Constant rate allocation in nymphal development in species of Hemiptera

Abstract. This study investigated the existence of rate isomorphy (the constant allocation of relative times to different stages of development under different abiotic conditions) in Macrolophus pygmaeus (Hemiptera: Miridae; a phytophagous and predatory insect). Replicated data were used from a range of temperatures regarding (i) the developmental period of each nymphal stage in relation to the total duration of nymph development, when feeding on three host plants either with different prey species or without prey, and (ii) its egg, total nymphal and preoviposition period, on two host plants, with different prey species. The proportion of time required for the development of each nymphal stage of M. pygmaeus is not different among the temperatures or the kind of food available. These proportions ranged among the different host plants, temperatures and prey presence/absence from 17.3–21.8% in the first, 14.5–18.8% in the second, 14.2–18.3% in the third, 16.5–21.0% in the fourth and from 25.4–30.6% in the fifth nymphal stage. Thus, temperature does not significantly affect the proportion of time spent in each nymphal stage and rate isomorphy exists in nymphal development. This phenomenon was also investigated using data from the literature, and it also occurs in several other Hemiptera species. Therefore, there appears to be a constant time allocation in the nymphal development of the higher taxonomic groups of insects. However, for M. pygmaeus, rate isomorphy does not hold when considering egg‐to‐egg development and the relative duration of times to egg hatch, total nymphal development and preoviposition period. The ecophysiological implications of this rate isomorphy phenomenon are discussed in relation to endocrinological mechanisms. Apart from its theoretical interest, the existence of rate isomorphy simplifies studies on the rate of development and the estimation of thermal constants of an insect, which are essential for the prediction of insect population dynamics. It is also proposed that the term ‘rate isomorphy’ does not strictly describe the phenomenon, and it is suggested that ‘constant rate allocation’ would be a more suitable term.     

A general rule for the dependence of developmental rate on temperature in ectothermic animals

In animals that do not regulate their body temperature by the production of heat, the proportion of the total developmental time spent in a particular developmental stage does not change with temperature. In the quasi-linear region of the relationship between developmental rate and temperature, all of the developmental stages appear to have the same species-specific lower developmental threshold. This trait, which is called developmental isomorphy, constrains developmental adaptations of ectotherms to their environments and facilitates the precise timing of life-history events.     

How to compare the lower developmental thresholds

According to the hypothesis of isomorphy rate, all the lower developmental thresholds of different developmental stages of an insect are equal. However, there is lack of a formal statistical method for testing whether there is a significant difference among the lower developmental thresholds on the basis of the traditional linear model describing developmental rate as a linear function of temperature. For comparing the lower developmental thresholds of different developmental stages, a new method based on the Chow test is proposed in the current study. Another feasible way based on the linear model proposed by Ikemoto and Takai is also proposed. The lower developmental thresholds can be compared by the analysis of covariance on this linear model. The current study can be used to test the hypothesis of isomorphy rate. When comparing the lower developmental thresholds of different geographical populations for one insect species, the two methods proposed here are also applicable.     

Common-intersection hypothesis of development rate lines of ectotherms within a taxon revisited

The relationship between development rate of an ectotherm and temperature in experiments where insects or mites are reared under several constant temperatures, while non-linear over the entire range, can be approximately described by a line in the mid-temperature range. It was hypothesized that the development rate lines of ectotherms within a taxon such as a family would have a common intersection. Thus for a given temperature, the development time should be the same for all the species within any specified taxon. In the current study, the data on temperature-dependent development rates of species of the Aphididae and Tetranychidae families were used to test the validity of the common-intersection hypothesis. The hypothesis was supported with either dataset used. In addition, the current study tested the common-intersection hypothesis through mathematical analysis on the basis of two linear relationships (i.e., the linear relationship between temperature and development rate and that between the lower developmental threshold and the sum of effective temperatures). An attempt was made to combine the rate isomorphy hypothesis that all the lower developmental thresholds of different stages were assumed to be equal for a single species with the common-intersection hypothesis for related species within a taxon and hypothesize that if these two hypotheses hold, then for any developmental stages a common temperature of all stages should exist.     

