Phenological tracking enables positive species responses to climate change

Earlier spring phenology observed in many plant species in recent decades provides compelling evidence that species are already responding to the rising global temperatures associated with anthropogenic climate change. There is great variability among species, however, in their phenological sensitivity to temperature. Species that do not phenologically "track" climate change may be at a disadvantage if their growth becomes limited by missed interactions with mutualists, or a shorter growing season relative to earlier-active competitors. Here, we set out to test the hypothesis that phenological sensitivity could be used to predict species performance in a warming climate, by synthesizing results across terrestrial warming experiments. We assembled data for 57 species across 24 studies where flowering or vegetative phenology was matched with a measure of species performance. Performance metrics included biomass, percent cover, number of flowers, or individual growth. We found that species that advanced their phenology with warming also increased their performance, whereas those that did not advance tended to decline in performance with warming. This indicates that species that cannot phenologically "track" climate may be at increased risk with future climate change, and it suggests that phenological monitoring may provide an important tool for setting future conservation priorities.     

Vulnerability of the northern Mongolian steppe to climate change: insights from flower production and phenology

The semiarid, northern Mongolian steppe, which still supports pastoral nomads who have used the steppe for millennia, has experienced an average 1.7 degrees C temperature rise over the past 40 years. Continuing climate change is likely to affect flowering phenology and flower numbers with potentially important consequences for plant community composition, ecosystem services, and herder livelihoods. Over the growing seasons of 2009 and 2010, we examined flowering responses to climate manipulation using open-top passive warming chambers (OTCs) at two locations on a south-facing slope: one on the moister, cooler lower slope and the other on the drier, warmer upper slope, where a watering treatment was added in a factorial design with warming. Canonical analysis of principal coordinates (CAP) revealed that OTCs reduced flower production and delayed peak flowering in graminoids as a whole but only affected forbs on the upper slope, where peak flowering was also delayed. OTCs affected flowering phenology in seven of eight species, which were examined individually, either by altering the time of peak flowering and/or the onset and/or cessation of flowering, as revealed by survival analysis. In 2010, which was the drier year, OTCs reduced flower production in two grasses but increased production in an annual forb found only on the upper slope. The particular effects of OTCs on phenology, and whether they caused an extension or contraction of the flowering season, differed among species, and often depended on year, or slope, or watering treatment; however, a relatively strong pattern emerged for 2010 when four species showed a contraction of the flowering season in OTCs. Watering increased flower production in two species in 2010, but slope location more often affected flowering phenology than did watering. Our results show the importance of taking landscape-scale variation into account in climate change studies and also contrasted with those of several studies set in cold, but wetter systems, where warming often causes greater or accelerated flower production. In cold, water-limited systems like the Mongolian steppe, warming may reduce flower numbers or the length of the flowering season by adding to water stress more than it relieves cold stress.     

Species' traits predict phenological responses to climate change in butterflies

How do species' traits help identify which species will respond most strongly to future climate change? We examine the relationship between species' traits and phenology in a well-established model system for climate change, the U.K. Butterfly Monitoring Scheme (UKBMS). Most resident U.K. butterfly species have significantly advanced their dates of first appearance during the past 30 years. We show that species with narrower larval diet breadth and more advanced overwintering stages have experienced relatively greater advances in their date of first appearance. In addition, species with smaller range sizes have experienced greater phenological advancement. Our results demonstrate that species' traits can be important predictors of responses to climate change, and they suggest that further investigation of the mechanisms by which these traits influence phenology may aid in understanding species' responses to current and future climate change.     

Antagonistic effect of natural habitat conversion on community adjustment to climate warming in nonbreeding waterbirds

Although the impacts of climate and land-use changes on biodiversity have been widely documented, their joint effects remain poorly understood. We evaluated how nonbreeding waterbird communities adjust to climate warming along a gradient of land-use change. Using midwinter waterbird counts (132 species) at 164 major nonbreeding sites in 22 Mediterranean countries, we assessed the changes in species composition from 1991 to 2010, relative to thermal niche position and breadth, in response to regional and local winter temperature anomalies and conversion of natural habitats. We observed a low-level, nonsignificant community adjustment to the temperature increase where natural habitat conversion occurred. At the sites affected by natural habitat conversion, the relative increase of warm-dwelling species in response to climate warming was 6 times lower and the relative species decline was 3 times higher than in the sites without natural habitat conversion. We found no evidence of community adjustment to climate warming when natural habitat conversion was >5% over 15 years. This strong negative effect suggests an antagonistic interaction between climate warming and habitat change. These results underline the importance of habitat conservation in community adjustment to climate warming.     

