Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands

Biological effects of climate change are expected to vary geographically, with a strong signature of latitude. For ectothermic animals, there is systematic latitudinal variation in the relationship between climate and thermal performance curves, which describe the relationship between temperature and an organism's fitness. Here, we ask whether these documented latitudinal patterns can be generalized to predict arthropod responses to warming across mid‐ and high temperate latitudes, for taxa whose thermal physiology has not been measured. To address this question, we used a novel natural experiment consisting of a series of urban warming gradients at different latitudes. Specifically, we sampled arthropods from a single common street tree species across temperature gradients in four US cities, located from 35.8 to 42.4° latitude. We captured 6746 arthropods in 34 families from 111 sites that varied in summer average temperature by 1.7–3.4 °C within each city. Arthropod responses to warming within each city were characterized as Poisson regression coefficients describing change in abundance per °C for each family. Family responses in the two midlatitude cities were heterogeneous, including significantly negative and positive effects, while those in high‐latitude cities varied no more than expected by chance within each city. We expected high‐latitude taxa to increase in abundance with warming, and they did so in one of the two high‐latitude cities; in the other, Queens (New York City), most taxa declined with warming, perhaps due to habitat loss that was correlated with warming in this city. With the exception of Queens, patterns of family responses to warming were consistent with predictions based on known latitudinal patterns in arthropod physiology relative to regional climate. Heterogeneous responses in midlatitudes may be ecologically disruptive if interacting taxa respond oppositely to warming.     

Infrared laser‐mediated local gene induction in medaka,zebrafish and Arabidopsis thaliana

Heat shock promoters are powerful tools for the precise control of exogenous gene induction in living organisms. In addition to the temporal control of gene expression, the analysis of gene function can also require spatial restriction. Recently, we reported a new method for in vivo, single‐cell gene induction using an infrared laser‐evoked gene operator (IR‐LEGO) system in living nematodes (Caenorhabditis elegans). It was demonstrated that infrared (IR) irradiation could induce gene expression in single cells without incurring cellular damage. Here, we report the application of IR‐LEGO to the small fish, medaka (Japanese killifish; Oryzias latipes) and zebrafish (Danio rerio), and a higher plant (Arabidopsis thaliana). Using easily observable reporter genes, we successfully induced gene expression in various tissues in these living organisms. IR‐LEGO has the potential to be a useful tool in extensive research fields for cell/tissue marking or targeted gene expression in local tissues of small fish and plants.     

Differential regulation of polygalacturonase and pectin methylesterase gene expression during and after heat stress in ripening tomato (Lycopersicon esculentum Mill.) fruits

The effects of extended heat stress on polygalacturonase (PG; EC 3.2.1.15) and pectin methylesterase (PME; EC 3.1.1.11) gene expression at mRNA, protein and activity levels in ripening tomato fruits were investigated. Steady state levels of PG mRNA declined at temperatures of 27°C and above, and a marked reduction in PG protein and activity was observed at temperatures of 32°C and above. Exogenous ethylene treatment did not reverse heat stress-induced inhibition of PG gene expression. Transfer of heat-stressed fruits to 20°C partly restored PG mRNA accumulation, but the rate of PG mRNA accumulation declined exponentially with duration of heat stress. Heat stress-induced inhibition of PME mRNA accumulation was recoverable even after 14 days of heat stress. In fruits held at 34°C, both PG and PME protein and activity continued to accumulate for about 4 days, but thereafter PG protein and activity declined while little change was observed in PME protein and activity. In spite of increases in mRNA levels of both PG and PME during the recovery of heat-stressed fruit at 20°C, levels of PG protein and activity declined in fruits heat-stressed for four or more days while PME protein and activity levels remained unchanged. Collectively, these data suggest that PG gene expression is being gradually and irreversibly shut off during heat stress, while PME gene expression is much less sensitive to heat stress.     