Testing the rate isomorphy hypothesis using five statistical methods

Abstract Organisms are said to be in developmental rate isomorphy when the proportions of developmental stage durations are unaffected by temperature. Comprehensive stage‐specific developmental data were generated on the cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), at eight temperatures ranging from 16°C to 30°C (in 2°C increments) and five analytical methods were used to test the rate isomorphy hypothesis, including: (i) direct comparison of lower developmental thresholds with standard errors based on the traditional linear equation describing developmental rate as the linear function of temperature; (ii) analysis of covariance to compare the lower developmental thresholds of different stages based on the Ikemoto‐Takai linear equation; (iii) testing the significance of the slope item in the regression line of versus temperature, where p is the ratio of the developmental duration of a particular developmental stage to the entire pre‐imaginal developmental duration for one insect or mite species; (iv) analysis of variance to test for significant differences between the ratios of developmental stage durations to that of pre‐imaginal development; and (v) checking whether there is an element less than a given level of significance in the p‐value matrix of rotating regression line. The results revealed no significant difference among the lower developmental thresholds or among the aforementioned ratios, and thus convincingly confirmed the rate isomorphy hypothesis.     

温度对产虫茶昆虫紫斑谷螟生长发育的影响

为探明温度对贵州主要产虫茶昆虫紫斑谷螟Pyralis farinalis (Linnaeus)生长发育的影响, 本研究以白茶Litsea coreana为寄主植物, 分别设置5个恒温（19, 22, 25, 28和31℃）条件, 研究温度对紫斑谷螟卵、 幼虫、 蛹和未成熟期平均发育历期、 发育速率和存活率的影响, 计算各虫态发育起点温度和有效积温。 结果表明： 温度对紫斑谷螟各虫态发育历期、 发育速率和存活率影响显著。 在19 ~ 31℃范围内, 各虫态的平均发育历期均随温度的升高而缩短, 卵期、 幼虫期、 蛹期及未成熟期均在31℃达到最小值, 分别为4.56±0.24, 43.33±1.50, 7.89±0.20和55.78±1.69 d。 紫斑谷螟各虫态发育速率与温度呈二次回归关系, 且极显著相关。 此外, 温度显著影响各虫态存活率, 卵的存活率在28℃时最高, 为93%; 幼虫和蛹的存活率则在25℃最高, 分别为88%和93%; 温度过高或过低均不利于其生长发育。 由直接最优法计算得到紫斑谷螟卵期、 幼虫期、 蛹期及未成熟期的发育起点温度分别为13.30, 15.48, 13.19和14.82℃, 有效积温依次为88.36, 679.51, 159.73和952.04日·度。 这些结果为紫斑谷螟的繁殖提供了基础参考数据, 对指导虫茶生产有实用参考价值。     

Temperature-dependent development and potential distribution of Episimus utilis (Lepidoptera: Tortricidae), a candidate biological control agent of Brazilian peppertree (Sapindales: Anacardiaceae) in Florida

The invasive Brazilian peppertree (Schinus terebinthifolius Raddi), native to South America, is widely established throughout central and south Florida. The defoliating leaflet-roller Episimus utilis Zimmerman was selected as potential biocontrol agent of this invasive species. The objectives of this study were to determine development rate and survival of E. utilis at seven constant temperatures (10, 15, 20, 25, 30, 33, and 35 degrees C) and generate prediction maps of the number of generations per year this species may exhibit in the United States. The rate of development of E. utilis as a function of temperature was modeled using linear regression to estimate a lower developmental threshold of 9.6 degrees C and the degree-day requirement of 588. The Logan nonlinear regression model was used to estimate an upper developmental threshold of 33 degrees C. Cold tolerance of E. utilis was examined using all insect stages, and each stage was exposed to three constant temperatures (10, 5, 0 degrees C) for 0.5, 1, 2, 4, and 8 d (or until all insects died). The pupal stage was the most cold tolerant with 100% mortality after 12 d at 0 degrees C. The pupal lethal times at 5 (Ltime50 = 10 d, Ltime90 = 28 d) and 0 degrees C (Ltime50 = 5 d, Ltime90 = 9 d) were used to generate isothermal lines to predict favorable regions for E. utilis establishment. A GIS map was generated to predict the number of generations of E. utilis (range, 0.5-9.8) across all Brazilian peppertree range in the United States. The potential for establishment of E. utilis and its probable distribution in the continental United States was examined.     

