Identifying engaging bird species and traits with community science observations.

Identifying rates at which birders engage with different species can inform the impact and efficacy of conservation outreach and the scientific use of community-collected biodiversity data. Species that are thought to be "charismatic" are often prioritized in conservation, and previous researchers have used sociological experiments and digital records to estimate charisma indirectly. In this study, we take advantage of community science efforts as another record of human engagement with animals that can reveal observer biases directly, which are in part driven by observer preference. We apply a multistage analysis to ask whether opportunistic birders contributing to iNaturalist engage more with larger, more colorful, and rarer birds relative to a baseline approximated from eBird contributors. We find that body mass, color contrast, and range size all predict overrepresentation in the opportunistic dataset. We also find evidence that, across 472 modeled species, 52 species are significantly overreported and 158 are significantly underreported, indicating a wide variety of species-specific effects. Understanding which birds are highly engaging can aid conservationists in creating impactful outreach materials and engaging new naturalists. The quantified differences between two prominent community science efforts may also be of use for researchers leveraging the data from one or both of them to answer scientific questions of interest.

A cloudy forecast for species distribution models: Predictive uncertainties abound for California birds after a century of climate and land-use change.

Correlative species distribution models are widely used to quantify past shifts in ranges or communities, and to predict future outcomes under ongoing global change. Practitioners confront a wide range of potentially plausible models for ecological dynamics, but most specific applications only consider a narrow set. Here, we clarify that certain model structures can embed restrictive assumptions about key sources of forecast uncertainty into an analysis. To evaluate forecast uncertainties and our ability to explain community change, we fit and compared 39 candidate multi- or joint species occupancy models to avian incidence data collected at 320 sites across California during the early 20th century and resurveyed a century later. We found massive (>20,000 LOOIC) differences in within-time information criterion across models. Poorer fitting models omitting multivariate random effects predicted less variation in species richness changes and smaller contemporary communities, with considerable variation in predicted spatial patterns in richness changes across models. The top models suggested avian environmental associations changed across time, contemporary avian occupancy was influenced by previous site-specific occupancy states, and that both latent site variables and species associations with these variables also varied over time. Collectively, our results recapitulate that simplified model assumptions not only impact predictive fit but may mask important sources of forecast uncertainty and mischaracterize the current state of system understanding when seeking to describe or project community responses to global change. We recommend that researchers seeking to make long-term forecasts prioritize characterizing forecast uncertainty over seeking to present a single best guess. To do so reliably, we urge practitioners to employ models capable of characterizing the key sources of forecast uncertainty, where predictors, parameters and random effects may vary over time or further interact with previous occurrence states.

To rarefy or not to rarefy: robustness and efficiency trade-offs of rarefying microbiome data.

MOTIVATION: Microbiome datasets provide rich information about microbial communities. However, vast library size variations across samples present great challenges for proper statistical comparisons. To deal with these challenges, rarefaction is often used in practice as a normalization technique, although there has been debate whether rarefaction should ever be used. Conventional wisdom and previous work suggested that rarefaction should never be used in practice, arguing that rarefying microbiome data is statistically inadmissible. These discussions, however, have been confined to particular parametric models and simulation studies. RESULTS: We develop a semiparametric graphical model framework for grouped microbiome data and analyze in the context of differential abundance testing the statistical trade-offs of the rarefaction procedure, accounting for latent variations and measurement errors. Under the framework, it can be shown rarefaction guarantees that subsequent permutation tests properly control the Type I error. In addition, the loss in sensitivity from rarefaction is solely due to increased measurement error; if the underlying variation in microbial composition is large among samples, rarefaction might not hurt subsequent statistical inference much. We develop the rarefaction efficiency index (REI) as an indicator for efficiency loss and illustrate it with a dataset on the effect of storage conditions for microbiome data. Simulation studies based on real data demonstrate that the impact of rarefaction on sensitivity is negligible when overdispersion is prominent, while low REI corresponds to scenarios in which rarefying might substantially lower the statistical power. Whether to rarefy or not ultimately depends on assumptions of the data generating process and characteristics of the data. AVAILABILITY AND IMPLEMENTATION: Source codes are publicly available at https://github.com/jcyhong/rarefaction. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Estimating and forecasting spatial population dynamics of apex predators using transnational genetic monitoring.