Soil nutrient supply modulates temperature-induction cues in mast-seeding grasses

Synchronous and intermittent reproduction in long-lived plants, known as mast seeding, is induced by climatic cues, but the mechanism explaining variation in masting among neighboring but edaphically segregated species is unknown. Soil nutrients can enhance flowering, and thus, populations on nutrient-rich soils may require less-favorable growing temperatures to flower. We tested this hypothesis by predicting the probability of flowering in response to air temperature for five species of alpine Chionochloa grasses in South Island, New Zealand, over 37 years and relating our predictions to soil N supply (NH4(+) + NO3(-)). Summer air temperatures better predicted flowering than spring air temperatures, which were correlated with soil N mineralization. Species on N-rich soils required lower mean temperatures to induce flowering and/or responded more consistently across a gradient of air temperatures, contributing to the higher probability of their tillers and tussocks flowering at low summer temperatures. Our results suggest that flowering primarily occurs in response to warm summer temperatures, but species on N-rich soils require less favorable growing conditions because they invest relatively less N in seeds. Thus, predicting masting requires a consideration of the interactions among climate, the internal resources of plants, and mineral nutrient uptake.     

Climate heterogeneity modulates impact of warming on tropical insects

Evolutionary history and physiology mediate species responses to climate change. Tropical species that do not naturally experience high temperature variability have a narrow thermal tolerance compared to similar taxa at temperate latitudes and could therefore be most vulnerable to warming. However, the thermal adaptation of a species may also be influenced by spatial temperature variations over its geographical range. Spatial climate gradients, especially from topography, may also broaden thermal tolerance and therefore act to buffer warming impacts. Here we show that for low-seasonality environments, high spatial heterogeneity in temperature correlates significantly with greater warming tolerance in insects globally. Based on this relationship, we find that climate change projections of direct physiological impacts on insect fitness highlight the vulnerability of tropical lowland areas to future warming. Thus, in addition to seasonality, spatial heterogeneity may play a critical role in thermal adaptation and climate change impacts particularly in the tropics.     

Phenological sequences reveal aggregate life history response to climatic warming

Climatic warming is associated with organisms breeding earlier in the season than is typical for their species. In some species, however, response to warming is more complex than a simple advance in the timing of all life history events preceding reproduction. Disparities in the extent to which different components of the reproductive phenology of organisms vary with climatic warming indicate that not all life history events are equally responsive to environmental variation. Here, we propose that our understanding of phenological response to climate change can be improved by considering entire sequences of events comprising the aggregate life histories of organisms preceding reproduction. We present results of a two-year warming experiment conducted on 33 individuals of three plant species inhabiting a low-arctic site. Analysis of phenological sequences of three key events for each species revealed how the aggregate life histories preceding reproduction responded to warming, and which individual events exerted the greatest influence on aggregate life history variation. For alpine chickweed (Cerastium alpinum), warming elicited a shortening of the duration of the emergence stage by 2.5 days on average, but the aggregate life history did not differ between warmed and ambient plots. For gray willow (Salix glauca), however, all phenological events monitored occurred earlier on warmed than on ambient plots, and warming reduced the aggregate life history of this species by 22 days on average. Similarly, in dwarf birch (Betula nana), warming advanced flower bud set, blooming, and fruit set and reduced the aggregate life history by 27 days on average. Our approach provides important insight into life history responses of many organisms to climate change and other forms of environmental variation. Such insight may be compromised by considering changes in individual phenological events in isolation.     

Process-based modeling of species' distributions: what limits temperate tree species' range boundaries?