Developmental database for phenology models: related insect and mite species have similar thermal requirements

Two values of thermal requirements, the lower developmental threshold (LDT), that is, the temperature at which development ceases, and the sum of effective temperatures, that is, day degrees above the LDT control the development of ectotherms and are used in phenology models to predict time at which the development of individual stages of a species will be completed. To assist in the rapid development of phenology models, we merged a previously published database of thermal requirements for insects, gathered by online search in CAB Abstracts, with independently collected data for insects and mites from original studies. The merged database comprises developmental times at various constant temperatures on 1,054 insect and mite species, many of them in several populations, mostly pests and their natural enemies, from all over the world. We show that closely related species share similar thermal requirements and therefore, for a species with unknown thermal requirements, the value of LDT and sum of effective temperatures of its most related species from the database can be used.     

不同地理种群短额负蝗对环境温度的适应性

[目的]本研究旨在探明短额负蝗Atractomorpha sinensis不同地理种群对环境温度响应的适应性差异.[方法]以大豆叶片为食物饲养,在恒温16,20,24,28和32℃,相对湿度70％,光周期16L:8D条件下,系统观测陕西延安、河南郑州、四川成都、云南曲靖和广东广州5个短额负蝗地理种群的生长发育过程,比较...     

Elevated water temperature impairs fertilization and embryonic development of whitefish Coregonus lavaretus

The adverse effects of high temperatures on the early life stages of anadromous whitefish Coregonus lavaretus were experimentally examined by assessing fertilization success, the percentage of developmental abnormalities, cumulative mortality and the rate of embryogenesis across a range of temperatures. Temperatures ≥ 7° C increased the proportion of unfertilized and abnormally dividing eggs, deformed embryos and consequent mortality. The higher the temperature, the more severe were the effects. When eggs were fertilized and constantly incubated at various temperatures, the effective level for 50% of the eggs and embryos (EL50) of temperature was 7·6° C at the developmental stage when eye pigmentation was visible. Fewer developmental abnormalities and a lower cumulative mortality rate were observed when embryos were exposed to high temperatures from the later, gastrula stage, than from fertilization or the four‐cell stage. Irrespective of retarded development in terms of day‐degrees (i.e. the sum of daily mean temperatures), a high incubation temperature reduced the development time of C. lavaretus, leading to earlier hatching, and hatched fry were shorter than at the reference temperature of 4–5° C. Global warming will particularly pose risks for stenothermic species such as C. lavaretus, with early life stages being especially susceptible. Thus, relatively small increases and fluctuations in river water temperatures during the spawning season of this anadromous species may have substantial negative impacts on its recruitment and population persistence.     

Growth versus molting time of caterpillars as a function of temperature,nutrient concentration and the phenolic rutin

