Heat-avoidance behavior associates with thermal sensitivity rather than tolerance in aphid assemblages.

How to predict animals' heat-avoidance behaviors is critical since behavior stands the first line for animals dealing with frequent heat events under ongoing climate warming. However, the discrepancy between the scarcity of research on heat-avoidance behaviors and the commonness of eco-physiological data for thermal tolerance and for thermal sensitivity such as the temperature-dependent survival time makes it difficult to link physiological thermal traits to heat-avoidance behavior. Aphids usually suck plant sap on a fixed site on the host plants at moderate temperatures, but they will leave and seek cooler feeding sites under stressful temperatures. Here we take the cereal aphid assemblages comprising different species with various development stages as a model system. We tested the hypotheses that heat tolerance (critical thermal maximum, CTmax) or heat sensitivity (temperature-dependent declining rate of survival time, similarly hereinafter) would associate with the temperature at which aphid activate heat-avoidance behavior. Specifically, we hypothesized the aphids with less heat tolerance or greater heat sensitivity would take a lower heat risk by leaving the host plant earlier. By mimicking the linear increase in ambient temperature during the daytime, we measured the CTmax and the heat-avoidance temperature (HAT, at which aphids leave the host plant to find cooler places) to understand their heat tolerance and heat-avoidance behavior. Then, we tested the survival time of aphids at different temperatures and calculated the slope of survival time declining with temperature to assess their heat sensitivity (HS). Finally, we examined the relationships between CTmax and HAT and between HS and HAT to understand if the heat-avoidance behavior associates with heat tolerance or with heat sensitivity. The results showed that HS and HAT had a strong correlation, with more heat sensitive individuals displayed lower HAT. By contrast, CTmax and HAT had a weak correlation. Our results thus provide evidence that heat sensitivity is a more reliable indicator than thermal tolerance linking with the heat-avoidance behavior in the aphid assemblages. Most existing studies use the indexes related to thermal tolerance to predict warming impacts. Our findings highlight the urgency to incorporate thermal sensitivity when predicting animal responses to climate change.

Interspecific differences in thermal tolerance landscape explain aphid community abundance under climate change.

A single critical thermal limit is often used to explain and infer the impact of climate change on geographic range and population abundance. However, it has limited application in describing the temporal dynamic and cumulative impacts of extreme temperatures. Here, we used a thermal tolerance landscape approach to address the impacts of extreme thermal events on the survival of co-existing aphid species (Metopolophium dirhodum, Sitobion avenae and Rhopalosiphum padi). Specifically, we built the thermal death time (TDT) models based on detailed survival datasets of three aphid species with three ages across a broad range of stressful high (34-40 °C) and low (-3∼-11 °C) temperatures to compare the interspecific and developmental stage variations in thermal tolerance. Using these TDT parameters, we performed a thermal risk assessment by calculating the potential daily thermal injury accumulation associated with the regional temperature variations in three wheat-growing sites along a latitude gradient. Results showed that M. dirhodum was the most vulnerable to heat but more tolerant to low temperatures than R. padi and S. avenae. R. padi survived better at high temperatures than Sitobion avenae and M. dirhodum but was sensitive to cold. R. padi was estimated to accumulate higher cold injury than the other two species during winter, while M. dirhodum accrued more heat injury during summer. The warmer site had higher risks of heat injury and the cooler site had higher risks of cold injury along a latitude gradient. These results support recent field observations that the proportion of R. padi increases with the increased frequency of heat waves. We also found that young nymphs generally had a lower thermal tolerance than old nymphs or adults. Our results provide a useful dataset and method for modelling and predicting the consequence of climate change on the population dynamics and community structure of small insects.

Survive a Warming Climate: Insect Responses to Extreme High Temperatures.

Global change includes a substantial increase in the frequency and intensity of extreme high temperatures (EHTs), which influence insects at almost all levels. The number of studies showing the ecological importance of EHTs has risen in recent years, but the knowledge is rather dispersed in the contemporary literature. In this article, we review the biological and ecological effects of EHTs actually experienced in the field, i.e., when coupled to fluctuating thermal regimes. First, we characterize EHTs in the field. Then, we summarize the impacts of EHTs on insects at various levels and the processes allowing insects to buffer EHTs. Finally, we argue that the mechanisms leading to positive or negative impacts of EHTs on insects can only be resolved from integrative approaches considering natural thermal regimes. Thermal extremes, perhaps more than the gradual increase in mean temperature, drive insect responses to climate change, with crucial impacts on pest management and biodiversity conservation.

