Linking energetics and overwintering in temperate insects

Overwintering insects cannot feed, and energy they take into winter must therefore fuel energy demands during autumn, overwintering, warm periods prior to resumption of development in spring, and subsequent activity. Insects primarily consume lipids during winter, but may also use carbohydrate and proteins as fuel. Because they are ectotherms, the metabolic rate of insects is temperature-dependent, and the curvilinear nature of the metabolic rate-temperature relationship means that warm temperatures are disproportionately important to overwinter energy use. This energy use may be reduced physiologically, by reducing the slope or elevation of the metabolic rate-temperature relationship, or because of threshold changes, such as metabolic suppression upon freezing. Insects may also choose microhabitats or life history stages that reduce the impact of overwinter energy drain. There is considerable capacity for overwinter energy drain to affect insect survival and performance both directly (via starvation) or indirectly (for example, through a trade-off with cryoprotection), but this has not been well-explored. Likewise, the impact of overwinter energy drain on growing-season performance is not well understood. I conclude that overwinter energetics provides a useful lens through which to link physiology and ecology and winter and summer in studies of insect responses to their environment.     

Urban environments provide new perspectives for forecasting vegetation phenology responses under climate warming

Given that already-observed temperature increase within cities far exceeds the projected global temperature rise by the end of the century, urban environments often offer a unique opportunity for studying ecosystem response to future warming. However, the validity of thermal gradients in space serving as a substitute for those in time is rarely tested. Here, we investigated vegetation phenology dynamics in China's 343 cities and empirically test whether phenological responses to spatial temperature rise in urban settings can substitute for those to temporal temperature rise in their natural counterparts based on satellite-derived vegetation phenology and land surface temperature from 2003 to 2018. We found prevalent advancing spring phenology with “high confidence” and delaying autumn phenology with “medium confidence” under the context of widespread urban warming. Furthermore, we showed that space cannot substitute for time in predicting phenological shifts under climate warming at the national scale and for most cities. The thresholds of ~11°C mean annual temperature and ~600 mm annual precipitation differentiated the magnitude of phenological sensitivity to temperature across space and through time. Below those thresholds, there existed stronger advanced spring phenology and delayed autumn phenology across the spatial urbanization gradients than through time, and vice versa. Despite the complex and diverse relationships between phenological sensitivities across space and through time, we found that the directions of the temperature changes across spatial gradients were converged (i.e., mostly increased), but divergent through temporal gradients (i.e., increased or decreased without a predominant direction). Similarly, vegetation phenology changes more uniformly over space than through time. These results suggested that the urban environments provide a real-world condition to understand vegetation phenology response under future warming.     

Developmental plasticity in the thermal tolerance of zebrafish Danio rerio

To evaluate developmental plasticity in thermal tolerance of zebrafish Danio rerio , common-stock zebrafish were reared from fertilization to adult in the five thermal regimes (two stable, two with constant diel cycles and one stochastic diel cycle) and their thermal tolerance at three acclimation temperatures compared. The energetic cost of developing in the five regimes was assessed by measuring body size over time. While acclimation accounted for most of the variability in thermal tolerance, there were also significant differences among fish reared in the different regimes, regardless of acclimation. Fish reared in more variable environments (as much as ±6° C diel cycle) had a greater tolerance than those from non-variable environments at the same mean temperature. Fish from the more variable environments were also significantly smaller than those from non-variable environments. These results indicate that the thermal history of individual zebrafish induces irreversible changes to the thermal tolerance of adults.     

Preferred temperature of intertidal ectotherms: Broad patterns and methodological approaches