Summary A factorial experiment tested the effects of varying nutrient concentration (normal versus diluted), presence or absence of the phenolic allelochemical rutin and daytime temperature (20, 25 and 30° C) on growth, molting and food utilization efficiencies of tobacco hornworms (Manduca sexta). Two of the utilization efficiencies (approximate digestibility and efficiency of conversion of ingested food) were unaffected by temperature; the third one, efficiency of conversion of digested food, was affected by temperature but there was no consistent effect. Lower temperatures significantly increased the proportion of the stadium spent molting, with larvae at a daytime temperature of 20° C spending 9% more of the stadium in molting than larvae at 30° C. Growth time was not influenced by nutrient concentration. When temperature was low and rutin absent, molt time and the proportion of the stadium spent molting were affected by nutrient concentration. Addition of the phenolic rutin did not have an appreciable effect on growth time or digestive processes. However, it increased molting time by 7 to 14% and thus increased the duration of the stadium and reduced relative growth rate. These results indicate that the effect of food quality on growth rate is a function of the thermal conditions of insect herbivores. At cooler temperatures, a disproportionate increase in time spent molting, rather than altered food utilization efficiencies, contributed to lower growth rates. The consequences for larval growth of fluctuating temperatures due to diurnal cycles and the presence of predators forcing larvae into thermally suboptimal microhabitats are discussed.     

Developmental and reproductive biology of Scirtothrips perseae (Thysanoptera: Thripidae): a new avocado pest in California

The developmental and reproductive biology of a new avocado pest, Scirtothrips perseae Nakahara, was determined in the laboratory at five constant temperatures, 15, 20, 25, 27.5 and 30 degrees C. At 20 degrees C, S. perseae exhibited greatest larval to adult survivorship (41%), and mated females produced a greater proportion of female offspring at this temperature when compared to 15, 25, 27.5 and 30 degrees C. Average lifetime fecundity and preoviposition period was greatest at 15 degrees C at 39.6 eggs per female and 17.6 days, respectively. Jackknifed estimates of net reproduction (Ro), capacity for increase (rc), intrinsic rate of increase (rm), and finite rate of increase (lambda) were all significantly greater at 20 degrees C than corresponding values at 15, 25 and 27.5 degrees C. Population doubling time (Td) was significantly lower at 20 degrees C, indicating S. perseae populations can double 33-71% faster at this temperature in comparison to 15, 25 and 27.5 degrees C. Mean adult longevity decreased with increasing temperature, from a maximum of 52.4 days at 15 degrees C to a minimum of 2.4 days at 30 degrees C. Developmental rates increased linearly with increasing temperatures for eggs and rates were non-linear for development of first and second instar larvae, propupae, pupae, and for egg to adult development. Linear regression and fitting of the modified Logan model to developmental rate data for egg to adult development estimated that 344.8 day degrees were required above a minimum threshold of 6.9 degrees C to complete development. An upper developmental threshold was estimated at 37.6 degrees C with an optimal temperature of 30.5 degrees C for egg to adult development. Unmated females produced only male offspring confirming arrhenotoky in S. perseae.     

温度对深点食螨瓢虫实验种群的影响

在５种温度下观察了深点食螨瓢虫各虫态的生长发育及成虫产卵的情况,由此拟合了各虫态的发育速率和温度的关系模型,求出了各阶段的发育起点温度和有效积温,组建了４种温度下的实验种群繁殖特征生命表,并算出了内禀增长能力、稳定年龄组配、瞬时出生率和瞬时死亡率等参数值。     

Study of intrapopulational variability of duration and temperature norms of development of the linden bug Pyrrhocoris apterus (Heteroptera, Pyrrhocoridae)

The existence of significant variability in duration and temperature norms of development between families within insect populations has been shown for the first time. This variability is inferfamily and therefore has genetic ground. Revealed for the first time is the statistically significant positive correlation between the regression coefficient of the development rate for temperature and the temperature threshold for development of eggs and larvae from different families. The greater the slope of the regression line of the development rate for temperature, the higher the temperature threshold value in this particular family. These results demonstrate for the first time the existence of genetic co-variation between the regression coefficient and the temperature threshold within the insect populations. It is suggested that the source of the interpopulational and interspecies changes in the temperature reaction norms of the insect development might be the intrapopulational hereditary variability of the development duration, regression coefficient, and the development threshold, this variability being an object of natural selection. It was shown that in all studied families and populations the values of the linear regression coefficient of development rates for temperature in eggs of the linden bug Pyrrhocoris apterus were markedly and statistically significantly higher, while the temperature threshold values—lower as compared with the corresponding parameters in larvae. These results obviously are in contradiction with the concept of the “isomorphism of development rates” (Jarosik et al., 2002), according to which the development threshold for all life cycle stages of a species should be the same, whereas only slopes of the regression lines of the development rate for temperature can differ. For the first time the absence of genetic covariation has been shown between the temperature norms of development of different life cycle stages of the species—eggs and larvae. This means that the regression coefficient as well as the sum of the degree-days and the development threshold in eggs and larvae are inherited independently and therefore they can be independently changed in evolution in correspondence with specific environmental conditions, under which these life cycle stages take place.     