The ongoing recovery of terrestrial large carnivores in North America and Europe is accompanied by intense controversy. On the one hand, reestablishment of large carnivores entails a recovery of their most important ecological role, predation. On the other hand, societies are struggling to relearn how to live with apex predators that kill livestock, compete for game species, and occasionally injure or kill people. Those responsible for managing these species and mitigating conflict often lack fundamental information due to a long-standing challenge in ecology: How do we draw robust population-level inferences for elusive animals spread over immense areas? Here we showcase the application of an effective tool for spatially explicit tracking and forecasting of wildlife population dynamics at scales that are relevant to management and conservation. We analyzed the world's largest dataset on carnivores comprising more than 35,000 noninvasively obtained DNA samples from over 6,000 individual brown bears (Ursus arctos), gray wolves (Canis lupus), and wolverines (Gulo gulo). Our analyses took into account that not all individuals are detected and, even if detected, their fates are not always known. We show unequivocal quantitative evidence of large carnivore recovery in northern Europe, juxtaposed with the finding that humans are the single-most important factor driving the dynamics of these apex predators. We present maps and forecasts of the spatiotemporal dynamics of large carnivore populations, transcending national boundaries and management regimes.

Proximity of restored hedgerows interacts with local floral diversity and species' traits to shape long-term pollinator metacommunity dynamics.

Disconnected habitat fragments are poor at supporting population and community persistence; restoration ecologists, therefore, advocate for the establishment of habitat networks across landscapes. Few empirical studies, however, have considered how networks of restored habitat patches affect metacommunity dynamics. Here, using a 10-year study on restored hedgerows and unrestored field margins within an intensive agricultural landscape, we integrate occupancy modelling with network theory to examine the interaction between local and landscape characteristics, habitat selection and dispersal in shaping pollinator metacommunity dynamics. We show that surrounding hedgerows and remnant habitat patches interact with the local floral diversity, bee diet breadth and bee body size to influence site occupancy, via colonisation and persistence dynamics. Florally diverse sites and generalist, small-bodied species are most important for maintaining metacommunity connectivity. By providing the first in-depth assessment of how a network of restored habitat influences long-term population dynamics, we confirm the conservation benefit of hedgerows for pollinator populations and demonstrate the importance of restoring and maintaining habitat networks within an inhospitable matrix.

A century of climate and land-use change cause species turnover without loss of beta diversity in California's Central Valley.

Climate and land-use changes are thought to be the greatest threats to biodiversity, but few studies have directly measured their simultaneous impacts on species distributions. We used a unique historic resource-early 20th-century bird surveys conducted by Joseph Grinnell and colleagues-paired with contemporary resurveys a century later to examine changes in bird distributions in California's Central Valley, one of the most intensively modified agricultural zones in the world and a region of heterogeneous climate change. We analyzed species- and community-level occupancy using multispecies occupancy models that explicitly accounted for imperfect detection probability, and developed a novel, simulation-based method to compare the relative influences of climate and land-use covariates on site-level species richness and beta diversity (measured by Jaccard similarity). Surprisingly, we show that mean occupancy, species richness and between-site similarity have remained remarkably stable over the past century. Stability in community-level metrics masked substantial changes in species composition; occupancy declines of some species were equally matched by increases in others, predominantly species with generalist or human-associated habitat preferences. Bird occupancy, richness and diversity within each era were driven most strongly by water availability (precipitation and percent water cover), indicating that both climate and land-use are important drivers of species distributions. Water availability had much stronger effects than temperature, urbanization and agricultural cover, which are typically thought to drive biodiversity decline.

Phylogenetic occupancy models integrate imperfect detection and phylogenetic signal to analyze community structure.