Preferred temperature (Tpref) has been measured in over 100 species of aquatic and 300 species of terrestrial ectotherms as a metric for assessing behavioural thermoregulation in variable environments and, as such, has been linked to ecological processes ranging from individual behaviour to population and community dynamics. Due to the asymmetric shape of performance curves, Tpref is typically lower than the optimal temperature (Topt, where physiological performance is at its peak), and the degree of this mismatch increases with variability in Tb. Intertidal ectotherms experience huge variability in Tb on a daily basis and therefore provide a good system to test whether the relationship between Tpref and variation in Tb holds in more extreme environments. A review of the literature, however, only revealed comparisons between Tpref and Topt for five intertidal species and measurements of Tpref for 23 species. An analysis of this limited literature for intertidal ectotherms showed a positive relationship between acclimation temperature and Tpref. There was, however, great variation in the methodologies employed to make these assessments. Factors contributing to behavioural thermoregulation in intertidal ectotherms including small body size; low mobility; interactions among individuals; endogenous clocks; metabolic effects; thermal sensitivity; sampling of the thermal environment and recent acclimation history were considered to varying degrees when measuring Tpref, confounding comparisons between species. The methodologies used to measure Tpref in intertidal ectotherms were reviewed in light of each of these factors, and methodologies proposed to standardize approaches. Given the theoretical predictions about the relationships between Tpref and variability in Tb, the spatial and temporal thermal variability experienced by intertidal ectotherms provides numerous opportunities to test these expectations if assessed in a standardized manner, and can potentially provide insights into the value of behavioural thermoregulation in the more thermally variable environments predicted to occur in the near future.     

Transgenerational and within‐generation plasticity shape thermal performance curves

Thermal performance curves (TPCs) compute the effects of temperature on the performance of ectotherms and are frequently used to predict the effect of environmental conditions and currently, climate change, on organismal vulnerability and sensitivity. Using Drosophila melanogaster as an animal model, we examined how different thermal environments affected the shape of the performance curve and their parameters. We measured the climbing speed as a measure of locomotor performance in adult flies and tested the ontogenetic and transgenerational effects of thermal environment on TPC shape. Parents and offspring were reared at 28 ± 0ºC (28C), 28 ± 4ºC (28V), and 30 ± 0ºC (30C). We found that both, environmental thermal variability (28V) and high temperature (30C) experienced during early ontogeny shaped the fruit fly TPC sensitivity. Flies reared at variable thermal environments shifted the TPC to the right and increased heat tolerance. Flies held at high and constant temperature exhibited lower maximum performance than flies reared at the variable thermal environment. Furthermore, these effects were extended to the next generation. The parental thermal environment had a significative effect on TPC and its parameters. Indeed, flies reared at 28V whose parents were held at a high and constant temperature (30C) had a lower heat tolerance than F1 of flies reared at 28C or 28V. Also, offspring of flies reared at variable thermal environment (28V) reached the maximum performance at a higher temperature than offspring of flies reared at 28C or 30C. Consequently, since TPC parameters are not fixed, we suggest cautiousness when using TPCs to predict the impact of climate change on natural populations.     

The influence of life history traits on the phenological response of British butterflies to climate variability since the late‐19th century

Many species of plants and animals have advanced their phenology in response to climate warming in recent decades. Most of the evidence available for these shifts is based on data from the last few decades, a period coinciding with rapid climate warming. Baseline data is required to put these recent phenological changes in a long‐term context. We analysed the phenological response of 51 resident British butterfly species using data from 83 500 specimens in the collections of the Natural History Museum, London, covering the period 1880–1970. Our analysis shows that only three species significantly advanced their phenology between 1880 and 1970, probably reflecting the relatively small increase in spring temperature over this period. However, the phenology of all but one of the species we analysed showed phenological sensitivity to inter‐annual climate variability and a significant advancement in phenology in years in which spring or summer temperatures were warm and dry. The phenologies of butterfly species were more sensitive to weather if the butterfly species was early flying, southerly distributed, and a generalist in terms of larval diet. This observation is consistent with the hypothesis that species with greater niche breadth may be more phenologically sensitive than species with important niche constraints. Comparison of our results with post‐1976 data from the UK Butterfly Monitoring Scheme show that species flying early in the year had a greater rate of phenological advancement prior to the mid‐1970s. Additionally, prior to the mid‐1970s, phenology was influenced by temperatures in March or April, whereas since 1976, February temperature had a stronger influence on the phenology. These results suggest that early flying species may be approaching the limits of phenological advancement in response to recent climate warming.     

