (ERCC) is developing commonly agreed-upon and tested controls for use in expression assays, a true industry-wide standard control.

High Quality Performance of High-throughput GeneChip® Probe Array System.

A high-throughput GeneChip® probe array platform was established. This system offers automated processing of 96 samples in the industry standard 96-well plate format. We demonstrate that this new technology can deliver the same performance as the standard cartridge probe arrays.

Parallel genotyping of over 10,000 SNPs using a one-primer assay on a high-density oligonucleotide array.

The analysis of single nucleotide polymorphisms (SNPs) is increasingly utilized to investigate the genetic causes of complex human diseases. Here we present a high-throughput genotyping platform that uses a one-primer assay to genotype over 10,000 SNPs per individual on a single oligonucleotide array. This approach uses restriction digestion to fractionate the genome, followed by amplification of a specific fractionated subset of the genome. The resulting reduction in genome complexity enables allele-specific hybridization to the array. The selection of SNPs was primarily determined by computer-predicted lengths of restriction fragments containing the SNPs, and was further driven by strict empirical measurements of accuracy, reproducibility, and average call rate, which we estimate to be >99.5%, >99.9%, and>95%, respectively [corrected]. With average heterozygosity of 0.38 and genome scan resolution of 0.31 cM, the SNP array is a viable alternative to panels of microsatellites (STRs). As a demonstration of the utility of the genotyping platform in whole-genome scans, we have replicated and refined a linkage region on chromosome 2p for chronic mucocutaneous candidiasis and thyroid disease, previously identified using a panel of microsatellite (STR) markers.