Biological communities are structured phylogenetically-closely related species are typically more likely to be found at the same sites. This may be, in part, because they respond similarly to environmental gradients. Accurately surveying biological communities is, however, made difficult by the fact that detection of species is not perfect. In recent years, numerous statistical methods have been developed that aim to overcome deficiencies in the species detection process. However, these methods do not allow investigators to assess phylogenetic community structure. Here, we introduce the phylogenetic occupancy model (POM), which accounts for imperfect species detection while assessing phylogenetic patterns in community structure. Using simulated data sets we show that the POM grants less biased estimates of phylogenetic structure than models without imperfect detection, and can correctly ascertain the effects of species traits on community composition while accounting for evolutionary non-independence of taxa. Integrating phylogenetic methods into widely used occupancy models will help clarify how evolutionary history influences modern day communities.

Warming and provenance limit tree recruitment across and beyond the elevation range of subalpine forest.

Climate niche models project that subalpine forest ranges will extend upslope with climate warming. These projections assume that the climate suitable for adult trees will be adequate for forest regeneration, ignoring climate requirements for seedling recruitment, a potential demographic bottleneck. Moreover, local genetic adaptation is expected to facilitate range expansion, with tree populations at the upper forest edge providing the seed best adapted to the alpine. Here, we test these expectations using a novel combination of common gardens, seeded with two widely distributed subalpine conifers, and climate manipulations replicated at three elevations. Infrared heaters raised temperatures in heated plots, but raised temperatures more in the forest than at or above treeline because strong winds at high elevation reduced heating efficiency. Watering increased season-average soil moisture similarly across sites. Contrary to expectations, warming reduced Engelmann spruce recruitment at and above treeline, as well as in the forest. Warming reduced limber pine first-year recruitment in the forest, but had no net effect on fourth-year recruitment at any site. Watering during the snow-free season alleviated some negative effects of warming, indicating that warming exacerbated water limitations. Contrary to expectations of local adaptation, low-elevation seeds of both species initially recruited more strongly than high-elevation seeds across the elevation gradient, although the low-provenance advantage diminished by the fourth year for Engelmann spruce, likely due to small sample sizes. High- and low-elevation provenances responded similarly to warming across sites for Engelmann spruce, but differently for limber pine. In the context of increasing tree mortality, lower recruitment at all elevations with warming, combined with lower quality, high-provenance seed being most available for colonizing the alpine, portends range contraction for Engelmann spruce. The lower sensitivity of limber pine to warming indicates a potential for this species to become more important in subalpine forest communities in the coming centuries.

Monte Carlo estimation of stage structured development from cohort data.

Cohort data are frequently collected to study stage-structured development and mortalities of many organisms, particularly arthropods. Such data can provide information on mean stage durations, among-individual variation in stage durations, and on mortality rates. Current statistical methods for cohort data lack flexibility in the specification of stage duration distributions and mortality rates. In this paper, we present a new method for fitting models of stage-duration distributions and mortality to cohort data. The method is based on a Monte Carlo within MCMC algorithm and provides Bayesian estimates of parameters of stage-structured cohort models. The algorithm is computationally demanding but allows for flexible specifications of stage-duration distributions and mortality rates. We illustrate the algorithm with an application to data from a previously published experiment on the development of brine shrimp from Mono Lake, California, through nine successive stages. In the experiment, three different food supply and temperature combination treatments were studied. We compare the mean duration of the stages among the treatments while simultaneously estimating mortality rates and among-individual variance of stage durations. The method promises to enable more detailed studies of development of both natural and experimental cohorts. An R package implementing the method and which allows flexible specification of stage duration distributions is provided.

Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass.