Dynamics of heat shock protein responses to thermal stress changes after metamorphosis in a lepidopteran insect.

In the last decade, unexpected high temperatures have been frequent in spring and early summer. Numerous studies have shown that such thermal stress has substantial effects on life-history traits that influence fitness of insects, but few have examined expression dynamics of heat shock proteins (Hsps) across developmental stages, especially as regards potential carry-over effects at the transcriptional level across metamorphosis. We exposed pupae of the oriental fruit moth ("OFM," Grapholita molesta Busck) to mild heat stress (38°C, 6 h) and then quantified expression patterns of six Hsps (Hsp90, 70, 60, 40, 21, and 11) from pupal through adult stages. Almost all Hsps showed a higher expression immediately after pupae were heat-stressed, but later dropped to normal levels after metamorphosis. Although upregulation of Hsps is transient and the effects carry over longer to early adult stage, upregulation will nonetheless have positive effects on adult fitness. The fitness of some insects may benefit from higher expression of chaperon genes after mild stress, in the form of higher fecundity and longer lifespan, as a carry-over effect. These results suggest that mild thermal stress can change genetic expression that later boosts adult fitness through a cascade effect.

Are extreme high temperatures at low or high latitudes more likely to inhibit the population growth of a globally distributed aphid?

Although climate warming can increase both mean temperature and its variability, it is often the effects of climate warming on short periods of extreme temperatures that are expected to have particularly large physiological and ecological consequences. Understanding the vulnerability of organisms at various latitudes to climate extremes is thus critical for understanding warming effects on regional biodiversity conservation and ecosystem management. While previous studies have shown that thermal responses depend on temperature regimes that organisms have previously experienced, this issue has not been considered much when comparing the effects of temperature extremes at different latitudes. To fill this gap, here we manipulated different combinations of amplitude and duration of daily high temperature extremes to simulate conditions at different latitudes. We tested the effects of those regimes on life-history traits and fitness of a globally-distributed aphid species, Rhopalosiphum padi. We compared our results with previous studies to better understand the extent to which these regimes affect conclusions based on comparisons under different mean temperatures. As a consequence of asymmetrical thermal performance curves, we hypothesized that the temperature regimes with higher daily maximum temperatures at higher latitudes would cause strong negative effects. Our results showed that these regimes with thermal extremes caused substantial decreases in life-history traits and fitness relative to the predictions from different mean temperatures. Specifically, the regime with higher daily maximum temperature reflecting a higher mid-latitude location had larger impacts on development, reproduction and population fitness than the regime representing a lower mid-latitude location. These findings have implications for understanding the vulnerability of organisms across latitudes to increasingly frequent extreme heat events under ongoing climate warming.

Wide diurnal temperature variation inhibits larval development and adult reproduction in the diamondback moth.

Although thermal variability is known to influence the performance of ectotherms, there is limited information on the influence of variation in diurnal temperature range (DTR) during early developmental stages. Here we test variation in DTR ( ±0 °C, ±4 °C, ±6 °C, ±8 °C, ±10 °C and±12 °C) with a constant mean temperature (25 °C) on the larval stage of diamondback moth (DBM), Plutella xylostella (L.), and assess immediate effects on larval development and survival, and delayed effects on pupal development and survival and adult longevity and reproductive performance. Wide amplitudes ( ±10 °C and±12 °C) inhibited larval development and adult performance, but increased the proportion of eggs laid early, while moderate amplitudes ( ±4 °C, ±6 °C and±8 °C) resulted in only minor effects. Larval development rate under wide amplitudes ( ±10 °C and±12 °C) was faster than predicted by a degree-hour model. Overall, the intrinsic rate of increase of the population was lowered with increasing DTR, despite mean temperatures being the same. These findings highlight marked cross-stage effects of DTR when temperatures fluctuate substantially, likely linked to maximum temperature, and they emphasize the importance of considering DTR when assessing effects of climate warming.

