Effects of temperature on the development and survival of an endangered butterfly,Lycaeides argyrognomon (Lepidoptera: Lycaenidae) with estimation of optimal and threshold temperatures using linear and nonlinear models

The effects of temperature on the development and survival of Lycaeides argyrognomon were examined in the laboratory. The eggs, larvae and pupae were reared at temperatures of 15, 17.5, 20, 25, 30 and 33°C under a long‐day photoperiod of 16‐h light and 8‐h darkness. The survival rates of the first–third instars ranged from 40.0 to 82.4%. The mortalities of the fourth instar were lower than those of the first–third instars. The development time of the overall immature stage decreased from 78.33 days at 15°C to 21.07 days at 30°C, and then increased to 24.33 days at 33°C. The common linear model and the Ikemoto–Takai model were used to estimate the thermal constant (K) and the developmental zero (T₀). The values of T₀ and K for the overall immature stages were 10.50°C and 418.83 degree‐days, and 9.71°C and 451.68 degree‐days by the common model and the Ikemoto–Takai model, respectively. The upper temperature thresholds (T_max) and the optimal temperatures (T_opt) of the egg, the first–third instars and the overall immature stages were estimated by the three nonlinear models. The ranges of T_opt estimated were from 30.33°C to 32.46°C in the overall immature stages and the estimates of T_max of the overall immature stages by the Briere‐1 and the Briere‐2 models were 37.18°C and 33.00°C, respectively. The method to predict the developmental period of L. argyrognomon using the nonlinear models was discussed based on the data of the average temperature per hour.     

Temperature‐dependent phenology and growth potential of the Andean potato tuber moth,Symmetrischema tangolias (Gyen) (Lep., Gelechiidae)

The Andean potato tuber moth, Symmetrischema tangolias (Gyen) [Lepidoptera, Gelechiidae], is an economically important pest of potato (Solanum tuberosum L.) in the mid‐elevated Andean region and an invasive pest of partially global importance. Determination of the pest's population life table parameters is essential for understanding population development and growth under a variety of climates and as part of a pest risk analysis. The development, mortality and reproduction were studied in two pest populations (from Peru and Ecuador) in which cohorts of each life stage were exposed to different constant temperatures ranging from 10°C to 28°C. Using the Insect Life Cycle Modeling software, nonlinear equations were fitted to the data and an overall phenology model established to simulate life table parameters based on temperature. The temperature‐dependent development curve was statistically well described for eggs by Ratkowsky's model and for larvae and pupae by Taylor's model. Variability in development time among individuals independent of temperature was significantly described by a log‐logistic model. Temperature effects on immature mortality were described using different nonlinear models. Optimal temperature for survival was between 14° and 17°C. Temperature effects on adult senescence and oviposition time were described by simple exponential models; within‐group variability was described by a Weibull distribution function. Fecundity per female due to temperature followed a nonlinear model indicating maximum reproduction at ~17°C. The established model revealed good convergence with historical life tables established at fluctuating temperatures. The results confirm that S. tangolias is more adapted to cooler temperature than the common potato tuber moth, Phthorimaea operculella (Zeller). S. tangolias develops at temperatures within the range of 8–28.8°C with a maximum finite rate of population increase (=1.053) at 21°C. The established process‐based physiological model can be used globally to simulate life table parameters for S. tangolias based on temperature and should prove helpful for evaluating the potential establishment risk and in adjusting pest management programmes.     

Temperature-dependent development of diapausing larvae of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae)

Temperature-dependent development rate, percent diapause induction (hibernation at low temperature and aestivation at high temperature), and survival of diapausing larvae of Chilo partellus (Swinhoe, 1885) were examined on 13 constant temperatures ranging from 8 to 40 °C. Development of hibernating and aestivating larvae occurred from 10 to 25 °C and 27–38 °C, respectively. However, no development occurred at 8 °C and 40 °C. To determine actual thermal conditions that affect development and trigger both kind of diapause (hibernation and aestivation), various thermal parameters were estimated by fitting the development rate data to two linear (Ordinary equation and Ikemoto & Takai) models and thirteen non-linear models. The lower thermal thresholds (T_min) for development of diapausing larvae of C. partellus were calculated as 9.60 °C and 10.29 °C using the ordinary linear model and Ikemoto & Takai model, respectively. Similarly, the thermal constants (K) estimated using the ordinary linear model was 333.33 degree-days and that estimated with Ikemoto & Takai model was 338.92 degree-days. Among the non-linear models, Lactin-2 followed by Lactin-1 were found to be the best as these models estimated the critical temperatures (T_min, T_max and T_opt) similar to those of observed values. Conclusively, the Ikemoto & Takai linear model and Lactin-2 followed by Lactin-1 non-linear models are useful and efficient for describing temperature-dependent development and estimating the temperature thresholds of diapausing larvae of C. partellus. Our findings provided fundamental information for estimation of thermal requirement and temperature based development models for diapausing larvae of C. partellus. This information will be highly useful for predicting the occurrence, seasonal emergence, number of generations and population dynamics of C. partellus.     

