Joint Effects Of Temperature Research Articles

Detection and Attribution of Human‐Perceived Warming Over China

AbstractWhile previous studies have largely focused on anthropogenic warming characterized by surface air temperature, little is known about the behaviors of human‐perceived temperature (HPT), which describe the “feels‐like” equivalent temperature by considering the joint effects of temperature, humidity and/or wind speed. Here we adopted an optimal fingerprinting method to compare seasonal mean HPTs in China with those from simulations conducted with multiple climate models participating in the Coupled Model Intercomparison Project Phase 6. We found clear anthropogenic signals in the observational records of changes in both summer and winter HPTs over the period 1971–2020. Moreover, the anthropogenic greenhouse gas influence was robustly detected, with clear separation from natural and anthropogenic aerosol forcings. The anthropogenic greenhouse gas forcing plays the dominant role (>90%) of human‐perceived warming. Urbanization effects contribute slightly and moderately to the estimated trends in summer and winter HPTs, respectively, in addition to the effects of external forcing.

Identifying the critical windows and joint effects of temperature and PM2.5 exposure on small for gestational age

Identifying the critical windows and joint effects of temperature and PM2.5 exposure on small for gestational age

Joint effects of temperature and copper exposure on developmental and gene-expression responses of the marine copepod Tigriopus japonicus.

There is growing contamination of copper (Cu) in the marine environment, particularly after the ban of organotin compounds and the increase of the use of Cu-based antifouling paints. Although there are increasing research interests in temperature-dependent chemical toxicity to aquatic organisms, most existing studies focused on acute impacts of chemicals at high concentrations. This study aimed to investigate the interacting effect of temperature and copper exposure at environmentally relevant concentrations on survival and development in the marine copepod Tigriopus japonicus with a partial life-cycle toxicity test. Expressions of five stress response genes in the copepod, namely two glutathione S-transferases (GST-S and GST-O), two heat shock proteins (HSP70 and HSP90), and glutathione reductase (GR) were also investigated. The copepod's survival was significantly impaired at 15 °C after development to adult stage, while its developmental time reduced significantly with increasing temperature. Copper at the two environmentally relevant test concentrations had no significant impacts on these apical endpoints whereas the interaction between Cu and temperature was more significant in modulating gene expressions. GST-S, GST-O and HSP90 genes in copepods exposed to 100 µg Cu L-1 were significantly upregulated at 20 °C. At 32 °C, most genes were either insignificantly expressed or down-regulated, compared to the control, likely suggesting that thermal stress inhibited the copepod's antioxidative defense system. Overall, the results revealed that the joint Cu and thermal stresses have significantly elicited antioxidative system in the copepods. It clearly demonstrated the need for more fundamental studies about potential impacts of different environmental factors such as temperature on chemical toxicity under realistic scenario of marine pollution.

Identifying the critical windows and joint effects of temperature and PM2.5 exposure on small for gestational age

The potential critical windows for extreme ambient temperature, air pollution exposure and small for gestational age (SGA) are still unclear, and no study has explored their joint effects on SGA. In a national multi-center prospective cohort, we included 179,761 pairs of mother-infant from 16 counties of 8 provinces in China during 2014–2018. Daily averaged temperature and PM2.5 concentration were matched to the maternal residential address to estimate personal exposure. Extreme temperature exposures were categorized by a series of percentile in each meteorological and geographic division for the entire pregnancy, each trimester and gestational week (GA-week). Generalized linear mixed models (GLMMs) and distributed lag nonlinear models (DLNMs) were used to estimate the whole pregnancy-, trimester-specific, and weekly-specific associations of extreme temperature and PM2.5 exposures with SGA. Combined effects were evaluated with the relative excess risk due to interaction (RERI) and proportion attributable to interaction (AP). We observed that by referring to temperature at the 41st − 50th percentile, heat (>90th percentile) exposure during 13th − 29th GA-weeks was associated with SGA; odds ratio (OR) and 95 % confidence intervals (CI) was 1.16 (1.06, 1.28). For cold (<=10th percentile), inverse associations were observed during the 1st − 8th GA-weeks. PM2.5 exposure during the 2nd − 5th and 19th − 27th GA-weeks was associated with SGA, with the strongest association in the 2nd GA-week (OR = 1.0017, 95 %CI: 1.0001, 1.0034, for a 10 μg/m3 increase). No interactive effects between ambient temperature and PM2.5 on SGA were observed. Our findings suggest the weekly susceptibility windows for heat and PM2.5 exposure were primarily the gestational weeks within the 2nd trimester, therefore, corresponding protective measures should be conveyed to pregnant women during routine prenatal visits to reduce exposures.