Niche-based models are widely used to understand what environmental factors determine species' distributions, but they do not provide a clear framework to study the processes involved in defining species' ranges. Here we used a process-based model to identify these processes and to assess the potential distribution of 17 North American boreal/temperate tree species. Using input of only climate and soil properties, the model reproduced the 17 species' distributions accurately. Our results allowed us to identify the climatic factors as well as the biological processes involved in limiting species' ranges. The model showed that climatic constraints limit species' distributions mainly through their impact on phenological processes, and secondarily through their impact on drought and frost mortality. The northern limit of species' ranges appears to be caused mainly by the inability to undergo full fruit ripening and/or flowering, while the southern limit is caused by the inability to flower or by frost injury to flowers. These findings about the ecological processes shaping tree species' distribution represent a crucial step toward obtaining a more complete picture of the potential impact of climate on species' ranges.     

Does including physiology improve species distribution model predictions of responses to recent climate change?

Thermal constraints on development are often invoked to predict insect distributions. These constraints tend to be characterized in species distribution models (SDMs) by calculating development time based on a constant lower development temperature (LDT). Here, we assessed whether species-specific estimates of LDT based on laboratory experiments can improve the ability of SDMs to predict the distribution shifts of six U.K. butterflies in response to recent climate warming. We find that species-specific and constant (5 degrees C) LDT degree-day models perform similarly at predicting distributions during the period of 1970-1982. However, when the models for the 1970-1982 period are projected to predict distributions in 1995-1999 and 2000-2004, species-specific LDT degree-day models modestly outperform constant LDT degree-day models. Our results suggest that, while including species-specific physiology in correlative models may enhance predictions of species' distribution responses to climate change, more detailed models may be needed to adequately account for interspecific physiological differences.     

Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps.

In the European Alps the increase in air temperature was more than twice the increase in global mean temperature over the last 50 years. The abiotic (glacial) and the biotic components (plants and vegetation) of the mountain environment are showing ample evidence of climate change impacts. In the Alps most small glaciers (80% of total glacial coverage and an important contribution to water resources) could disappear in the next decades. Recently climate change was demonstrated to affect higher levels of ecological systems, with vegetation exhibiting surface area changes, indicating that alpine and nival vegetation may be able to respond in a fast and flexible way in response to 1-2 degrees C warming. We analyzed the glacier evolution (terminus fluctuations, mass balances, surface area variations), local climate, and vegetation succession on the forefield of Sforzellina Glacier (Upper Valtellina, central Italian Alps) over the past three decades. We aimed to quantify the impacts of climate change on coupled biotic and abiotic components of high alpine ecosystems, to verify if an acceleration was occurring on them during the last decade (i.e., 1996-2006) and to assess whether new specific strategies were adopted for plant colonization and development. All the glaciological data indicate that a glacial retreat and shrinkage occurred and was much stronger after 2002 than during the last 35 years. Vegetation started to colonize surfaces deglaciated for only one year, with a rate at least four times greater than that reported in the literature for the establishment of scattered individuals and about two times greater for the well-established discontinuous early-successional community. The colonization strategy changed: the first colonizers are early-successional, scree slopes, and perennial clonal species with high phenotypic plasticity rather than pioneer and snowbed species. This impressive acceleration coincided with only slight local summer warming (approximately -0.5 degree C) and a poorly documented local decrease in the snow cover depth and duration. Are we facing accelerated ecological responses to climatic changes and/or did we go beyond a threshold over which major ecosystem changes may occur in response to even minor climatic variations?     

Building phenological models from presence/absence data for a butterfly fauna.

Species phenology is increasingly being used to explore the effects of climate change and other environmental stressors. Long-term monitoring data sets are essential for understanding both patterns manifest by individual species and more complex patterns evident at the community level. This study used records of 78 butterfly species observed on 626 days across 27 years at a site in northern California, USA, to build quadratic logistic regression models of the observation probability of each species for each day of the year. Daily species probabilities were summed to develop a potential aggregate species richness (PASR) model, indicating expected daily species richness. Daily positive and negative contributions to PASR were calculated, which can be used to target optimum sampling time frames. Residuals to PASR indicate a rate of decline of 0.12 species per year over the course of the study. When PASR was calculated for wet and dry years, wet years were found to delay group phenology by up to 17 days and reduce the maximum annual expected species from 32.36 to 30. Three tests to determine how well the PASR model reflected the butterfly fauna dynamics were all positive: We correlated probabilities developed with species presence/absence data to observed abundance by species, tested species' predicted phenological patterns against known biological characteristics, and compared the PASR curve to a spline-fitted curve calculated from the original species richness observations. Modeling individual species' flight windows was possible from presence/absence data, an approach that could be used on other similar records for butterfly communities with seasonal phenologies, and for common species with far fewer dates than used here. It also provided a method to assess sample frequency guidelines for other butterfly monitoring programs.     