The interface between roots and soil, known as the rhizosphere, is a dynamic habitat in the soil ecosystem. Unraveling the factors that control rhizosphere community assembly is a key starting point for understanding the diversity of plant-microbial interactions that occur in soil. The goals of this study were to determine how environmental factors shape rhizosphere microbial communities, such as local soil characteristics and the regional climate, and to determine the relative influence of the rhizosphere on microbial community assembly compared to the pressures imposed by the local and regional environment. We identified the bacteria present in the soil immediately adjacent to the roots of wild oat (A vena spp.) in three California grasslands using deep Illumina 16S sequencing. Rhizosphere communities were more similar to each other than to the surrounding soil communities from which they were derived, despite the fact that the grasslands studied were separated by hundreds of kilometers. The rhizosphere was the dominant factor structuring bacterial community composition (38% variance explained), and was comparable in magnitude to the combined local and regional effects (22% and 21%, respectively). Rhizosphere communities were most influenced by factors related to the regional climate (soil moisture and temperature), while background soil communities were more influenced by soil characteristics (pH, CEC, exchangeable cations, clay content). The Avena core microbiome was strongly phylogenetically clustered according to the metrics NRI and NTI, which indicates that selective processes likely shaped these communities. Furthermore, 17% of these taxa were not detectable in the background soil, even with a robust sequencing depth of approximately 70,000 sequences per sample. These results support the hypothesis that roots select less abundant or possibly rare populations in the soil microbial community, which appear to be lineages of bacteria that have made a physiological tradeoff for rhizosphere competence at the expense of their competitiveness in non-rhizosphere soil.

Diversification practices reduce organic to conventional yield gap.

Agriculture today places great strains on biodiversity, soils, water and the atmosphere, and these strains will be exacerbated if current trends in population growth, meat and energy consumption, and food waste continue. Thus, farming systems that are both highly productive and minimize environmental harms are critically needed. How organic agriculture may contribute to world food production has been subject to vigorous debate over the past decade. Here, we revisit this topic comparing organic and conventional yields with a new meta-dataset three times larger than previously used (115 studies containing more than 1000 observations) and a new hierarchical analytical framework that can better account for the heterogeneity and structure in the data. We find organic yields are only 19.2% (±3.7%) lower than conventional yields, a smaller yield gap than previous estimates. More importantly, we find entirely different effects of crop types and management practices on the yield gap compared with previous studies. For example, we found no significant differences in yields for leguminous versus non-leguminous crops, perennials versus annuals or developed versus developing countries. Instead, we found the novel result that two agricultural diversification practices, multi-cropping and crop rotations, substantially reduce the yield gap (to 9 ± 4% and 8 ± 5%, respectively) when the methods were applied in only organic systems. These promising results, based on robust analysis of a larger meta-dataset, suggest that appropriate investment in agroecological research to improve organic management systems could greatly reduce or eliminate the yield gap for some crops or regions.

The importance of individual developmental variation in stage-structured population models.

Population stage structure is fundamental to ecology, and models of this structure have proven useful in many different systems. Many ecological variables other than stage, such as habitat type, site occupancy and metapopulation status are also modelled using transitions among discrete states. Transitions among life stages can be characterised by the distribution of time spent in each stage, including the mean and variance of each stage duration and within-individual correlations among multiple stage durations. Three modelling traditions represent stage durations differently. Matrix models can be derived as a long-run approximation from any distribution of stage durations, but they are often interpreted directly as a Markov model for stage transitions. Statistical stage-duration distribution models accommodate the variation typical of cohort development data, but such realism has rarely been incorporated in population theory or statistical population models. Delay-differential equation models include lags but no variation, except in limited cases. We synthesise these models in one framework and illustrate how individual variation and correlations in development can impact population growth. Furthermore, different development models can yield the same long-term matrix transition rates but different sensitivities and elasticities. Finally, we discuss future directions for estimating realistic stage duration models from data.

An approximate Bayesian computation approach to parameter estimation in a stochastic stage-structured population model.

Complex population processes may require equally complex models, which can lead to analytically intractable estimation problems. Approximate Bayesian computation (ABC) is a computational tool for parameter estimation in situations where likelihoods cannot be computed. Instead of using likelihoods, ABC methods quantify the similarities between an observed data set and repeated simulations from a model. A practical obstacle to implementing an ABC algorithm is selecting summary statistics and distance metrics that accurately capture the main features of the data. We demonstrate the application of a sequential Monte Carlo ABC sampler (ABC SMC) to parameter estimation of a general stochastic stage-structured population model with ongoing reproduction and heterogeneity in development and mortality. Individual variation in demographic traits has considerable consequences for population dynamics in many systems, but including it in a population model by explicitly allowing stage durations to follow a realistic distribution creates a complex model. We applied the ABC SMC to fit the model to a simulated representative data set with known underlying parameters to evaluate the performance of the algorithm. We also introduced a systematic method for selecting summary statistics and distance metrics, using simulated data and receiver operating characteristic (ROC) curves from classification theory. Evaluations suggest that the approach is promising for model inference in our example of realistic stage-structured population models.