Phenological modularity in amphibian calling behaviour: Geographic trends and local determinants

Phenology of species, the coupling of vital activities to specific times of the year, plays a main role in ecosystem functioning and is expected to be affected by global change. We analysed the temporal structure of 52 amphibian communities in South America encompassing a latitudinal range from 7º to 34º south. Phenological modularity – species tendencies to aggregate along the months – is here introduced as a ubiquitous property of biodiversity architecture. Further, we identified an increase in phenological modularity with species richness, available energy and in communities with lower thermal dependence (i.e. the rate of change in the number of species active along the year associated with the environmental temperature). These patterns are in agreement with predictions derived from several ecological hypotheses: complexity‐stability, species‐energy and metabolic ecology. However, no direct association between modularity and the phylogenetic structure of communities was observed. A structural equation model that outperformed all the plausible alternative models considered supports these results. Modularity is reported here as a main feature of the phenology of communities that depends on environmental conditions. Here, we report for the first time a putative connection between community species richness and the degree of temporal structure – phenological modularity; the thermal dependence shows that communities at low latitudes are more vulnerable to climate change; energetic environments also promote communities with phenological modularity; and latitudinal patterns of phylogenetic community structure can give us clues of which species would be important to the conservation of community processes. These results call for further theoretical analyses to support the connection between phenological modularity, community stability and vulnerability to global change.     

Functional analysis of Normalized Difference Vegetation Index curves reveals overwinter mule deer survival is driven by both spring and autumn phenology

Large herbivore populations respond strongly to remotely sensed measures of primary productivity. Whereas most studies in seasonal environments have focused on the effects of spring plant phenology on juvenile survival, recent studies demonstrated that autumn nutrition also plays a crucial role. We tested for both direct and indirect (through body mass) effects of spring and autumn phenology on winter survival of 2315 mule deer fawns across a wide range of environmental conditions in Idaho, USA. We first performed a functional analysis that identified spring and autumn as the key periods for structuring the among-population and among-year variation of primary production (approximated from 1 km Advanced Very High Resolution Radiometer Normalized Difference Vegetation Index (NDVI)) along the growing season. A path analysis showed that early winter precipitation and direct and indirect effects of spring and autumn NDVI functional components accounted for 45% of observed variation in overwinter survival. The effect size of autumn phenology on body mass was about twice that of spring phenology, while direct effects of phenology on survival were similar between spring and autumn. We demonstrate that the effects of plant phenology vary across ecosystems, and that in semi-arid systems, autumn may be more important than spring for overwinter survival.     

Long‐term changes in autumn migration dates at the Strait of Gibraltar reflect population trends of soaring birds

A growing body of work shows that climate change is the cause of a number of directional shifts in the spring phenology of migratory birds. However, changes in autumn phenology are well studied and their consistency across species, as well as their link with population trends, remains uncertain. We investigate changes in the autumn migration dates of 11 species of soaring birds over the Strait of Gibraltar over a 16‐year period. Using models corrected for phylogeny, we assessed whether ecological and morphological characteristics, as well as population trends, account for interspecific shifts in migration times. We recorded different phenological changes in different periods of the migration season and suggest that these differences are due to age‐dependent responses. The variable best predicting advances in migration dates was population trend: species that did not advance their autumn migration dates were those showing a decline in their European breeding populations. We repeated our tests on a dataset representing the migration date of soaring birds across the Pyrenees Mountains and found that population trends at this site also predicted phenological shifts. Our results suggest that flexibility in migratory strategy and population trends may be related, such that different adaptive capacity in migration timing may be more relevant than other ecological traits in determining the conservation status of migratory birds in Europe and perhaps other regions.     