Temperature‐dependent development of Neoseiulus barkeri (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae) at seven constant temperatures

Abstract The effect of seven constant temperatures of 15, 20, 25, 27, 30, 35 and 37°C on developmental time of Neoseiulus barkeri Hughes were determined in laboratory conditions under 65%± 5% RH and a photoperiod of 12 : 12 (L : D) h on nymphal stages of Tetranychus urticae Koch. Total developmental time of females (from egg to adult emergence) at the above‐mentioned temperatures was 26.59, 14.43, 6.32, 5.64, 4.59, 3.98 and 4.67 days, respectively. Developmental rate of the N. barkeri increased as temperature increased from 15 to 35°C, but declined at 37°C. A linear and two nonlinear models were fitted to developmental rate of immature stages of N. barkeri to predict the developmental rate as a function of temperature, as well as to estimate the thermal constant (K) and critical temperatures (i.e., T_min, T_opt and T_max). The estimated values of the T_min and K for total developmental time using the linear model were 12.07°C and 86.20 degree‐days (DD), respectively. The T_min and T_max estimated by the Sharpe‐Schoolfield‐Ikemoto (SSI) model were 11.90°C and 37.41°C, respectively. The estimated T_opt for overall immature stage development of N. barkeri by the Lactin and SSI models were 33.89°C and 24.51°C, respectively. Based on the biological criteria of model evaluation, the linear and SSI models were found to be the best models for describing the developmental rate of overall immature stages of N. barkeri and estimating the temperature thresholds.     

Temperature-dependent development of Lista haraldusalis (Walker) (Lepidoptera: Pyralidae) on Platycarya strobilacea

The effect of constant temperatures on development and survival of Lista haraldusalis (Walker) (Lepidoptera: Pyralidae), a newly reported insect species used to produce insect tea in Guizhou province (China), was studied in laboratory conditions at seven temperatures (19 °C, 22 °C, 25 °C, 28 °C, 31 °C, 34 °C, and 37 °C) on Platycarya strobilacea. Increasing the temperature from 19 °C to 31 °C led to a significant decrease in the developmental time from egg to adult emergence, and then the total developmental time increased at 34 °C. Egg incubation was the stage where L. haraldusalis experienced the highest mortality at all temperatures. The survival of L. haraldusalis was significantly higher at 25 °C and 28 °C, whereas none of the eggs hatched at 37 °C. Common and Ikemoto linear models were used to describe the relationship between the temperature and the developmental rate for each immature stage of L. haraldusalis. The estimated values of the lower temperature threshold and thermal constant of the total immature stages using Common and Ikemoto linear models were 11.34 °C and 11.20 °C, and 939.85 and 950.41 degree-days, respectively. Seven nonlinear models were used to fit the experimental data to estimate the developmental rate of L. haraldusalis. Based on the biological significance for model evaluation, Ikemoto linear, Logan-6, and SSI were the best models that fitted each immature stage of L. haraldusalis and they were used to estimate the temperature thresholds. These thermal requirements and temperature thresholds are crucial for facilitating the development of factory-based mass rearing of L. haraldusalis.     

Susceptibility of Phthorimaea operculella Zeller (Lepidoptera; Gelechiidae) to its granulovirus PoGV with larval age

