Incorporating plant phenological responses into species distribution models reduces estimates of future species loss and turnover.

Anthropogenetic climate change has caused range shifts among many species. Species distribution models (SDMs) are used to predict how species ranges may change in the future. However, most SDMs rarely consider how climate-sensitive traits, such as phenology, which affect individuals' demography and fitness, may influence species' ranges. Using > 120 000 herbarium specimens representing 360 plant species distributed across the eastern United States, we developed a novel 'phenology-informed' SDM that integrates phenological responses to changing climates. We compared the ranges of each species forecast by the phenology-informed SDM with those from conventional SDMs. We further validated the modeling approach using hindcasting. When examining the range changes of all species, our phenology-informed SDMs forecast less species loss and turnover under climate change than conventional SDMs. These results suggest that dynamic phenological responses of species may help them adjust their ecological niches and persist in their habitats as the climate changes. Plant phenology can modulate species' responses to climate change, mitigating its negative effects on species persistence. Further application of our framework will contribute to a generalized understanding of how traits affect species distributions along environmental gradients and facilitate the use of trait-based SDMs across spatial and taxonomic scales.

Comparing two spatial variables with the probability of agreement.

Computing the agreement between 2 continuous sequences is of great interest in statistics when comparing 2 instruments or one instrument with a gold standard. The probability of agreement quantifies the similarity between 2 variables of interest, and it is useful for determining what constitutes a practically important difference. In this article, we introduce a generalization of the PA for the treatment of spatial variables. Our proposal makes the PA dependent on the spatial lag. We establish the conditions for which the PA decays as a function of the distance lag for isotropic stationary and nonstationary spatial processes. Estimation is addressed through a first-order approximation that guarantees the asymptotic normality of the sample version of the PA. The sensitivity of the PA with respect to the covariance parameters is studied for finite sample size. The new method is described and illustrated with real data involving autumnal changes in the green chromatic coordinate (Gcc), an index of "greenness" that captures the phenological stage of tree leaves, is associated with carbon flux from ecosystems, and is estimated from repeated images of forest canopies.

Logging response alters trajectories of reorganization after loss of a foundation tree species.

Forest insect outbreaks cause large changes in ecosystem structure, composition, and function. Humans often respond to insect outbreaks by conducting salvage logging, which can amplify the immediate effects, but it is unclear whether logging will result in lasting differences in forest structure and dynamics when compared with forests affected only by insect outbreaks. We used 15 years of data from an experimental removal of Tsuga canadensis (L.) Carr. (Eastern hemlock), a foundation tree species within eastern North American forests, and contrasted the rate, magnitude, and persistence of response trajectories between girdling (emulating mortality from insect outbreak) and timber harvest treatments. Girdling and logging were equally likely to lead to large changes in forest structure and dynamics, but logging resulted in faster rates of change. Understory light increases and community composition changes were larger and more rapid in the logged plots. Tree seedling and understory vegetation abundance increased more in the girdled plots; this likely occurred because seedlings grew rapidly into the sapling- and tree-size classes after logging and quickly shaded out plants on the forest floor. Downed deadwood pools increased more after logging but standing deadwood pools increased dramatically after girdling. Understory light levels remained elevated for a longer time after girdling. Perhaps because the window of opportunity for understory species to establish was longer in the girdled plots, total species richness increased more in the girdled than logged plots. Despite the potential for greater diversity in the girdled plots, Betula lenta L. (black birch) was the most abundant tree species recruited into the sapling- and tree-size classes in both the girdled and logged plots and is poised to dominate the new forest canopy. The largest difference between the girdling and logging treatments-deadwood structure and quantity-will persist and continue to bolster aboveground carbon storage and structural and habitat diversity in the girdled plots. Human responses to insect outbreaks hasten forest reorganization and remove structural resources that may further alter forest response to ongoing climate stress and future disturbances.

Complex climate-mediated effects of urbanization on plant reproductive phenology and frost risk.