Role of larval host plants in the climate-driven range expansion of the butterfly Polygonia c-album

1. Some species have expanded their ranges during recent climate warming and the availability of breeding habitat and species' dispersal ability are two important factors determining expansions. The exploitation of a wide range of larval host plants should increase an herbivorous insect species' ability to track climate by increasing habitat availability. Therefore we investigated whether the performance of a species on different host plants changed towards its range boundary, and under warmer temperatures. 2. We studied the polyphagous butterfly Polygonia c-album, which is currently expanding its range in Britain and apparently has altered its host plant preference from Humulus lupulus to include other hosts (particularly Ulmus glabra and Urtica dioica). We investigated insect performance (development time, larval growth rate, adult size, survival) and adult flight morphology on these host plants under four rearing temperatures (18-28.5 degrees C) in populations from core and range margin sites. 3. In general, differences between core and margin populations were small compared with effects of rearing temperature and host plant. In terms of insect performance, host plants were generally ranked U. glabra > or = U. dioica > H. lupulus at all temperatures. Adult P. c-album can either enter diapause or develop directly and higher temperatures resulted in more directly developing adults, but lower survival rates (particularly on the original host H. lupulus) and smaller adult size. 4. Adult flight morphology of wild-caught individuals from range margin populations appeared to be related to increased dispersal potential relative to core populations. However, there was no difference in laboratory reared individuals, and conflicting results were obtained for different measures of flight morphology in relation to larval host plant and temperature effects, making conclusions about dispersal potential difficult. 5. Current range expansion of P. c-album is associated with the exploitation of more widespread host plants on which performance is improved. This study demonstrates how polyphagy may enhance the ability of species to track climate change. Our findings suggest that observed differences in climate-driven range shifts of generalist vs. specialist species may increase in the future and are likely to lead to greatly altered community composition.     

温度对巨膜长蝽生长发育与繁殖的影响

【目的】近年来巨膜长蝽Jakowleffia setulosa (Jakovlev)由稳定种群的荒漠昆虫上升为暴发性发生并迁移至农区危害的农业害虫。由于缺乏巨膜长蝽生物学基础研究,给监测预警及综合防治带来许多困难。本研究旨在探明温度对巨膜长蝽发育和繁殖的影响。【方法】本实验以白茎盐生草Halogeton arachnoideus Moq.为寄主植物,分别在7个恒温（13,18,23,28,33,35和37℃）下研究了温度对巨膜长蝽各虫态平均发育历期、发育速率、成活率、产卵量和种群参数的影响。【结果】在13~37℃范围内,各虫态的发育历期随温度的升高而缩短,13℃完成一个世代发育需要82.63 d,37℃只需要14.61 d。各虫态的发育速率（V）与温度（T）的关系均符合多项式回归模型,且极显著相关。采用直接最优法分析,巨膜长蝽世代的发育起点温度为8.30℃,有效积温为555.77日·度,在宁夏一年可发生2代。巨膜长蝽世代存活率均在33℃时最高,为35.44%。28～37℃之间单雌产卵量较多,达到10粒以上,通过方程拟合得到理论上雌虫产卵最适温度为34.59℃,产卵量最高可达到16.73粒/雌;种群趋势指数在13℃为零,18～23℃小于1,种群呈负增长;28～37℃大于1,且33℃时最高,为2.77;净增殖率、内禀增长率及周限增长率均在37℃时最高,分别为7.24, 0.3912和1.4787;种群世代周期以13℃时最长,为45.8936 d,37℃时最短,为5.0608。【结论】巨膜长蝽在28～35℃下存活率、增长指数和繁殖力较高,说明该温度范围是巨膜长蝽生长发育和繁殖的适宜温度。本研究为有效开展巨膜长蝽的监测预报及综合防控提供了科学依据。     

