Nonlinear life table response experiment analysis: Decomposing nonlinear and nonadditive population growth responses to changes in environmental drivers.

Life table response experiments (LTREs) decompose differences in population growth rate between environments into separate contributions from each underlying demographic rate. However, most LTRE analyses make the unrealistic assumption that the relationships between demographic rates and environmental drivers are linear and independent, which may result in diminished accuracy when these assumptions are violated. We extend regression LTREs to incorporate nonlinear (second-order) terms and compare the accuracy of both approaches for three previously published demographic datasets. We show that the second-order approach equals or outperforms the linear approach for all three case studies, even when all of the underlying vital rate functions are linear. Nonlinear vital rate responses to driver changes contributed most to population growth rate responses, but life history changes also made substantial contributions. Our results suggest that moving from linear to second-order LTRE analyses could improve our understanding of population responses to changing environments.

Adaptation to distinct habitats is maintained by contrasting selection at different life stages in sunflower ecotypes.

Conspecific populations living in adjacent but contrasting microenvironments represent excellent systems for studying natural selection. These systems are valuable because gene flow is expected to force genetic homogeneity except at loci experiencing divergent selection. A history of reciprocal transplant and common garden studies in such systems, and a growing number of genomic studies, have contributed to understanding how selection operates in natural populations. While selection can vary across different fitness components and life stages, few studies have investigated how this ultimately affects allele frequencies and the maintenance of divergence between populations. Here, we study two sunflower ecotypes in distinct, adjacent habitats by combining demographic models with genome-wide sequence data to estimate fitness and allele frequency change at multiple life stages. This framework allows us to estimate that only local ecotypes are likely to experience positive population growth (λ > 1) and that the maintenance of divergent adaptation appears to be mediated via habitat- and life stage-specific selection. We identify genetic variation, significantly driven by loci in chromosomal inversions, associated with different life history strategies in neighbouring ecotypes that optimize different fitness components and may contribute to the maintenance of distinct ecotypes.

Range dynamics mediated by compensatory life stage responses to experimental climate manipulations.

The expectations of polar or upslope distributional shifts of species ranges in response to warming climate conditions have been recently questioned. Diverse responses of different life stages to changing temperature and moisture regimes may alter these predicted range dynamics. Furthermore, the climate driver(s) influencing demographic rates, and the contribution of each demographic rate to population growth rate (λ), may shift across a species range. We investigated these demographic effects by experimentally manipulating climate and measuring responses of λ in nine populations spanning the elevation range of an alpine plant (Ivesia lycopodioides). Populations exhibited stable growth rates (λ ~ 1) under naturally wet conditions and declining rates (λ < 1) under naturally dry conditions. However, opposing vital rate responses to experimental heating and watering lead to negligible or negative effects on population stability. These findings indicate that life stage-specific responses to changing climate can disrupt the current relationships between population stability and climate across species ranges.

Resource availability and heterogeneity shape the self-organisation of regular spatial patterning.

Explaining large-scale ordered patterns and their effects on ecosystem functioning is a fundamental and controversial challenge in ecology. Here, we coupled empirical and theoretical approaches to explore how competition and spatial heterogeneity govern the regularity of colony dispersion in fungus-farming termites. Individuals from different colonies fought fiercely, and inter-nest distances were greater when nests were large and resources scarce-as expected if competition is strong, large colonies require more resources and foraging area scales with resource availability. Building these principles into a model of inter-colony competition showed that highly ordered patterns emerged under high resource availability and low resource heterogeneity. Analysis of this dynamical model provided novel insights into the mechanisms that modulate pattern regularity and the emergent effects of these patterns on system-wide productivity. Our results show how environmental context shapes pattern formation by social-insect ecosystem engineers, which offers one explanation for the marked variability observed across ecosystems.

Latitudinal gradients in population growth do not reflect demographic responses to climate.