1 Granulovirus PoGV is a strong candidate to substitute for chemical insecticides in integrated pest management (IPM) of the potato tuber moth Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae). Generally, susceptibility to baculoviruses decreases with increasing larval age. For effective field applications, knowledge of the age‐related change in susceptibility is crucial. 2 The relative susceptibility of various instars of P. operculella larvae to PoGV was studied by leaf‐disc bioassays in the laboratory at 26 °C incubation temperature. The LC₅₀ increased from 4 × 10⁶ granules/mL for neonate larvae to 1.2 × 10⁷, 1.1 × 10⁸, 4.4 × 10⁸, and 4.2 × 10⁹ granules/mL, signifying resistance ratios of 3, 29, 110, and 1051, for 5, 6, 7, and 9‐day‐old larvae, respectively. 3 The relationship between log‐LC₅₀ values and log‐larval weight was significantly linear. A logistic function described significantly the relation between larval weights and physiological age measured in degree‐days (DD > 13.4 °C). Both functions allowed prediction of the activity ratio of PoGV for different larval ages by using temperature summation to express physiological age. 4 PoGV was found to be highly active against P. operculella larvae up to a physiological age of approximately 50 DD (>13.4 °C) (i.e. the first third of the total larval development time). Thereafter, the virus rapidly lost its activity against older larvae. Prospects for applying this knowledge in the field are discussed.     

Temperature related effects on embryonic development of the Mediterranean locust, Dociostaurus maroccanus

Laboratory studies were conducted to assess the effect of temperature on the development of the eggs of Dociostaurus maroccanus (Thunberg) (Orthoptera, Acrididae) during anatrepsis (stages I–XIV) and during catatrepsis (stages XV–XX). The developmental rates of anatrepsis were studied at five constant temperatures ranging from 10 to 30°C. Egg development occurred over the entire range but at 10°C the embryos were unable to complete anatrepsis. The relationship between temperature and developmental times for completing anatrepsis was analysed by the non‐linear Logan type III model. The optimal temperature estimated for the development of eggs during anatrepsis was 24.7°C; the lower and upper thermal thresholds were 9°C and 31°C, respectively. Once the embryos completed anatrepsis, only those incubated at 15°C continued morphogenesis beyond stage XIV (diapause stage) without a low‐temperature exposure period. The developmental rate of catatrepsis was studied at four constant temperatures ranging from 15°C to 30°C after exposure to low‐temperature, 10°C, for 30, 60 or 90 days. For catatrepsis, temperature and developmental time were linearly and inversely related. Linear regression was used to estimate the lower developmental threshold and the degree days requirements for catatrepsis. Both decreased with longer exposure to the low temperature; the former from 13.8°C to 10.5°C and the latter from 212.8 to 171.5 degree days, following 30 and 90 days at 10°C, respectively. Our results improve the ability of decision support systems for Mediterranean locust pest management by providing better forecasts to land managers and pest advisors.     

Temperature dependent development and temperature thresholds of Rhyncaphytoptus ficifoliae Keifer (Diptilomiopidae)

The effects of temperature on developmental rate of Rhyncaphytoptus ficifoliae Keifer (Diptilomiopidae) were determined at six constant temperatures (17, 20, 25, 30, 33 and 36 °C) on fig leaves. The total developmental time of females decreased as temperature increased from 17 (21.62 days) to 33 °C (6.02 days), and then increased at 36 °C (6.47 days). Using the ordinary and Ikemoto and Takai (2000) linear models the estimated lower temperature thresholds (T_min) for total developmental time of females were 10.78 and 10.37 °C and the constant temperatures (k) were 140.25 and 144.78°-days (DD), respectively. Data also were fitted to SSI nonlinear temperature-dependent model. The estimated T_L, intrinsic optimum temperature (T_Ф) and T_h for total immature stages of females by SSI model were 11.11, 23.72 and 37.98 °C, respectively. With use of the obtained data from rearing R. ficifoliae under constant temperatures in laboratory and temperature data in Khorramabad region in 2017, the real developmental rate of this mite in natural conditions was described. The highest (100%) and lowest values (51.67%) of survival rate for immature stages were found at 25 and 36 °C, respectively. The presented information could be used to predict the population dynamics of main pest R. ficifoliae for an effective management.     

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.     

Cold tolerance characteristics of Korean population of potato tuber moth,Phthorimaea operculella (Zeller), (Lepidoptera: Gelechiidae)

Potato tuber moth (PTM), Phthorimaea operculella (Zeller), (Lepidoptera: Gelechiidae) is an invasive insect pest damaging solanaceous crops. We measured the supercooling point (SCP) and survival at low temperature of different development stages to determine which would be capable of overwintering in the Korean climate and adapting to low temperatures. The SCP ranges from ?23.8°C of the egg to ?16.8 of fourth instar larvae (L4). After short periods of low temperature acclimation in L3 (third instar larva), L4 and prepupae, only the prepupal stage showed a significant lowered SCP from ?20.78 to ?22.37°C. When exposed to different subzero temperature for two hours the egg turned out to be the most cold tolerant stage showing LT₅₀ of ?21.7°C followed by the pupal stage with ?15.89°C. One hundred percent mortality was observed when the larvae or adults were exposed to temperatures below ?15.1°C even for a period as short as 2 h. The results suggest that PTM pupae and egg would be the main overwintering stage in Korea where winter temperature does not drop below ?15°C.     