Extreme temperature events alter demographic rates, relative fitness, and community structure.

The frequency and magnitude of extreme events are predicted to increase under future climate change. Despite recent advancements, we still lack a detailed understanding of how changes in the frequency and amplitude of extreme climate events are linked to the temporal and spatial structure of natural communities. To answer this question, we used a combination of laboratory experiments, field experiments, and analysis of multi-year field observations to reveal the effects of extreme high temperature events on the demographic rates and relative dominance of three co-occurrence aphid species which differ in their transmission efficiency of different agricultural pathogens. We then linked the geographical shift in their relative dominance to frequent extreme high temperatures through a meta-analysis. We found that both frequency and amplitude of extreme high temperatures altered demographic rates of species. However, these effects were species-specific. Increasing the frequency and amplitude of extreme temperature events altered which species had the highest fitness. Importantly, this change in relative fitness of species was consistent with significant changes in the relative dominance of species in natural communities in a 1 year long field heating experiment and 6 year long field survey of natural populations. Finally, at a global spatial scale, we found the same relationship between relative abundance of species and frequency of extreme temperatures. Together, our results indicate that changes in frequency and amplitude of extreme high temperatures can alter the temporal and spatial structure of natural communities, and that these changes are driven by asymmetric effects of high temperatures on the demographic rates and fitness of species. They also highlight the importance of understanding how extreme events affect the life-history of species for predicting the impacts of climate change at the individual and community level, and emphasize the importance of using a broad range of approaches when studying climate change.

Daily temperature extremes play an important role in predicting thermal effects.

Organisms in natural environments experience diel temperature fluctuations, including sporadic extreme conditions, rather than constant temperatures. Studies based mainly on model organisms have tended to focus on responses to average temperatures or short-term heat stress, which overlooks the potential impact of daily fluctuations, including stressful daytime periods and milder night-time periods. Here, we focus on daily maximum temperatures, while holding night-time temperatures constant, to specifically investigate the effects of high temperature on demographic parameters and fitness in the English grain aphid Sitobion avenae. We then compared the observed effects of different daily maximum temperatures with predictions from constant temperature-performance expectations. Moderate daily maximum temperatures depressed aphid performance while extreme conditions had dramatic effects, even when mean temperatures were below the critical maximum. Predictions based on daily average temperature underestimated negative effects of temperature on performance by ignoring daily maximum temperature, while predictions based on daytime maximum temperatures overestimated detrimental impacts by ignoring recovery under mild night-time temperatures. Our findings suggest that daily maximum temperature will play an important role in regulating natural population dynamics and should be considered in predictions. These findings have implications for natural population dynamics, particularly when considering the expected increase in extreme temperature events under climate change.

Stage-specific heat effects: timing and duration of heat waves alter demographic rates of a global insect pest.

The frequency and duration of periods with high temperatures are expected to increase under global warming. Thus, even short-lived organisms are increasingly likely to experience periods of hot temperatures at some point of their life-cycle. Despite recent progress, it remains unclear how various temperature experiences during the life-cycle of organisms affect demographic traits. We simulated hot days (daily mean temperature of 30 °C) increasingly experienced under field conditions and investigated how the timing and duration of such hot days during the life cycle of Plutella xylostella affects adult traits. We show that hot days experienced during some life stages (but not all) altered adult lifespan, fecundity, and oviposition patterns. Importantly, the effects of hot days were contingent on which stage was affected, and these stage-specific effects were not always additive. Thus, adults that experience different temporal patterns of hot periods (i.e., changes in timing and duration) during their life-cycle often had different demographic rates and reproductive patterns. These results indicate that we cannot predict the effects of current and future climate on natural populations by simply focusing on changes in the mean temperature. Instead, we need to incorporate the temporal patterns of heat events relative to the life-cycle of organisms to describe population dynamics and how they will respond to future climate change.

Night warming on hot days produces novel impacts on development, survival and reproduction in a small arthropod.