Spatial gradients in population growth, such as across latitudinal or elevational gradients, are often assumed to primarily be driven by variation in climate, and are frequently used to infer species' responses to climate change. Here, we use a novel demographic, mixed-model approach to dissect the contributions of climate variables vs. other latitudinal or local site effects on spatiotemporal variation in population performance in three perennial bunchgrasses. For all three species, we find that performance of local populations decreases with warmer and drier conditions, despite latitudinal trends of decreasing population growth toward the cooler and wetter northern portion of each species' range. Thus, latitudinal gradients in performance are not predictive of either local or species-wide responses to climate. This pattern could be common, as many environmental drivers, such as habitat quality or species' interactions, are likely to vary with latitude or elevation, and thus influence or oppose climate responses.

Dynamic shifts in social network structure and composition within a breeding hybrid population.

Mating behaviour and the timing of reproduction can inhibit genetic exchange between closely related species; however, these reproductive barriers are challenging to measure within natural populations. Social network analysis provides promising tools for studying the social context of hybridization, and the exchange of genetic variation, more generally. We test how social networks within a hybrid population of California Callipepla californica and Gambel's quail Callipepla gambelii change over discrete periods of a breeding season. We assess patterns of phenotypic and genotypic assortment, and ask whether altered associations between individuals (association rewiring), or changes to the composition of the population (individual turnover) drive network dynamics. We use genetic data to test whether social associations and relatedness between individuals correlate with patterns of parentage within the hybrid population. To achieve these aims, we combine RFID association data, phenotypic data and genomic measures with social network analyses. We adopt methods from the ecological network literature to quantify shifts in network structure and to partition changes into those due to individual turnover and association rewiring. We integrate genomic data into networks as node-level attributes (ancestry) and edges (relatedness, parentage) to test links between social and parentage networks. We show that rewiring of associations between individuals that persist across network periods, rather than individual turnover, drives the majority of the changes in network structure throughout the breeding season, and that the traits involved in phenotypic/genotypic assortment were highly dynamic over time. Social networks were randomly assorted based on genetic ancestry, suggesting weak behavioural reproductive isolation within this hybrid population. Finally, we show that the strength of associations within the social network, but not levels of genetic relatedness, predicts patterns of parentage. Social networks play an important role in population processes such as the transmission of disease and information, yet there has been less focus on how networks influence the exchange of genetic variation. By integrating analyses of social structure, phenotypic assortment and reproductive outcomes within a hybrid zone, we demonstrate the utility of social networks for analysing links between social context and gene flow within wild populations.

Aridity weakens population-level effects of multiple species interactions on Hibiscus meyeri.

Predicting how species' abundances and ranges will shift in response to climate change requires a mechanistic understanding of how multiple factors interact to limit population growth. Both abiotic stress and species interactions can limit populations and potentially set range boundaries, but we have a poor understanding of when and where each is most critical. A commonly cited hypothesis, first proposed by Darwin, posits that abiotic factors (e.g., temperature, precipitation) are stronger determinants of range boundaries in apparently abiotically stressful areas ("stress" indicates abiotic factors that reduce population growth), including desert, polar, or high-elevation environments, whereas species interactions (e.g., herbivory, competition) play a stronger role in apparently less stressful environments. We tested a core tenet of this hypothesis-that population growth rate is more strongly affected by species interactions in less stressful areas-using experimental manipulations of species interactions affecting a common herbaceous plant, Hibiscus meyeri (Malvaceae), across an aridity gradient in a semiarid African savanna. Population growth was more strongly affected by four distinct species interactions (competition with herbaceous and shrubby neighbors, herbivory, and pollination) in less stressful mesic areas than in more stressful arid sites. However, contrary to common assumptions, this effect did not arise because of greater density or diversity of interacting species in less stressful areas, but rather because aridity reduced sensitivity of population growth to these interactions. Our work supports classic predictions about the relative strength of factors regulating population growth across stress gradients, but suggests that this pattern results from a previously unappreciated mechanism that may apply to many species worldwide.

Spatial patterning of soil microbial communities created by fungus-farming termites.