Estimation of stage duration distributions and mortality under repeated cohort censuses.

Many processes in nature can be viewed as arising from subjects progressing through sequential stages and may be described by multistage models. Examples include disease development and the physiological development of plants and animals. We develop a multistage model for sampling designs where a small set of subjects is followed and the number of subjects in each stage is assessed repeatedly for a sequence of time points, but for which the subjects cannot be identified. The motivating problem is the laboratory study of developing arthropods through stage frequency data. Our model assumes that the same individuals are censused at each time, introducing among sample dependencies. This type of data often occur in laboratory studies of small arthropods but their detailed analysis has received little attention. The likelihood of the model is derived from a stochastic model of the development and mortality of the individuals in the cohort. We present an MCMC scheme targeting the posterior distribution of the times of development and times of death of individuals. This is a novel type of MCMC that uses customized proposals to explore a posterior with disconnected support arising from the fact that individual identities are unknown. The MCMC algorithm may be used for inference about parameters governing stage duration distributions and mortality rates. The method is demonstrated by fitting the development model to stage frequency data of a mealybug cohort placed on a grape vine.

Statistical ecology comes of age.

The desire to predict the consequences of global environmental change has been the driver towards more realistic models embracing the variability and uncertainties inherent in ecology. Statistical ecology has gelled over the past decade as a discipline that moves away from describing patterns towards modelling the ecological processes that generate these patterns. Following the fourth International Statistical Ecology Conference (1-4 July 2014) in Montpellier, France, we analyse current trends in statistical ecology. Important advances in the analysis of individual movement, and in the modelling of population dynamics and species distributions, are made possible by the increasing use of hierarchical and hidden process models. Exciting research perspectives include the development of methods to interpret citizen science data and of efficient, flexible computational algorithms for model fitting. Statistical ecology has come of age: it now provides a general and mathematically rigorous framework linking ecological theory and empirical data.

General models for resource use or other compositional count data using the Dirichlet-multinomial distribution.

Many ecological studies investigate how organisms use resources, such as habitats or foods, in relation to availability or other variables. Related statistical problems include analysis of proportions of species or genotypes in a community or population. These require statistical modeling of compositional count data: data on relative proportions of each category collected as counts. Common methods for analyzing compositional count data lack one or more important considerations. Some methods lack explicit accommodation of count data, dealing instead with proportions. Others do not handle between-sample heterogeneity for overdispersed data. Yet others do not allow general types of relationships between explanatory variables and resource use. All three components have been combined in a Bayesian framework, but for frequentist hypothesis tests and AIC model selection, maximum-likelihood estimation is needed. Here we propose the Dirichlet-multinomial distribution to accommodate overdispersed compositional count data. This approach can be used flexibly in combination with explanatory models, but the only correlations among compositional proportions that it can accommodate are the negative correlations due to the fact that proportions must sum to 1. Many existing models can be generalized to use the Dirichlet-multinomial distribution for residual variation, and the flexibility of the approach allows new hypotheses that have often not been considered in resource preference analysis, including that availability has no relation to use. We also highlight a new design for resource use studies, with multiple individual-use data sets from each of multiple sites, with different explanatory data for each site. We illustrate the approach with three examples. For two previously published habitat use data sets, we support the original conclusions and show that use is not unrelated to availability. For a data set of pollen collected by multiple bees from each of two sites, pollen use differs between the sites. Using bootstrap goodness-of-fit tests, we illustrate that the Dirichlet-multinomial is acceptable for two of the examples but unsuitable for one of the habitat use examples.

Using uncertainty estimates in analyses of population time series.