Lethal and sublethal behavioural responses of saline water beetles to acute heat and osmotic stress

1. As species' physiological breadth determines their potential to deal with environmental changes, and influences individuals' survival and the persistence of populations, information about lethal and sublethal responses could be fundamental for conservation purposes. 2. We used a standard experimental approach to explore mortality and behavioural avoidance responses (i.e. flight and emersion from the water) to a combination of acute heat and osmotic stress on six species of saline water beetles (belonging to Enochrus, Nebrioporus, and Ochthebius genera). 3. Heat stress affected survival and behavioural responses in all of the species, whereas osmotic stress and the interaction between both stressors only showed significant effects for the Ochthebius genus. Behavioural and survival patterns were highly interrelated across the stress gradients. The Enochrus and Nebrioporus studied species showed maximum avoidance activity at 35–40 °C, and a short (< 30 min) exposure to 45 °C was lethal. Ochthebius species were the most heat tolerant and displayed increasing behavioural responses with increasing temperature. In the Nebrioporus and Ochthebius genera, the species occupying lotic, more environmentally stable habitats, showed greater mortality, and avoidance responses were higher or initiated at lower stress thresholds than lentic species. In contrast, both Enochrus species displayed a similar mortality, and the lentic species E. bicolor emerged and flew more than the lotic E. falcarius, in concordance with its higher dispersal capacity. 4. Avoidance responses could provide interesting information about species' physiological amplitudes as a complement to lethal responses. The lotic species here studied showed narrower physiological amplitude (i.e. N. baeticus and O. glaber) or lower dispersal ability (i.e. E. falcarius) than their lentic relatives; both traits could result in a higher vulnerability of lotic species to thermal habitat changes.     

Temperature‐induced water stress in high‐latitude forests in response to natural and anthropogenic warming

The Arctic is particularly sensitive to climate change, but the independent effects of increasing atmospheric CO₂ concentration (pCO₂) and temperature on high‐latitude forests are poorly understood. Here, we present a new, annually resolved record of stable carbon isotope (δ¹³C) data determined from Larix cajanderi tree cores collected from far northeastern Siberia in order to investigate the physiological response of these trees to regional warming. The tree‐ring record, which extends from 1912 through 1961 (50 years), targets early twentieth‐century warming (ETCW), a natural warming event in the 1920s to 1940s that was limited to Northern hemisphere high latitudes. Our data show that net carbon isotope fractionation (Δ¹³C), decreased by 1.7‰ across the ETCW, which is consistent with increased water stress in response to climate warming and dryer soils. To investigate whether this signal is present across the northern boreal forest, we compiled published carbon isotope data from 14 high‐latitude sites within Europe, Asia, and North America. The resulting dataset covered the entire twentieth century and spanned both natural ETCW and anthropogenic Late Twentieth‐Century Warming (~0.7 °C per decade). After correcting for a ~1‰ increase in Δ¹³C in response to twentieth century pCO₂ rise, a significant negative relationship (r = ?0.53, P < 0.0001) between the average, annual Δ¹³C values and regional annual temperature anomalies is observed, suggesting a strong control of temperature on the Δ¹³C value of trees growing at high latitudes. We calculate a 17% increase in intrinsic water‐use efficiency within these forests across the twentieth century, of which approximately half is attributed to a decrease in stomatal conductance in order to conserve water in response to drying conditions, with the other half being attributed to increasing pCO₂. We conclude that annual tree‐ring records from northern high‐latitude forests record the effects of climate warming and pCO₂ rise across the twentieth century.     

Evaluation of reference genes for quantitative real-time PCR analysis of messenger RNAs and microRNAs in rainbow trout Oncorhynchus mykiss under heat stress

We assessed the expression stability of several messenger (m)RNAs and micro (mi)RNAs from liver and head kidney of rainbow trout Oncorhynchus mykiss using high-throughput RNA sequencing (RNA-seq) and miRNA-seq data. Additionally, four commonly used reference genes and one small non-coding RNA (u6) were also selected to identify ideal reference mRNAs and miRNAs for quantitative real-time (qrt)-PCR analysis of heat stress responses. GeNorm, NormFinder, BestKeeper and comparative ΔC_t were employed for analysis of qrt-PCR data to systematically assess the expression stability of candidate mRNAs and miRNAs and stability was ranked using geometric means. β-actin and ef1-α were the most stably expressed reference mRNAs in liver and head kidney, respectively and ssa-mir-26a-5p and ssa-mir-462b-5p were the most stably expressed miRNAs in these tissues. This is the first identification of appropriate reference mRNAs and miRNAs for qrt-PCR analysis of O. mykiss under heat stress.     