Spatially overdispersed mounds of fungus-farming termites (Macrotermitinae) are hotspots of nutrient availability and primary productivity in tropical savannas, creating spatial heterogeneity in communities and ecosystem functions. These termites influence the local availability of nutrients in part by redistributing nutrients across the landscape, but the links between termite ecosystem engineering and the soil microbes that are the metabolic agents of nutrient cycling are little understood. We used DNA metabarcoding of soils from Odontotermes montanus mounds to examine the influence of termites on soil microbial communities in a semi-arid Kenyan savanna. We found that bacterial and fungal communities were compositionally distinct in termite-mound topsoils relative to the surrounding savanna, and that bacterial communities were more diverse on mounds. The higher microbial alpha and beta diversity associated with mounds created striking spatial patterning in microbial community composition, and boosted landscape-scale microbial richness and diversity. Selected enzyme assays revealed consistent differences in potential enzymatic activity, suggesting links between termite-induced heterogeneity in microbial community composition and the spatial distribution of ecosystem functions. We conducted a large-scale field experiment in which we attempted to simulate termites' effects on microbes by fertilizing mound-sized patches; this altered both bacterial and fungal communities, but in a different way than natural mounds. Elevated levels of inorganic nitrogen, phosphorus and potassium may help to explain the distinctive fungal communities in termite-mound soils, but cannot account for the distinctive bacterial communities associated with mounds.

Can Community Structure Causally Determine Dynamics of Constituent Species? A Test Using a Host-Parasite Community.

Structures of communities have been widely studied with the assumption that they not only are a useful bookkeeping tool but also can causally influence dynamics of the populations from which they emerge. However, convincing tests of this assumption have remained elusive because generally the only way to alter a community property is by manipulating its constituent populations, thereby preventing independent measurements of effects on those populations. There is a growing body of evidence that methods like convergent cross-mapping (CCM) can be used to make inferences about causal interactions using state space reconstructions of coupled time series, a method that relies on only observational data. Here we show that CCM can be used to test the causal effects of community properties using a well-studied Slovakian rodent-ectoparasite community. CCM identified causal drivers across the organizational scales of this community, including evidence that host dynamics were influenced by the degree to which the community at large was connected and clustered. Our findings add to the growing literature on the importance of community structures in disease dynamics and argue for a broader use of causal inference in the analysis of community dynamics.

Assessing Behavioral Associations in a Hybrid Zone through Social Network Analysis: Complex Assortative Behaviors Structure Associations in a Hybrid Quail Population.

Behavior can strongly influence rates and patterns of hybridization between animal populations and species. Yet few studies have examined reproductive behaviors in natural hybrid zones within the fine-scale social context in which they naturally occur. We use radio-frequency identification tags with social network analyses to test whether phenotypic similarity in plumage and mass correlate with social behavior throughout a breeding season in a California and Gambel's quail hybrid zone. We use a novel approach to partition phenotypic variation in a way that does not confound differences between sexes and species, and we illustrate the complex ways that phenotype and behavior structure the social environment, mating opportunities, and male-male associations. Associations within the admixed population were random with respect to species-specific plumage but showed strong patterns of assortment based on sexually dimorphic plumage, monomorphic plumage, and mass. Weak behavioral reproductive isolation in this admixed population may be the result of complex patterns of phenotypic assortment based on multiple traits rather than a lack of phenotypic discrimination. More generally, our results support the utility of social network analyses for analyzing behavioral factors affecting genetic exchange between populations and species.

Incorporating local adaptation into forecasts of species' distribution and abundance under climate change.

Populations of many species are genetically adapted to local historical climate conditions. Yet most forecasts of species' distributions under climate change have ignored local adaptation (LA), which may paint a false picture of how species will respond across their geographic ranges. We review recent studies that have incorporated intraspecific variation, a potential proxy for LA, into distribution forecasts, assess their strengths and weaknesses, and make recommendations for how to improve forecasts in the face of LA. The three methods used so far (species distribution models, response functions, and mechanistic models) reflect a trade-off between data availability and the ability to rigorously demonstrate LA to climate. We identify key considerations for incorporating LA into distribution forecasts that are currently missing from many published studies, including testing the spatial scale and pattern of LA, the confounding effects of LA to nonclimatic or biotic drivers, and the need to incorporate empirically based dispersal or gene flow processes. We suggest approaches to better evaluate these aspects of LA and their effects on species-level forecasts. In particular, we highlight demographic and dynamic evolutionary models as promising approaches to better integrate LA into forecasts, and emphasize the importance of independent model validation. Finally, we urge closer examination of how LA will alter the responses of central vs. marginal populations to allow stronger generalizations about changes in distribution and abundance in the face of LA.