Urbanization can affect the timing of plant reproduction (i.e. flowering and fruiting) and associated ecosystem processes. However, our knowledge of how plant phenology responds to urbanization and its associated environmental changes is limited. Herbaria represent an important, but underutilized source of data for investigating this question. We harnessed phenological data from herbarium specimens representing 200 plant species collected across 120 yr from the eastern US to investigate the spatiotemporal effects of urbanization on flowering and fruiting phenology and frost risk (i.e. time between the last frost date and flowering). Effects of urbanization on plant reproductive phenology varied significantly in direction and magnitude across species ranges. Increased urbanization led to earlier flowering in colder and wetter regions and delayed fruiting in regions with wetter spring conditions. Frost risk was elevated with increased urbanization in regions with colder and wetter spring conditions. Our study demonstrates that predictions of phenological change and its associated impacts must account for both climatic and human effects, which are context dependent and do not necessarily coincide. We must move beyond phenological models that only incorporate temperature variables and consider multiple environmental factors and their interactions when estimating plant phenology, especially at larger spatial and taxonomic scales.

Induced drought strongly affects richness and composition of ground-dwelling ants in the eastern Amazon.

Species loss in tropical regions is forecast to occur under environmental change scenarios of low precipitation. One of the main questions is how drought will affect invertebrates, a key group for ecosystem functioning. We use 1 year of data from a long-term rainwater exclusion experiment in primary Amazonian rainforest to test whether induced water stress and covarying changes in soil moisture, soil respiration, and tree species richness, diversity, size, and total biomass affected species richness and composition (relative abundance) of ground-dwelling ants. Data on ant abundance and environmental variables were collected at two sites (control and experimental) in the Eastern Amazon. Since 2002, drought has been induced in the experimental plot by excluding 50% of normal rainfall. Ant species richness in the experiment plot was reduced and some generalist species responded positively. Ant species richness also increased in the experimental plot with increasing diversity of the plant species of the leaf litter. The relative abundance of ants differed between plots. The experimental plot was characterized by a higher frequency of generalist and other species that appeared to be favored by the reduction in rainfall. Between-plot comparisons suggested loss and changes in ant species composition in tropical forests were affected by increasing dryness. These changes could ultimately lead to cascading effects on ecosystem processes and the services they mediate.

Phenological displacement is uncommon among sympatric angiosperms.

Interactions between species can influence successful reproduction, resulting in reproductive character displacement, where the similarity of reproductive traits - such as flowering time - among close relatives growing together differ from when growing apart. Evidence for the overall prevalence and direction of this phenomenon, and its stability under environmental change, remains untested across large scales. Using the power of crowdsourcing, we gathered phenological information from over 40 000 herbarium specimens, and investigated displacement in flowering time across 110 animal-pollinated species in the eastern USA. Overall, flowering time displacement is not common across large scales. However, displacement is generally greater among species pairs that flower close in time, regardless of direction. Furthermore, with climate change, the flowering times of closely related species are predicted, on average, to shift further apart by the mid-21st century. We demonstrate that the degree and direction of phenological displacement among co-occurring closely related species pairs varies tremendously. However, future climate change may alter the differences in reproductive timing among many of these species pairs, which may have significant consequences for species interactions and gene flow. Our study provides one promising path towards understanding how the phenological landscape is structured and may respond to future environmental change.

Clockwise and counterclockwise hysteresis characterize state changes in the same aquatic ecosystem.

Incremental increases in a driver variable, such as nutrients or detritus, can trigger abrupt shifts in aquatic ecosystems that may exhibit hysteretic dynamics and a slow return to the initial state. A model system for understanding these dynamics is the microbial assemblage that inhabits the cup-shaped leaves of the pitcher plant Sarracenia purpurea. With enrichment of organic matter, this system flips within three days from an oxygen-rich state to an oxygen-poor state. In a replicated greenhouse experiment, we enriched pitcher-plant leaves at different rates with bovine serum albumin (BSA), a molecular substitute for detritus. Changes in dissolved oxygen (DO) and undigested BSA concentration were monitored during enrichment and recovery phases. With increasing enrichment rates, the dynamics ranged from clockwise hysteresis (low), to environmental tracking (medium), to novel counter-clockwise hysteresis (high). These experiments demonstrate that detrital enrichment rate can modulate a diversity of hysteretic responses within a single aquatic ecosystem, and suggest different management strategies may be needed to mitigate the effects of high vs. low rates of detrital enrichment.

Broadening the ecological mindset.