Real‐time cell analysis and heat shock protein gene expression in the TcA Tribolium castaneum cell line in response to environmental stress conditions

The rust red flour beetle, Tribolium castaneum (Herbst, 1797) (Coleoptera: Tenebrionidae), is a pest of stored grain and one of the most studied insect model species. Some of the previous studies involved heat response studies in terms of survival and heat shock protein expression, which are regulated to protect other proteins against environmental stress conditions. In the present study, we characterize the impedance profile with the xCELLigence Real‐Time Cell Analyzer and study the effect of increased temperature in cell growth and viability in the cell line BCIRL‐TcA‐CLG1 (TcA) of T. castaneum. This novel system measures cells behavior in real time and is applied for the first time to insect cells. Additionally, cells are exposed to heat shock, increased salinity, acidic pH and UV‐A light with the aim of measuring the expression levels of Hsp27, Hsp68a, and Hsp83 genes. Results show a high thermotolerance of TcA in terms of cell growth and viability. This result is likely related to gene expression results in which a significant up‐regulation of all studied Hsp genes is observed after 1 h of exposure to 40 °C and UV light. All 3 genes show similar expression patterns, but Hsp27 seems to be the most affected. The results of this study validate the RTCA method and reveal the utility of insect cell lines, real‐time analysis and gene expression studies to better understand the physiological response of insect cells, with potential applications in different fields of biology such as conservation biology and pest management.     

Post‐heading heat stress and yield impact in winter wheat of China

Wheat is sensitive to high temperatures, but the spatial and temporal variability of high temperature and its impact on yield are often not known. An analysis of historical climate and yield data was undertaken to characterize the spatial and temporal variability of heat stress between heading and maturity and its impact on wheat grain yield in China. Several heat stress indices were developed to quantify heat intensity, frequency, and duration between heading and maturity based on measured maximum temperature records of the last 50 years from 166 stations in the main wheat‐growing region of China. Surprisingly, heat stress between heading and maturity was more severe in the generally cooler northern wheat‐growing regions than the generally warmer southern regions of China, because of the delayed time of heading with low temperatures during the earlier growing season and the exposure of the post‐heading phase into the warmer part of the year. Heat stress between heading and maturity has increased in the last decades in most of the main winter wheat production areas of China, but the rate was higher in the south than in the north. The correlation between measured grain yields and post‐heading heat stress and average temperature were statistically significant in the entire wheat‐producing region, and explained about 29% of the observed spatial and temporal yield variability. A heat stress index considering the duration and intensity of heat between heading and maturity was required to describe the correlation of heat stress and yield variability. Because heat stress is a major cause of yield loss and the number of heat events is projected to increase in the future, quantifying the future impact of heat stress on wheat production and developing appropriate adaptation and mitigation strategies are critical for developing food security policies in China and elsewhere.     

Short‐term heat stress impairs testicular functions in the American oyster,Crassostrea virginica: Molecular mechanisms and induction of oxidative stress and apoptosis in spermatogenic cells