Sea otters, kelp forests, and the extinction of Steller's sea cow.

The late Pleistocene extinction of so many large-bodied vertebrates has been variously attributed to two general causes: rapid climate change and the effects of humans as they spread from the Old World to previously uninhabited continents and islands. Many large-bodied vertebrates, especially large apex predators, maintain their associated ecosystems through top-down forcing processes, especially trophic cascades, and megaherbivores also exert an array of strong indirect effects on their communities. Thus, a third possibility for at least some of the Pleistocene extinctions is that they occurred through habitat changes resulting from the loss of these other keystone species. Here we explore the plausibility of this mechanism, using information on sea otters, kelp forests, and the recent extinction of Steller's sea cows from the Commander Islands. Large numbers of sea cows occurred in the Commander Islands at the time of their discovery by Europeans in 1741. Although extinction of these last remaining sea cows during early years of the Pacific maritime fur trade is widely thought to be a consequence of direct human overkill, we show that it is also a probable consequence of the loss of sea otters and the co-occurring loss of kelp, even if not a single sea cow had been killed directly by humans. This example supports the hypothesis that the directly caused extinctions of a few large vertebrates in the late Pleistocene may have resulted in the coextinction of numerous other species.

Both life-history plasticity and local adaptation will shape range-wide responses to climate warming in the tundra plant Silene acaulis.

Many predictions of how climate change will impact biodiversity have focused on range shifts using species-wide climate tolerances, an approach that ignores the demographic mechanisms that enable species to attain broad geographic distributions. But these mechanisms matter, as responses to climate change could fundamentally differ depending on the contributions of life-history plasticity vs. local adaptation to species-wide climate tolerances. In particular, if local adaptation to climate is strong, populations across a species' range-not only those at the trailing range edge-could decline sharply with global climate change. Indeed, faster rates of climate change in many high latitude regions could combine with local adaptation to generate sharper declines well away from trailing edges. Combining 15 years of demographic data from field populations across North America with growth chamber warming experiments, we show that growth and survival in a widespread tundra plant show compensatory responses to warming throughout the species' latitudinal range, buffering overall performance across a range of temperatures. However, populations also differ in their temperature responses, consistent with adaptation to local climate, especially growing season temperature. In particular, warming begins to negatively impact plant growth at cooler temperatures for plants from colder, northern populations than for those from warmer, southern populations, both in the field and in growth chambers. Furthermore, the individuals and maternal families with the fastest growth also have the lowest water use efficiency at all temperatures, suggesting that a trade-off between growth and water use efficiency could further constrain responses to forecasted warming and drying. Taken together, these results suggest that populations throughout species' ranges could be at risk of decline with continued climate change, and that the focus on trailing edge populations risks overlooking the largest potential impacts of climate change on species' abundance and distribution.

Wind and rain are the primary climate factors driving changing phenology of an aerial insectivore.

While the ecological effects of climate change have been widely observed, most efforts to document these impacts in terrestrial systems have concentrated on the impacts of temperature. We used tree swallow (Tachycineta bicolor) nest observations from two widely separated sites in central Alaska to examine the aspects of climate affecting breeding phenology at the northern extent of this species' range. We found that two measures of breeding phenology, annual lay and hatch dates, are more strongly predicted by windiness and precipitation than by temperature. At our longest-monitored site, breeding phenology has advanced at nearly twice the rate seen in more southern populations, and these changes correspond to long-term declines in windiness. Overall, adverse spring climate conditions known to negatively impact foraging success of swallows (wet, windy weather) appear to influence breeding phenology more than variation in temperature. Separate analyses show that short windy periods significantly delay initiation of individual clutches within years. While past reviews have emphasized that increasing variability in climate conditions may create physiological and ecological challenges for natural populations, we find that long-term reductions in inclement weather corresponded to earlier reproduction in one of our study populations. To better predict climate change impacts, ecologists need to more carefully test effects of multiple climate variables, including some, like windiness, that may be of paramount importance to some species, but have rarely been considered as strong drivers of ecological responses to climate alteration.

