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.

Demographic responses of hybridizing cinquefoils to changing climate in the Colorado Rocky Mountains.

Hybridization between taxa generates new pools of genetic variation that can lead to different environmental responses and demographic trajectories over time than seen in parental lineages. The potential for hybrids to have novel environmental tolerances may be increasingly important in mountainous regions, which are rapidly warming and drying due to climate change. Demographic analysis makes it possible to quantify within- and among-species responses to variation in climate and to predict population growth rates as those conditions change. We estimated vital rates and population growth in 13 natural populations of two cinquefoil taxa (Potentilla hippiana and P. pulcherrima) and their hybrid across elevation gradients in the Southern Rockies. Using three consecutive years of environmental and demographic data, we compared the demographic responses of hybrid and parental taxa to environmental variation across space and time. All three taxa had lower predicted population growth rates under warm, dry conditions. However, the magnitude of these responses varied among taxa and populations. Hybrids had consistently lower predicted population growth rates than P. hippiana. In contrast, hybrid performance relative to P. pulcherrima varied with population and climate, with the hybrid maintaining relatively stable growth rates while populations of P. pulcherrima shrank under warm, dry conditions. Our findings demonstrate that hybrids in this system are neither intrinsically unfit nor universally more vigorous than parents, suggesting that the demographic consequences of hybridization are context-dependent. Our results also imply that shifts to warmer and drier conditions could have particularly negative repercussions for P. pulcherrima, which is currently the most abundant taxon in the study area, possibly as a legacy of more favorable historical climates. More broadly, the distributions of these long-lived taxa are lagging behind their demographic trajectories, such that the currently less common P. hippiana could become the most abundant of the Potentilla taxa as this region continues to warm and dry.

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.

Genetically based demographic reconstructions require careful consideration of generation time.

Bakker et al. use Robinson et al.'s reconstruction of three species of vulture to illustrate how incorrect generation time estimates can yield inaccurate results, underscoring the importance of generation time specification for genetically based reconstructions, especially for comparisons and species of conservation concern.

Demographic consequences of mutualism disruption: Browsing and big-headed ant invasion drive acacia population declines.

Across the globe, biological invasions have disrupted mutualisms, producing reverberating consequences for ecosystems. Although invasive species frequently trigger mutualism disruptions, few studies have quantified the demographic mechanisms by which mutualism breakdown may generate population effects. In a Kenyan savanna, the invasive big-headed ant (Pheidole megacephala) has disrupted a foundational mutualism between the monodominant whistling-thorn tree (Acacia drepanolobium) and native ants (Crematogaster spp.) that deter browsing by large mammalian herbivores. We conducted experiments to quantify the demographic consequences of this mutualism disruption in the presence and absence of large mammalian herbivores. Invasion by P. megacephala exacerbated population declines of A. drepanolobium, primarily through decreased survival and reproduction of adult trees. However, these fitness reductions were small compared to those resulting from the presence of large mammalian herbivores, which negatively impacted growth and survival. Contrary to expectation, the expulsion of metabolically costly Crematogaster mutualists by P. megacephala did not result in higher population growth rates for trees protected from large mammalian herbivores. Our results suggest that invasive P. megacephala may impose a direct metabolic cost to trees exceeding that of native mutualists while providing no protection from browsing by large mammalian herbivores. Across landscapes, we expect that invasion by P. megacephala will reduce A. drepanolobium populations, but that the magnitude and demographic pathways of this effect will hinge on the presence and abundance of browsers.

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.

Climate warming threatens the persistence of a community of disturbance-adapted native annual plants.

With ongoing climate change, populations are expected to exhibit shifts in demographic performance that will alter where a species can persist. This presents unique challenges for managing plant populations and may require ongoing interventions, including in situ management or introduction into new locations. However, few studies have examined how climate change may affect plant demographic performance for a suite of species, or how effective management actions could be in mitigating climate change effects. Over the course of two experiments spanning 6 yr and four sites across a latitudinal gradient in the Pacific Northwest, United States, we manipulated temperature, precipitation, and disturbance intensity, and quantified effects on the demography of eight native annual prairie species. Each year we planted seeds and monitored germination, survival, and reproduction. We found that disturbance strongly influenced demographic performance and that seven of the eight species had increasingly poor performance with warmer conditions. Across species and sites, we observed 11% recruitment (the proportion of seeds planted that survived to reproduction) following high disturbance, but just 3.9% and 2.3% under intermediate and low disturbance, respectively. Moreover, mean seed production following high disturbance was often more than tenfold greater than under intermediate and low disturbance. Importantly, most species exhibited precipitous declines in their population growth rates (λ) under warmer-than-ambient experimental conditions and may require more frequent disturbance intervention to sustain populations. Aristida oligantha, a C4 grass, was the only species to have λ increase with warmer conditions. These results suggest that rising temperatures may cause many native annual plant species to decline, highlighting the urgency for adaptive management practices that facilitate their restoration or introduction to newly suitable locations. Frequent and intense disturbances are critical to reduce competitors and promote native annuals' persistence, but even such efforts may prove futile under future climate regimes.