Is climate warming more consequential towards poles? The phenology of Lepidoptera in Finland

The magnitude and direction of phenological shifts from climate warming could be predictably variable across the planet depending upon the nature of physiological controls on phenology, the thermal sensitivity of the developmental processes and global patterns in the climate warming. We tested this with respect to the flight phenology of adult nocturnal moths (3.33 million captures of 334 species) that were sampled at sites in southern and northern Finland during 1993–2012 (with years 2005–2012 treated as an independent model validation data set). We compared eight competing models of physiological controls on flight phenology to each species and found strong support for thermal controls of phenology in 66% of the species generations. Among species with strong thermal control of phenology in both the south and north, the average development rate was higher in northern vs. southern populations at 10 °C, but about the same at 15 and 20 °C. With a 3 °C increase in temperature (approximating A2 scenario of IPPC for 2090–2099 relative to 1980–1999) these species were predicted to advance their phenology on average by 17 (SE ± 0.3) days in the south vs. 13 (±0.4) days in the north. The higher development rates at low temperatures of poleward populations makes them less sensitive to climate warming, which opposes the tendency for stronger phenological advances in the north from greater increases in temperature.     

Predicting Climate Change Impacts on the Amount and Duration of Autumn Colors in a New England Forest

Climate change affects the phenology of many species. As temperature and precipitation are thought to control autumn color change in temperate deciduous trees, it is possible that climate change might also affect the phenology of autumn colors. Using long-term data for eight tree species in a New England hardwood forest, we show that the timing and cumulative amount of autumn color are correlated with variation in temperature and precipitation at specific times of the year. A phenological model driven by accumulated cold degree-days and photoperiod reproduces most of the interspecific and interannual variability in the timing of autumn colors. We use this process-oriented model to predict changes in the phenology of autumn colors to 2099, showing that, while responses vary among species, climate change under standard IPCC projections will lead to an overall increase in the amount of autumn colors for most species.     

Forecasting phenology under global warming

As a consequence of warming temperatures around the world, spring and autumn phenologies have been shifting, with corresponding changes in the length of the growing season. Our understanding of the spatial and interspecific variation of these changes, however, is limited. Not all species are responding similarly, and there is significant spatial variation in responses even within species. This spatial and interspecific variation complicates efforts to predict phenological responses to ongoing climate change, but must be incorporated in order to build reliable forecasts. Here, we use a long-term dataset (1953–2005) of plant phenological events in spring (flowering and leaf out) and autumn (leaf colouring and leaf fall) throughout Japan and South Korea to build forecasts that account for these sources of variability. Specifically, we used hierarchical models to incorporate the spatial variability in phenological responses to temperature to then forecast species'' overall and site-specific responses to global warming. We found that for most species, spring phenology is advancing and autumn phenology is getting later, with the timing of events changing more quickly in autumn compared with the spring. Temporal trends and phenological responses to temperature in East Asia contrasted with results from comparable studies in Europe, where spring events are changing more rapidly than are autumn events. Our results emphasize the need to study multiple species at many sites to understand and forecast regional changes in phenology.     

Plasticity of life-cycle, physiological thermal traits and Hsp70 gene expression in an insect along the ontogeny: Effect of temperature variability

It is considered that extreme environmental temperature, rather than mean temperatures exert a selective pressure in ectotherms. Consequently, it is important to understand how the predicted increase in temperature variance with a higher frequency of extreme events in climate change is likely to impact on organisms. Thermal tolerance traits (i.e. chill-coma, recovery time, Hsp70 expression) are directly linked with performance in ectotherms and have consequences in life-history traits. We examined the effects of temperature variability on thermal tolerance and life-history traits through ontogeny of an insect with a complex life-cycle: the yellow mealworm beetle Tenebrio molitor. We established two common gardens with 100 recently ovoposited eggs each. Larvae were reared from hatching to adult on either a variable (mean=18 °C and a variance of 6.8 °C) or constant (18±1 °C) thermal environment. Development rate and growth rate were similar between thermal environments. Results indicate that larvae reared in a variable environment are more cold-tolerant than larvae of a constant environment. Interestingly, these results are reversed in the adult stage, outlining an inter-stage physiological cost. Gene expression pattern of an Hsp70 gene was well correlated with larval thermotolerance to cold in the variable environment but higher gene expression in adults is not correlated with individual's thermotolerance. We conclude that chill-coma, recovery time and Hsp70 gene expression are plastic in response to a thermal environment but also change significantly their responses depending on the ontogenetic stage, implying that the response of adult individuals is linked to early stages of the life-cycle.     