Heat and Mass Transfer Kinetics on the Chemical and Sensory Quality of Arabica Coffee Beans

Roasting has been used by the coffee industry to promote changes in the physical and chemical structure of coffee beans that influence the sensory quality of coffee beverages. However, there are no standardization rules for the temperature and roasting time. Thus, this study evaluated the influence of four roasting profiles obtained by two different roasters on the chemical and sensory quality of the coffee bean. Baked, light, medium, and dark roasting were evaluated using medium infrared spectroscopy and cupping test. Individual and joint effects of temperature and time for each roasting profile were observed on the loss of grain mass. There are specific regions in the infrared spectrum that can be used as markers to discriminate the roasting profiles and the type of roaster used. Despite the difference observed in the ranges of the infrared spectra, the roasters did not present significant differences in the average of the final sensory notes. This result shows the need to use analytical chemical techniques together with sensory analysis in order to better determine differences between coffee samples. Therefore, differences observed in the chemical analyzes and in the sensory attributes of roasted coffee are related to the roasting profile and type of roaster.

Effects of Temperature and Salinity on Seed Germination of Three Common Grass Species.

Temperature and salinity significantly affect seed germination, but the joint effects of temperature and salinity on seed germination are still unclear. To explore such effects, a controlled experiment was conducted, where three temperature levels (i.e., 15, 20, and 25°C) and five salinity levels (i.e., 0, 25, 50, 100, and 200 mmol/L) were crossed, resulting in 15 treatments (i.e., 3 temperature levels × 5 salinity levels). Three typical grass species (Festuca arundinacea, Bromus inermis, and Elymus breviaristatus) were used, and 25 seeds of each species were sown in petri dishes under these treatments. Germination percentages and germination rates were calculated on the basis of the daily recorded germinated seed numbers of each species. Results showed that temperature and salinity significantly affected seed germination percentage and germination rate, which differed among species. Specifically, F. arundinacea had the highest germination percentage, followed by E. breviaristatus and B. inermis, with a similar pattern also found regarding the accumulated germination rate and daily germination rate. Generally, F. arundinacea was not sensitive to temperature within the range of 15–25°C, while the intermediate temperature level improved the germination percentage of B. inermis, and the highest temperature level benefited the germination percentage of E. breviaristatus. Moreover, F. arundinacea was also not sensitive to salinity within the range of 0–200 mmol/L, whereas high salinity levels significantly decreased the germination percentage of B. inermis and E. breviaristatus. Thus, temperature and salinity can jointly affect seed germination, but these differ among plant species. These results can improve our understanding of seed germination in saline soils in the face of climate change.

The lack of low temperature tolerance of tropical seagrasses strongly restricts their geographical distribution

Temperature is considered to be the main factor controlling the growth and eco-distribution of seagrasses. In this study, the joint effects of temperature (27, 24, 21, 18 and 15 °C) combined with three light intensities (0, 200 and 800 μmol m−2 s−1) on chlorophyll fluorescence and activities of antioxidative enzymes were examined for three tropical seagrasses Enhalus acoroides, Thalassia hemperichii and Cymodocea rotundata. The results showed that low temperature could damage the PSII donor side, PSII reaction centers and end electron acceptor pool, thereby directly injured their photosynthetic performance. Furthermore, the lower the temperature and the higher the light intensity, the greater the damage incurred. The antioxidant defense system of seagrass cannot sufficiently counter low temperature stress (for temperatures below 21 °C) under high light. These results help explain why the ecological distribution of these three tropical seagrasses is limited to the low tidal coastal area of warm tropical regions.