Egg incubation temperature differently affects female and male hatching dynamics and larval fitness in a leafhopper

Temperature effects on ectotherms are widely studied particularly in insects. However, the life-history effects of temperature experienced during a window of embryonic development, that is egg stage, have rarely been considered. We simulated fluctuating temperatures and examined how this affects the operational sex ratio (OSR) of hatching as well as nymph and adult fitness in a leafhopper, Scaphoideus titanus. Specifically, after a warm or cold incubation we compared males and females hatching dynamics with their consequences on the sex ratio in the course of time, body size, weight, and developmental rate of the two populations, all reared on the same posthatching temperature. Males and females eggs respond differently, with females more sensitive to variation in incubation temperature. The different responses of both sexes have consequences on the sex ratio dynamic of hatchings with a weaker protandry after warm incubation. Temperatures experienced by eggs have more complex consequences on posthatching development. Later nymphal instars that hatched from eggs exposed to warm temperature were larger and bigger but developmental rate of the two populations was not affected. Our study demonstrates how incubation temperature could affect operational sex ratio and posthatching development in an insect and how this may be critical for population growth.     

Ontogenetic stage-dependent effect of temperature on developmental and metabolic rates in a holometabolous insect

Different hypotheses attempt to explain how different stages of organisms with complex life cycles respond to environmental changes. Most studies have focused at the among-species level showing similar responses to temperature throughout ontogeny. However, there is no agreement about the pattern expected at the intraspecific scale where a strong selective effect is expected. In this paper, we studied the effects of thermal treatments on a life history trait (developmental rate) and a physiological trait (metabolic rate) during development in the fruitfly Drosophila buzzatii. First, we estimated the rate of development during larval life (LDR) and the pupal stage (PDR) in flies derived from two natural populations exposed to several thermal treatments. Our results showed that the developmental rate ratio, LDR/PDR, did not vary between populations, and that the effects of thermal treatments were stage specific. Second, we studied the relationship between developmental rate (DR) and metabolic rate (MR) in each life cycle stage. We found that allometric relationships between DR and MR varied throughout ontogeny, a pattern that shed light on the mechanisms responsible for thermal plasticity. We conclude that, although different populations may show developmental rate isomorphy; larvae and pupae may choose alternative “decisions” in terms of life-history evolution and physiological traits when confronted to different thermal environments.     

Development and Survival of Chironomus tepperi Skuse (Diptera: Chironomidae) at a Range of Constant Temperatures

Chironomus tepperi Skuse were reared individually at a range of constant temperatures from 12.5 to 37.5°C (2.5°C intervals), with development and survival monitored at regular intervals. C. tepperi is protandrous, with males developing significantly faster than females at the majority of temperatures examined, due primarily to a shorter final instar. Some individuals completed development at all temperatures, however emergent adults failed to successfully inflate their appendages at 37.5°C. Developmental rate increased with increasing temperature up to 32.5°C, but fell at 35°C. Low adult emergence at 37.5°C precluded a reliable estimate of total development time at that temperature. Survival to adult emergence varied from 10 to 60%, with highest mortality in the pupal stage at all temperatures. Degree-days (DD) and developmental zero (DZ) estimates for egg to adult development are 150.5 DD and 10.5°C for males and 167.1 DD and 10.3°C for females. DD and DZ estimates are presented for each developmental stage. The significance of wide thermal tolerances in a colonist midge species is discussed.