Portfolio effects, climate change, and the persistence of small populations: analyses on the rare plant Saussurea weberi.

The mechanisms that stabilize small populations in the face of environmental variation are crucial to their long-term persistence. Building from diversity-stability concepts in community ecology, within-population diversity is gaining attention as an important component of population stability. Genetic and microhabitat variation within populations can generate diverse responses to common environmental fluctuations, dampening temporal variability across the population as a whole through portfolio effects. Yet, the potential for portfolio effects to operate at small scales within populations or to change with systematic environmental shifts, such as climate change, remain largely unexplored. We tracked the abundance of a rare alpine perennial plant, Saussurea weberi, in 49 1-m2 plots within a single population over 20 yr. We estimated among-plot correlations in log annual growth rate to test for population-level synchrony and quantify portfolio effects across the 20-yr study period and also in 5-yr subsets based on June temperature quartiles. Asynchrony among plots, due to different plot-level responses to June temperature, reduced overall fluctuations in abundance and the probability of decline in population models, even when accounting for the effects of density dependence on dynamics. However, plots became more synchronous and portfolio effects decreased during the warmest years of the study, suggesting that future climate warming may erode stabilizing mechanisms in populations of this rare plant.

Varying demographic impacts of different fisheries on three Mediterranean seabird species.

Fisheries have an enormous economic importance, but reconciling their socio-economic features with the conservation and sustainability of marine ecosystems presents major challenges. Bycatch mortality from fisheries is clearly among the most serious global threats for marine ecosystems, affecting a wide range of top predators. Recent estimates report ca. 200,000 seabirds killed annually by bycatch in European waters. However, there is an urgent need to rigorously estimate actual mortality rates and quantify effects of bycatch on populations. The Mediterranean Sea is one of the most impacted regions. Here, we estimate for the first time both bycatch mortality rates and their population-level effects on three endemic and vulnerable Mediterranean taxa: Scopoli's shearwater, Mediterranean shag, and Audouin's gull, that die in different types of fishing gears: longlines, gillnets and sport trolling, respectively. We use multi-event capture-recapture modelling to estimate crucial demographic parameters, including the probabilities of dying in different fishing gears. We then build stochastic demography models to forecast the viability of the populations under different management scenarios. Longline bycatch was particularly severe for adults of Scopoli's shearwaters and Audouin's gulls (ca. 28% and 23% of total mortality, respectively) and also for immature gulls (ca. 90% of mortality). Gillnets had a lower impact, but were still responsible for ca. 9% of juvenile mortality on shags, whereas sport trolling only slightly influenced total mortality in gulls. Bycatch mortality has high population-level impacts in all three species, with shearwaters having the highest extinction risk under current mortality rates. Different life-history traits and compensatory demographic mechanisms between the three species are probably influencing the different bycatch impact: for shearwaters, urgent conservation actions are required to ensure the viability of their populations. Results will be very useful for guiding future seabird conservation policies and moving towards an ecosystem-based approach to sustainable fisheries management.

Demographic compensation and tipping points in climate-induced range shifts.

To persist, species are expected to shift their geographical ranges polewards or to higher elevations as the Earth's climate warms. However, although many species' ranges have shifted in historical times, many others have not, or have shifted only at the high-latitude or high-elevation limits, leading to range expansions rather than contractions. Given these idiosyncratic responses to climate warming, and their varied implications for species' vulnerability to climate change, a critical task is to understand why some species have not shifted their ranges, particularly at the equatorial or low-elevation limits, and whether such resilience will last as warming continues. Here we show that compensatory changes in demographic rates are buffering southern populations of two North American tundra plants against the negative effects of a warming climate, slowing their northward range shifts, but that this buffering is unlikely to continue indefinitely. Southern populations of both species showed lower survival and recruitment but higher growth of individual plants, possibly owing to longer, warmer growing seasons. Because of these and other compensatory changes, the population growth rates of southern populations are not at present lower than those of northern ones. However, continued warming may yet prove detrimental, as most demographic rates that improved in moderately warmer years declined in the warmest years, with the potential to drive future population declines. Our results emphasize the need for long-term, range-wide measurement of all population processes to detect demographic compensation and to identify nonlinear responses that may lead to sudden range shifts as climatic tipping points are exceeded.