Assessment of vegetation growth and drought conditions using satellite-based vegetation health indices in Jing-Jin-Ji region of China

Terrestrial vegetation growth activity plays pivotal roles on regional development, which has attracted wide attention especially in water resources shortage areas. The paper investigated the spatiotemporal change characteristics of vegetation growth activity using satellite-based Vegetation Health Indices (VHIs) including smoothed Normalized Difference Vegetation Index (SMN), smoothed Brightness Temperature (SMT), Vegetation Condition Index (VCI), Temperature Condition Index (TCI) and VHI, based on 7-day composite temporal resolution and 16 km spatial resolution gridded data, and also estimated the drought conditions for the period of 1982–2016 in Jing-Jin-Ji region of China. The Niño 3.4 was used as a substitution of El Niño Southern Oscillation (ENSO) to reveal vegetation sensitivity to ENSO using correlation and wavelet analysis. Results indicated that monthly SMN has increased throughout the year especially during growing season, starts at approximate April and ends at about October. The correlation analysis between SMN and SMT, SMN and precipitation indicated that the vegetation growth was affected by joint effects of temperature and precipitation. The VCI during growing season was positive trends dominated and vice versa for TCI. The relationships between VHIs and drought make it possible to identify and quantify drought intensity, duration and affected area using different ranges of VHIs. Generally, the intensity and affected area of drought had mainly decreased, but the trends varied for different drought intensities, regions and time periods. Large-scale global climate anomalies such as Niño 3.4 exerted obvious impacts on the VHIs. The Niño 3.4 was mainly negatively correlated to VCI and positively correlated to TCI, and the spatial distributions of areas with positive (negative) correlation coefficients were mainly opposite. The linear relationships between Niño 3.4 and VHIs were in accordance with results of nonlinear relationships revealed using wavelet analysis. The results are of great importance to assess the vegetation growth activity, to monitor and quantify drought using satellite-based VHIs in Jing-Jin-Ji region.

Global Heat Wave Hazard Considering Humidity Effects during the 21st Century.

Humidity is a significant factor contributing to heat stress, but without enough consideration in studies of quantifying heat hazard or heat risk assessment. Here, the simplified wet-bulb globe temperature (WBGT) considering joint effects of temperature and humidity was utilized as a heat index and the number of annual total heat wave days (HWDs) was employed to quantify heat hazard. In order to evaluate the humidity effects on heat waves, we quantified the difference in the number of HWDs over global land based on air temperature and WBGT. Spatial and temporal changes in surface air temperature, relative humidity, WBGT, and the difference in HWDs were analyzed using multi-model simulations for the reference period (1986–2005) and different greenhouse gas emission scenarios. Our analysis suggests that annual mean WBGT has been increasing since 1986, which is consistent with the rising trend in surface air temperature despite a slight decrease in relative humidity. Additionally, changes in annual mean WBGT are smaller and more spatially uniform than those in annual mean air temperature as a cancelation effect between temperature and water vapor. Results show that there is an underestimation of around 40–140 days in the number of HWDs per year in most regions within 15° latitude of the equator (the humid and warm tropics) during 2076–2095 without considering humidity effects. However, the estimation of HWDs has limited distinction between using WBGT and temperature alone in arid or cold regions.

Vitelline utilization under the joint influences of temperature and photoperiod in the Ussuri catfish (Pelteobagrus ussuriensis)

The joint effects of temperature (18–30 °C) and photoperiod (0–24 h) on yolk utilization in the yolk-sac larvae of Pelteobagrus ussuriensis were investigated under laboratory conditions using a central composite design (face-centered) and response surface methodology. The results indicated that a suitable environmental temperature and photoperiod significantly increased yolk utilization. In contrast, unsuitable environments (e.g., low temperatures and complete darkness; low temperatures and continuous lighting; high temperatures and complete darkness; and high temperatures and continuous lighting) significantly reduced yolk utilization, albeit to varying degrees. Temperature affected yolk utilization independently of photoperiod, and was more important than photoperiod. Yolk utilization was synchronous with larval growth, showing the conversion of vitelline nutrients into larval growth. Predicated upon the reliable second-order relationship of yolk utilization with temperature and photoperiod, the optimal temperature-photoperiod combination was derived via model optimization and verified. The application of our results may help to increase the efficiency of seed production in the larviculture of this species.

Temperature modulates the interaction between fungicide pollution and disease: evidence from a Daphnia-microparasitic yeast model.