Testing the match–mismatch hypothesis in bighorn sheep in the context of climate change

In species with long gestation, females commit to reproduction several months before parturition. If cues driving conception date are uncoupled from spring conditions, parturition could be mistimed. Mismatch may increase with global change if the rate of temporal changes in autumn cues differs from the rate of change in spring conditions. Using 17 years of data on climate and vegetation phenology, we show that autumn temperature and precipitation, but not vegetation phenology, explain parturition date in bighorn sheep. Although autumn cues drive the timing of conception, they do not predict conditions at parturition in spring. We calculated the mismatch between individual parturition date and spring green-up, assessed whether mismatch increased over time and investigated the consequences of mismatch on lamb neonatal survival, weaning mass and overwinter survival. Mismatch fluctuated over time but showed no temporal trend. Temporal changes in green-up date did not lead to major fitness consequence of mismatch. Detailed data on individually marked animals revealed no effect of mismatch on neonatal or overwinter survival, but lamb weaning mass was negatively affected by mismatch. Capital breeders might be less sensitive to mismatch than income breeders because they are less dependent on daily food acquisition. Herbivores in seasonal environments may access sufficient forage to sustain lactation before or after the spring ‘peak’ green-up, and partly mitigate the consequences of a mismatch. Thus, the effect of phenological mismatch on fitness may be affected by species life history, highlighting the complexity in quantifying trophic mismatches in the context of climate change.     

Predicting the sensitivity of butterfly phenology to temperature over the past century

Studies to date have documented substantial variation among species in the degree to which phenology responds to temperature and shifts over time, but we have a limited understanding of the causes of such variation. Here, we use a spatially and temporally extensive data set (ca. 48 000 observations from across Canada) to evaluate the utility of museum collection records in detecting broad‐scale phenology‐temperature relationships and to test for systematic differences in the sensitivity of phenology to temperature (days °C^?1) of Canadian butterfly species according to relevant ecological traits. We showed that the timing of flight season predictably responded to temperature both across space (variation in average temperature from site to site in Canada) and across time (variation from year to year within each individual site). This reveals that collection records, a vastly underexploited resource, can be applied to the quantification of broad‐scale relationships between species' phenology and temperature. The timing of the flight season of earlier fliers and less mobile species was more sensitive to temperature than later fliers and more mobile species, demonstrating that ecological traits can account for some of the interspecific variation in species' phenological sensitivity to temperature. Finally, we found that phenological sensitivity to temperature differed across time and space implying that both dimensions of temperature will be needed to translate species' phenological sensitivity to temperature into accurate predictions of species' future phenological shifts. Given the widespread temperature sensitivity of flight season timing, we can expect long‐term temporal shifts with increased warming [ca. 2.4 days °C^?1 (0.18 SE)] for many if not most butterfly species.     

西安4种落叶乔木物候期对气候变化的响应

以西安1979—2018年的气候资料和植物物候观测资料为基础,采用分段回归和趋势倾向率等方法,分析了毛白杨(Populus tomentosa)、杜梨(Pyrus betulifolia)、七叶树(Aesculus chinensis)和灯台树(Bothrocaryum controversum)4种落叶乔木展叶盛期和叶全变色期的生长趋势,使用偏相关分析探讨了气温、降水和日照时数与物候期的关系并通过偏最小二乘回归(Partial Least Squares, PLS)判断气候变量对物候期的综合影响。结果表明：(1)1979—2018年,4种乔木的生长季长度延长,整体表现为春季物候期提前,秋季物候期推迟;(2)展叶盛期物候指标与叶全变色期物候指标,转折均发生在1982年;转折后,物候特征变化显著,春季物候的提前速率和秋季物候的推迟速率加快,展叶盛期平均提前3.8d/10a,叶全变色期平均推迟4.7d/10a;(3)展叶盛期与春季气温表现为极显著负相关,叶变色期与秋季气温表现为显著正相关;降水对植物物候的影响不显著;春季物候与日照时数呈现极显著负相关关系,秋季物候期与日照时数呈不显著正相关...     