Climate change and population genetic structure of marine species

Climate change influences populations by reducing or extirpating local populations, by disrupting patterns of migration and by shifting geographical distributions. These events can affect genetic population structure in several ways. Molecular markers have been used in numerous population genetic and phylogeographical studies of marine species and have detected population responses to climate change in the last few decades, such as range expansions, adaptative shifts and declines or increases in abundance. Little is known, however, about the molecular and physiological basis of adaptive responses to climate change in marine Mediterranean species. The Mediterranean Sea ecosystem is a ‘living laboratory’ with native species that are challenged by environmental change and by invasive species and a ‘gene-climate’ approach should be adopted as a way of focusing on the relationship between climate warming and genetic diversity.     

Tropical amphibians in shifting thermal landscapes under land‐use and climate change

Land‐cover and climate change are both expected to alter species distributions and contribute to future biodiversity loss. However, the combined effects of land‐cover and climate change on assemblages, especially at the landscape scale, remain understudied. Lowland tropical amphibians may be particularly susceptible to changes in land cover and climate warming because many species have narrow thermal safety margins resulting from air and body temperatures that are close to their critical thermal maxima (CT_max). We examined how changing thermal landscapes may alter the area of thermally suitable habitat (TSH) for tropical amphibians. We measured microclimates in 6 land‐cover types and CT_max of 16 frog species in lowland northeastern Costa Rica. We used a biophysical model to estimate core body temperatures of frogs exposed to habitat‐specific microclimates while accounting for evaporative cooling and behavior. Thermally suitable habitat area was estimated as the portion of the landscape where species CT_max exceeded their habitat‐specific maximum body temperatures. We projected changes in TSH area 80 years into the future as a function of land‐cover change only, climate change only, and combinations of land‐cover and climate‐change scenarios representing low and moderate rates of change. Projected decreases in TSH area ranged from 16% under low emissions and reduced forest loss to 30% under moderate emissions and business‐as‐usual land‐cover change. Under a moderate emissions scenario (A1B), climate change alone contributed to 1.7‐ to 4.5‐fold greater losses in TSH area than land‐cover change only, suggesting that future decreases in TSH from climate change may outpace structural habitat loss. Forest‐restricted species had lower mean CT_max than species that occurred in altered habitats, indicating that thermal tolerances will likely shape assemblages in changing thermal landscapes. In the face of ongoing land‐cover and climate change, it will be critical to consider changing thermal landscapes in strategies to conserve ectotherm species.     

Relation between extinction and assisted colonization of plants in the arctic‐alpine and boreal regions

Assisted colonization of vascular plants is considered by many ecologists an important tool to preserve biodiversity threatened by climate change. I argue that assisted colonization may have negative consequences in arctic‐alpine and boreal regions. The observed slow movement of plants toward the north has been an argument for assisted colonization. However, these range shifts may be slow because for many plants microclimatic warming (ignored by advocates of assisted colonization) has been smaller than macroclimatic warming. Arctic‐alpine and boreal plants may have limited possibilities to disperse farther north or to higher elevations. I suggest that arctic‐alpine species are more likely to be driven to extinction because of competitive exclusion by southern species than by increasing temperatures. If so, the future existence of arctic‐alpine and boreal flora may depend on delaying or preventing the migration of plants toward the north to allow northern species to evolve to survive in a warmer climate. In the arctic‐alpine region, preventing the dispersal of trees and shrubs may be the most important method to mitigate the negative effects of climate change. The purported conservation benefits of assisted colonization should not be used to promote the migration of invasive species by forestry.     

Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers

The timing of life history traits is central to lifetime fitness and nowhere is this more evident or well studied as in the phenology of flowering in governing plant reproductive success. Recent changes in the timing of environmental events attributable to climate change, such as the date of snowmelt at high altitudes, which initiates the growing season, have had important repercussions for some common perennial herbaceous wildflower species. The phenology of flowering at the Rocky Mountain Biological Laboratory (Colorado, USA) is strongly influenced by date of snowmelt, which makes this site ideal for examining phenological responses to climate change. Flower buds of Delphinium barbeyi, Erigeron speciosus, and Helianthella quinquenervis are sensitive to frost, and the earlier beginning of the growing season in recent years has exposed them to more frequent mid-June frost kills. From 1992 to 1998, on average 36.1% of Helianthella buds were frosted, but for 1999-2006 the mean is 73.9%; in only one year since 1998 have plants escaped all frost damage. For all three of these perennial species, there is a significant relationship between the date of snowmelt and the abundance of flowering that summer. Greater snowpack results in later snowmelt, later beginning of the growing season, and less frost mortality of buds. Microhabitat differences in snow accumulation, snowmelt patterns, and cold air drainage during frost events can be significant; an elevation difference of only 12 m between two plots resulted in a temperature difference of almost 2 degrees C in 2006 and a difference of 37% in frost damage to buds. The loss of flowers and therefore seeds can reduce recruitment in these plant populations, and affect pollinators, herbivores, and seed predators that previously relied on them. Other plant species in this environment are similarly susceptible to frost damage so the negative effects for recruitment and for consumers dependent on flowers and seeds could be widespread. These findings point out the paradox of increased frost damage in the face of global warming, provide important insights into the adaptive significance of phenology, and have general implications for flowering plants throughout the region and anywhere climate change is having similar impacts.     

Protected area characteristics that help waterbirds respond to climate warming

Protected area networks help species respond to climate warming. However, the contribution of a site's environmental and conservation-relevant characteristics to these responses is not well understood. We investigated how composition of nonbreeding waterbird communities (97 species) in the European Union Natura 2000 (N2K) network (3018 sites) changed in response to increases in temperature over 25 years in 26 European countries. We measured community reshuffling based on abundance time series collected under the International Waterbird Census relative to N2K sites’ conservation targets, funding, designation period, and management plan status. Waterbird community composition in sites explicitly designated to protect them and with management plans changed more quickly in response to climate warming than in other N2K sites. Temporal community changes were not affected by the designation period despite greater exposure to temperature increase inside late-designated N2K sites. Sites funded under the LIFE program had lower climate-driven community changes than sites that did not received LIFE funding. Our findings imply that efficient conservation policy that helps waterbird communities respond to climate warming is associated with sites specifically managed for waterbirds.     

Nitrogen regulation of the climate-carbon feedback: evidence from a long-term global change experiment

Modeling studies have shown that nitrogen (N) strongly regulates ecosystem responses and feedback to climate warming. However, it remains unclear what mechanisms underlie N regulation of ecosystem-climate interactions. To examine N regulation of ecosystem feedback to climate change, we have conducted a warming and clipping experiment since November 1999 in a tallgrass prairie of the Great Plains, USA. Infrared heaters were used to elevate soil temperature by an average of 1.96 degrees C at a depth of 2.5 cm from 2000 to 2008. Yearly biomass clipping mimicked hay or biofuel feedstock harvest. We measured carbon (C) and N concentrations, estimated their content and C:N ratio in plant, root, litter, and soil pools. Warming significantly stimulated C storage in aboveground plant, root, and litter pools by 17%, 38%, and 29%, respectively, averaged over the nine years (all P < 0.05) but did not change soil C content or N content in any pool. Plant C:N ratio and nitrogen use efficiency increased in the warmed plots compared to the control plots, resulting primarily from increased dominance of C4 plants in the community. Clipping significantly decreased C and N storage in plant and litter pools (all P < 0.05) but did not have interactive effects with warming on either C or N pools over the nine years. Our results suggest that increased ecosystem nitrogen use efficiency via a shift in species composition toward C4 dominance rather than plant N uptake is a key mechanism underlying warming stimulation of plant biomass growth.     