Demographic compensation among populations: what is it, how does it arise and what are its implications?

Most species are exposed to significant environmental gradients across their ranges, but vital rates (survival, growth, reproduction and recruitment) need not respond in the same direction to those gradients. Opposing vital rate trends across environments, a phenomenon that has been loosely called 'demographic compensation', may allow species to occupy larger geographical ranges and alter their responses to climate change. Yet the term has never been precisely defined, nor has its existence or strength been assessed for multiple species. Here, we provide a rigorous definition, and use it to develop a strong test for demographic compensation. By applying the test to data from 26 published, multi-population demographic studies of plants, we show that demographic compensation commonly occurs. We also investigate the mechanisms by which this phenomenon arises by assessing which demographic processes and life stages are most often involved. In addition, we quantify the effect of demographic compensation on variation in population growth rates across environmental gradients, a potentially important determinant of the size of a species' geographical range. Finally, we discuss the implications of demographic compensation for the responses of single populations and species' ranges to temporal environmental variation and to ongoing environmental trends, e.g. due to climate change.

Lead poisoning and the deceptive recovery of the critically endangered California condor.

Endangered species recovery programs seek to restore populations to self-sustaining levels. Nonetheless, many recovering species require continuing management to compensate for persistent threats in their environment. Judging true recovery in the face of this management is often difficult, impeding thorough analysis of the success of conservation programs. We illustrate these challenges with a multidisciplinary study of one of the world's rarest birds-the California condor (Gymnogyps californianus). California condors were brought to the brink of extinction, in part, because of lead poisoning, and lead poisoning remains a significant threat today. We evaluated individual lead-related health effects, the efficacy of current efforts to prevent lead-caused deaths, and the consequences of any reduction in currently intensive management actions. Our results show that condors in California remain chronically exposed to harmful levels of lead; 30% of the annual blood samples collected from condors indicate lead exposure (blood lead ≥ 200 ng/mL) that causes significant subclinical health effects, measured as >60% inhibition of the heme biosynthetic enzyme δ-aminolevulinic acid dehydratase. Furthermore, each year, ∼20% of free-flying birds have blood lead levels (≥450 ng/mL) that indicate the need for clinical intervention to avert morbidity and mortality. Lead isotopic analysis shows that lead-based ammunition is the principle source of lead poisoning in condors. Finally, population models based on condor demographic data show that the condor's apparent recovery is solely because of intensive ongoing management, with the only hope of achieving true recovery dependent on the elimination or substantial reduction of lead poisoning rates.

Mechanisms of plant-plant interactions: concealment from herbivores is more important than abiotic-stress mediation in an African savannah.

Recent work on facilitative plant-plant interactions has emphasized the importance of neighbours' amelioration of abiotic stress, but the facilitative effects of neighbours in reducing plant apparency to herbivores have received less attention. Whereas theory on stress reduction predicts that competition should be more important in less stressful conditions, with facilitation becoming more important in harsh environments, apparency theory suggests that facilitation should be greater in the presence of herbivores, where it is disadvantageous to be conspicuous regardless of abiotic stress level. We tested the relative strength of neighbours' stress reduction versus apparency reduction on survival, growth, reproduction and lifetime fitness of Hibiscus meyeri, a common forb in central Kenya, using neighbour removals conducted inside and outside large-herbivore exclosures replicated in arid and mesic sites. In the absence of herbivores, neighbours competed with H. meyeri in mesic areas and facilitated H. meyeri in arid areas, as predicted by stress-reduction mechanisms. By contrast, neighbours facilitated H. meyeri in the presence of herbivory, regardless of aridity level, consistent with plant apparency. Our results show that the facilitative effects arising from plant apparency are stronger than the effects arising from abiotic stress reduction in this system, suggesting that plant-apparency effects may be particularly important in systems with extant large-herbivore communities.