Temperature-dependent development of Xyleborus fornicatus （Coleoptera： Scolytidae）, the shot-hole borer of tea in Sri Lanka： Implications for distribution and abundance

The effect of temperature on the rate of development of Xyleborus fornicatus （Eichh.） was determined by rearing individuals under a range of constant temperatures （15 - 32℃）. Rates of development changed in a linear fashion over a wide range of temperatures. Estimates of lower development thresholds were obtained for eggs （15.7±0.5℃）, larvae （15.8±0.8℃） and pupae （14.3±1.4℃） and the degree days （DD） for development were 70±4.4, 95±8.5 and 72±5.1 DD, respectively. Optimum temperature for development was around 30~C for all stages. Temperature fluctuation in cooler High Country areas （above 1400 m） with a mean temperature around 15℃ seems to be critical for the development of the pest, which may be responsible for the near absence of pest in those areas. Temperature fluctuations （18- 30℃） in the Mid Country region （600- 1200 m） favor the development of the pest compared to development under constant conditions. The altitudinal distribution of the shot-hole borer across tea growing areas in Sri Lanka is, therefore, mainly governed by temperature.     

Temperature‐dependant development of Nasonia vitripennis on five forensically important carrion fly species

The effects of temperature and host species on the development of Nasonia vitripennis Walker (Hymenoptera: Pteromalidae), a forensically important parasitoid of carrion flies, were studied under laboratory conditions. Development time of N. vitripennis on five species of Calliphoridae (Diptera), Calliphora albifrontalis Malloch, Calliphora dubia Macquart, Lucilia sericata Meigen, Chrysomya rufifacies Macquart, and Chrysomya megacephala Fabricius, were determined under eight constant temperatures (15, 18, 21, 24, 27, 30, 33, and 36 °C). Thermal requirements for development (developmental thresholds, thermal constant, and optimum temperature) of N. vitripennis in each host species were estimated using linear and nonlinear models. Upper and lower developmental thresholds ranged between 36.6–38.4 and 9.6–11.1 °C, respectively. The optimum temperature for development was estimated at between 30.6 and 31.8 °C. Statistical differences in the development time of N. vitripennis on the various calliphorid host species were evident within all temperature treatments, particularly at the upper and lower temperature range investigated. As such, it is recommended that insect‐based estimates of time since death in forensic investigations relying on parasitoid evidence should use host‐specific development data where available.     

Age-specific fecundity and life table of Trissolcus semistriatus, an egg parasitoid of the sunn pest Eurygaster integriceps

The effects of temperature on age‐specific fecundity and life table parameters of the egg parasitoid Trissolcus semistriatus (Nees, 1834) (Hymenoptera: Scelionidae) were examined under four constant temperature conditions (17, 20, 26 and 32°C), using eggs of the sunn pest Eurygaster integriceps Puton, 1881 (Hemiptera: Scutelleridae), an important pest of wheat, as hosts. The intrinsic rate of increase increased linearly, while the mean generation time and the doubling time decreased with increases in temperature. The net reproductive rate, however, varied without clear correlation with temperature. Fecundity tended to be higher at higher temperatures. The total number of eggs per female was estimated as 52.0 and 116.4 eggs, respectively, at 17°C and 32°C, with the highest fecundity rate during the first day of oviposition. The oviposition rate fluctuated from 4.4 to 14.3 eggs per day. Oviposition and postoviposition periods and longevity decreased when temperature increased. Maximum longevity for females was 21.6 days at 20°C, and female parasitoids lived longer than males at all temperatures. The development period ranged from 7.1 days (32°C) to 35.6 days (17°C) for males and from 8.4 days (32°C) to 37.2 days (17°C) for females. The development of female T. semistriatus required 166.7 degree‐days (DD) above a theoretical threshold of 11.8°C and the development of males required 142.9 DD above 13.1°C. The numbers of generations per year for female and male T. semistriatus, given the temperature in Tekirdag, Turkey, were estimated to be 9.0 and 8.8, respectively. The potential of the egg parasitoid for the control of E. integriceps is discussed.     