Over the past three decades, the Harvard Forest Summer Research Program in Ecology (HF-SRPE) has been at the forefront of expanding the ecological tent for minoritized or otherwise marginalized students. By broadening the definition of ecology to include fields such as data science, software engineering, and remote sensing, we attract a broader range of students, including those who may not prioritize field experiences or who may feel unsafe working in rural or urban field sites. We also work towards a more resilient society in which minoritized or marginalized students can work safely, in part by building teams of students and mentors. Teams collaborate on projects that require a diversity of approaches and create opportunities for students and mentors alike to support one another and share leadership. Finally, HF-SRPE promotes an expanded view of what it means to become an ecologist. We value and support diverse career paths for ecologists to work in all parts of society, to diversify the face of ecology, and to bring different perspectives together to ensure innovations in environmental problem solving for our planet.

Trade-Offs in Cold Resistance at the Northern Range Edge of the Common Woodland Ant Aphaenogaster picea (Formicidae).

Geographic variation in low temperatures at poleward range margins of terrestrial species often mirrors population variation in cold resistance, suggesting that range boundaries may be set by evolutionary constraints on cold physiology. The northeastern woodland ant Aphaenogaster picea occurs up to approximately 45°N in central Maine. We combined presence/absence surveys with classification tree analysis to characterize its northern range limit and assayed two measures of cold resistance operating on different timescales to determine whether and how marginal populations adapt to environmental extremes. The range boundary of A. picea was predicted primarily by temperature, but low winter temperatures did not emerge as the primary correlate of species occurrence. Low summer temperatures and high seasonal variability predicted absence above the boundary, whereas high mean annual temperature (MAT) predicted presence in southern Maine. In contrast, assays of cold resistance across multiple sites were consistent with the hypothesis of local cold adaptation at the range edge: among populations, there was a 4-min reduction in chill coma recovery time across a 2° reduction in MAT. Baseline resistance and capacity for additional plastic cold hardening shifted in opposite directions, with hardening capacity approaching zero at the coldest sites. This trade-off between baseline resistance and cold-hardening capacity suggests that populations at range edges may adapt to colder temperatures through genetic assimilation of plastic responses, potentially constraining further adaptation and range expansion.

Species interactions slow warming-induced upward shifts of treelines on the Tibetan Plateau.

The alpine treeline is commonly regarded as being sensitive to climatic warming because regeneration and growth of trees at treeline generally are limited by low temperature. The alpine treelines of the Tibetan Plateau (TP) occur at the highest elevations (4,900 m above sea level) in the Northern Hemisphere. Ongoing climatic warming is expected to shift treelines upward. Studies of treeline dynamics at regional and local scales, however, have yielded conflicting results, indicating either unchanging treeline elevations or upward shifts. To reconcile this conflict, we reconstructed in detail a century of treeline structure and tree recruitment at sites along a climatic gradient of 4 °C and mean annual rainfall of 650 mm on the eastern TP. Species interactions interacted with effects of warming on treeline and could outweigh them. Densification of shrubs just above treeline inhibited tree establishment, and slowed upward movement of treelines on a time scale of decades. Interspecific interactions are major processes controlling treeline dynamics that may account for the absence of an upward shift at some TP treelines despite continued climatic warming.

Frost controls spring phenology of juvenile Smith fir along elevational gradients on the southeastern Tibetan Plateau.

Impacts of climatic means on spring phenology are well documented, whereas the role of climatic variance, such as occurrence of spring frosts, has long been neglected. A large elevational gradient of forests on the southeastern Tibetan Plateau provides an ideal platform to explore correlates of spring phenology and environmental factors. We tested the hypothesis that spring frost was a major factor regulating the timing of bud-leaf phenology by combining 5 years of in situ phenological observations of Abies georgei var. smithii with concurrent air temperature data along two altitudinal gradients. Mean lapse rate for the onset of bud swelling and leaf unfolding was 3.1 ± 0.5 days/100 m and 3.0 ± 0.6 days/100 m, respectively. Random forest analysis and conditional inference trees revealed that the frequency of freezing events was a critical factor in determining the timing of bud swelling, independent of topographic differences, varying accumulation of chilling days, and degree-days. In contrast, the onset of leaf unfolding was primarily controlled by the bud swelling onset. Thus, the timing of bud swelling and leaf unfolding appear to be controlled directly and indirectly, respectively, by spring frost. Using space-for-time substitution, the frequency of spring freezing events decreased by 7.1 days with 1 °C of warming. This study provides evidence for impacts of late spring frosts on spring phenology, which have been underappreciated in research on phenological sensitivity to climate but should be included in phenology models. Fewer spring freezing events with warming have important implications for the upward migration of alpine forests and treelines.