Global temperature is increasing due to anthropogenic activities. Abnormal temperature has devastating effects on growth, reproduction, and development of aquatic organisms. In this study, we examined the effects of short‐term exposure to elevated temperatures (28 and 32°C for 1 week) on testicular functions, heat shock protein‐70 (HSP70), dinitrophenyl protein (DNP, a biomarker of reactive oxygen species [ROS]), and nitrotyrosine protein (NTP, an indicator of reactive nitrogen species [RNS]) expressions, protein carbonyl (PC, a measure of ROS) contents, nitrates/nitrites (NOx, a metabolite of nitric oxide) levels, extrapallial fluid (EPF) conditions, and cellular apoptosis in American oyster (Crassostrea virginica). Higher temperatures significantly decreased (~26%) sperm production in oysters compared with controls (24°C). HSP70, NTP, and DNP expressions were increased after heat exposure, consistent with increased EPF pH, and cellular apoptosis. The enhanced apoptosis in spermatogenic cells is associated with increased caspase 3/7 activity, PC contents, and NOx levels in testicular tissues. Together these results suggest that elevated temperature drastically increases oxidative stress and cellular apoptosis which in turn leads to decreased testicular functions in oysters. To the best of our knowledge, this study reports the first findings on the impacts of elevated temperatures on testicular functions in oysters.     

Gas exchange and water relations of spring wheat under full‐season infrared warming

Gas exchange and water relations were evaluated under full‐season in situ infrared (IR) warming for hard red spring wheat (Triticum aestivum L. cv. Yecora Rojo) grown in an open field in a semiarid desert region of the southwest USA. A temperature free‐air controlled enhancement (T‐FACE) apparatus utilizing IR heaters maintained canopy air temperature above 3.0 m Heated plots of wheat by 1.3 and 2.7 °C (0.2 and 0.3 °C below the targeted set‐points of Reference plots with dummy heaters) during daytime and nighttime, respectively. Control plots had no apparatus. Every 6 weeks during 2007–2009 wheat was sown under the three warming treatments (i.e., Control, Heated, Reference) in three replicates in a 3 × 3 Latin square (LSQ) design on six plantings during 4 months (i.e., January, March, September, December), or in a natural temperature variation treatment (i.e., Control) in three replicates in a randomized complete block (RCB) design on nine plantings during 7 months (i.e., January, February, April, June, July, August, October). Soil temperature (T_s) and volumetric soil‐water content (θ_s) were 1.3 °C warmer and 14% lower in Heated compared with Reference plots, respectively. Other than a 1% shading effect, no artifacts on gas exchange or water relations were associated with the IR warming apparatus. IR warming increased carbon gain characteristic of an increase in metabolic rates to higher temperature that may have been attributed to the well‐watered wheat crop and the supplemental irrigation that minimized plant‐to‐air water vapor pressure differences between IR‐warmed and nonwarmed plots. Nevertheless, seasonal oscillations in the IR warming response on carbon gain occurred. IR warming decreased leaf water status and provided thermal protection during freeze events. IR warming is an effective experimental methodology to investigate the impact of global climate change on agronomic cropping and natural ecosystems to a wide range of natural and artificially imposed air temperatures.     

Mating success at high temperature in highland‐ and lowland‐derived populations as well as in heat knock‐down selected Drosophila buzzatii

Thermal‐stress selection can affect multiple fitness components including mating success. Reproductive success is one of the most inclusive measures of overall fitness, and mating success is a major component of reproduction. However, almost no attention has been spent to test how mating success can be affected by thermal‐stress selection. In this study, we examine the mating success in the cactophilic Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae) derived from two natural populations that nearly represent the ends of an altitudinal cline for heat knock‐down resistance. Furthermore, we extended the analysis using laboratory lines artificially selected for high and low heat knock‐down resistance. Mating success at high temperature was found to be higher in the lowland than the highland population after a heat pre‐treatment. Moreover, individuals selected for heat knock‐down resistance showed higher mating success at high temperature than did individuals selected for low knock‐down resistance. These results indicate that adaptation to thermal stress can confer an advantage on fitness‐related traits including mating success and highlight the benefits of earlier heat exposure as an adaptive plastic response affecting mating success under stress of higher temperature.     