An asymmetric increase in night-time temperatures (NTs) on hot days is one of the main features of global climate change. But the biological effects of an increased night-time temperature combined with high daytime temperature are unclear. We used six thermal regimens to simulate NTs on hot days and investigated the effects of night warming on life-history traits of the English grain aphid Sitobion avenae. Experimental temperatures fluctuated in continuous diurnal cycles, increasing from 27 °C to a maximum 35 °C and then declining to 27 °C gradually before further dropping to different minima (13, 16, 19, 21, 23 or 25 °C) representing NTs. When compared to expectations based on constant temperatures, night warming raised the optimum temperature for development by 3 °C, in contrast to results from experiments where temperature variability was altered symmetrically or in a parallel manner. Night warming also reduced aphid survival under heat from 75% to 37% and depressed adult performance by up to 50%. Overall, night warming exacerbated the detrimental effects of hot days on the intrinsic rate of population increase, which was predicted to drop by 30% when night-time minimum temperatures exceeded 20 °C. Our novel findings on development challenge the 'Kaufmann effect', suggesting this is inapplicable to night warming likely to be encountered in nature. Although many average temperature models predict increasing pest outbreaks, our results suggest that outbreaks of some species might decrease due to the effects of night warming on population dynamics.

Age-stage two-sex life tables of Panonychus ulmi (Acari: Tetranychidae), on different apple varieties.

To understand the influence of different apple varieties on the development and reproduction of the European red mite, Panonychus ulmi (Koch) (Acari: Tetranychidae), age-stage two-sex life tables of P. ulmi on 'Fuji,' 'Starkrimson Delicious,' 'Golden Delicious,' and 'Granny Smith' varieties were constructed under laboratory conditions at 23 +/- 1 degrees C, 75 +/- 5% relative humidity, and a photoperiod of 16:8 (L:D) h. Results showed that total development time of immature females was shorter on Fuji than on the other varieties, and this was because of its shorter egg duration. Immature survival of P. ulmi was 74.51-78.00% among four apple varieties, and no significant differences were found. The total fecundity per female was significantly higher on Golden Delicious (34.12 eggs per female) than that on Fuji (27.15 eggs per female), Starkrimson Delicious (25.15 eggs per female), and Granny Smith (20.62 eggs per female). Based on the intrinsic rate of population increase, Fuji and Golden Delicious were more suitable than Starkrimson Delicious and Granny Smith.

The interspecific variations in molecular responses to various doses of heat and cold stress: The case of cereal aphids.

Insects are currently subjected to unprecedented thermal stress due to recent increases in the frequency and amplitude of temperature extremes. Understanding molecular responses to thermal stress is critically important to appreciate how species react to thermal stress. Three co-occurring cosmopolitan species are found within the guild of cereal aphids: Sitobion avenae, Ropalosiphum padi and Metopolophium dirhodum. Earlier reports have shown that increasing frequency of temperature extremes causes a shift in dominant species within guilds of cereal aphids by differently altering the population's growth. We hypothesize that a differential molecular response to stress among species may partially explain these changes. Heat shock proteins (HSPs) are molecular chaperones well known to play an important role in protecting against the adverse effects of thermal stress. However, few studies on molecular chaperones have been conducted in cereal aphids. In this study, we compared the heat and cold tolerance between three aphid species by measuring the median lethal time (Lt50) and examined the expression profiles of seven hsp genes after exposures to comparable thermal injury levels and also after same exposure durations. Results showed that R. padi survived comparatively better at high temperatures than the two other species but was more cold-sensitive. Hsp genes were induced more strongly by heat than cold stress. Hsp70A was the most strongly up-regulated gene in response to both heat and cold stress. R. padi had more heat inducible genes and significantly higher mRNA levels of hsp70A, hsp10, hsp60 and hsp90 than the other two species. Hsps ceased to be expressed at 37 °C in M. dirhodum and S. avenae while expression was maintained in R. padi. In contrast, M. dirhodum was more cold tolerant and had more cold inducible genes than the others. These results confirm species-specific differences in molecular stress responses and suggest that differences in induced expression of hsps may be related to species' thermal tolerance, thus causing the changes in the relative abundance.

Climate change, host plant availability, and irrigation shape future region-specific distributions of the Sitobion grain aphid complex.