Temperature‐dependent developmental model of Neoseiulus californicus (McGregor) (Acari,Phytoseiidae)

The developmental time and survival of immature stages of Neoseiulus californicus were studied at nine constant temperatures (12, 16, 24, 24, 28 32, 36, 38 and 40°C), 60–70% RH, and a photoperiod of 16 : 8 (L : D) h. The total mortality of immature N. californicus was lowest at 24°C (4.5%) and highest at 38°C (15.2%). The total developmental time decreased with increasing temperature between 12°C (18.38 days) and 32°C (2.98 days), and increased beyond 32°C. The relationship between the developmental rate and temperature was fitted by five nonlinear developmental rate models (Logan 6, Lactin 1, 2 and Briere 1, 2). The nonlinear shape of temperature development was best described by the Lactin 1 model (r² = 0.98). The developmental variation of each stage was well described by the three‐parameter Weibull distribution model (r² = 0.91–0.93). The temperature‐dependent developmental models of N. californicus developed in this study could be used to determine optimal temperature conditions for its mass rearing, to predict its seasonal population dynamics in fruit tree orchards or greenhouse crops, or to develop a population dynamics model of N. californicus.     

Development rate and lower temperature threshold in the eggs of Eurygaster integriceps (Heteroptera: Scutelleridae)

The sunn pest, Eurygaster integriceps Put. has a wide distribution in the Palearctic region. It is the most important pest problem of wheat in Turkey. The objective of this study was to attain better knowledge of the development of the sunn pest eggs. The lower temperature threshold and development rate of eggs were determined at 17, 20, 23, 26 and 32°C ± 1°C in the laboratory. A linear model was used to describe the developmental rate and temperature. The egg development required 90.9 degree‐days above the theoretical threshold of 11.7°C. The development time was 17.6 ± 0.1 days at 17°C, and 4.5 ± 0.01 days at 32°C. Incubation time was inversely related to temperature. The study showed that the eggs of E. integriceps needed shorter periods of time to complete their development than immature stages of their parasitoids Trissolcus spp.     

Diapause development in early and late emerging phenotypes of Delia floralis

The turnip fly, Delia floralis Fall6n （Diptera： Anthomyiidae） is an important insect pest of brassica vegetable crops in the holarctic region. Different populations have strongly varying temperature requirements for fly emergence, a challenge for accurate prediction of activity. This study focused on diapause development in one early and one late emerging phenotype. The physiological state after various treatments was deduced from emergence data. Our results showed a slow diapause progression at chilling conditions for both populations and diapause ended about 7 months after pupae were formed for the early population. For the late population held at 4℃ diapause did not end, no matter how long the duration of chilling. These pupae required a period with elevated temperatures above 6~C to continue development. At constant non-chilling conditions （18℃） from the time pupae were formed both populations completed diapause most rapidly. These results indicate that chilling delayed, rather than accelerated development and was not a prerequisite for diapause development. For post-diapause, results indicated a linear relationship between rate of development and temperature within the range of 6-18℃and a theoretical base temperature for development of about 2℃ for both populations. In conclusion, D. floralis pupae are in diapause throughout a long winter period, and delayed emergence of the late population appears to be caused by prolonged diapause regulated by a developmental temperature threshold. The study has added information on the biology of turnip fly populations, a prerequisite for improved pest control.     

Temperature‐dependent development of Aproceros leucopoda (Hymenoptera: Argidae), an invasive pest of elms in Europe

The temperature‐dependent development of Aproceros leucopoda Takeuchi, 1939 (Hymenoptera: Argidae), an invasive pest of elms in Europe, was studied in the laboratory on Siberian elm (Ulmus pumila) at six constant temperatures (10.9, 15.0, 19.5, 23.0, 24.3 and 27.0°C) and at a photoperiod of 16L:8D. The larvae of the species developed through 4–7 instars, and it was the 6th instar individuals of which continued their development at the highest rate. The developmental threshold (T_min) and the thermal constant (K) were determined by the linear model and Lactin‐2 model for egg, larval, prepupal and pupal stages and one whole generation. The estimated values of T_min and K by the two models for one generation were 7.3 and 7.1°C, and 426.5 and 432.7 degree‐days, respectively. Based on the survival and fecundity rates, the optimal temperature range for the species may be expected to be between 15.0 and 19.5°C. Allowing for the period of diapause, it was estimated that A. leucopoda might potentially develop through up to four or five generations per year in Hungary. These results may contribute to the better understanding of the biology of an invasive alien species in Europe.