Cloning of heat shock protein genes from the brown planthopper,Nilaparvata lugens,and the small brown planthopper,Laodelphax striatellus,and their expression in relation to thermal stress

Three heat shock protein （HSP） genes （hsp70, hsc70, hsp90） were partially cloned from the brown planthopper Nilaparvata lugens and the small brown planthopper Laodelphax striatellus （Homoptera： Delphacidae）, which are serious pests of the rice plant. Sequence comparisons at the deduced amino acid level showed that the three HSPs of planthoppers were most homologous to corresponding HSPs of dipteran and lepidopteran species. Identities of both heat shock cognate 70 and HSP90 were higher than HSP70 in both species. Identity of the HSP70 between the two planthopper species was only 81%, a value much lower than seen among fly and moth groups. Effects of heat and cold shocks were demonstrated on expression of the three hsp genes in the two planthopper species. Heat shock （40 ℃） upregulated the hsp90 level but did not change the hsc70 level in either the nymph and adult stages of either species. On the other hand, the hsp70 level was only upregulated in L. striatellus. This heat shock response was prompt and lasted only for 1 h after treatment. In contrast, cold shock at 4℃ did not change the expression levels of any hsp in either species.     

Cloning of heat shock protein genes from the brown planthopper,Nilaparvata lugens,and the small brown planthopper,Laodelphax striatellus,and their expression in relation to thermal stress

Three heat shock protein (HSP) genes (hsp70, hsc70, hsp90) were partially cloned from the brown planthopper Nilaparvata lugens and the small brown planthopper Laodelphax striatellus (Homoptera: Delphacidae), which are serious pests of the rice plant. Sequence comparisons at the deduced amino acid level showed that the three HSPs of planthoppers were most homologous to corresponding HSPs of dipteran and lepi‐dopteran species. Identities of both heat shock cognate 70 and HSP90 were higher than HSP70 in both species. Identity of the HSP70 between the two planthopper species was only 81%, a value much lower than seen among fly and moth groups. Effects of heat and cold shocks were demonstrated on expression of the three hsp genes in the two planthopper species. Heat shock (40 °C) upregulated the hsp90 level but did not change the hsc70 level in either the nymph and adult stages of either species. On the other hand, the hsp70 level was only upregulated in L. striatellus. This heat shock response was prompt and lasted only for 1 h after treatment. In contrast, cold shock at 4°C did not change the expression levels of any hsp in either species.     

Chaperoning stem cells: a role for heat shock proteins in the modulation of stem cell self‐renewal and differentiation?

Self‐renewal and differentiation of stem cells are tightly regulated processes subject to intrinsic and extrinsic signals. Molecular chaperones and co‐chaperones, especially heat shock proteins (Hsp), are ubiquitous molecules involved in the modulation of protein conformational and complexation states. The function of Hsp, which are typically associated with stress response and tolerance, is well characterized in differentiated cells, while their role in stem cells remains unclear. It appears that embryonic stem cells exhibit increased stress tolerance and concomitant high levels of chaperone expression. This review critically evaluates stem cell research from a molecular chaperone perspective. Furthermore, we propose a model of chaperone‐modulated self‐renewal in mouse embryonic stem cells.     

烟蚜热激蛋白基因MpHsp70的克隆及在UV-B胁迫下的表达分析

【目的】为探讨烟蚜Myzus persicae适应UV-B胁迫的分子机制。【方法】采用RT-PCR和RACE技术克隆了烟蚜热激蛋白基因Hsp70的全长,利用生物信息学方法分析了其特征;采用实时荧光定量PCR检测了不同时长(0,15,30,60,90和120 min) UV-B胁迫下烟蚜成虫中该基因的相对表达量。【结果】克隆获得烟蚜Hsp70基因并命名为MpHsp70(GenBank登录号:MF509827),该基因全长为2 221 bp,开放阅读框(ORF) 1 965 bp,编码654个氨基酸,蛋白相对分子量为71. 41kD,等电点(p I)为5. 34,末端高度保守序列EEVD显示该蛋白属于胞质热激蛋白。系统进化关系分析表明,MpHsp70与多种昆虫的Hsp70的同源性较高,表现出Hsp70基因的高度保守性。实时荧光定量PCR分析表明,随着UV-B照射时间的延长,烟蚜成虫体内MpHsp70基因的表达量先上升后下降,当照射时间为30 min时表达量最大。【结论】烟蚜MpHsp70基因可以响应UV-B的胁迫,它可能在烟蚜适应UV-B胁迫过程中起到重要作用。     