Recording and monitoring wildlife is crucial for the conservation of wild species and the protection of their environment. The most common type of information reported from a monitoring scheme is a time series of population abundance estimates, but the potential of such data for analyzing population dynamics is limited due to lack of information on sampling error. Recent work has shown that replicating the sampling process and analyzing replicates jointly in a dynamical model can considerably increase estimation efficiency compared to analyzing population estimates alone. This method requires that independent replicates are available, and model fitting can be complex in general. Often, however, population estimates are accompanied by standard errors, or standard errors may be estimated from raw data using a sampling model. We evaluate a method where standard errors are used in combination with population estimates to account for sampling variability in state-space models of population dynamics. The method is simple and lends itself readily to data derived from many sampling procedures but ignores uncertainty in the standard errors themselves. We simulate data from a Gaussian state-space model where several observations, which may come from different sites, are available for the population at each time. Fitting the simulated data, we show that the method yields similar or even better results than a method utilizing all observations, even when there are few observations at each time. This holds under a range of simulation settings involving heteroscedastic observation error, site effects, and correlation among observations. We illustrate the approach on real data from the North American Breeding Bird Survey and show that it performs well in comparison to a more difficult maximum-likelihood analysis of the full data under non-Gaussian sampling error.

Estimating tree growth from complex forest monitoring data.

Understanding tree growth as a function of tree size is important for a multitude of ecological and management applications. Determining what limits growth is of central interest, and forest inventory permanent plots are an abundant source of long-term information but are highly complex. Observation error and multiple sources of shared variation (spatial plot effects, temporal repeated measures, and a mosaic of sampling intervals) make these data challenging to use for growth estimation. We account for these complexities and incorporate potential limiting factors (tree size, competition, and resource supply) into a hierarchical state-space model. We estimate the diameter growth of white fir (Abies concolor) in the Sierra Nevada of California from forest inventory data, showing that estimating such a model is feasible in a Bayesian framework using readily available modeling tools. In this forest, white fir growth depends strongly on tree size, total plot basal area, and unexplained variation between individual trees. Plot-level resource supply variables (representing light, water, and nutrient availability) do not have a strong impact on inventory-size trees. This approach can be applied to other networks of permanent forest plots, leading to greater ecological insights on tree growth.

Concordant and opposing effects of climate and land-use change on avian assemblages in California's most transformed landscapes.

Climate and land-use change could exhibit concordant effects that favor or disfavor the same species, which would amplify their impacts, or species may respond to each threat in a divergent manner, causing opposing effects that moderate their impacts in isolation. We used early 20th century surveys of birds conducted by Joseph Grinnell paired with modern resurveys and land-use change reconstructed from historic maps to examine avian change in Los Angeles and California's Central Valley (and their surrounding foothills). Occupancy and species richness declined greatly in Los Angeles from urbanization, strong warming (+1.8°C), and drying (-77.2 millimeters) but remained stable in the Central Valley, despite large-scale agricultural development, average warming (+0.9°C), and increased precipitation (+11.2 millimeters). While climate was the main driver of species distributions a century ago, the combined impacts of land-use and climate change drove temporal changes in occupancy, with similar numbers of species experiencing concordant and opposing effects.

Estimating spatially variable and density-dependent survival using open-population spatial capture-recapture models.

Open-population spatial capture-recapture (OPSCR) models use the spatial information contained in individual detections collected over multiple consecutive occasions to estimate not only occasion-specific density, but also demographic parameters. OPSCR models can also estimate spatial variation in vital rates, but such models are neither widely used nor thoroughly tested. We developed a Bayesian OPSCR model that not only accounts for spatial variation in survival using spatial covariates but also estimates local density-dependent effects on survival within a unified framework. Using simulations, we show that OPSCR models provide sound inferences on the effect of spatial covariates on survival, including multiple competing sources of mortality, each with potentially different spatial determinants. Estimation of local density-dependent survival was possible but required more data due to the greater complexity of the model. Not accounting for spatial heterogeneity in survival led to up to 10% positive bias in abundance estimates. We provide an empirical demonstration of the model by estimating the effect of country and density on cause-specific mortality of female wolverines (Gulo gulo) in central Sweden and Norway. The ability to make population-level inferences on spatial variation in survival is an essential step toward a fully spatially explicit OPSCR model capable of disentangling the role of multiple spatial drivers of population dynamics.