Temperature is expected to modulate the responses of organisms to stress. Here, we aimed to assess the influence of temperature on the interaction between parasitism and fungicide contamination. Specifically, using the cladoceran Daphnia as a model system, we explored the isolated and interactive effects of parasite challenge (yeast Metschnikowia bicuspidata) and exposure to fungicides (copper sulphate and tebuconazole) at two temperatures (17 and 20 °C), in a fully factorial design. Confirming a previous study, M. bicuspidata infection and copper exposure caused independent effects on Daphnia life history, whereas infection was permanently suppressed with tebuconazole exposure. Here, we show that higher temperature generally increased the virulence of the parasite, with the hosts developing signs of infection earlier, reproducing less and dying at an earlier age. These effects were consistent across copper concentrations, whereas the joint effects of temperature (which enhanced the difference between non-infected and infected hosts) and the anti-parasitic action of tebuconazole resulted in a more pronounced parasite × tebuconazole interaction at the higher temperature. Thus, besides independently influencing parasite and contaminant effects, the temperature can act as a modulator of interactions between pollution and disease.

Relationship of RNA/DNA ratio to somatic growth of Nile tilapia juveniles (Oreochromis niloticus) under joint effects of temperature and salinity

Tilapia juveniles are a very important life stage, and reliably assessing their growth performance is of prime importance in aquaculture production. The suitability of the RNA/DNA as a bioindicator for growth evaluation in tilapia has not yet been reported. In this study, we examined suitability of RNA/DNA ratio for assessing growth of tilapia juveniles and variation in the ratio under the concurrent influences of temperature and salinity using the central composite design and response surface methodology. Results showed that under our experimental conditions, the synergistic effects of temperature and salinity on the RNA/DNA ratio were highly significant (P < 0.01), and the ratio varied with the two factors in a nonlinear fashion; the temperature × salinity interaction was detected at 1% significance level, and had a negative effect on the RNA/DNA ratio particularly at higher temperatures. Temperature was found to have a greater influence on RNA/DNA ratios than salinity. A model of the relation between RNA/DNA, temperature and salinity was developed, with an R2 greater than 98%. The linear relationships of absolute growth, cumulative growth and specific growth of tilapia juveniles to RNA/DNA ratio all showed an R2 of greater than 95%. Our results indicate that the RNA/DNA ratio was a responsive and accurate bioindicator for evaluating the growth performance of juvenile tilapia. These ratio-based models are neither temperature- nor salinity-dependent, and could be readily applicable to freshwater or brackish water aquaculture within temperature–salinity combinations ranging from 16 to 36°C and 0–16 ppt.

Effect of high-energy electro-pulses on the compression deformation behavior of Ti-6Al-4V alloy

Compression tests of Ti–6Al–4V alloy were conducted using an electron universal testing machine with discharge voltages that range from 50 V to 70 V and strain rate of 0.01 s−1. Isothermal compression at equivalent temperatures was also performed on a universal testing machine with furnace, with the same strain rate. Results show that the deformability of Ti–6Al–4V alloy can be significantly improved by high-energy electro-pulses, and the deformation resistance and yield stress were also decreased. Moreover, the effect of high-energy electropulses on compression mechanical properties of Ti–6Al–4V alloy increased with increasing discharge voltage. However, elongation and deformation resistance of compressions with high-energy electro-pulses were higher than isothermal compressions at equivalent temperatures. This result proved that the deformability improvement of Ti–6Al–4V alloy by high-energy electro-pulses results from the joint effects of temperature and electro-plasticity. Fracture modes in different experimental conditions were analyzed by observing the fracture morphologies of specimens by using a scanning electron microscope. Under high-energy electro-pulses, the micro morphology of compression fracture changes from elongated oval to equiaxed dimples, and the fracture modes transfer from intergranular to transgranular fracture.

Disentangling climate change effects on species interactions: effects of temperature, phenological shifts, and body size

Climate-mediated shifts in species' phenologies are expected to alter species interactions, but predicting the consequences of this is difficult because phenological shifts may be driven by different climate factors that may or may not be correlated. Temperature could be an important factor determining effects of phenological shifts by altering species' growth rates and thereby the relative size ratios of interacting species. We tested this hypothesis by independently manipulating temperature and the relative hatching phenologies of two competing amphibian species. Relative shifts in hatching time generally altered the strength of competition, but the presence and magnitude of this effect was temperature dependent and joint effects of temperature and hatching phenology were non-additive. Species that hatched relatively early or late performed significantly better or worse, respectively, but only at higher temperatures and not at lower temperatures. As a consequence, climate-mediated shifts in hatching phenology or temperature resulted in stronger or weaker effects than expected when both factors acted in concert. Furthermore, consequences of phenological shifts were asymmetric; arriving relatively early had disproportional stronger (or weaker) effects than arriving relatively late, and this varied with species identity. However, consistent with recent theory, these seemingly idiosyncratic effects of phenological shifts could be explained by species-specific differences in growth rates across temperatures and concordant shifts in relative body size of interacting species. Our results emphasize the need to account for environmental conditions when predicting the effects of phenological shifts, and suggest that shifts in size-structured interactions can mediate the impact of climate change on natural communities.