Ocean cleaning stations under a changing climate: biological responses of tropical and temperate fish‐cleaner shrimp to global warming

Cleaning symbioses play an important role in the health of certain coastal marine communities. These interspecific associations often occur at specific sites (cleaning stations) where a cleaner organism (commonly a fish or shrimp) removes ectoparasites/damaged tissue from a ‘client’ (a larger cooperating fish). At present, the potential impact of climate change on the fitness of cleaner organisms remains unknown. This study investigated the physiological and biochemical responses of tropical (Lysmata amboinensis) and temperate (L. seticaudata) cleaner shrimp to global warming. Specifically, thermal limits (CTMax), metabolic rates, thermal sensitivity, heat shock response (HSR), lipid peroxidation [malondialdehyde (MDA) concentration], lactate levels, antioxidant (GST, SOD and catalase) and digestive enzyme activities (trypsin and alkaline phosphatase) at current and warming (+3 °C) temperature conditions. In contrast to the temperate species, CTMax values decreased significantly from current (24–27 °C) to warming temperature conditions (30 °C) for the tropical shrimp, where metabolic thermal sensitivity was affected and the HSR was significantly reduced. MDA levels in tropical shrimp increased dramatically, indicating extreme cellular lipid peroxidation, which was not observed in the temperate shrimp. Lactate levels, GST and SOD activities were significantly enhanced within the muscle tissue of the tropical species. Digestive enzyme activities in the hepatopancreas of both species were significantly decreased by warmer temperatures. Our data suggest that the tropical cleaner shrimp will be more vulnerable to global warming than the temperate Lysmata seticaudata; the latter evolved in a relatively unstable environment with seasonal thermal variations that may have conferred greater adaptive plasticity. Thus, tropical cleaning symbioses may be challenged at a greater degree by warming‐related anthropogenic forcing, with potential cascading effects on the health and structuring of tropical coastal communities (e.g. coral reefs).     

Standardized short‐term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites

Coral bleaching is one of the main drivers of reef degradation. Most corals bleach and suffer mortality at just 1–2°C above their maximum monthly mean temperatures, but some species and genotypes resist or recover better than others. Here, we conducted a series of 18‐hr short‐term acute heat stress assays side‐by‐side with a 21‐day long‐term heat stress experiment to assess the ability of both approaches to resolve coral thermotolerance differences reflective of in situ reef temperature thresholds. Using a suite of physiological parameters (photosynthetic efficiency, coral whitening, chlorophyll a, host protein, algal symbiont counts, and algal type association), we assessed bleaching susceptibility of Stylophora pistillata colonies from the windward/exposed and leeward/protected sites of a nearshore coral reef in the central Red Sea, which had previously shown differential mortality during a natural bleaching event. Photosynthetic efficiency was most indicative of the expected higher thermal tolerance in corals from the protected reef site, denoted by an increased retention of dark‐adapted maximum quantum yields at higher temperatures. These differences were resolved using both experimental setups, as corroborated by a positive linear relationship, not observed for the other parameters. Notably, short‐term acute heat stress assays resolved per‐colony (genotype) differences that may have been masked by acclimation effects in the long‐term experiment. Using our newly developed portable experimental system termed the Coral Bleaching Automated Stress System (CBASS), we thus highlight the potential of mobile, standardized short‐term acute heat stress assays to resolve fine‐scale differences in coral thermotolerance. Accordingly, such a system may be suitable for large‐scale determination and complement existing approaches to identify resilient genotypes/reefs for downstream experimental examination and prioritization of reef sites for conservation/restoration. Development of such a framework is consistent with the recommendations of the National Academy of Sciences and the Reef Restoration and Adaptation Program committees for new intervention and restoration strategies.