BACKGROUND: Understanding where species occur using species distribution models has become fundamental to ecology. Although much attention has been paid to invasive species, questions about climate change related range shifts of widespread insect pests remain unanswered. Here, we incorporated bioclimatic factors and host plant availability into CLIMEX models to predict distributions under future climate scenarios of major cereal pests of the Sitobion grain aphid complex (Sitobion avenae, S. miscanthi, and S. akebiae). Additionally, we incorporated the application of irrigation in our models to explore the relevance of a frequently used management practice that may interact with effects of climate change of the pest distributions. RESULTS: Our models predicted that the area potentially at high risk of outbreaks of the Sitobion grain aphid complex would increase from 41.3% to 53.3% of the global land mass. This expansion was underlined by regional shifts in both directions: expansion of risk areas in North America, Europe, most of Asia, and Oceania, and contraction of risk areas in South America, Africa, and Australia. In addition, we found that host plant availability limited the potential distribution of pests, while the application of irrigation expanded it. CONCLUSION: Our study provides insights into potential risk areas of insect pests and how climate, host plant availability, and irrigation affect the occurrence of the Sitobion grain aphid complex. Our results thereby support agricultural policy makers, farmers, and other stakeholders in their development and application of management practices aimed at maximizing crop yields and minimizing economic losses. © 2023 Society of Chemical Industry.

Correction: Wang et al. Current and Potential Future Global Distribution of the Raisin Moth Cadra figulilella (Lepidoptera: Pyralidae) under Two Different Climate Change Scenarios. Biology 2023, 12, 435.

In the original publication [...].

Current and Potential Future Global Distribution of the Raisin Moth Cadra figulilella (Lepidoptera: Pyralidae) under Two Different Climate Change Scenarios.

Global trade facilitates the introduction of invasive species that can cause irreversible damage to agriculture and the environment, as well as stored food products. The raisin moth (Cadra figulilella) is an invasive pest that poses a significant threat to fruits and dried foods. Climate change may exacerbate this threat by expanding moth's distribution to new areas. In this study, we used CLIMEX and MaxEnt niche modeling tools to assess the potential global distribution of the raisin moth under current and future climate change scenarios. Our models projected that the area of suitable distribution for the raisin moth could increase by up to 36.37% by the end of this century under high emission scenario. We also found that excessive precipitation decreased the probability of raisin moth establishment and that the optimum temperature range for the species during the wettest quarter of the year was 0-18 °C. These findings highlight the need for future research to utilize a combined modeling approach to predict the distribution of the raisin moth under current and future climate conditions more accurately. Our results could be used for environmental risk assessments, as well as to inform international trade decisions and negotiations on phytosanitary measures with regards to this invasive species.

Parasitoid ecology along geographic gradients: lessons for climate change studies.

One method to study the impact of climate change on host-parasitoid relationships is to compare populations along geographical gradients in latitude, altitude, or longitude. Indeed, temperatures, which vary along geographic gradients, directly shape the life traits of parasitoids and indirectly shift their populations through trophic interactions with hosts and plants. We explored the pros and cons of using these comparisons along gradients. We highlighted that the longitudinal gradients, although understudied, are well correlated to winter warming and summer heat waves and we draw attention to the impact of the increase in extreme events, which will probably be the determining parameters of the effect of climate change on host-parasitoid relationships.

Potential distribution of invasive crop pests under climate change: incorporating mitigation responses of insects into prediction models.

Climate change facilitates biological invasions globally. Predicting potential distribution shifts of invasive crop pests under climate change is essential for global food security in the context of ongoing world population increase. However, existing predictions often omit the capacity of crop pests to mitigate the impacts of climate change by using microclimates, as well as through thermoregulation, life history variation and evolutionary responses. Microclimates provide refugia buffering climate extremes. Thermoregulation and life history variation can reduce the effects of diurnal and seasonal temperature variability. Evolutionary responses allow insects to adapt to long-term climate change. Neglecting these ecological processes may lead to overestimations in the negative impacts of climate change on invasive pests whereas in turn cause underestimations in their range expansions. To improve model predictions, we need to incorporate the fine-scale microclimates experienced by invasive crop pests and the mitigation responses of insects to climate change into species distribution models.