Widespread sampling biases in herbaria revealed from large-scale digitization.

Nonrandom collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases. We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE). We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via 'founder effects'. Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.

Critical temperature and precipitation thresholds for the onset of xylogenesis of Juniperus przewalskii in a semi-arid area of the north-eastern Tibetan Plateau.

Background and Aims: The onset of xylogenesis plays an important role in tree growth and carbon sequestration, and it is thus a key variable in modelling the responses of forest ecosystems to climate change. Temperature regulates the resumption of cambial activity, but little is known about the effect of water availability on the onset of xylogenesis in cold but semi-arid regions. Methods: The onset of xylogenesis during 2009-2014 was monitored by weekly microcoring Juniperus przewalskii trees at upper and lower treelines on the north-eastern Tibetan Plateau. A logistic regression was used to calculate the probability of xylogenic activity at a given temperature and a two-dimensional reverse Gaussian model to fit the differences between the observed and estimated days of xylogenesis onset at given temperatures and precipitation within a certain time window. Key Results: The thermal thresholds at the beginning of the growing season were highly variable, suggesting that temperature was not the only factor initiating xylem growth under cold and dry climatic conditions. The onset of xylogenesis was well predicted for climatic thresholds characterized by a cumulative precipitation of 17.0 ± 5.6 mm and an average minimum temperature of 1.5 ± 1.4 °C for a period of 12 d. Conclusions: Xylogenesis in semi-arid regions with dry winters and springs can start when both critical temperature and precipitation thresholds are reached. Such findings contribute to our knowledge of the environmental drivers of growth resumption that previously had been investigated largely in cold regions without water shortages during early growing seasons. Models of the onset of xylogenesis should include water availability to improve predictions of xylem phenology in dry areas. A mismatch between the thresholds of temperature and moisture for the onset of xylogenesis may increase forest vulnerability in semi-arid areas under forecasted warmer and drier conditions.

Environmental toxicants impair liver and kidney function and sperm quality of captive pandas.

Captive pandas are exposed to higher concentrations of environmental toxins in their food source and from atmospheric pollution than wild pandas. Moreover, the Qinling panda subspecies had significantly higher concentrations of toxic chemicals in its feces. To determine whether these toxicants also accumulate in panda's blood and impair its health, concentrations of persistent organic pollutants (POPs) and heavy metals were measured in blood samples. Four heavy metals (As, Cd, Cr and Pb), PCDD/Fs and PCBs were detected in blood drawn from captive Qinling pandas. Time spent in captivity was a better predictor of toxicant concentration accumulation than was panda age. More than 50% of the studied pandas were outside the normal levels for 11 health parameters, and five (ALT, LDH, Ca, Cl, TB) of the 11 parameters classified as abnormal were correlated with blood pollutant concentrations. The proportion of live sperm was significantly lower and the aberrance ratio of sperm was significantly greater for captive pandas than for wild ones. A short-term solution to reduce the health impacts of pollution and toxicant exposure of Qinling pandas is to relocate breeding centers to less contaminated areas and to strictly control the quality of their food provided. A longer term solution depends on improving air quality by reducing toxic emissions.

A global database of ant species abundances.

What forces structure ecological assemblages? A key limitation to general insights about assemblage structure is the availability of data that are collected at a small spatial grain (local assemblages) and a large spatial extent (global coverage). Here, we present published and unpublished data from 51 ,388 ant abundance and occurrence records of more than 2,693 species and 7,953 morphospecies from local assemblages collected at 4,212 locations around the world. Ants were selected because they are diverse and abundant globally, comprise a large fraction of animal biomass in most terrestrial communities, and are key contributors to a range of ecosystem functions. Data were collected between 1949 and 2014, and include, for each geo-referenced sampling site, both the identity of the ants collected and details of sampling design, habitat type, and degree of disturbance. The aim of compiling this data set was to provide comprehensive species abundance data in order to test relationships between assemblage structure and environmental and biogeographic factors. Data were collected using a variety of standardized methods, such as pitfall and Winkler traps, and will be valuable for studies investigating large-scale forces structuring local assemblages. Understanding such relationships is particularly critical under current rates of global change. We encourage authors holding additional data on systematically collected ant assemblages, especially those in dry and cold, and remote areas, to contact us and contribute their data to this growing data set.