Pollinator effectiveness varies with experimental shifts in flowering time

The earlier flowering times exhibited by many plant species are a conspicuous sign of climate change. Altered phenologies have caused concern that species could suffer population declines if they flower at times when effective pollinators are unavailable. For two perennial wildflowers, Tradescantia ohiensis and Asclepias incarnata, we used an experimental approach to explore how changing phenology affects the taxonomic composition of the pollinator assemblage and the effectiveness of individual pollinator taxa. After finding in the previous year that fruit set varied with flowering time, we manipulated flowering onset in greenhouses, placed plants in the field over the span of five weeks, and measured pollinator effectiveness as the number of seeds produced after a single visit to a flower. The average effectiveness of pollinators and the expected rates of pollination success were lower for plants of both species flowering earlier than for plants flowering at historical times, suggesting there could be reproductive costs to earlier flowering. Whereas for A. incarnata, differences in average seed set among weeks were due primarily to changes in the composition of the pollinator assemblage, the differences for T. ohiensis were driven by the combined effects of compositional changes and increases over time in the effectiveness of some pollinator taxa. Both species face the possibility of temporal mismatch between the availability of the most effective pollinators and the onset of flowering, and changes in the effectiveness of individual pollinator taxa through time may add an unexpected element to the reproductive consequences of such mismatches.     

Plant-mediated and nonadditive effects of two global change drivers on an insect herbivore community

Warmer temperatures can alter the phenology and distribution of individual species. However, differences across species may blur community-level phenological responses to climate or cause biotic homogenization by consistently favoring certain taxa. Additionally, the response of insect communities to climate will be subject to plant-mediated effects, which may or may not overshadow the direct effect of rising temperatures on insects. Finally, recent evidence for the importance of interaction effects between global change drivers suggests that phenological responses of communities to climate may be altered by other drivers. We used a natural temperature gradient (generated by elevation and topology), combined with experimental nitrogen fertilization, to investigate the effects of elevated temperature and globally increasing anthropogenic nitrogen deposition on the structure and phenology of a seminatural grassland herbivore assemblage (lepidopteran insects). We found that both drivers, alone and in combination, severely altered how the relative abundance and composition of species changed through time. Importantly, warmer temperatures were associated with biotic homogenization, such that herbivore assemblages in the warmest plots had more similar species composition than those in intermediate or cool plots. Changes in herbivore composition and abundance were largely mediated by changes in the plant community, with increased nonnative grass cover under high treatment levels being the strongest determinant of herbivore abundance. In addition to compositional changes, total herbivore biomass more than doubled under elevated nitrogen and increased more than fourfold with temperature, bearing important functional implications for herbivores as consumers and as a prey resource. The crucial role of nonnative plant dominance in mediating responses of herbivores to change, combined with the frequent nonadditive (positive and negative) effects of the two drivers, and the differential responses of species, highlight that understanding complex ecosystem responses will benefit from multifactor, multitrophic experiments at community scales or larger.     

Behaviour moderates climate warming vulnerability in high-rocky-shore snails: interactions of habitat use, energy consumption and environmental temperature

High-rocky-shore intertidal animals are predicted to be generally more vulnerable to climate warming than lower-shore species, because their thermal tolerances lie closer to maximum environmental temperatures (T _e). However, this prediction is based on taxonomically and ecologically limited information. The present study investigated the effect of habitat use on climate warming vulnerability of the tropical high-shore snail, Echinolittorina malaccana (from Brunei Darussalam, 5°N), which aestivates in sun-exposed or shaded habitats. The thermal regimes of these habitats differed vastly, but snails showed similar daily energy consumption in either habitat, due to temperature-insensitive metabolism (TIM) between 35 and 46 °C in the sun-resting snails. However, maximum T _e values in the shade and the sun were 35 and 46 °C, respectively, suggesting that sun-resting snails, which presently experience temperatures near the incipient lethal temperature range (46–56 °C), should be more threatened by further warming than shade-resting snails, which have an 11 °C ‘safety margin’. Thus, vulnerability of high-shore species to climate warming could be moderated by availability of shaded habitat, making predictions for these species more complex than previously realized.