Bacterial Symbionts Confer Thermal Tolerance to Cereal Aphids Rhopalosiphum padi and Sitobion avenae.

High-temperature events are evidenced to exert significant influence on the population performance and thermal biology of insects, such as aphids. However, it is not yet clear whether the bacterial symbionts of insects mediate the thermal tolerance traits of their hosts. This study is intended to assess the putative association among the chronic and acute thermal tolerance of two cereal aphid species, Rhopalosiphum padi (L.) and Sitobion avenae (F.), and the abundance of their bacterial symbionts. The clones of aphids were collected randomly from different fields of wheat crops and were maintained under laboratory conditions. Basal and acclimated CTmax and chronic thermal tolerance indices were measured for 5-day-old apterous aphid individuals and the abundance (gene copy numbers) of aphid-specific and total (16S rRNA) bacterial symbionts were determined using real-time RT-qPCR. The results reveal that R. padi individuals were more temperature tolerant under chronic exposure to 31 °C and also exhibited about 1.0 °C higher acclimated and basal CTmax values than those of S. avenae. Moreover, a significantly higher bacterial symbionts' gene abundance was recorded in temperature-tolerant aphid individuals than the susceptible ones for both aphid species. Although total bacterial (16S rRNA) abundance per aphid was higher in S. avenae than R. padi, the gene abundance of aphid-specific bacterial symbionts was nearly alike for both of the aphid species. Nevertheless, basal and acclimated CTmax values were positively and significantly associated with the gene abundance of total symbiont density, Buchnera aphidicola, Serratia symbiotica, Hamilton defensa, Regiella insecticola and Spiroplasma spp. for R. padi, and with the total symbiont density, total bacteria (16S rRNA) and with all aphid-specific bacterial symbionts (except Spiroplasma spp.) for S. avenae. The overall study results corroborate the potential role of the bacterial symbionts of aphids in conferring thermal tolerance to their hosts.

Climate warming promotes pesticide resistance through expanding overwintering range of a global pest.

Climate change has the potential to change the distribution of pests globally and their resistance to pesticides, thereby threatening global food security in the 21st century. However, predicting where these changes occur and how they will influence current pest control efforts is a challenge. Using experimentally parameterised and field-tested models, we show that climate change over the past 50 years increased the overwintering range of a global agricultural insect pest, the diamondback moth (Plutella xylostella), by ~2.4 million km2 worldwide. Our analysis of global data sets revealed that pesticide resistance levels are linked to the species' overwintering range: mean pesticide resistance was 158 times higher in overwintering sites compared to sites with only seasonal occurrence. By facilitating local persistence all year round, climate change can promote and expand pesticide resistance of this destructive species globally. These ecological and evolutionary changes would severely impede effectiveness of current pest control efforts and potentially cause large economic losses.

Aged virgin adults respond to extreme heat events with phenotypic plasticity in an invasive species, Drosophila suzukii.

Climate warming has increased the frequency of extreme heat events. Alien species usually invade new areas with a low-density population and often have limited mating opportunities due to the unsynchronized emergence of adults. Early-emerging virgin adults often have to wait to mate with later-emerging partners at the cost of aging, which reduces thermal tolerance. To understand the adaptive strategies of virgin males/females versus those of mated males/females in response to heat stress during aging, we conducted a fully factorial experiment to test the basal and plastic heat tolerance (CTmax, critical thermal maximum) of males and females with different mating statuses (virgin and mated) at different ages (5, 10, and 15 days after eclosion) after different acclimation regimes (null, rapid and developmental heat acclimation) in a well-known invasive species, Drosophila suzukii. We found that mating could change the heat tolerance of adults during aging. Mated females had higher basal heat tolerance than virgin females, while mated males had lower tolerance than virgin males. Mating could generally decrease the acclimation capacity (i.e., plasticity of heat tolerance) during aging. Aged virgin adults had a much higher acclimation capacity than aged mated adults. Our findings suggest that phenotypic plasticity of heat tolerance may be a main strategy used by virgin adults to cope with heat events. The phenotypic plasticity of thermal tolerance could increase the invasion success of alien species in new areas by allowing them to rapid respond to local temperature changes.