Different temperature perception in high‐elevation plants: new insight into phenological development and implications for climate change in the alpine tundra

In alpine habitats, predicted warmer and longer growing seasons will influence plant phenology, with important implications for species adaptation and vegetation dynamics. However, little is known on the temperature sensitivity of different phenophases and on the characteristics allowing phenological variation among and within species. By integrating interannual micro‐climatic variability with experimental warming, we explored how the phenology of three alpine species is influenced by temperature and what mechanisms underlie intra‐ and inter‐specific phenological differences. The present study demonstrated that alpine plants have different temperature responses during their reproductive cycle, do not have constant thermal thresholds and heat‐use efficiencies to achieve the seed dispersal stage and can change their temperature sensitivity to flower along snowmelt gradients. In addition, the length of the reproductive cycle, which proved to be species‐specific under experimental warming, does not seem to be the only life‐history trait under selective pressure due to the short‐length of the snow‐free period. In a warming climate scenario, the phenology of sexual reproduction will be considerably altered, and alpine plants may be subjected to changes in population dynamics driven by altered perception of environmental cues appropriate for coordinating the timing of key life‐history events.     

To freeze or not to freeze? An evolutionary perspective on the cold-hardiness strategies of overwintering ectotherms

We address the question of whether freeze-tolerance, freeze-avoidance, or mixed strategy represents the best adaptation for overwintering ectotherms to endure severe winter. To this end, we develop an optimization fitness model that takes into account different physiological parameters such as energetic level, the physiological stress associated with each strategy, and climatic variables. The results show that the freeze-tolerance strategy is strongly dependent on a low sensitivity to the number of freezing days and on a capacity to reduce stress associated with freezing. This strategy is also favored when the initial energetic level is low compared to the freeze-avoidance strategy, which is favored by a high initial energetic level, a low stress associated with the supercooling, and a low sensitivity of this strategy to climatic conditions. From a theoretical point of view, the mixed strategy permits survival in harsher environments but requires the optimization of all parameters involved in both cold-hardiness strategies. However, the mixed strategy shows energetic advantages in variable environments allowing animals to resist the harshest periods. From the model results, it appears that the physiological processes developed by ectotherms to reduce these stresses might be a key to understanding the evolution of the cold-hardiness strategies.     

Three‐dimensional change in temperature sensitivity of northern vegetation phenology

Understanding how the temperature sensitivity of phenology changes with three spatial dimensions (altitude, latitude, and longitude) is critical for the prediction of future phenological synchronization. Here we investigate the spatial pattern of temperature sensitivity of spring and autumn phenology with altitude, latitude, and longitude during 1982–2016 across mid‐ and high‐latitude Northern Hemisphere (north of 30°N). We find distinct spatial patterns of temperature sensitivity of spring phenology (hereafter “spring S_T”) among altitudinal, latitudinal, and longitudinal gradient. Spring S_T decreased with altitude mostly over eastern Europe, whereas the opposite occurs in eastern North America and the north China plain. Spring S_T decreased with latitude mainly in the boreal regions of North America, temperate Eurasia, and the arid/semi‐arid regions of Central Asia. This distribution may be related to the increased temperature variance, decreased precipitation, and radiation with latitude. Compared to spring S_T, the spatial pattern of temperature sensitivity of autumn phenology (hereafter “autumn S_T”) is more heterogeneous, only showing a clear spatial pattern of autumn S_T along the latitudinal gradient. Our results highlight the three‐dimensional view to understand the phenological response to climate change and provide new metrics for evaluating phenological models. Accordingly, establishing a dense, high‐quality three‐dimensional observation system of phenology data is necessary for enhancing our ability to both predict phenological changes under changing climatic conditions and to facilitate sustainable management of ecosystems.     

Metabolic coping strategies in cold tolerant reptiles

The reality of metabolic cold adaptation in ectotherms is disputed. Reptiles differ in many important aspects of their thermal ecology from aquatic ectotherms, and their thermophysiology is therefore difficult to analyze in conventional terms. Evidence is presented in support of the view that both phenotypic metabolic cold acclimation and genotypic metabolic cold adaptation are important coping strategies in cold tolerant reptiles. Functional explanations of these paradoxical adaptations are discussed in the light of a multidimensional energetic model of the reptilian thermal niche.