Predicting population dynamics of the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae) resulting from novel interactions of temperature and selenium

Changes in trophic level interactions due to global climate change and the increasing occurrence of pollution are likely to have consequences for natural enemies. Specifically, information regarding the effects of these factors on insect parasitoids is relatively sparse. We examined the individual and joint effects of temperature and the pollutant selenium on the fitness correlates of the parasitoid wasp Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae), parasitizing Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). Our specific objective was to determine in a factorial experiment how three temperatures (constant 28.6°C, constant 33°C and a fluctuating temperature between 28.6 and 33°C) and three concentrations of seleno-dl-methionine (0.00, 21.21, and 42.42 µg/g) affected the parasitoid's fitness and life history. Parasitoids failed to complete development at the constant 33°C, but developed significantly faster at the fluctuating temperature compared to the constant 28.6°C. There were significant declines due to increased temperature, but not selenium, on C. marginiventris survival time, adult body weight, body size, hind tibia length, female life span and number of progeny that survived to adulthood. Mean generation times and the intrinsic rate of increase (r) further show that both of these life table statistics declined under conditions of increased temperatures. We discuss the implications of these results in helping to understand and predict the effectiveness of biological control programs and pest management strategies as climate changes in the presence of metal and metalloid pollution.

Effects of temperature and oxygen concentration in sediment toxicity testing

Joint effects of temperature and oxygen concentrations for the results of sediment toxicity tests were studied at 10 and 20 °C with 40% and 80% dissolved oxygen (DO) saturation. Growth, feeding rate, and reproduction of Lumbriculus variegatus (Oligochaete) and growth, emergence, and survival of Chironomus riparius (Diptera) were tested in a polluted and in a reference sediment. Both the feeding of L. variegatus and the emergence of C. riparius were significantly retarded at low temperature. Additionally, differences in the sex ratio of the emerged adults of C. riparius were observed. The oxygen concentration alone did not have any significant effect on the endpoints, but significant combined effects of polluted sediment and low DO were observed on the biomass of L. variegatus. The standard sediment toxicity tests might offer only limited data for risk assessment of contaminated sediments at sites where the actual conditions largely differ from the laboratory conditions.

Shape and size variation on the wing of Drosophila mediopunctata: influence of chromosome inversions and genotype-environment interaction

The second chromosome of Drosophila mediopunctata is highly polymorphic for inversions. Previous work reported a significant interaction between these inversions and collecting date on wing size, suggesting the presence of genotype-environment interaction. We performed experiments in the laboratory to test for the joint effects of temperature and chromosome inversions on size and shape of the wing in D. mediopunctata. Size was measured as the centroid size, and shape was analyzed using the generalized least squares Procrustes superimposition followed by discriminant analysis and canonical variates analysis of partial warps and uniform components scores. Our findings show that wing size and shape are influenced by temperature, sex, and karyotype. We also found evidence suggestive of an interaction between the effects of karyotype and temperature on wing shape, indicating the existence of genotype-environment interaction for this trait in D. mediopunctata. In addition, the association between wing size and chromosome inversions is in agreement with previous results indicating that these inversions might be accumulating alleles adapted to different temperatures. However, no significant interaction between temperature and karyotype for size was found--in spite of the significant presence of temperature-genotype (cross) interaction. We suggest that other ecological factors--such as larval crowding--or seasonal variation of genetic content within inversions may explain the previous results.

Climate envelopes of mire complex types in fennoscandia

.Peatlands are characteristic features of the Fennoscandian landscape, about one‐quarter of the land surface being classified as peatland. The aim of this work was to determine the extent to which the distribution of four main mire complex types (aapa mire, blanket bog, palsa mire, raised bog) can be modelled on the basis of climatological parameters. Additionally, the relative importance of different climatological variables in influencing the distribution of different mire complex types was scrutinized using the variation partitioning method. Variation partitioning is a novel statistical approach that provides deeper understanding of the importance of different explanatory variable groups for geographical patterns than traditional regression methods. The variation in the distribution of mire complex types was decomposed into independent and joint effects of temperature, precipitation and spatial variables.The distributional limits of aapa mires, palsa mires and raised bogs were primarily associated with thermal factors, whereas moisture regime also played an obvious role for blanket bogs. A considerable amount of variation in the distribution of mire complex types was accounted for by the joint effects of explanatory variables and may thus be causally related to two or all three groups of variables. Although the present distribution of mire complex types corresponded well to the contemporary climate in Fennoscandia, our results indicate that the climate envelopes of palsa mires are narrow. Thus, they can be expected to be extremely sensitive to changes in future climatic conditions.

Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly.

We investigated four predictions about how temperature, photoperiod and sex affect the life history plasticity and foraging activity of a damselfly. (i) As predicted, increased temperatures increased foraging activity and growth rates, but in contrast with the prediction, late photoperiod (high time stress) did not affect foraging activity and growth rate. (ii) Unexpectedly, the increase in growth rate at increasing temperatures was not larger under high time stress. (iii) As predicted, age and size at emergence decreased at higher temperatures and at the late photoperiod. Temperature-induced life history shifts were direct or the result of behavioural growth mediation depending on the temperature range. Photoperiod-induced life history shifts were direct. (iv) As predicted, males emerged before females but at a smaller size. The degree of sexual size dimorphism was influenced by the joint effects of temperature and photoperiod. We could only detect genetic variation in size plasticity to photoperiod. The match between the sex-specific life history responses to temperature and photoperiod and predictions by relevant optimality models suggests adaptive life history plasticity to these variables.

Joint effects of temperature, food quality, and season on the development of the cerambycid Morimus funereus under laboratory conditions

AbstractThe effects of constant temperature (23 °C), food quality (B, natural diet i.e. powdered oak bark; B + C, natural diet enriched with powdered sweet crackers) and season on larval development of the cerambycid Morimus funereus L. were studied. The temperature of 23 °C exerted an unfavourable effect on larvae collected from oak stumps in September and bred on B; i.e. the larvae died within 30 days. When the larvae consumed B + C the unfavourable effect of temperature was abolished and the larvae increased their weight by 543%, 897% and 1179% in 1, 2 and 3 months, respectively. Newly hatched summer‐ and winter‐larvae developed successfully on B + C, while all the winter‐larvae died within 40 days on B. Larvae of an identical parentage hatched in different phases of the annual cycle and showed seasonal differences in the rate of development and survival when reared on B + C at 23 °C. The fastest development and the highest survival rate were observed in larvae which emerged in early‐ and midsummer, whereas the slowest development and the lowest survival rate were in those hatched in late summer. The synchronized seasonal changes of adults and their offspring, as expressed at different levels of biological organization, suggest the existence of an endogenous annual rhythm which is dependent upon the expression of different genes in the course of the annual cycle.RésuméEffects combinés au laboratoire de la température, de la qualité de l'aliment et de la saison sur le développement du cérambycide, Morinus funereusL'étude a porté sur les effets d'une température constante (23 °C), de la qualité de l'aliment, ‐B = aliment naturel, c'est‐à‐dire de l'écorce de chêne pulvérisée; B + C = aliment naturel enrichi avec de la poudre de biscuits sucrés –, et de la saison sur le développement larvaire de M. funereus L. La température de 23 °C a été défavorable aux larves récoltées en septembre dans des souches de chênes et élevées sur aliment B: les larves étaient mortes en 30 jours. Avec aliment B + C, l'effet défavorable a été neutralisé et le poids des larves augmenté de 543%, 897% et 1179% en 1, 2 et 3 mois. Des larves néonates d'été ou d'hiver se sont bien développées sur B + C, mais toutes les larves d'hiver étaient mortes sur B en 40 j. Des larves de mêmes parents, écloses à différentes époques de l'année, ont présenté des différences saisonnières du taux de survie et de la vitesse de développement lors de leur élevage à 23 °C sur B + C. Le développement le plus rapide et la meilleure survie ont été obtenus avec des larves écloses au début ou au milieu de l'été; tandis que le développement le plus lent et la plus mauvaise survie ont été obtenus avec les larves écloses à la fin de l'été. Les changements saisonniers synchrones des adultes et de leurs descendants, exprimés à différents niveaux d'organisation biologique, suggèrent l'existence d'un rythme annuel endogène qui dépend de l'expression de différents gènes au cours du cycle annuel.