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.

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.

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.

Breeding transients in capture-recapture modeling and their consequences for local population dynamics.

Standard procedures for capture-mark-recapture modelling (CMR) for the study of animal demography include running goodness-of-fit tests on a general starting model. A frequent reason for poor model fit is heterogeneity in local survival among individuals captured for the first time and those already captured or seen on previous occasions. This deviation is technically termed a transience effect. In specific cases, simple, uni-state CMR modeling showing transients may allow researchers to assess the role of these transients on population dynamics. Transient individuals nearly always have a lower local survival probability, which may appear for a number of reasons. In most cases, transients arise due to permanent dispersal, higher mortality, or a combination of both. In the case of higher mortality, transients may be symptomatic of a cost of first reproduction. A few studies working at large spatial scales actually show that transients more often correspond to survival costs of first reproduction rather than to permanent dispersal, bolstering the interpretation of transience as a measure of costs of reproduction, since initial detections are often associated with first breeding attempts. Regardless of their cause, the loss of transients from a local population should lower population growth rate. We review almost 1000 papers using CMR modeling and find that almost 40% of studies fitting the searching criteria (N = 115) detected transients. Nevertheless, few researchers have considered the ecological or evolutionary meaning of the transient phenomenon. Only three studies from the reviewed papers considered transients to be a cost of first reproduction. We also analyze a long-term individual monitoring dataset (1988-2012) on a long-lived bird to quantify transients, and we use a life table response experiment (LTRE) to measure the consequences of transients at a population level. As expected, population growth rate decreased when the environment became harsher while the proportion of transients increased. LTRE analysis showed that population growth can be substantially affected by changes in traits that are variable under environmental stochasticity and deterministic perturbations, such as recruitment, fecundity of experienced individuals, and transient probabilities. This occurred even though sensitivities and elasticities of these parameters were much lower than those for adult survival. The proportion of transients also increased with the strength of density-dependence. These results have implications for ecological and evolutionary studies and may stimulate other researchers to explore the ecological processes behind the occurrence of transients in capture-recapture studies. In population models, the inclusion of a specific state for transients may help to make more reliable predictions for endangered and harvested species.

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.

Asynchrony in individual and subpopulation fecundity stabilizes reproductive output of an alpine plant population.

Population-wide outcomes such as abundance, reproductive output, or mean survival can be stabilized by non-synchronous variation in the performance of individuals or subpopulations. Such "portfolio effects" have been increasingly documented at the scale of subpopulations and are thought to play an important role in generating stability of population phenomena in the face of environmental variation. However, few studies quantify the strength and origin of portfolio effects at the finer scale of individuals. We used 16 yr of fruit production and climate data for an alpine plant to dissect the scale of portfolio effects in reproduction, as well as the contribution of individual traits including size and flowering time in driving reproductive output. Asynchrony in reproductive success substantially reduces variation in population-level reproductive output, with approximately one-fourth of this stabilizing effect arising from individual differences, mostly not those characterized by measured traits, and approximately three-fourths from asynchrony across subpopulations. These results emphasize the different scales and causes of portfolio effects. The decomposition for portfolio effects we provide can facilitate similar breakdowns of the strength and causes of these effects in other systems.

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.

Ecological Function Analysis: Incorporating Species Roles into Conservation.

Effective conservation strategies must ensure that species remain not just extant, but able to maintain key roles in species interactions and in the maintenance of communities and ecosystems. Such ecological functions, however, have not been well incorporated into management or policy. We present a framework for quantifying ecological function that is complementary to population viability analysis (PVA) and that allows function to be integrated into strategic planning processes. Ecological function analysis (EFA) focuses on preventing secondary extinctions and maintaining ecosystem structure, biogeochemical processes, and resiliency. EFA can use a range of modeling approaches and, because most species interactions are relatively weak, EFA needs to be performed for relatively few species or functions, making it a realistic way to improve conservation management.

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.

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.