Atmospheric deposition exposes Qinling pandas to toxic pollutants.

The giant panda (Ailuropoda melanoleuca) is one of the most endangered animals in the world, and it is recognized worldwide as a symbol for conservation. A previous study showed that wild and captive pandas, especially those of the Qinling subspecies, were exposed to toxicants in their diet of bamboo; the ultimate origin of these toxicants is unknown. Here we show that atmospheric deposition is the most likely origin of heavy metals and persistent organic pollutants (POPs) in the diets of captive and wild Qinling pandas. Average atmospheric deposition was 199, 115, and 49 g·m-2 ·yr-1 in the center of Xi'an City, at China's Shaanxi Wild Animal Research Center (SWARC), and at Foping National Nature Reserve (FNNR), respectively. Atmospheric deposition of heavy metals (As, Cd, Cr, Pb, Hg, Co, Cu, Zn, Mn, and Ni) and POPs was highest at Xi'an City, intermediate at SWARC, and lowest at FNNR. Soil concentrations of the aforementioned heavy metals other than As and Zn also were significantly higher at SWARC than at FNNR. Efforts to conserve Qinling pandas may be compromised by air pollution attendant to China's economic development. Improvement of air quality and reductions of toxic emissions are urgently required to protect China's iconic species.

Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species.

BACKGROUND: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism's transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. RESULTS: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. CONCLUSIONS: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.

Using codispersion analysis to quantify and understand spatial patterns in species-environment relationships.

The analysis of spatial patterns in species-environment relationships can provide new insights into the niche requirements and potential co-occurrence of species, but species abundance and environmental data are routinely collected at different spatial scales. Here, we investigate the use of codispersion analysis to measure and assess the scale, directionality and significance of complex relationships between plants and their environment in large forest plots. We applied codispersion analysis to both simulated and field data on spatially located tree species basal area and environmental variables. The significance of the observed bivariate spatial associations between the basal area of key species and underlying environmental variables was tested using three null models. Codispersion analysis reliably detected directionality (anisotropy) in bivariate species-environment relationships and identified relevant scales of effects. Null model-based significance tests applied to codispersion analyses of forest plot data enabled us to infer the extent to which environmental conditions, tree sizes and/or tree spatial positions underpinned the observed basal area-environment relationships, or whether relationships were a result of other unmeasured factors. Codispersion analysis, combined with appropriate null models, can be used to infer hypothesized ecological processes from spatial patterns, allowing us to start disentangling the possible drivers of plant species-environment relationships.

Using codispersion analysis to characterize spatial patterns in species co-occurrences.

Visualizing and quantifying spatial patterns of co-occurrence (i.e., of two or more species, or of species and underlying environmental variables) can suggest hypotheses about processes that structure species assemblages and their relevant spatial scales. Statistical models of spatial co-occurrence generally assume that underlying spatial processes are isotropic and stationary, but many ecologically realistic spatial processes are anisotropic and non-stationary. Here, we introduce codispersion analysis to ecologists and use it to detect and quantify anisotropic and nonstationary patterns and their relevant spatial scales in bivariate co-occurrence data. Simulated data illustrated that codispersion analysis can accurately characterize complex spatial patterns. Analysis of co-occurrence of common tree species growing in a 35-ha plot revealed both positive and negative codispersion between different species; positive codispersion values reflected positive correlation in species abundance (aggregation), whereas negative codispersion values reflected negative correlation in species abundance (segregation). Comparisons of observed patterns with those simulated using two different null models showed that the codispersion of most species pairs differed significantly from random expectation. We conclude that codispersion analysis can be a useful exploratory tool to guide ecologists interested in modeling spatial processes.